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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ５５　　　

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RegulationofcarotenoidbiosynthesisinfruitsZHANGDanDan(张丹丹)１ZENGQing(曾琴)１２JIANGGuoXiang(蒋国祥)１

JIANGYueMing(蒋跃明)１ amp DUANXueWu(段学武)１lowast

１SouthChinaBotanicalGardenChineseAcademyofSciencesGuangzhou５１０６５０China２UniversityofChineseAcademyofSciencesBeijing１０００４９China

ReceivedDecember２１２０１７acceptedJanuary１７２０１８

　　lowast Correspondingauthor(Emailxwduanscbgaccn＋８６２０３７２５２９６０)

Abstract　CarotenoidsareaclassofisoprenoidswidelydistributedinplantsalgaefungiandbacteriaCarotenoidsareessentialcomponentsforhumandietprovidinghealthpromotingandnutritionalbenefitsFruitsarethemajorsourceofcarotenoidsforhumanconsumptionCarotenoidbiosynthesisandregulationinfruitsareofgreatimportancefordevelopmentandmaintenanceofnutritionalqualityInrecentyearssignificantprogresshasbeen madeinunderstandingthebiosynthesisandregulationofcarotenoidsintomatoandother widelyconsumedfruitsCarotenoidaccumulationinfruitsishighlyregulatedbydevelopmentalprogramsenvironmentalfactorsandmetabolicsignalsatmultiplelevelsInthisreviewwehighlightrecentinsightsintotranscriptional(transcriptionfactoralternativeRNAsplicingepigeneticmodificationmiRNA)postＧtranscriptionalandhormoneregulationofcarotenoidbiosynthesisinplantsespeciallyinfruits

Keywords　CarotenoidbiosynthesisFruitTranscriptionfactorsPosttranscriptionalregulationdoi１０１６２６２jcnki１００５Ｇ０８４１２０１８０１００５

１　Introduction

　Carotenoidsareaclassof４０Ｇcarbonisoprenoidswith＞７５０memberswidelydistributedinplantsalgaefungiandbacteria[１]CarotenoidsconstitutethemainpigmentsinfruitsresultinginthetypicalyelloworangeandredcolorcharacteristicsCarotenoidsareinvolvedinthegrowthdevelopmentandresponsesofplantsto the environmental stimuliIn green photosynthetic tissuescarotenoids participate inphotosystemassemblylightＧharvestingandphotoprotection[２]InnonＧgreentissuescarotenoidsconferplantsvividcolortoattractpollinatorsandseeddispersersCarotenoidsalsoserveasprecursorstothebiosynthesisofphytohormonesabscisicacids(ABA)andstrigolactones(SLs)whicharekeyregulatorsofdevelopmentandstressresponseinplants[３]MoreimportantlycarotenoidsareessentialcomponentsforhumandietCarotenoidsprovidehealthbenefitstohumansasprovitaminAandnaturalantioxidant[４]Additionallycarotenoidsenhancetheimmunefunctionavoidsunburnreactionsanddelayagingandtheonsetofcertaintypesofcancer[５]

Consideringtheimportanceofcarotenoidsin plantphysiologicalprocessesandin human healthsignificantprogresshasbeen madeinunderstandingcarotenoid metabolism andregulationinplantsCurrentlythecarotenoidbiosynthesispathwayinplantshasbeen wellilluminatedThe mechanismunderlyingtheregulationofgeneorproteinsinthecarotenoidbiosynthesispathwayhasbeengraduallyunveiledInfruitsgreatadvancesincarotenoidbiosynthesisandregulationhavealsobeenmadeintomatoasamodelfruitaswellasotherfruitsHoweverincontrasttogreenplanttissuesfruitscontainmore

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５６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

complexcarotenoidcompositionsimplyingthatvariousandmultifacetedregulatorymechanismsmayexistinfruits[６]Thereviewfocusesonrecentunderstandingoftheregulationofcarotenoidbiosynthesisincludingtranscriptionalposttranscriptionalandhormoneregulationinplantsespeciallyinfruits

２　Diversityofcarotenoidsinfruits

　Fruitsarethe majorsourceofcarotenoidsforpromotinghumanhealthandprovidingnutritionalbenefitsAlargenumberoffruitsaccumulatecarotenoidsCarotenoidcontentandcompositionvarygreatlyamongdifferentspeciesoffruitsBasedonthetotalcarotenoidcontentsfruitscanbeclassifiedintofourgroups[７](１)low (＜１μgg－１freshweight(fw))suchasstrawberry[８](２)moderate(１mdash５μgg－１fw)suchaswhiteＧfleshpeach[９](３)high(５mdash２０μgg－１fw)suchasyellowpepper[１０]and(４)veryhigh(＞２０μgg－１fw)suchasredＧfleshsweetorange[１１]InadditiontogeneticvariationdevelopmentalstageandtissuespecificitygreatlyinfluencecarotenoidcompositionsandcontentsinfruitsAtthegreenstageoffruitscarotenoidsare maskedbychlorophyllsandthepredominantcarotenoidisluteinfollowedbyβＧcaroteneviolaxanthinandneoxanthin [７]Thischaracterisverycommon among different species offruits When ripeningremarkable differencesin carotenoidcompositionsandcontentsareexhibitedamongdifferentspeciesevendifferentcultivarsortissueswithinthesamespeciesMostoftenmorecarotenoidsaccumulateinpeeltissuesthaninpulptissues[１２]Table１summarizestotalcarotenoidcontentsandthemajorcarotenoidspresentinediblepartsofthemostwidelyconsumedfruits

Table１　Carotenoidsaccumulationinediblepartsofthemostwidelyconsumedfruits(ripe)worldwide１)

Fruitspecies Totalcarotenoidcontent Majorcarotenoid References

Apple ９mdash２４μggdw Xanthophyll [１３]

Banana(ripe) １６mdash１０５μggfw βＧCaronteneαＧCarontene [１４]

Grape １５mdash３μggfw LuteinβＧCarontene [１５]

Citrus(redfleshGrapefruit) １３mdash７４μggfw βＧCaronteneLycopenelutein [１６]

Citrus(yellowfleshgrapefruit) １２mdash６０μggfw βＧCaronteneluteinZeaxanthinβＧCryptoxanthin [１６]

Citrus(whitefleshgrapefruit) ＞２μggfw PhytoeneViolaxanthinZeaxanthin [１７]

Citrus(mandarin) ＞２５μggfw βＧCryptoxanthinPhytoeneβＧCaronteneζＧCaronteneViolaxanthin

Citrus(redＧfleshsweetorange) ４５mdash１０７μggfw Phytoenephytofluenelycopene９ＧcisＧViolaxanthin [１０１９]

Citrus(yellowＧfleshsweetorange) ２mdash１０μggfw ９ＧcisＧViolaxanthinantheraxanthin [１０１９]

Kiwifruit ＞３０μggfw βＧCaronteneLutein [２０]

Mango ＞１９０μggfw βＧCaronteneViolaxanthinLutein [２１]

Melon(orangeflesh) ５５０μggdw βＧCaronteneβＧcryptoxanthin [２２]

Papaya(yellowflesh) ３３６μggfw βＧCryptoxanthinβＧCarontene [２３]

Papaya(redflesh) ５９２μggfw LycopeneβＧCryptoxanthinζＧCaronteneβＧCarontene [２３]

Peach(yellowflesh) １０mdash１２μggfw AntheraxanthinLuteoxanthinZeaxanthin [９]

Peach(whiteflesh) ＜２μggfw ViolaxanthinLuteinZeaxanthin [９]

Pepper(red) １８０mdash１１００μggdw CapsanthinβＧCryptoxanthinZeaxanthinβＧCarontene [１１]

Pepper(yellow) １２mdash２０μggfw LuteinβＧCarontene [１１]

Strawberry ＜０３μggfw βＧCaronteneLutein [８]

Tomato ５mdash１３５μggfw LycopeneβＧCarontenePhytoenePhytofluene [２４]

Watermelon(redＧflesh) ３０mdash７０μggfw Lycopene [２５]

Watermelon(yellowＧflesh) ５μggfw ViolaxanthinLutein [２５２６]

　　１)fwindicatesfreshweightdwindicatesdryweight

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ５７　　　

　CitrusisoneofthemosteconomicallyimportantediblefruitsworldwidewiththemostdiversecarotenoidcompositionMostcultivatedcitrusesarenaturalorartificialhybridsoffourcoreancestralspeciescitronpummelomandarine and papeda The commercially important cultivated citrusinclude orangegrapefruitmandarinandlemonCarotenoidaccumulationvariesgreatlyin differentcitrusspeciesMandarinand orangeaccumulate primarily βＧcryptoxanthin and violaxanthinwhile grapefruitandpummeloarerichinphytoenephytoflueneandlycopene[１７１８２７２８]Inadditionlemonandlimecontainlowlevelsofcarotenoids[１８]

TomatohasbeenwidelyusedasamodelfruittoresearchcarotenoidmetabolismTomatofruitdisplaysdiversecolorvariationwhichisattributedbythedifferentialcarotenoidaccumulationRedtomatomainlycontainslycopeneaccountingforupto９０ofthetotalcarotenoids[２４]SomemutanttomatofruitswithdiversecolorsarecharacterizedbyabnormalcarotenoidbiosynthesisForexampleorangetmutant[２９]orangeredDeltamutant[３０]andorangeBeltamutantfruit[３１]accumulateprimarilyproＧlycopeneδＧcaroteneandβＧcarotenerespectively

PapayaisanimportantcommercialfruitcultivatedintropicalandsubtropicalareasandisrichincarotenoidThecompositionsofcarotenoidinpapayadeterminethefruitcolorYellowＧfleshedpapayavarietyaccumulatesmainlyβＧcryptoxanthinandβＧcarotenewhileredＧfleshedcultivarmainlylycopene[２３]

SimilartopapayadifferentcarotenoidcompositionsgivepepperfruitdiversecolorsRedpeppercontainsthehighestcarotenoidcontentamongallthecommonediblefruitswiththecontentofupto１１００μgg－１fwThepredominantcarotenoidsinredpepperarecapsanthin[３２]YellowpepperarerichinluteinandαＧorβＧcarotenewhileorangepeppercontainsprimarilycapsanthinluteinandorβＧcarotene[３３３４]

Watermelonisoneofthe mostpopularfruitsinthe worldFleshcoloristheimportanttraitofwatermelonCarotenoidsareresponsiblefordiversecolorsin watermelonfruit [２５]RedＧfleshedwatermelonsconsistedprimarilyoflycopenewithasmallamountofphytoenephytoflueneζＧcaroteneαＧcaroteneluteinzeaxanthinandviolaxanthin[２５]whileviolaxanthinandluteinconstitutethemajorcarotenoidsinorangeＧfleshedwatermelon[２５２６]

３　Biosynthesisofcarotenoids

　Inhigherplantscarotenoidsaresynthesizedinvarioustypesofplastidsincludingproplastidsetioplastschloroplastsamyloplastsandchromoplasts[３５]ThecarontenoidbiosynthesispathwayhasbeenwellestablishedwhichinvolvesthreeimportantprocessesbiosynthesisofprecursorformationoflinearchaincarotenoidsandcyclizationoflycopeneThegenesandenzymesinvolvedintheseprocessesforplantsareillustratedinFigure１Alargenumberofgenesfromfruitsinrelationtocarotenoidbiosynthesisandregulationalsohavebeenclonedandcharacterized

Thebiosynthesisofcarotenoidsdependsonthesupplyoftwobasicbuildingblocksofcarotenoidsisopentenyldiphosphate(IPP)anddimethylallyldiphosphate(DMAPP)[６]whichareproducedvia２CＧmethylＧDＧerythritolＧ４Ｇphosphate(MEP)pathwaySevenenzymesareinvolvedinMEPpathwayincluding１ＧdeoxyxyluloseＧ５Ｇphosphatesynthase(DXS)１ＧdexoyＧDＧxylulose５Ｇphosphatereductoisomerase(DXR)MEPcytidylyltransferase(MCT)４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritol(CDPＧME)kinase(CMK)２ＧCＧmethylＧDＧerythritol２４Ｇcyclodiphosphate (MECDP)synthase (MDS)(e)Ｇ４ＧhydroxyＧ３ＧmethylbutＧ２ＧenＧ１Ｇyldiphosphate(HMBPP)synthase(HDS)and HMBPPsynthasereductase (HDR)[３６]ThefirststepinMEPpathwayisregulatedbyDXSarateＧlimitingenzymeincarotenogensisTheoverexpressionofDXSenhancescarotenoidaccumulationin ArabidopsiswhilethemutationofDXSresultsinnocarotenoidaccumulation[３７]AnotherkeyregulatorystepisHDRthelastenzymeinMEPpathwaywhichcatalyzestheproductionofIPP[３８]IPPisisomerizedtoDMAPPviaIPPisomeraseIPPandDMAPPundergocondensationreactionsgeneratingthemajorcarotenoidprecursorgeranylgeranyldiphosphate (GGPP)Thereactionsarecatalyzed byisopentenyldiphosphateisomerase (IPI)and

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５８　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

Figure１　BiosynthesisandregulationofcarotenoidsinplantsThegreyrectanglesrepresentthesubstratesandmetabolitesinthecarotenoid biosynthesispathwayTheblueellipsesrepresenttheenzymesandtheirgenesinvolvedincarotenoidbiosynthesisThegreenellipsesrepresenttranscriptionfactorsregulatingcarotenoidbiosynthesisTheredellipsesrepresentproteinsinvolvedintheposttranscriptionalregulationofcarotenoidbiosynthesisTheyellowellipsesrepresenttheproteinsinvolvedinepigeneticmodificationofcarotenoidbiosynthesisThepurpleellipsesrepresentmiRNAinvolvedintheregulationofcarotenoidbiosynthesisBCHnonＧhemeβＧcarotenehydroxylaseCDPＧME４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritolCDPＧME２P２ＧphosphoＧ４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritolCMKCDPＧMEkinaseCRTISOcarotenoidisomerase CYP９７A and CYP９７Ccytochrome P４５０Ｇtype monooxygenase ９７C DMAPPdimethylallyldiphosphateDXPdeoxyＧDＧxylulose５ＧphosphateDXR１ＧdexoyＧDＧxylulose５ＧphosphatereductoisomeraseDXS１ＧdeoxyxyluloseＧ５ＧphosphatesynthaseG３Pglyceraldehyde３ＧphosphateGGPPgeranylgeranyldiphosphateGGPPSGGPPsynthaseHDRHMBPPreductaseHDSHMBPPsynthaseHMBPP(e)Ｇ４ＧhydroxyＧ３ＧmethylbutＧ２ＧenＧ１ＧyldiphosphateIPIisopentenyldiphosphateisomeraseIPPisopentenyldiphosphateLCYBlycopeneβＧcyclaseLCYElycopeneεＧcyclaseMCTMEPcytidylyltransferaseMDSMECDPsynthaseMECDP２CＧmethylＧDＧerythritol２４ＧcyclodiphosphateMEP２CＧmethylＧDＧerythritolＧ４Ｇphosphate NSY Neoxanthin synthasePDSphytoene desaturasePSYphytoenesynthaseVDEviolaxanthindeＧepoxidaseZDSζＧcarotenedesaturaseZEPzeaxanthinepoxidaseZＧISOζＧcaroteneisomerase

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ５９　　　

geranylgeranyldiphosphate(GGPP)synthase(GGPPS)[３９]ThecondensationoftwoGGPPmoleculescatalyzedbyphytoenesynthase(PSY)formsuncolored１５Ｇcis

phytoenethefirstcarotenoidproductThisstepisregardedasthemostimportantregulatorystepincarotenoidbiosynthesis[３９]TomatocontainsthreePSYgenesPSY１PSY２andPSY３whichexhibittissueＧspecificexpressionmainlyinfruitinpetalandinrootrespectivelyDuringtomatoripeningtheaccumulationofcarotenoidcorrelateswiththeexpressionofPSY１ [４０４１]TransgenictomatobyantisenseinhibitionofPSY１producesonly３ofthecarotenoidinwildtypewildtypefruit[４２]SimilarresultsregardingtherelationshipbetweenupregulatedexpressionofPSYgenesandincreasedcarotenoidaccumulationhavebeenreportedinalargenumberoffruitssuchascitrus[４３]pepper[３４]persimmon[４４]loquat[１２]watermelon [２５]andbanana[４５]Uncoloredphytoenethenundergoesaseriesofdesaturationandisomerizationreactionsto generateredＧcolored allＧtransＧlycopenethe predominatepigmentinredtomatoand watermelonfruitsThesereactionsaresequentiallycatalyzedbyphytoenedesaturase(PDS)ζＧcarotenedesaturase(ZDS)ζＧcaroteneisomerase(ZＧISO)andcarotenoidisomerase(CRTISO)[３９]

Downstreaminthecarotenoidbiosynthesispathwaythecyclizationoflycopeneislocatedatthebranchingpointofthepathwaywhichproduceaseriesofcarotene(Figure１)[６７３９]ThecyclizationoflycopeneinvolvestwoenzymeslycopeneβＧcyclase(LCYB)andlycopeneεＧcyclase(LCYE)LCYBcatalyzesatwoＧstepreactiontoproduceβＧcarotenewithtwoβＧringsAεＧringandaβＧringaresequentiallyaddedtolycopeneformingαＧcarotene(βεＧcarotene)whichiscatalyzedbyLCYEandLCYBFollowingthecyclizationoflycopeneαＧcaroteneandβＧcarotenearesubjectedtohydroxylationandepoxidationformingaseriesofxanthophylls[６７３９]TheαＧcaroteneissequentiallycatalyzedbytwohydroxylasesCYP９７A and CYP９７CgeneratingluteinthefinalproductofαＧbranchincarotenoid biosynthesispathwayβＧcaroteneundergoestwostepsofhydroxylationandtwostepsofepoxidationcatalyzedbyβＧcarotenehydroxylase (BCH)andzeaxanthinepoxidase (ZEP)sequentiallyformingβＧcryptoxanthinzeaxanthinantheraxanthinandviolaxanthin[６７３９]Theconversionofviolaxanthinintoneoxanthinbyneoxanthinsynthase(NXS)completesthecorebiosynthesispathway[４６]

４　Transcriptionalregulationofcarotenoidbiosynthesis

４１　TranscriptionfactorTranscriptionalregulationplaysavitalroleinfruitdevelopmentandripeningaswellasabioticstresses

ItiswellknownthattranscriptionfactorsareinvolvedintranscriptionregulationofstructureandfunctiongenesincarotenoidbiosynthesispathwayAlthoughthegenesinvolvedinthebiosynthesisofcarotenoidbiosynthesishavebeenidentifiedandcharacterizedfromvariousfruits(Figure１)onlyafewtranscriptionfactorshavebeendemonstratedtodirectlyregulatetheexpressionofthesefunctiongenesinthepathwayThetranscriptionalcontrolofcarotenoidaccumulationhasbeenmostlystudiedintomatoduringripeningThesetranscriptionfactorsinclude RINR２R３ＧMYBNACSGR１PIF１RAP２２EIN３etcHowevermostofthesetranscriptionfactorsexertbroadeffectsonfruitripeningieethylenesynthesisfruitsofteningcolorformationaromaandflavorproductionandareunlikelytobespecificregulatorsofcarotenoidbiosynthesis

RIPENINGＧINHIBITOR (RIN)isa memberoftranscriptionfactorfamilycontaining MADSＧboxwhichplaysanessentialroleinfruitripeningasaglobalmasterregulator[４７]MarteletalreportedthatRINinteractswithSlPSY１thespecificPSYgeneassociatedwithcarotenoidbiosynthesisintomato[４８]FujisawaetalidentifiedanumberofRINＧtargetedgenesincarotenoidbiosynthesispathwaybychromatinimmunoprecipitationcoupled with DNA microarrayanalysisandfoundthatRIN regulatescarotenoidaccumulationviapositivelyregulatingPSY１ZISOandCRTISOinadirectmanneraswellaspositivelycontrollingZDSandnegativelyregulatingLYCBandLYCEbyanindirecteffectintomatofruit[４９]

VＧmybmyeloblastosisviraloncogenehomolog(MYB)proteinsbelongtoalargefamilyoftranscriptionfactorsinplantsThemajorityofMYBareR２R３ＧMYBsubfamilywithtworepeatsinitsMYBdomain

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６０　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

TheR２R３ＧMYBTFsplaykeyrolesinregulatingplantＧspecificprocessesincludingprimaryandsecondarymetabolismgrowthanddevelopmentandresponsetoabioticandbioticstresses [５０]IncitrusCrMYB６８an R２R３ＧMYBtranscriptionalfactorcandirectlybindandnegativelyregulateCrBCH２resultinginthedelayinthetransformationofαＧandβＧcaroteneandtheinhibitionofpeeldeＧgreeningincitrus[５１]SimilarlySagawaetalidentifiedanR２R３ＧMYBtranscriptionfactorReducedCarotenoidPigmentation１(RCP１)whichpositivelyregulatescarotenoidbiosynthesisduringMimuluslewisiiflowerdevelopmentLossＧofＧfunctionmutationsinRCP１resultindownＧregulationofallcarotenoidbiosyntheticgenesandreducecarotenoidcontentwhileoverexpressionofthisgeneinthercp１ mutantbackgroundrestorescarotenoidproduction[５２]Thereforeinadditiontoregulatinganthocyanins[５３]R２R３ＧMYBisalsoinvolvedintheregulationofcarotenoidbiosynthesisinfruits

NAMATAF１２andCUC２ (NAC)transcriptionfactorsareoneofthelargestfamiliesofplantＧspecifictranscription factors which areimplicated in plant growth and developmentflavonoidbiosynthesiswoodformationandstressresponses [５４]TheroleofNACtranscriptionfactorsinregulatingfruitripeningandsenescencehasbeenreportedintomato[５５]banana[５６]andlitchi[５４]IntomatoSlNAC１and SlNAC４ positivelyregulatetomatofruitripeningbutexhibitdifferentialcharacteristicsAntisensesuppression ofSlNAC１ resultsin delayed ethylene production andfruitripeningbuthigherlevelsofethylenebiosynthesisandaccumulationoftotalcarotenoidandlycopeneaccompaniedbyupＧregulatedexpressionofgenesrelatedtolycopeneandethylenebiosynthesis [５５]DifferentfromSlNAC１reducedexpressionofSlNAC４byRNAinterference(RNAi)intomatodelayedfruitripeningdecreasedethylenesynthesisandreducedcarotenoidsbyalteringcarotenoidpathwayflux[５７]AdditionallyFuetalreportedthatpapayaCpNAC２actsasatranscriptionalactivatorofCpPDS２４CpZDSCpLCYＧeandCpCHYＧb by directly bindingtotheirpromotersand promotestheirtranscription[５８]

SomeothertranscriptionfactorshavealsobeenreportedtobeinvolvedinthetranscriptionalregulationofstructuregenesinthecarotenoidbiosynthesispathwayIntomatoSlSGR１aSTAYＧGREENproteinphysicallyinteracts with PSY１ to suppress PSY１ expressionthus negatively regulatinglycopeneproductionduringfruitripening[５９]PhytochromeＧinteractingfactor１downＧregulatetheaccumulationofcarotenoidbybindingtothepromoterofPSYandrepressingPSYexpressioninArabidopsisseedlings[６０]SimilarlyAtPAP２２amemberoftheAPETALA２ (AP２)ethyleneＧresponsiveelementＧbindingproteintranscriptionfactorfamilydirectlybinds withthepromotersofPSY andPDS toregulatecarotenoidbiosynthesisinArabidopsis [６１]PapayaCpEIN３aanethyleneresponsivefactordirectlybindswiththepromotersofCpPDS４andCpCHYＧbandpromotestheirtranscription[５８]InadditionoverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor(CrbHLH１)intomatolowerslycopeneaccumulationanddownＧregulatecarotenoidbiosyntheticgeneexpressionintomatofruit[６２]EctopicexpressionofanArabidopsisBZR１Ｇ１Dtranscriptionfactorinbrassinosteroidsignalingenhancescarotenoidaccumulationandfruitqualityattributesintomato[６３]４２　Epigeneticmodification

EpigeneticmodificationincludingthemethylationofDNACpGislandsandthemodificationofhistonesthatassociatedwithDNAinchromosomesplayaveryimportantroleinregulatinggeneexpressionEpigeneticmodification possiblyisimplicatedinregulation ofcarotenoid biosynthesis (Figure１)Cazzonellietalreportedahistonemethyltransferaseenzyme(SET DOMAIN GROUP８SDG８)thatmethylateshistoneH３onLys４andor３６(H３K４andH３K３６)inArabidopsisthalianawhichisrequiredforexpressionofCRTISOgeneMutationofSDG８resultsindownＧregulatedexpressionofCRTISOgeneimpairedlutein biosynthesis andincreased shoot branchingThis wasthefirstreportregardinginvolvementofepigeneticmodificationinregulationofcarotenoidbiosynthesis[６４]４３　AlternativeRNAsplicing

AlternativeRNAsplicingisanimportantregulationofgeneexpressioninhighereukaryotesRecentlyAlvarezetalfoundthatalternativesplicingofPSYisimplicatedinregulationofcarotenogenesisinArabidopsisArabidopsispredominantlypossessasinglePSYgenewithtwoalternativesplicevariants

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６１　　　

(ASV)inlength andintheexonintronretention oftheir５1049011UTRsASV１ with along ５1049011UTR(untranslatedregion)isinvolvedindevelopmentallyregulatedcarotenoidformationwhileASV２withashort５1049011UTRispreferentiallyinduced whenanimmediateincreaseinthecarotenoidpathwayfluxisrequired[６５]４４　microRNAs

MicroRNAs(miRNAs)arekeyregulatorsofgeneexpressionineukaryotesandplayapivotalroleintheregulationofvariousbiologicalaswellas metabolicprocessesInterestinglyanartificialmaturemicroRNAs (amiRNAs)successfullytargetedthe PSY mRNA andreduced PSY mRNA levelinPhaeodactylumtricornutumwhichfurtherreducedthelevelsofcarotenoidsinthePtricornutumamiRNAknockdownlines[６６]ItwasspeculatedthatmiRNApossiblyisinvolvedinthetranscriptionregulationofcarotenoidbiosynthesisinplants

５　PostＧtranscriptionalregulationofcarotenoidsbiosynthesis

　InadditiontotranscriptionregulationofstructuregenesinvolvedinthecarotenoidpathwayrecentstudieshaverevealedotherregulatorymechanismstocontrolbiosyntheticenzymelevelsandactivitiesinplantssuchaspostＧtranscriptionalregulation (Figure１)Theseregulatory mechanismspossiblyarepresentduringfruitdevelopmentandripening

ORANGE(OR)isaplastidＧlocalizedproteincarryingacysteineＧrichzincfingerdomainPreviousstudiedshowedthatORpromotescarotenoidaccumulationincalliofrice[６７]andsweetpotato [６８]FurtherZhouetalfoundthatArabidopsisORandPSYphysicallyinteractwitheachotherinplastidsresultingin minimaleffecton expression ofPSY gene [６９]Howeveroverexpression of AtORsignificantlyincreasedtheamountofenzymaticallyactivePSYwhereasanatoratorＧlikedoublemutantexhibitsadramaticallyreducedPSYlevelTheresultrevealedanovelmechanismunderlyingregulationofcarotenoidbiosynthesisviaposttranscriptionalmodificationofPSYinplants[６９]

Inanotherimportantliterature on postＧtranscriptionalregulation Welsch et alreported thatdegradationmodificationofproteinincarotenoidbiosynthesispathwayisimplicatedinregulationofcarotenoidbiosynthesisClpproteasesystemthemostabundantandcomplexsolubleproteasesystemintheplastidwasshowntotargetPSYTheabsenceofCLPC１CLPP４andCLPR１Ｇ２enhancedthelevelsofactivePSYandseveralothercarotenogenicenzymes[７０]ThereforeORproteincounterbalancesClpＧmediatedproteolysisinmaintainingPSYproteinhomeostasis

Theauthors1049011researchteamalsodiscoveredanindirectlypostＧtranscriptionalregulatorymechanismtoregulateexpressionofPSYgeneinbananafruitSulfoxidationofproteinsbyreactiveoxygenspeciescancauseconformationalalterationorfunctionalimpairmentswhichcouldbereversedby Metsulfoxidereductase(Msr)ItwasfoundthatCaM１isasubstrateofMaMsrA７anditssulforxidationisrepairedbyMaMsrA７MaHY５Ｇ１actingasatranscriptionalrepressorofMaPSY１MaPSY２andMaPSY３inbananafruitisa CaMＧbindingproteinSulfoxidationregulationof MaCaM１ by MaMsrA７altersexpressionofMaPSY１MaPSY２andMaPSY３genesbymodifyingMaHY５Ｇ１transcriptionalactivity(nopublisheddata)

TwootherproteinsalsohavebeenreportedtoberelatedtoposttranscriptionalregulationofcarotenoidbiosynthesisSlSGR１atomatoSTAYＧGREENproteinregulateslycopeneaccumulationduringtomatofruitripeningviadirectinteractionwithPSY１[５９]AnotherexampleisthepostＧtranslationalregulationofDXSJＧproteinJ２０ (chaperoneproteindnaJ２０)interactsdirectlywithDXSregulatingDXSproteinlevelandactivitybyidentifyingunfoldedormisfolded(damaged)formsofDXSandtargetingthemtotheHsp７０systemforproperfoldingundernormalconditionsordegradationuponstress[７１]

６　Hormonalregulationofcarotenoidbiosynthesis

　Fruitripeningisacomplexandgeneticallyprogrammedprocesswhichinvolvesaseriesoforganolepticphysiologicaland biochemical changesresulting in the development of edible quality [７２]

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PhytohormonesplaycrucialrolesinfruitripeningwhichhasbeenshowntoaffectcarotenoidaccumulationinfruitsMajorprogressregardingtheinvolvementofphytohormonesinregulatingcarotenoidbiosynthesishasbeenachievedinfruits

Ethyleneplaysa centralrolein climactericfruitripeningTherole ofethylenein carotenoidaccumulationinclimactericfruitshasbeenwidelystudiedIntomatoethyleneinitiatesfruitripeningresultinginarapidcolorshiftfromgreentoredwithincreasedlycopeneaccumulationanddecreasedβＧxanthophyllsandchlorophyllscontentsTheroleofethyleneinregulatingcarotenoidbiosynthesisduringtomatofruitripeninginvolvesacomplexregulatorynetworkoftranscriptionfactorsRINasamasterregulatorbindstothepromotersofgenesinvolvedinfruitripeningprocessesincludingcarotenoidbiosynthesis[４８４９７３]APETALA２a(AP２a)isamemberofAP２ERFsuperfamilywhichregulatestomatofruitripeningbyregulatingethylenebiosynthesisandsignalingRepressionofAP２abyRNAinterference (RNAi)resultsin decreasedlevels ofphytoeneandlycopenebut higherβＧcaroteneaccumulationconsistentwithdownＧregulatedexpressionofPDSCtRＧb２andCtrlSOandupＧregulatedexpressionofZEP１MoreoverseveralripeningＧrelatedregulatorsRIPENINGＧINHIBITOR (RIN)NONＧRIPENING (NOR)andCOLORLESSNONＧRIPENING (CNR)functionupstreamofAP２aandpositivelyregulateitsexpression[７４]SlERF６anothermemberofAP２ERFsuperfamilyisanegativeregulatorofcarotenoidaccumulationReducedexpressionofSlERF６byRNAienhancedbothcarotenoidandethylenelevelsduringfruitripening[７５]InadditionthreeothertranscriptionfactorsarerelatedtotheethylenepathwayincludingTAGL１FRUITFULL１and２whichhavebeenreportedtopositivelyregulatecarotenoidaccumulationduringtomatoripening[７６mdash７８]

Auxinisinvolvedincellexpansionanddivisiontissuedifferentiationorgandevelopmentandarangeofphysiologicalprocess[７９]Recentlyincreasingevidencesshowthatauxinalsoplaysanimportantroleinregulatingfruitripening[８０]TheleveloffreeIAA (themostabundantauxin)tendstodeclinepriortotheonsetoftomatofruitripening[８１]AuxinnegativelycontrolscarotenoidaccumulationintomatofruitExogenousIAA treatmentsignificantlyreduceslycopeneaccumulationbutenhancesthelevelsofneoxanthinandviolaxanthinaccompaniedbydownＧregulatedexpressionofPsy１Psy３PdsZisoandCrtisoandupＧregulatedexpressionofβＧLcy１andCrtrＧβ１ [８２]Howeverwhetherauxindirectlyregulatesthegenesincarotenoidpathwayremainsunknown

Abscisicacid (ABA)isa key hormoneinvolvedintuningresponsestoabioticstressesLittleinformationisavailableabouttheinvolvementofABAinregulatingcarotenoidaccumulationduringtomatofruitripeningABA hasbeenreportedto beimplicatedinfruitripeningandinfluencecarotenoidaccumulationintomato[８３]andstrawberry[８４]fruit

JAssuchasmethyljasmonicacidjasmonicacidandotherderivativesareplantendogenoushormones[８５]JAsalsoplayimportantrolesinfruitripeningLietalreportedthatJAinduceethyleneproductionbyMdMYC２ＧmediatedandMdERF３ＧmediatedupregulationofMdACS１gene[８６]Applicationofmethyljasmonate(MeJA)increasestheaccumulationofanthocyaninβＧcarotenecontentsandseveralphenoliccompounds[８７]LiuetalfurtherilluminatedtheroleofJAinregulatingcarotenoidaccumulationduringtomatofruitripeningwithJAＧdeficientmutants(spr２anddef１)anda３５∷prosystransgenicline(３５∷prosyswithincreasedJAlevelsandconstitutiveJAsignaling)andfoundthatlycopeneaccumulationissignificantlyinhibitedinspr２anddef１fruitbutenhancedin３５S∷prosysfruitaccompaniedbyasimilartrendofexpressionoflycopenebiosyntheticgenes[８８]Inadditionethyleneproductionisdepressedinspr２anddef１fruitbutincreasedin３５S∷prosysfruitMoreovertheexogenousapplicationofMeJAtoNeverripe (Nr)an ethyleneＧinsensitive mutantresultsin enhancedlycopene accumulation andexpressionoflycopenebiosyntheticgenes [８８]TheseresultsindicatedthatJA promoteslycopenebiosynthesisinamannerindependentofethylene

７　Futureresearchdirections

　CarotenoidmetabolismandregulationhavebeenwidelyresearchedinplantsHoweverthecarotenoidＧ

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relatedstudieshavebeenmostlyfocusedonmodelspeciessuchasArabidopsisandtomatoThemolecularmechanismsunderlyingcarotenoid metabolism andregulationin otherfruitspeciesarestillpoorlyunderstoodConsideringthediversityofcarotenoidsinfruitsitisnecessarytoinvestigatethenovelgenesandregulationmechanismsrelatedtocarotenoidbiosynthesisinplants

Carotenoid accumulation is cooperatively controlled at multiple levelsincluding developmentalprogramsenvironmentalfactorsand metabolicsignalsTranscriptionfactorsplayimportantroleinregulatingcarotenoidbiosynthesisHoweveronlyafewtranscriptionfactorsinvolvedincarotenoidbiosynthesisareidentifiedandtranscriptionregulationismainlyrelatedtoexpressionofPSYMoreovermostofthesetranscriptionfactorsexerttheirinfluencesviaregulatingfruitripeningnotspecificcarotenoidbiosynthesisＧrelated genesTheinteracting partners oftranscriptionfactorsinvolvedincarotenoidmetabolicnetworkalsoremaintobeidentifiedPostＧtranscriptionalregulationalternativeRNAsplicingepigeneticmodificationandmiRNAareofimportanceinplantgrowthanddevelopmentandresponsetoabioticstressHoweverlittleinformationregardingtheinvolvementofthesemechanismsinregulating carotenoid metabolism in planteven in Arabidopsisis available Application ofphytohormonescontributestoregulatecarotenoidcontentand maintainfruitqualityinagricultureandpostharvesttreatmentThemechanismunderlyingregulationofcarotenoidmetabolismbyphytohormonesespeciallycrossＧtalkamongdifferentphytohormonesarestillfarfrombeingunderstoodInthefuturestudiesbetterunderstandingofcarotenoid metabolismandregulationinfruitswillnotonlyhaveanimportantimpactongeneticimprovementandpostharvesttreatmentbutalsowillstrengthenknowledgeofcarotenoidregulationinplants

Acknowledgements

ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(GrantNos３１７７２０４１３１３２２０４４and３１５０１５４５)ScienceandTechnologyPlanningProjectofGuangdongProvince(GrantNo２０１５B０９０９０１０５８)ScienceandTechnologyPlanningProjectofGuangzhou (GrantNo２０１６０４０２００４８)andTalentProgramofGuangdongProvince(No２０１４TX０１N０４９)

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２００７４７１mdash１９[７３]FujisawaMShimaYHiguchiNetalDirecttargetsofthetomatoＧripeningregulatorRINidentifiedbytranscriptomeandchromatin

immunoprecipitationanalysesPlanta２０１２２３５１１０７mdash１１２２[７４]KarlovaRRosinFMBusscherＧLangeJetalTranscriptomeandmetaboliteprofilingshowthatAPETALA２aisamajorregulatorof

tomatofruitripeningPlantCell２０１１２３９２３mdash９４１[７５]LeeJMJoungJGMcQuinnRetalCombinedtranscriptomegeneticdiversityandmetaboliteprofilingintomatofruitrevealsthatthe

ethyleneresponsefactorSlERF６playsanimportantroleinripeningandcarotenoidaccumulationPlantJournal２０１２７０１９１mdash２０４[７６]ShimaYFujisawaMKitagawaMetalTomatoFRUITFULLhomologsregulatefruitripeningviaethylenebiosynthesisBioscience

BiotechnologyandBiochemistry２０１４７８２３１mdash２３７[７７]VrebalovJPanILArroyoAJMetalFleshyfruitexpansionandripeningareregulatedbythetomatoSHATTERPROOFgene

TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

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５６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

complexcarotenoidcompositionsimplyingthatvariousandmultifacetedregulatorymechanismsmayexistinfruits[６]Thereviewfocusesonrecentunderstandingoftheregulationofcarotenoidbiosynthesisincludingtranscriptionalposttranscriptionalandhormoneregulationinplantsespeciallyinfruits

２　Diversityofcarotenoidsinfruits

　Fruitsarethe majorsourceofcarotenoidsforpromotinghumanhealthandprovidingnutritionalbenefitsAlargenumberoffruitsaccumulatecarotenoidsCarotenoidcontentandcompositionvarygreatlyamongdifferentspeciesoffruitsBasedonthetotalcarotenoidcontentsfruitscanbeclassifiedintofourgroups[７](１)low (＜１μgg－１freshweight(fw))suchasstrawberry[８](２)moderate(１mdash５μgg－１fw)suchaswhiteＧfleshpeach[９](３)high(５mdash２０μgg－１fw)suchasyellowpepper[１０]and(４)veryhigh(＞２０μgg－１fw)suchasredＧfleshsweetorange[１１]InadditiontogeneticvariationdevelopmentalstageandtissuespecificitygreatlyinfluencecarotenoidcompositionsandcontentsinfruitsAtthegreenstageoffruitscarotenoidsare maskedbychlorophyllsandthepredominantcarotenoidisluteinfollowedbyβＧcaroteneviolaxanthinandneoxanthin [７]Thischaracterisverycommon among different species offruits When ripeningremarkable differencesin carotenoidcompositionsandcontentsareexhibitedamongdifferentspeciesevendifferentcultivarsortissueswithinthesamespeciesMostoftenmorecarotenoidsaccumulateinpeeltissuesthaninpulptissues[１２]Table１summarizestotalcarotenoidcontentsandthemajorcarotenoidspresentinediblepartsofthemostwidelyconsumedfruits

Table１　Carotenoidsaccumulationinediblepartsofthemostwidelyconsumedfruits(ripe)worldwide１)

Fruitspecies Totalcarotenoidcontent Majorcarotenoid References

Apple ９mdash２４μggdw Xanthophyll [１３]

Banana(ripe) １６mdash１０５μggfw βＧCaronteneαＧCarontene [１４]

Grape １５mdash３μggfw LuteinβＧCarontene [１５]

Citrus(redfleshGrapefruit) １３mdash７４μggfw βＧCaronteneLycopenelutein [１６]

Citrus(yellowfleshgrapefruit) １２mdash６０μggfw βＧCaronteneluteinZeaxanthinβＧCryptoxanthin [１６]

Citrus(whitefleshgrapefruit) ＞２μggfw PhytoeneViolaxanthinZeaxanthin [１７]

Citrus(mandarin) ＞２５μggfw βＧCryptoxanthinPhytoeneβＧCaronteneζＧCaronteneViolaxanthin

Citrus(redＧfleshsweetorange) ４５mdash１０７μggfw Phytoenephytofluenelycopene９ＧcisＧViolaxanthin [１０１９]

Citrus(yellowＧfleshsweetorange) ２mdash１０μggfw ９ＧcisＧViolaxanthinantheraxanthin [１０１９]

Kiwifruit ＞３０μggfw βＧCaronteneLutein [２０]

Mango ＞１９０μggfw βＧCaronteneViolaxanthinLutein [２１]

Melon(orangeflesh) ５５０μggdw βＧCaronteneβＧcryptoxanthin [２２]

Papaya(yellowflesh) ３３６μggfw βＧCryptoxanthinβＧCarontene [２３]

Papaya(redflesh) ５９２μggfw LycopeneβＧCryptoxanthinζＧCaronteneβＧCarontene [２３]

Peach(yellowflesh) １０mdash１２μggfw AntheraxanthinLuteoxanthinZeaxanthin [９]

Peach(whiteflesh) ＜２μggfw ViolaxanthinLuteinZeaxanthin [９]

Pepper(red) １８０mdash１１００μggdw CapsanthinβＧCryptoxanthinZeaxanthinβＧCarontene [１１]

Pepper(yellow) １２mdash２０μggfw LuteinβＧCarontene [１１]

Strawberry ＜０３μggfw βＧCaronteneLutein [８]

Tomato ５mdash１３５μggfw LycopeneβＧCarontenePhytoenePhytofluene [２４]

Watermelon(redＧflesh) ３０mdash７０μggfw Lycopene [２５]

Watermelon(yellowＧflesh) ５μggfw ViolaxanthinLutein [２５２６]

　　１)fwindicatesfreshweightdwindicatesdryweight

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ５７　　　

　CitrusisoneofthemosteconomicallyimportantediblefruitsworldwidewiththemostdiversecarotenoidcompositionMostcultivatedcitrusesarenaturalorartificialhybridsoffourcoreancestralspeciescitronpummelomandarine and papeda The commercially important cultivated citrusinclude orangegrapefruitmandarinandlemonCarotenoidaccumulationvariesgreatlyin differentcitrusspeciesMandarinand orangeaccumulate primarily βＧcryptoxanthin and violaxanthinwhile grapefruitandpummeloarerichinphytoenephytoflueneandlycopene[１７１８２７２８]Inadditionlemonandlimecontainlowlevelsofcarotenoids[１８]

TomatohasbeenwidelyusedasamodelfruittoresearchcarotenoidmetabolismTomatofruitdisplaysdiversecolorvariationwhichisattributedbythedifferentialcarotenoidaccumulationRedtomatomainlycontainslycopeneaccountingforupto９０ofthetotalcarotenoids[２４]SomemutanttomatofruitswithdiversecolorsarecharacterizedbyabnormalcarotenoidbiosynthesisForexampleorangetmutant[２９]orangeredDeltamutant[３０]andorangeBeltamutantfruit[３１]accumulateprimarilyproＧlycopeneδＧcaroteneandβＧcarotenerespectively

PapayaisanimportantcommercialfruitcultivatedintropicalandsubtropicalareasandisrichincarotenoidThecompositionsofcarotenoidinpapayadeterminethefruitcolorYellowＧfleshedpapayavarietyaccumulatesmainlyβＧcryptoxanthinandβＧcarotenewhileredＧfleshedcultivarmainlylycopene[２３]

SimilartopapayadifferentcarotenoidcompositionsgivepepperfruitdiversecolorsRedpeppercontainsthehighestcarotenoidcontentamongallthecommonediblefruitswiththecontentofupto１１００μgg－１fwThepredominantcarotenoidsinredpepperarecapsanthin[３２]YellowpepperarerichinluteinandαＧorβＧcarotenewhileorangepeppercontainsprimarilycapsanthinluteinandorβＧcarotene[３３３４]

Watermelonisoneofthe mostpopularfruitsinthe worldFleshcoloristheimportanttraitofwatermelonCarotenoidsareresponsiblefordiversecolorsin watermelonfruit [２５]RedＧfleshedwatermelonsconsistedprimarilyoflycopenewithasmallamountofphytoenephytoflueneζＧcaroteneαＧcaroteneluteinzeaxanthinandviolaxanthin[２５]whileviolaxanthinandluteinconstitutethemajorcarotenoidsinorangeＧfleshedwatermelon[２５２６]

３　Biosynthesisofcarotenoids

　Inhigherplantscarotenoidsaresynthesizedinvarioustypesofplastidsincludingproplastidsetioplastschloroplastsamyloplastsandchromoplasts[３５]ThecarontenoidbiosynthesispathwayhasbeenwellestablishedwhichinvolvesthreeimportantprocessesbiosynthesisofprecursorformationoflinearchaincarotenoidsandcyclizationoflycopeneThegenesandenzymesinvolvedintheseprocessesforplantsareillustratedinFigure１Alargenumberofgenesfromfruitsinrelationtocarotenoidbiosynthesisandregulationalsohavebeenclonedandcharacterized

Thebiosynthesisofcarotenoidsdependsonthesupplyoftwobasicbuildingblocksofcarotenoidsisopentenyldiphosphate(IPP)anddimethylallyldiphosphate(DMAPP)[６]whichareproducedvia２CＧmethylＧDＧerythritolＧ４Ｇphosphate(MEP)pathwaySevenenzymesareinvolvedinMEPpathwayincluding１ＧdeoxyxyluloseＧ５Ｇphosphatesynthase(DXS)１ＧdexoyＧDＧxylulose５Ｇphosphatereductoisomerase(DXR)MEPcytidylyltransferase(MCT)４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritol(CDPＧME)kinase(CMK)２ＧCＧmethylＧDＧerythritol２４Ｇcyclodiphosphate (MECDP)synthase (MDS)(e)Ｇ４ＧhydroxyＧ３ＧmethylbutＧ２ＧenＧ１Ｇyldiphosphate(HMBPP)synthase(HDS)and HMBPPsynthasereductase (HDR)[３６]ThefirststepinMEPpathwayisregulatedbyDXSarateＧlimitingenzymeincarotenogensisTheoverexpressionofDXSenhancescarotenoidaccumulationin ArabidopsiswhilethemutationofDXSresultsinnocarotenoidaccumulation[３７]AnotherkeyregulatorystepisHDRthelastenzymeinMEPpathwaywhichcatalyzestheproductionofIPP[３８]IPPisisomerizedtoDMAPPviaIPPisomeraseIPPandDMAPPundergocondensationreactionsgeneratingthemajorcarotenoidprecursorgeranylgeranyldiphosphate (GGPP)Thereactionsarecatalyzed byisopentenyldiphosphateisomerase (IPI)and

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５８　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

Figure１　BiosynthesisandregulationofcarotenoidsinplantsThegreyrectanglesrepresentthesubstratesandmetabolitesinthecarotenoid biosynthesispathwayTheblueellipsesrepresenttheenzymesandtheirgenesinvolvedincarotenoidbiosynthesisThegreenellipsesrepresenttranscriptionfactorsregulatingcarotenoidbiosynthesisTheredellipsesrepresentproteinsinvolvedintheposttranscriptionalregulationofcarotenoidbiosynthesisTheyellowellipsesrepresenttheproteinsinvolvedinepigeneticmodificationofcarotenoidbiosynthesisThepurpleellipsesrepresentmiRNAinvolvedintheregulationofcarotenoidbiosynthesisBCHnonＧhemeβＧcarotenehydroxylaseCDPＧME４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritolCDPＧME２P２ＧphosphoＧ４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritolCMKCDPＧMEkinaseCRTISOcarotenoidisomerase CYP９７A and CYP９７Ccytochrome P４５０Ｇtype monooxygenase ９７C DMAPPdimethylallyldiphosphateDXPdeoxyＧDＧxylulose５ＧphosphateDXR１ＧdexoyＧDＧxylulose５ＧphosphatereductoisomeraseDXS１ＧdeoxyxyluloseＧ５ＧphosphatesynthaseG３Pglyceraldehyde３ＧphosphateGGPPgeranylgeranyldiphosphateGGPPSGGPPsynthaseHDRHMBPPreductaseHDSHMBPPsynthaseHMBPP(e)Ｇ４ＧhydroxyＧ３ＧmethylbutＧ２ＧenＧ１ＧyldiphosphateIPIisopentenyldiphosphateisomeraseIPPisopentenyldiphosphateLCYBlycopeneβＧcyclaseLCYElycopeneεＧcyclaseMCTMEPcytidylyltransferaseMDSMECDPsynthaseMECDP２CＧmethylＧDＧerythritol２４ＧcyclodiphosphateMEP２CＧmethylＧDＧerythritolＧ４Ｇphosphate NSY Neoxanthin synthasePDSphytoene desaturasePSYphytoenesynthaseVDEviolaxanthindeＧepoxidaseZDSζＧcarotenedesaturaseZEPzeaxanthinepoxidaseZＧISOζＧcaroteneisomerase

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ５９　　　

geranylgeranyldiphosphate(GGPP)synthase(GGPPS)[３９]ThecondensationoftwoGGPPmoleculescatalyzedbyphytoenesynthase(PSY)formsuncolored１５Ｇcis

phytoenethefirstcarotenoidproductThisstepisregardedasthemostimportantregulatorystepincarotenoidbiosynthesis[３９]TomatocontainsthreePSYgenesPSY１PSY２andPSY３whichexhibittissueＧspecificexpressionmainlyinfruitinpetalandinrootrespectivelyDuringtomatoripeningtheaccumulationofcarotenoidcorrelateswiththeexpressionofPSY１ [４０４１]TransgenictomatobyantisenseinhibitionofPSY１producesonly３ofthecarotenoidinwildtypewildtypefruit[４２]SimilarresultsregardingtherelationshipbetweenupregulatedexpressionofPSYgenesandincreasedcarotenoidaccumulationhavebeenreportedinalargenumberoffruitssuchascitrus[４３]pepper[３４]persimmon[４４]loquat[１２]watermelon [２５]andbanana[４５]Uncoloredphytoenethenundergoesaseriesofdesaturationandisomerizationreactionsto generateredＧcolored allＧtransＧlycopenethe predominatepigmentinredtomatoand watermelonfruitsThesereactionsaresequentiallycatalyzedbyphytoenedesaturase(PDS)ζＧcarotenedesaturase(ZDS)ζＧcaroteneisomerase(ZＧISO)andcarotenoidisomerase(CRTISO)[３９]

Downstreaminthecarotenoidbiosynthesispathwaythecyclizationoflycopeneislocatedatthebranchingpointofthepathwaywhichproduceaseriesofcarotene(Figure１)[６７３９]ThecyclizationoflycopeneinvolvestwoenzymeslycopeneβＧcyclase(LCYB)andlycopeneεＧcyclase(LCYE)LCYBcatalyzesatwoＧstepreactiontoproduceβＧcarotenewithtwoβＧringsAεＧringandaβＧringaresequentiallyaddedtolycopeneformingαＧcarotene(βεＧcarotene)whichiscatalyzedbyLCYEandLCYBFollowingthecyclizationoflycopeneαＧcaroteneandβＧcarotenearesubjectedtohydroxylationandepoxidationformingaseriesofxanthophylls[６７３９]TheαＧcaroteneissequentiallycatalyzedbytwohydroxylasesCYP９７A and CYP９７CgeneratingluteinthefinalproductofαＧbranchincarotenoid biosynthesispathwayβＧcaroteneundergoestwostepsofhydroxylationandtwostepsofepoxidationcatalyzedbyβＧcarotenehydroxylase (BCH)andzeaxanthinepoxidase (ZEP)sequentiallyformingβＧcryptoxanthinzeaxanthinantheraxanthinandviolaxanthin[６７３９]Theconversionofviolaxanthinintoneoxanthinbyneoxanthinsynthase(NXS)completesthecorebiosynthesispathway[４６]

４　Transcriptionalregulationofcarotenoidbiosynthesis

４１　TranscriptionfactorTranscriptionalregulationplaysavitalroleinfruitdevelopmentandripeningaswellasabioticstresses

ItiswellknownthattranscriptionfactorsareinvolvedintranscriptionregulationofstructureandfunctiongenesincarotenoidbiosynthesispathwayAlthoughthegenesinvolvedinthebiosynthesisofcarotenoidbiosynthesishavebeenidentifiedandcharacterizedfromvariousfruits(Figure１)onlyafewtranscriptionfactorshavebeendemonstratedtodirectlyregulatetheexpressionofthesefunctiongenesinthepathwayThetranscriptionalcontrolofcarotenoidaccumulationhasbeenmostlystudiedintomatoduringripeningThesetranscriptionfactorsinclude RINR２R３ＧMYBNACSGR１PIF１RAP２２EIN３etcHowevermostofthesetranscriptionfactorsexertbroadeffectsonfruitripeningieethylenesynthesisfruitsofteningcolorformationaromaandflavorproductionandareunlikelytobespecificregulatorsofcarotenoidbiosynthesis

RIPENINGＧINHIBITOR (RIN)isa memberoftranscriptionfactorfamilycontaining MADSＧboxwhichplaysanessentialroleinfruitripeningasaglobalmasterregulator[４７]MarteletalreportedthatRINinteractswithSlPSY１thespecificPSYgeneassociatedwithcarotenoidbiosynthesisintomato[４８]FujisawaetalidentifiedanumberofRINＧtargetedgenesincarotenoidbiosynthesispathwaybychromatinimmunoprecipitationcoupled with DNA microarrayanalysisandfoundthatRIN regulatescarotenoidaccumulationviapositivelyregulatingPSY１ZISOandCRTISOinadirectmanneraswellaspositivelycontrollingZDSandnegativelyregulatingLYCBandLYCEbyanindirecteffectintomatofruit[４９]

VＧmybmyeloblastosisviraloncogenehomolog(MYB)proteinsbelongtoalargefamilyoftranscriptionfactorsinplantsThemajorityofMYBareR２R３ＧMYBsubfamilywithtworepeatsinitsMYBdomain

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６０　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

TheR２R３ＧMYBTFsplaykeyrolesinregulatingplantＧspecificprocessesincludingprimaryandsecondarymetabolismgrowthanddevelopmentandresponsetoabioticandbioticstresses [５０]IncitrusCrMYB６８an R２R３ＧMYBtranscriptionalfactorcandirectlybindandnegativelyregulateCrBCH２resultinginthedelayinthetransformationofαＧandβＧcaroteneandtheinhibitionofpeeldeＧgreeningincitrus[５１]SimilarlySagawaetalidentifiedanR２R３ＧMYBtranscriptionfactorReducedCarotenoidPigmentation１(RCP１)whichpositivelyregulatescarotenoidbiosynthesisduringMimuluslewisiiflowerdevelopmentLossＧofＧfunctionmutationsinRCP１resultindownＧregulationofallcarotenoidbiosyntheticgenesandreducecarotenoidcontentwhileoverexpressionofthisgeneinthercp１ mutantbackgroundrestorescarotenoidproduction[５２]Thereforeinadditiontoregulatinganthocyanins[５３]R２R３ＧMYBisalsoinvolvedintheregulationofcarotenoidbiosynthesisinfruits

NAMATAF１２andCUC２ (NAC)transcriptionfactorsareoneofthelargestfamiliesofplantＧspecifictranscription factors which areimplicated in plant growth and developmentflavonoidbiosynthesiswoodformationandstressresponses [５４]TheroleofNACtranscriptionfactorsinregulatingfruitripeningandsenescencehasbeenreportedintomato[５５]banana[５６]andlitchi[５４]IntomatoSlNAC１and SlNAC４ positivelyregulatetomatofruitripeningbutexhibitdifferentialcharacteristicsAntisensesuppression ofSlNAC１ resultsin delayed ethylene production andfruitripeningbuthigherlevelsofethylenebiosynthesisandaccumulationoftotalcarotenoidandlycopeneaccompaniedbyupＧregulatedexpressionofgenesrelatedtolycopeneandethylenebiosynthesis [５５]DifferentfromSlNAC１reducedexpressionofSlNAC４byRNAinterference(RNAi)intomatodelayedfruitripeningdecreasedethylenesynthesisandreducedcarotenoidsbyalteringcarotenoidpathwayflux[５７]AdditionallyFuetalreportedthatpapayaCpNAC２actsasatranscriptionalactivatorofCpPDS２４CpZDSCpLCYＧeandCpCHYＧb by directly bindingtotheirpromotersand promotestheirtranscription[５８]

SomeothertranscriptionfactorshavealsobeenreportedtobeinvolvedinthetranscriptionalregulationofstructuregenesinthecarotenoidbiosynthesispathwayIntomatoSlSGR１aSTAYＧGREENproteinphysicallyinteracts with PSY１ to suppress PSY１ expressionthus negatively regulatinglycopeneproductionduringfruitripening[５９]PhytochromeＧinteractingfactor１downＧregulatetheaccumulationofcarotenoidbybindingtothepromoterofPSYandrepressingPSYexpressioninArabidopsisseedlings[６０]SimilarlyAtPAP２２amemberoftheAPETALA２ (AP２)ethyleneＧresponsiveelementＧbindingproteintranscriptionfactorfamilydirectlybinds withthepromotersofPSY andPDS toregulatecarotenoidbiosynthesisinArabidopsis [６１]PapayaCpEIN３aanethyleneresponsivefactordirectlybindswiththepromotersofCpPDS４andCpCHYＧbandpromotestheirtranscription[５８]InadditionoverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor(CrbHLH１)intomatolowerslycopeneaccumulationanddownＧregulatecarotenoidbiosyntheticgeneexpressionintomatofruit[６２]EctopicexpressionofanArabidopsisBZR１Ｇ１Dtranscriptionfactorinbrassinosteroidsignalingenhancescarotenoidaccumulationandfruitqualityattributesintomato[６３]４２　Epigeneticmodification

EpigeneticmodificationincludingthemethylationofDNACpGislandsandthemodificationofhistonesthatassociatedwithDNAinchromosomesplayaveryimportantroleinregulatinggeneexpressionEpigeneticmodification possiblyisimplicatedinregulation ofcarotenoid biosynthesis (Figure１)Cazzonellietalreportedahistonemethyltransferaseenzyme(SET DOMAIN GROUP８SDG８)thatmethylateshistoneH３onLys４andor３６(H３K４andH３K３６)inArabidopsisthalianawhichisrequiredforexpressionofCRTISOgeneMutationofSDG８resultsindownＧregulatedexpressionofCRTISOgeneimpairedlutein biosynthesis andincreased shoot branchingThis wasthefirstreportregardinginvolvementofepigeneticmodificationinregulationofcarotenoidbiosynthesis[６４]４３　AlternativeRNAsplicing

AlternativeRNAsplicingisanimportantregulationofgeneexpressioninhighereukaryotesRecentlyAlvarezetalfoundthatalternativesplicingofPSYisimplicatedinregulationofcarotenogenesisinArabidopsisArabidopsispredominantlypossessasinglePSYgenewithtwoalternativesplicevariants

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６１　　　

(ASV)inlength andintheexonintronretention oftheir５1049011UTRsASV１ with along ５1049011UTR(untranslatedregion)isinvolvedindevelopmentallyregulatedcarotenoidformationwhileASV２withashort５1049011UTRispreferentiallyinduced whenanimmediateincreaseinthecarotenoidpathwayfluxisrequired[６５]４４　microRNAs

MicroRNAs(miRNAs)arekeyregulatorsofgeneexpressionineukaryotesandplayapivotalroleintheregulationofvariousbiologicalaswellas metabolicprocessesInterestinglyanartificialmaturemicroRNAs (amiRNAs)successfullytargetedthe PSY mRNA andreduced PSY mRNA levelinPhaeodactylumtricornutumwhichfurtherreducedthelevelsofcarotenoidsinthePtricornutumamiRNAknockdownlines[６６]ItwasspeculatedthatmiRNApossiblyisinvolvedinthetranscriptionregulationofcarotenoidbiosynthesisinplants

５　PostＧtranscriptionalregulationofcarotenoidsbiosynthesis

　InadditiontotranscriptionregulationofstructuregenesinvolvedinthecarotenoidpathwayrecentstudieshaverevealedotherregulatorymechanismstocontrolbiosyntheticenzymelevelsandactivitiesinplantssuchaspostＧtranscriptionalregulation (Figure１)Theseregulatory mechanismspossiblyarepresentduringfruitdevelopmentandripening

ORANGE(OR)isaplastidＧlocalizedproteincarryingacysteineＧrichzincfingerdomainPreviousstudiedshowedthatORpromotescarotenoidaccumulationincalliofrice[６７]andsweetpotato [６８]FurtherZhouetalfoundthatArabidopsisORandPSYphysicallyinteractwitheachotherinplastidsresultingin minimaleffecton expression ofPSY gene [６９]Howeveroverexpression of AtORsignificantlyincreasedtheamountofenzymaticallyactivePSYwhereasanatoratorＧlikedoublemutantexhibitsadramaticallyreducedPSYlevelTheresultrevealedanovelmechanismunderlyingregulationofcarotenoidbiosynthesisviaposttranscriptionalmodificationofPSYinplants[６９]

Inanotherimportantliterature on postＧtranscriptionalregulation Welsch et alreported thatdegradationmodificationofproteinincarotenoidbiosynthesispathwayisimplicatedinregulationofcarotenoidbiosynthesisClpproteasesystemthemostabundantandcomplexsolubleproteasesystemintheplastidwasshowntotargetPSYTheabsenceofCLPC１CLPP４andCLPR１Ｇ２enhancedthelevelsofactivePSYandseveralothercarotenogenicenzymes[７０]ThereforeORproteincounterbalancesClpＧmediatedproteolysisinmaintainingPSYproteinhomeostasis

Theauthors1049011researchteamalsodiscoveredanindirectlypostＧtranscriptionalregulatorymechanismtoregulateexpressionofPSYgeneinbananafruitSulfoxidationofproteinsbyreactiveoxygenspeciescancauseconformationalalterationorfunctionalimpairmentswhichcouldbereversedby Metsulfoxidereductase(Msr)ItwasfoundthatCaM１isasubstrateofMaMsrA７anditssulforxidationisrepairedbyMaMsrA７MaHY５Ｇ１actingasatranscriptionalrepressorofMaPSY１MaPSY２andMaPSY３inbananafruitisa CaMＧbindingproteinSulfoxidationregulationof MaCaM１ by MaMsrA７altersexpressionofMaPSY１MaPSY２andMaPSY３genesbymodifyingMaHY５Ｇ１transcriptionalactivity(nopublisheddata)

TwootherproteinsalsohavebeenreportedtoberelatedtoposttranscriptionalregulationofcarotenoidbiosynthesisSlSGR１atomatoSTAYＧGREENproteinregulateslycopeneaccumulationduringtomatofruitripeningviadirectinteractionwithPSY１[５９]AnotherexampleisthepostＧtranslationalregulationofDXSJＧproteinJ２０ (chaperoneproteindnaJ２０)interactsdirectlywithDXSregulatingDXSproteinlevelandactivitybyidentifyingunfoldedormisfolded(damaged)formsofDXSandtargetingthemtotheHsp７０systemforproperfoldingundernormalconditionsordegradationuponstress[７１]

６　Hormonalregulationofcarotenoidbiosynthesis

　Fruitripeningisacomplexandgeneticallyprogrammedprocesswhichinvolvesaseriesoforganolepticphysiologicaland biochemical changesresulting in the development of edible quality [７２]

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６２　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

PhytohormonesplaycrucialrolesinfruitripeningwhichhasbeenshowntoaffectcarotenoidaccumulationinfruitsMajorprogressregardingtheinvolvementofphytohormonesinregulatingcarotenoidbiosynthesishasbeenachievedinfruits

Ethyleneplaysa centralrolein climactericfruitripeningTherole ofethylenein carotenoidaccumulationinclimactericfruitshasbeenwidelystudiedIntomatoethyleneinitiatesfruitripeningresultinginarapidcolorshiftfromgreentoredwithincreasedlycopeneaccumulationanddecreasedβＧxanthophyllsandchlorophyllscontentsTheroleofethyleneinregulatingcarotenoidbiosynthesisduringtomatofruitripeninginvolvesacomplexregulatorynetworkoftranscriptionfactorsRINasamasterregulatorbindstothepromotersofgenesinvolvedinfruitripeningprocessesincludingcarotenoidbiosynthesis[４８４９７３]APETALA２a(AP２a)isamemberofAP２ERFsuperfamilywhichregulatestomatofruitripeningbyregulatingethylenebiosynthesisandsignalingRepressionofAP２abyRNAinterference (RNAi)resultsin decreasedlevels ofphytoeneandlycopenebut higherβＧcaroteneaccumulationconsistentwithdownＧregulatedexpressionofPDSCtRＧb２andCtrlSOandupＧregulatedexpressionofZEP１MoreoverseveralripeningＧrelatedregulatorsRIPENINGＧINHIBITOR (RIN)NONＧRIPENING (NOR)andCOLORLESSNONＧRIPENING (CNR)functionupstreamofAP２aandpositivelyregulateitsexpression[７４]SlERF６anothermemberofAP２ERFsuperfamilyisanegativeregulatorofcarotenoidaccumulationReducedexpressionofSlERF６byRNAienhancedbothcarotenoidandethylenelevelsduringfruitripening[７５]InadditionthreeothertranscriptionfactorsarerelatedtotheethylenepathwayincludingTAGL１FRUITFULL１and２whichhavebeenreportedtopositivelyregulatecarotenoidaccumulationduringtomatoripening[７６mdash７８]

Auxinisinvolvedincellexpansionanddivisiontissuedifferentiationorgandevelopmentandarangeofphysiologicalprocess[７９]Recentlyincreasingevidencesshowthatauxinalsoplaysanimportantroleinregulatingfruitripening[８０]TheleveloffreeIAA (themostabundantauxin)tendstodeclinepriortotheonsetoftomatofruitripening[８１]AuxinnegativelycontrolscarotenoidaccumulationintomatofruitExogenousIAA treatmentsignificantlyreduceslycopeneaccumulationbutenhancesthelevelsofneoxanthinandviolaxanthinaccompaniedbydownＧregulatedexpressionofPsy１Psy３PdsZisoandCrtisoandupＧregulatedexpressionofβＧLcy１andCrtrＧβ１ [８２]Howeverwhetherauxindirectlyregulatesthegenesincarotenoidpathwayremainsunknown

Abscisicacid (ABA)isa key hormoneinvolvedintuningresponsestoabioticstressesLittleinformationisavailableabouttheinvolvementofABAinregulatingcarotenoidaccumulationduringtomatofruitripeningABA hasbeenreportedto beimplicatedinfruitripeningandinfluencecarotenoidaccumulationintomato[８３]andstrawberry[８４]fruit

JAssuchasmethyljasmonicacidjasmonicacidandotherderivativesareplantendogenoushormones[８５]JAsalsoplayimportantrolesinfruitripeningLietalreportedthatJAinduceethyleneproductionbyMdMYC２ＧmediatedandMdERF３ＧmediatedupregulationofMdACS１gene[８６]Applicationofmethyljasmonate(MeJA)increasestheaccumulationofanthocyaninβＧcarotenecontentsandseveralphenoliccompounds[８７]LiuetalfurtherilluminatedtheroleofJAinregulatingcarotenoidaccumulationduringtomatofruitripeningwithJAＧdeficientmutants(spr２anddef１)anda３５∷prosystransgenicline(３５∷prosyswithincreasedJAlevelsandconstitutiveJAsignaling)andfoundthatlycopeneaccumulationissignificantlyinhibitedinspr２anddef１fruitbutenhancedin３５S∷prosysfruitaccompaniedbyasimilartrendofexpressionoflycopenebiosyntheticgenes[８８]Inadditionethyleneproductionisdepressedinspr２anddef１fruitbutincreasedin３５S∷prosysfruitMoreovertheexogenousapplicationofMeJAtoNeverripe (Nr)an ethyleneＧinsensitive mutantresultsin enhancedlycopene accumulation andexpressionoflycopenebiosyntheticgenes [８８]TheseresultsindicatedthatJA promoteslycopenebiosynthesisinamannerindependentofethylene

７　Futureresearchdirections

　CarotenoidmetabolismandregulationhavebeenwidelyresearchedinplantsHoweverthecarotenoidＧ

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relatedstudieshavebeenmostlyfocusedonmodelspeciessuchasArabidopsisandtomatoThemolecularmechanismsunderlyingcarotenoid metabolism andregulationin otherfruitspeciesarestillpoorlyunderstoodConsideringthediversityofcarotenoidsinfruitsitisnecessarytoinvestigatethenovelgenesandregulationmechanismsrelatedtocarotenoidbiosynthesisinplants

Carotenoid accumulation is cooperatively controlled at multiple levelsincluding developmentalprogramsenvironmentalfactorsand metabolicsignalsTranscriptionfactorsplayimportantroleinregulatingcarotenoidbiosynthesisHoweveronlyafewtranscriptionfactorsinvolvedincarotenoidbiosynthesisareidentifiedandtranscriptionregulationismainlyrelatedtoexpressionofPSYMoreovermostofthesetranscriptionfactorsexerttheirinfluencesviaregulatingfruitripeningnotspecificcarotenoidbiosynthesisＧrelated genesTheinteracting partners oftranscriptionfactorsinvolvedincarotenoidmetabolicnetworkalsoremaintobeidentifiedPostＧtranscriptionalregulationalternativeRNAsplicingepigeneticmodificationandmiRNAareofimportanceinplantgrowthanddevelopmentandresponsetoabioticstressHoweverlittleinformationregardingtheinvolvementofthesemechanismsinregulating carotenoid metabolism in planteven in Arabidopsisis available Application ofphytohormonescontributestoregulatecarotenoidcontentand maintainfruitqualityinagricultureandpostharvesttreatmentThemechanismunderlyingregulationofcarotenoidmetabolismbyphytohormonesespeciallycrossＧtalkamongdifferentphytohormonesarestillfarfrombeingunderstoodInthefuturestudiesbetterunderstandingofcarotenoid metabolismandregulationinfruitswillnotonlyhaveanimportantimpactongeneticimprovementandpostharvesttreatmentbutalsowillstrengthenknowledgeofcarotenoidregulationinplants

Acknowledgements

ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(GrantNos３１７７２０４１３１３２２０４４and３１５０１５４５)ScienceandTechnologyPlanningProjectofGuangdongProvince(GrantNo２０１５B０９０９０１０５８)ScienceandTechnologyPlanningProjectofGuangzhou (GrantNo２０１６０４０２００４８)andTalentProgramofGuangdongProvince(No２０１４TX０１N０４９)

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[６８]KimSHAhnYOAhnMJetalCloningandcharacterizationofanOrangegenethatincreasescarotenoidaccumulationandsaltstresstoleranceintransgenicsweetpotatoculturesPlantPhysiologyandBiochemistry２０１３７０４４５mdash４５４

[６９]ZhouXWelschRYang YetalArabidopsisORproteinsarethemajorposttranscriptionalregulatorsofphytoenesynthaseincontrollingcarotenoidbiosynthesisProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１５１１２３５５８mdash

３５６３[７０]WelschRZhouXYuanHetalClpproteaseandORdirectlycontroltheproteostasisofphytoenesynthasethecrucialenzymefor

carotenoidbiosynthesisinArabidopsisMolecularPlant２０１８１１１４９mdash１６２

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６６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[７１]PulidoPToledoＧOrtizGPhillipsMAetalArabidopsisJＧProteinJ２０deliversthefirstenzymeoftheplastidialisoprenoidpathwaytoproteinqualitycontrolPlantCell２０１３２５４１８３mdash４１９４

[７２]PrasannaVPrabhaTNTharanathanRNFruitripeningphenomenamdashAnoverviewCriticalReviewsinFoodScienceandNutrition

２００７４７１mdash１９[７３]FujisawaMShimaYHiguchiNetalDirecttargetsofthetomatoＧripeningregulatorRINidentifiedbytranscriptomeandchromatin

immunoprecipitationanalysesPlanta２０１２２３５１１０７mdash１１２２[７４]KarlovaRRosinFMBusscherＧLangeJetalTranscriptomeandmetaboliteprofilingshowthatAPETALA２aisamajorregulatorof

tomatofruitripeningPlantCell２０１１２３９２３mdash９４１[７５]LeeJMJoungJGMcQuinnRetalCombinedtranscriptomegeneticdiversityandmetaboliteprofilingintomatofruitrevealsthatthe

ethyleneresponsefactorSlERF６playsanimportantroleinripeningandcarotenoidaccumulationPlantJournal２０１２７０１９１mdash２０４[７６]ShimaYFujisawaMKitagawaMetalTomatoFRUITFULLhomologsregulatefruitripeningviaethylenebiosynthesisBioscience

BiotechnologyandBiochemistry２０１４７８２３１mdash２３７[７７]VrebalovJPanILArroyoAJMetalFleshyfruitexpansionandripeningareregulatedbythetomatoSHATTERPROOFgene

TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ５７　　　

　CitrusisoneofthemosteconomicallyimportantediblefruitsworldwidewiththemostdiversecarotenoidcompositionMostcultivatedcitrusesarenaturalorartificialhybridsoffourcoreancestralspeciescitronpummelomandarine and papeda The commercially important cultivated citrusinclude orangegrapefruitmandarinandlemonCarotenoidaccumulationvariesgreatlyin differentcitrusspeciesMandarinand orangeaccumulate primarily βＧcryptoxanthin and violaxanthinwhile grapefruitandpummeloarerichinphytoenephytoflueneandlycopene[１７１８２７２８]Inadditionlemonandlimecontainlowlevelsofcarotenoids[１８]

TomatohasbeenwidelyusedasamodelfruittoresearchcarotenoidmetabolismTomatofruitdisplaysdiversecolorvariationwhichisattributedbythedifferentialcarotenoidaccumulationRedtomatomainlycontainslycopeneaccountingforupto９０ofthetotalcarotenoids[２４]SomemutanttomatofruitswithdiversecolorsarecharacterizedbyabnormalcarotenoidbiosynthesisForexampleorangetmutant[２９]orangeredDeltamutant[３０]andorangeBeltamutantfruit[３１]accumulateprimarilyproＧlycopeneδＧcaroteneandβＧcarotenerespectively

PapayaisanimportantcommercialfruitcultivatedintropicalandsubtropicalareasandisrichincarotenoidThecompositionsofcarotenoidinpapayadeterminethefruitcolorYellowＧfleshedpapayavarietyaccumulatesmainlyβＧcryptoxanthinandβＧcarotenewhileredＧfleshedcultivarmainlylycopene[２３]

SimilartopapayadifferentcarotenoidcompositionsgivepepperfruitdiversecolorsRedpeppercontainsthehighestcarotenoidcontentamongallthecommonediblefruitswiththecontentofupto１１００μgg－１fwThepredominantcarotenoidsinredpepperarecapsanthin[３２]YellowpepperarerichinluteinandαＧorβＧcarotenewhileorangepeppercontainsprimarilycapsanthinluteinandorβＧcarotene[３３３４]

Watermelonisoneofthe mostpopularfruitsinthe worldFleshcoloristheimportanttraitofwatermelonCarotenoidsareresponsiblefordiversecolorsin watermelonfruit [２５]RedＧfleshedwatermelonsconsistedprimarilyoflycopenewithasmallamountofphytoenephytoflueneζＧcaroteneαＧcaroteneluteinzeaxanthinandviolaxanthin[２５]whileviolaxanthinandluteinconstitutethemajorcarotenoidsinorangeＧfleshedwatermelon[２５２６]

３　Biosynthesisofcarotenoids

　Inhigherplantscarotenoidsaresynthesizedinvarioustypesofplastidsincludingproplastidsetioplastschloroplastsamyloplastsandchromoplasts[３５]ThecarontenoidbiosynthesispathwayhasbeenwellestablishedwhichinvolvesthreeimportantprocessesbiosynthesisofprecursorformationoflinearchaincarotenoidsandcyclizationoflycopeneThegenesandenzymesinvolvedintheseprocessesforplantsareillustratedinFigure１Alargenumberofgenesfromfruitsinrelationtocarotenoidbiosynthesisandregulationalsohavebeenclonedandcharacterized

Thebiosynthesisofcarotenoidsdependsonthesupplyoftwobasicbuildingblocksofcarotenoidsisopentenyldiphosphate(IPP)anddimethylallyldiphosphate(DMAPP)[６]whichareproducedvia２CＧmethylＧDＧerythritolＧ４Ｇphosphate(MEP)pathwaySevenenzymesareinvolvedinMEPpathwayincluding１ＧdeoxyxyluloseＧ５Ｇphosphatesynthase(DXS)１ＧdexoyＧDＧxylulose５Ｇphosphatereductoisomerase(DXR)MEPcytidylyltransferase(MCT)４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritol(CDPＧME)kinase(CMK)２ＧCＧmethylＧDＧerythritol２４Ｇcyclodiphosphate (MECDP)synthase (MDS)(e)Ｇ４ＧhydroxyＧ３ＧmethylbutＧ２ＧenＧ１Ｇyldiphosphate(HMBPP)synthase(HDS)and HMBPPsynthasereductase (HDR)[３６]ThefirststepinMEPpathwayisregulatedbyDXSarateＧlimitingenzymeincarotenogensisTheoverexpressionofDXSenhancescarotenoidaccumulationin ArabidopsiswhilethemutationofDXSresultsinnocarotenoidaccumulation[３７]AnotherkeyregulatorystepisHDRthelastenzymeinMEPpathwaywhichcatalyzestheproductionofIPP[３８]IPPisisomerizedtoDMAPPviaIPPisomeraseIPPandDMAPPundergocondensationreactionsgeneratingthemajorcarotenoidprecursorgeranylgeranyldiphosphate (GGPP)Thereactionsarecatalyzed byisopentenyldiphosphateisomerase (IPI)and

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５８　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

Figure１　BiosynthesisandregulationofcarotenoidsinplantsThegreyrectanglesrepresentthesubstratesandmetabolitesinthecarotenoid biosynthesispathwayTheblueellipsesrepresenttheenzymesandtheirgenesinvolvedincarotenoidbiosynthesisThegreenellipsesrepresenttranscriptionfactorsregulatingcarotenoidbiosynthesisTheredellipsesrepresentproteinsinvolvedintheposttranscriptionalregulationofcarotenoidbiosynthesisTheyellowellipsesrepresenttheproteinsinvolvedinepigeneticmodificationofcarotenoidbiosynthesisThepurpleellipsesrepresentmiRNAinvolvedintheregulationofcarotenoidbiosynthesisBCHnonＧhemeβＧcarotenehydroxylaseCDPＧME４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritolCDPＧME２P２ＧphosphoＧ４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritolCMKCDPＧMEkinaseCRTISOcarotenoidisomerase CYP９７A and CYP９７Ccytochrome P４５０Ｇtype monooxygenase ９７C DMAPPdimethylallyldiphosphateDXPdeoxyＧDＧxylulose５ＧphosphateDXR１ＧdexoyＧDＧxylulose５ＧphosphatereductoisomeraseDXS１ＧdeoxyxyluloseＧ５ＧphosphatesynthaseG３Pglyceraldehyde３ＧphosphateGGPPgeranylgeranyldiphosphateGGPPSGGPPsynthaseHDRHMBPPreductaseHDSHMBPPsynthaseHMBPP(e)Ｇ４ＧhydroxyＧ３ＧmethylbutＧ２ＧenＧ１ＧyldiphosphateIPIisopentenyldiphosphateisomeraseIPPisopentenyldiphosphateLCYBlycopeneβＧcyclaseLCYElycopeneεＧcyclaseMCTMEPcytidylyltransferaseMDSMECDPsynthaseMECDP２CＧmethylＧDＧerythritol２４ＧcyclodiphosphateMEP２CＧmethylＧDＧerythritolＧ４Ｇphosphate NSY Neoxanthin synthasePDSphytoene desaturasePSYphytoenesynthaseVDEviolaxanthindeＧepoxidaseZDSζＧcarotenedesaturaseZEPzeaxanthinepoxidaseZＧISOζＧcaroteneisomerase

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ５９　　　

geranylgeranyldiphosphate(GGPP)synthase(GGPPS)[３９]ThecondensationoftwoGGPPmoleculescatalyzedbyphytoenesynthase(PSY)formsuncolored１５Ｇcis

phytoenethefirstcarotenoidproductThisstepisregardedasthemostimportantregulatorystepincarotenoidbiosynthesis[３９]TomatocontainsthreePSYgenesPSY１PSY２andPSY３whichexhibittissueＧspecificexpressionmainlyinfruitinpetalandinrootrespectivelyDuringtomatoripeningtheaccumulationofcarotenoidcorrelateswiththeexpressionofPSY１ [４０４１]TransgenictomatobyantisenseinhibitionofPSY１producesonly３ofthecarotenoidinwildtypewildtypefruit[４２]SimilarresultsregardingtherelationshipbetweenupregulatedexpressionofPSYgenesandincreasedcarotenoidaccumulationhavebeenreportedinalargenumberoffruitssuchascitrus[４３]pepper[３４]persimmon[４４]loquat[１２]watermelon [２５]andbanana[４５]Uncoloredphytoenethenundergoesaseriesofdesaturationandisomerizationreactionsto generateredＧcolored allＧtransＧlycopenethe predominatepigmentinredtomatoand watermelonfruitsThesereactionsaresequentiallycatalyzedbyphytoenedesaturase(PDS)ζＧcarotenedesaturase(ZDS)ζＧcaroteneisomerase(ZＧISO)andcarotenoidisomerase(CRTISO)[３９]

Downstreaminthecarotenoidbiosynthesispathwaythecyclizationoflycopeneislocatedatthebranchingpointofthepathwaywhichproduceaseriesofcarotene(Figure１)[６７３９]ThecyclizationoflycopeneinvolvestwoenzymeslycopeneβＧcyclase(LCYB)andlycopeneεＧcyclase(LCYE)LCYBcatalyzesatwoＧstepreactiontoproduceβＧcarotenewithtwoβＧringsAεＧringandaβＧringaresequentiallyaddedtolycopeneformingαＧcarotene(βεＧcarotene)whichiscatalyzedbyLCYEandLCYBFollowingthecyclizationoflycopeneαＧcaroteneandβＧcarotenearesubjectedtohydroxylationandepoxidationformingaseriesofxanthophylls[６７３９]TheαＧcaroteneissequentiallycatalyzedbytwohydroxylasesCYP９７A and CYP９７CgeneratingluteinthefinalproductofαＧbranchincarotenoid biosynthesispathwayβＧcaroteneundergoestwostepsofhydroxylationandtwostepsofepoxidationcatalyzedbyβＧcarotenehydroxylase (BCH)andzeaxanthinepoxidase (ZEP)sequentiallyformingβＧcryptoxanthinzeaxanthinantheraxanthinandviolaxanthin[６７３９]Theconversionofviolaxanthinintoneoxanthinbyneoxanthinsynthase(NXS)completesthecorebiosynthesispathway[４６]

４　Transcriptionalregulationofcarotenoidbiosynthesis

４１　TranscriptionfactorTranscriptionalregulationplaysavitalroleinfruitdevelopmentandripeningaswellasabioticstresses

ItiswellknownthattranscriptionfactorsareinvolvedintranscriptionregulationofstructureandfunctiongenesincarotenoidbiosynthesispathwayAlthoughthegenesinvolvedinthebiosynthesisofcarotenoidbiosynthesishavebeenidentifiedandcharacterizedfromvariousfruits(Figure１)onlyafewtranscriptionfactorshavebeendemonstratedtodirectlyregulatetheexpressionofthesefunctiongenesinthepathwayThetranscriptionalcontrolofcarotenoidaccumulationhasbeenmostlystudiedintomatoduringripeningThesetranscriptionfactorsinclude RINR２R３ＧMYBNACSGR１PIF１RAP２２EIN３etcHowevermostofthesetranscriptionfactorsexertbroadeffectsonfruitripeningieethylenesynthesisfruitsofteningcolorformationaromaandflavorproductionandareunlikelytobespecificregulatorsofcarotenoidbiosynthesis

RIPENINGＧINHIBITOR (RIN)isa memberoftranscriptionfactorfamilycontaining MADSＧboxwhichplaysanessentialroleinfruitripeningasaglobalmasterregulator[４７]MarteletalreportedthatRINinteractswithSlPSY１thespecificPSYgeneassociatedwithcarotenoidbiosynthesisintomato[４８]FujisawaetalidentifiedanumberofRINＧtargetedgenesincarotenoidbiosynthesispathwaybychromatinimmunoprecipitationcoupled with DNA microarrayanalysisandfoundthatRIN regulatescarotenoidaccumulationviapositivelyregulatingPSY１ZISOandCRTISOinadirectmanneraswellaspositivelycontrollingZDSandnegativelyregulatingLYCBandLYCEbyanindirecteffectintomatofruit[４９]

VＧmybmyeloblastosisviraloncogenehomolog(MYB)proteinsbelongtoalargefamilyoftranscriptionfactorsinplantsThemajorityofMYBareR２R３ＧMYBsubfamilywithtworepeatsinitsMYBdomain

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６０　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

TheR２R３ＧMYBTFsplaykeyrolesinregulatingplantＧspecificprocessesincludingprimaryandsecondarymetabolismgrowthanddevelopmentandresponsetoabioticandbioticstresses [５０]IncitrusCrMYB６８an R２R３ＧMYBtranscriptionalfactorcandirectlybindandnegativelyregulateCrBCH２resultinginthedelayinthetransformationofαＧandβＧcaroteneandtheinhibitionofpeeldeＧgreeningincitrus[５１]SimilarlySagawaetalidentifiedanR２R３ＧMYBtranscriptionfactorReducedCarotenoidPigmentation１(RCP１)whichpositivelyregulatescarotenoidbiosynthesisduringMimuluslewisiiflowerdevelopmentLossＧofＧfunctionmutationsinRCP１resultindownＧregulationofallcarotenoidbiosyntheticgenesandreducecarotenoidcontentwhileoverexpressionofthisgeneinthercp１ mutantbackgroundrestorescarotenoidproduction[５２]Thereforeinadditiontoregulatinganthocyanins[５３]R２R３ＧMYBisalsoinvolvedintheregulationofcarotenoidbiosynthesisinfruits

NAMATAF１２andCUC２ (NAC)transcriptionfactorsareoneofthelargestfamiliesofplantＧspecifictranscription factors which areimplicated in plant growth and developmentflavonoidbiosynthesiswoodformationandstressresponses [５４]TheroleofNACtranscriptionfactorsinregulatingfruitripeningandsenescencehasbeenreportedintomato[５５]banana[５６]andlitchi[５４]IntomatoSlNAC１and SlNAC４ positivelyregulatetomatofruitripeningbutexhibitdifferentialcharacteristicsAntisensesuppression ofSlNAC１ resultsin delayed ethylene production andfruitripeningbuthigherlevelsofethylenebiosynthesisandaccumulationoftotalcarotenoidandlycopeneaccompaniedbyupＧregulatedexpressionofgenesrelatedtolycopeneandethylenebiosynthesis [５５]DifferentfromSlNAC１reducedexpressionofSlNAC４byRNAinterference(RNAi)intomatodelayedfruitripeningdecreasedethylenesynthesisandreducedcarotenoidsbyalteringcarotenoidpathwayflux[５７]AdditionallyFuetalreportedthatpapayaCpNAC２actsasatranscriptionalactivatorofCpPDS２４CpZDSCpLCYＧeandCpCHYＧb by directly bindingtotheirpromotersand promotestheirtranscription[５８]

SomeothertranscriptionfactorshavealsobeenreportedtobeinvolvedinthetranscriptionalregulationofstructuregenesinthecarotenoidbiosynthesispathwayIntomatoSlSGR１aSTAYＧGREENproteinphysicallyinteracts with PSY１ to suppress PSY１ expressionthus negatively regulatinglycopeneproductionduringfruitripening[５９]PhytochromeＧinteractingfactor１downＧregulatetheaccumulationofcarotenoidbybindingtothepromoterofPSYandrepressingPSYexpressioninArabidopsisseedlings[６０]SimilarlyAtPAP２２amemberoftheAPETALA２ (AP２)ethyleneＧresponsiveelementＧbindingproteintranscriptionfactorfamilydirectlybinds withthepromotersofPSY andPDS toregulatecarotenoidbiosynthesisinArabidopsis [６１]PapayaCpEIN３aanethyleneresponsivefactordirectlybindswiththepromotersofCpPDS４andCpCHYＧbandpromotestheirtranscription[５８]InadditionoverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor(CrbHLH１)intomatolowerslycopeneaccumulationanddownＧregulatecarotenoidbiosyntheticgeneexpressionintomatofruit[６２]EctopicexpressionofanArabidopsisBZR１Ｇ１Dtranscriptionfactorinbrassinosteroidsignalingenhancescarotenoidaccumulationandfruitqualityattributesintomato[６３]４２　Epigeneticmodification

EpigeneticmodificationincludingthemethylationofDNACpGislandsandthemodificationofhistonesthatassociatedwithDNAinchromosomesplayaveryimportantroleinregulatinggeneexpressionEpigeneticmodification possiblyisimplicatedinregulation ofcarotenoid biosynthesis (Figure１)Cazzonellietalreportedahistonemethyltransferaseenzyme(SET DOMAIN GROUP８SDG８)thatmethylateshistoneH３onLys４andor３６(H３K４andH３K３６)inArabidopsisthalianawhichisrequiredforexpressionofCRTISOgeneMutationofSDG８resultsindownＧregulatedexpressionofCRTISOgeneimpairedlutein biosynthesis andincreased shoot branchingThis wasthefirstreportregardinginvolvementofepigeneticmodificationinregulationofcarotenoidbiosynthesis[６４]４３　AlternativeRNAsplicing

AlternativeRNAsplicingisanimportantregulationofgeneexpressioninhighereukaryotesRecentlyAlvarezetalfoundthatalternativesplicingofPSYisimplicatedinregulationofcarotenogenesisinArabidopsisArabidopsispredominantlypossessasinglePSYgenewithtwoalternativesplicevariants

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６１　　　

(ASV)inlength andintheexonintronretention oftheir５1049011UTRsASV１ with along ５1049011UTR(untranslatedregion)isinvolvedindevelopmentallyregulatedcarotenoidformationwhileASV２withashort５1049011UTRispreferentiallyinduced whenanimmediateincreaseinthecarotenoidpathwayfluxisrequired[６５]４４　microRNAs

MicroRNAs(miRNAs)arekeyregulatorsofgeneexpressionineukaryotesandplayapivotalroleintheregulationofvariousbiologicalaswellas metabolicprocessesInterestinglyanartificialmaturemicroRNAs (amiRNAs)successfullytargetedthe PSY mRNA andreduced PSY mRNA levelinPhaeodactylumtricornutumwhichfurtherreducedthelevelsofcarotenoidsinthePtricornutumamiRNAknockdownlines[６６]ItwasspeculatedthatmiRNApossiblyisinvolvedinthetranscriptionregulationofcarotenoidbiosynthesisinplants

５　PostＧtranscriptionalregulationofcarotenoidsbiosynthesis

　InadditiontotranscriptionregulationofstructuregenesinvolvedinthecarotenoidpathwayrecentstudieshaverevealedotherregulatorymechanismstocontrolbiosyntheticenzymelevelsandactivitiesinplantssuchaspostＧtranscriptionalregulation (Figure１)Theseregulatory mechanismspossiblyarepresentduringfruitdevelopmentandripening

ORANGE(OR)isaplastidＧlocalizedproteincarryingacysteineＧrichzincfingerdomainPreviousstudiedshowedthatORpromotescarotenoidaccumulationincalliofrice[６７]andsweetpotato [６８]FurtherZhouetalfoundthatArabidopsisORandPSYphysicallyinteractwitheachotherinplastidsresultingin minimaleffecton expression ofPSY gene [６９]Howeveroverexpression of AtORsignificantlyincreasedtheamountofenzymaticallyactivePSYwhereasanatoratorＧlikedoublemutantexhibitsadramaticallyreducedPSYlevelTheresultrevealedanovelmechanismunderlyingregulationofcarotenoidbiosynthesisviaposttranscriptionalmodificationofPSYinplants[６９]

Inanotherimportantliterature on postＧtranscriptionalregulation Welsch et alreported thatdegradationmodificationofproteinincarotenoidbiosynthesispathwayisimplicatedinregulationofcarotenoidbiosynthesisClpproteasesystemthemostabundantandcomplexsolubleproteasesystemintheplastidwasshowntotargetPSYTheabsenceofCLPC１CLPP４andCLPR１Ｇ２enhancedthelevelsofactivePSYandseveralothercarotenogenicenzymes[７０]ThereforeORproteincounterbalancesClpＧmediatedproteolysisinmaintainingPSYproteinhomeostasis

Theauthors1049011researchteamalsodiscoveredanindirectlypostＧtranscriptionalregulatorymechanismtoregulateexpressionofPSYgeneinbananafruitSulfoxidationofproteinsbyreactiveoxygenspeciescancauseconformationalalterationorfunctionalimpairmentswhichcouldbereversedby Metsulfoxidereductase(Msr)ItwasfoundthatCaM１isasubstrateofMaMsrA７anditssulforxidationisrepairedbyMaMsrA７MaHY５Ｇ１actingasatranscriptionalrepressorofMaPSY１MaPSY２andMaPSY３inbananafruitisa CaMＧbindingproteinSulfoxidationregulationof MaCaM１ by MaMsrA７altersexpressionofMaPSY１MaPSY２andMaPSY３genesbymodifyingMaHY５Ｇ１transcriptionalactivity(nopublisheddata)

TwootherproteinsalsohavebeenreportedtoberelatedtoposttranscriptionalregulationofcarotenoidbiosynthesisSlSGR１atomatoSTAYＧGREENproteinregulateslycopeneaccumulationduringtomatofruitripeningviadirectinteractionwithPSY１[５９]AnotherexampleisthepostＧtranslationalregulationofDXSJＧproteinJ２０ (chaperoneproteindnaJ２０)interactsdirectlywithDXSregulatingDXSproteinlevelandactivitybyidentifyingunfoldedormisfolded(damaged)formsofDXSandtargetingthemtotheHsp７０systemforproperfoldingundernormalconditionsordegradationuponstress[７１]

６　Hormonalregulationofcarotenoidbiosynthesis

　Fruitripeningisacomplexandgeneticallyprogrammedprocesswhichinvolvesaseriesoforganolepticphysiologicaland biochemical changesresulting in the development of edible quality [７２]

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６２　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

PhytohormonesplaycrucialrolesinfruitripeningwhichhasbeenshowntoaffectcarotenoidaccumulationinfruitsMajorprogressregardingtheinvolvementofphytohormonesinregulatingcarotenoidbiosynthesishasbeenachievedinfruits

Ethyleneplaysa centralrolein climactericfruitripeningTherole ofethylenein carotenoidaccumulationinclimactericfruitshasbeenwidelystudiedIntomatoethyleneinitiatesfruitripeningresultinginarapidcolorshiftfromgreentoredwithincreasedlycopeneaccumulationanddecreasedβＧxanthophyllsandchlorophyllscontentsTheroleofethyleneinregulatingcarotenoidbiosynthesisduringtomatofruitripeninginvolvesacomplexregulatorynetworkoftranscriptionfactorsRINasamasterregulatorbindstothepromotersofgenesinvolvedinfruitripeningprocessesincludingcarotenoidbiosynthesis[４８４９７３]APETALA２a(AP２a)isamemberofAP２ERFsuperfamilywhichregulatestomatofruitripeningbyregulatingethylenebiosynthesisandsignalingRepressionofAP２abyRNAinterference (RNAi)resultsin decreasedlevels ofphytoeneandlycopenebut higherβＧcaroteneaccumulationconsistentwithdownＧregulatedexpressionofPDSCtRＧb２andCtrlSOandupＧregulatedexpressionofZEP１MoreoverseveralripeningＧrelatedregulatorsRIPENINGＧINHIBITOR (RIN)NONＧRIPENING (NOR)andCOLORLESSNONＧRIPENING (CNR)functionupstreamofAP２aandpositivelyregulateitsexpression[７４]SlERF６anothermemberofAP２ERFsuperfamilyisanegativeregulatorofcarotenoidaccumulationReducedexpressionofSlERF６byRNAienhancedbothcarotenoidandethylenelevelsduringfruitripening[７５]InadditionthreeothertranscriptionfactorsarerelatedtotheethylenepathwayincludingTAGL１FRUITFULL１and２whichhavebeenreportedtopositivelyregulatecarotenoidaccumulationduringtomatoripening[７６mdash７８]

Auxinisinvolvedincellexpansionanddivisiontissuedifferentiationorgandevelopmentandarangeofphysiologicalprocess[７９]Recentlyincreasingevidencesshowthatauxinalsoplaysanimportantroleinregulatingfruitripening[８０]TheleveloffreeIAA (themostabundantauxin)tendstodeclinepriortotheonsetoftomatofruitripening[８１]AuxinnegativelycontrolscarotenoidaccumulationintomatofruitExogenousIAA treatmentsignificantlyreduceslycopeneaccumulationbutenhancesthelevelsofneoxanthinandviolaxanthinaccompaniedbydownＧregulatedexpressionofPsy１Psy３PdsZisoandCrtisoandupＧregulatedexpressionofβＧLcy１andCrtrＧβ１ [８２]Howeverwhetherauxindirectlyregulatesthegenesincarotenoidpathwayremainsunknown

Abscisicacid (ABA)isa key hormoneinvolvedintuningresponsestoabioticstressesLittleinformationisavailableabouttheinvolvementofABAinregulatingcarotenoidaccumulationduringtomatofruitripeningABA hasbeenreportedto beimplicatedinfruitripeningandinfluencecarotenoidaccumulationintomato[８３]andstrawberry[８４]fruit

JAssuchasmethyljasmonicacidjasmonicacidandotherderivativesareplantendogenoushormones[８５]JAsalsoplayimportantrolesinfruitripeningLietalreportedthatJAinduceethyleneproductionbyMdMYC２ＧmediatedandMdERF３ＧmediatedupregulationofMdACS１gene[８６]Applicationofmethyljasmonate(MeJA)increasestheaccumulationofanthocyaninβＧcarotenecontentsandseveralphenoliccompounds[８７]LiuetalfurtherilluminatedtheroleofJAinregulatingcarotenoidaccumulationduringtomatofruitripeningwithJAＧdeficientmutants(spr２anddef１)anda３５∷prosystransgenicline(３５∷prosyswithincreasedJAlevelsandconstitutiveJAsignaling)andfoundthatlycopeneaccumulationissignificantlyinhibitedinspr２anddef１fruitbutenhancedin３５S∷prosysfruitaccompaniedbyasimilartrendofexpressionoflycopenebiosyntheticgenes[８８]Inadditionethyleneproductionisdepressedinspr２anddef１fruitbutincreasedin３５S∷prosysfruitMoreovertheexogenousapplicationofMeJAtoNeverripe (Nr)an ethyleneＧinsensitive mutantresultsin enhancedlycopene accumulation andexpressionoflycopenebiosyntheticgenes [８８]TheseresultsindicatedthatJA promoteslycopenebiosynthesisinamannerindependentofethylene

７　Futureresearchdirections

　CarotenoidmetabolismandregulationhavebeenwidelyresearchedinplantsHoweverthecarotenoidＧ

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６３　　　

relatedstudieshavebeenmostlyfocusedonmodelspeciessuchasArabidopsisandtomatoThemolecularmechanismsunderlyingcarotenoid metabolism andregulationin otherfruitspeciesarestillpoorlyunderstoodConsideringthediversityofcarotenoidsinfruitsitisnecessarytoinvestigatethenovelgenesandregulationmechanismsrelatedtocarotenoidbiosynthesisinplants

Carotenoid accumulation is cooperatively controlled at multiple levelsincluding developmentalprogramsenvironmentalfactorsand metabolicsignalsTranscriptionfactorsplayimportantroleinregulatingcarotenoidbiosynthesisHoweveronlyafewtranscriptionfactorsinvolvedincarotenoidbiosynthesisareidentifiedandtranscriptionregulationismainlyrelatedtoexpressionofPSYMoreovermostofthesetranscriptionfactorsexerttheirinfluencesviaregulatingfruitripeningnotspecificcarotenoidbiosynthesisＧrelated genesTheinteracting partners oftranscriptionfactorsinvolvedincarotenoidmetabolicnetworkalsoremaintobeidentifiedPostＧtranscriptionalregulationalternativeRNAsplicingepigeneticmodificationandmiRNAareofimportanceinplantgrowthanddevelopmentandresponsetoabioticstressHoweverlittleinformationregardingtheinvolvementofthesemechanismsinregulating carotenoid metabolism in planteven in Arabidopsisis available Application ofphytohormonescontributestoregulatecarotenoidcontentand maintainfruitqualityinagricultureandpostharvesttreatmentThemechanismunderlyingregulationofcarotenoidmetabolismbyphytohormonesespeciallycrossＧtalkamongdifferentphytohormonesarestillfarfrombeingunderstoodInthefuturestudiesbetterunderstandingofcarotenoid metabolismandregulationinfruitswillnotonlyhaveanimportantimpactongeneticimprovementandpostharvesttreatmentbutalsowillstrengthenknowledgeofcarotenoidregulationinplants

Acknowledgements

ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(GrantNos３１７７２０４１３１３２２０４４and３１５０１５４５)ScienceandTechnologyPlanningProjectofGuangdongProvince(GrantNo２０１５B０９０９０１０５８)ScienceandTechnologyPlanningProjectofGuangzhou (GrantNo２０１６０４０２００４８)andTalentProgramofGuangdongProvince(No２０１４TX０１N０４９)

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TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

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５８　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

Figure１　BiosynthesisandregulationofcarotenoidsinplantsThegreyrectanglesrepresentthesubstratesandmetabolitesinthecarotenoid biosynthesispathwayTheblueellipsesrepresenttheenzymesandtheirgenesinvolvedincarotenoidbiosynthesisThegreenellipsesrepresenttranscriptionfactorsregulatingcarotenoidbiosynthesisTheredellipsesrepresentproteinsinvolvedintheposttranscriptionalregulationofcarotenoidbiosynthesisTheyellowellipsesrepresenttheproteinsinvolvedinepigeneticmodificationofcarotenoidbiosynthesisThepurpleellipsesrepresentmiRNAinvolvedintheregulationofcarotenoidbiosynthesisBCHnonＧhemeβＧcarotenehydroxylaseCDPＧME４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritolCDPＧME２P２ＧphosphoＧ４Ｇ(cytidine５1049011Ｇdiphospho)Ｇ２ＧCＧmethylＧDＧerythritolCMKCDPＧMEkinaseCRTISOcarotenoidisomerase CYP９７A and CYP９７Ccytochrome P４５０Ｇtype monooxygenase ９７C DMAPPdimethylallyldiphosphateDXPdeoxyＧDＧxylulose５ＧphosphateDXR１ＧdexoyＧDＧxylulose５ＧphosphatereductoisomeraseDXS１ＧdeoxyxyluloseＧ５ＧphosphatesynthaseG３Pglyceraldehyde３ＧphosphateGGPPgeranylgeranyldiphosphateGGPPSGGPPsynthaseHDRHMBPPreductaseHDSHMBPPsynthaseHMBPP(e)Ｇ４ＧhydroxyＧ３ＧmethylbutＧ２ＧenＧ１ＧyldiphosphateIPIisopentenyldiphosphateisomeraseIPPisopentenyldiphosphateLCYBlycopeneβＧcyclaseLCYElycopeneεＧcyclaseMCTMEPcytidylyltransferaseMDSMECDPsynthaseMECDP２CＧmethylＧDＧerythritol２４ＧcyclodiphosphateMEP２CＧmethylＧDＧerythritolＧ４Ｇphosphate NSY Neoxanthin synthasePDSphytoene desaturasePSYphytoenesynthaseVDEviolaxanthindeＧepoxidaseZDSζＧcarotenedesaturaseZEPzeaxanthinepoxidaseZＧISOζＧcaroteneisomerase

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ５９　　　

geranylgeranyldiphosphate(GGPP)synthase(GGPPS)[３９]ThecondensationoftwoGGPPmoleculescatalyzedbyphytoenesynthase(PSY)formsuncolored１５Ｇcis

phytoenethefirstcarotenoidproductThisstepisregardedasthemostimportantregulatorystepincarotenoidbiosynthesis[３９]TomatocontainsthreePSYgenesPSY１PSY２andPSY３whichexhibittissueＧspecificexpressionmainlyinfruitinpetalandinrootrespectivelyDuringtomatoripeningtheaccumulationofcarotenoidcorrelateswiththeexpressionofPSY１ [４０４１]TransgenictomatobyantisenseinhibitionofPSY１producesonly３ofthecarotenoidinwildtypewildtypefruit[４２]SimilarresultsregardingtherelationshipbetweenupregulatedexpressionofPSYgenesandincreasedcarotenoidaccumulationhavebeenreportedinalargenumberoffruitssuchascitrus[４３]pepper[３４]persimmon[４４]loquat[１２]watermelon [２５]andbanana[４５]Uncoloredphytoenethenundergoesaseriesofdesaturationandisomerizationreactionsto generateredＧcolored allＧtransＧlycopenethe predominatepigmentinredtomatoand watermelonfruitsThesereactionsaresequentiallycatalyzedbyphytoenedesaturase(PDS)ζＧcarotenedesaturase(ZDS)ζＧcaroteneisomerase(ZＧISO)andcarotenoidisomerase(CRTISO)[３９]

Downstreaminthecarotenoidbiosynthesispathwaythecyclizationoflycopeneislocatedatthebranchingpointofthepathwaywhichproduceaseriesofcarotene(Figure１)[６７３９]ThecyclizationoflycopeneinvolvestwoenzymeslycopeneβＧcyclase(LCYB)andlycopeneεＧcyclase(LCYE)LCYBcatalyzesatwoＧstepreactiontoproduceβＧcarotenewithtwoβＧringsAεＧringandaβＧringaresequentiallyaddedtolycopeneformingαＧcarotene(βεＧcarotene)whichiscatalyzedbyLCYEandLCYBFollowingthecyclizationoflycopeneαＧcaroteneandβＧcarotenearesubjectedtohydroxylationandepoxidationformingaseriesofxanthophylls[６７３９]TheαＧcaroteneissequentiallycatalyzedbytwohydroxylasesCYP９７A and CYP９７CgeneratingluteinthefinalproductofαＧbranchincarotenoid biosynthesispathwayβＧcaroteneundergoestwostepsofhydroxylationandtwostepsofepoxidationcatalyzedbyβＧcarotenehydroxylase (BCH)andzeaxanthinepoxidase (ZEP)sequentiallyformingβＧcryptoxanthinzeaxanthinantheraxanthinandviolaxanthin[６７３９]Theconversionofviolaxanthinintoneoxanthinbyneoxanthinsynthase(NXS)completesthecorebiosynthesispathway[４６]

４　Transcriptionalregulationofcarotenoidbiosynthesis

４１　TranscriptionfactorTranscriptionalregulationplaysavitalroleinfruitdevelopmentandripeningaswellasabioticstresses

ItiswellknownthattranscriptionfactorsareinvolvedintranscriptionregulationofstructureandfunctiongenesincarotenoidbiosynthesispathwayAlthoughthegenesinvolvedinthebiosynthesisofcarotenoidbiosynthesishavebeenidentifiedandcharacterizedfromvariousfruits(Figure１)onlyafewtranscriptionfactorshavebeendemonstratedtodirectlyregulatetheexpressionofthesefunctiongenesinthepathwayThetranscriptionalcontrolofcarotenoidaccumulationhasbeenmostlystudiedintomatoduringripeningThesetranscriptionfactorsinclude RINR２R３ＧMYBNACSGR１PIF１RAP２２EIN３etcHowevermostofthesetranscriptionfactorsexertbroadeffectsonfruitripeningieethylenesynthesisfruitsofteningcolorformationaromaandflavorproductionandareunlikelytobespecificregulatorsofcarotenoidbiosynthesis

RIPENINGＧINHIBITOR (RIN)isa memberoftranscriptionfactorfamilycontaining MADSＧboxwhichplaysanessentialroleinfruitripeningasaglobalmasterregulator[４７]MarteletalreportedthatRINinteractswithSlPSY１thespecificPSYgeneassociatedwithcarotenoidbiosynthesisintomato[４８]FujisawaetalidentifiedanumberofRINＧtargetedgenesincarotenoidbiosynthesispathwaybychromatinimmunoprecipitationcoupled with DNA microarrayanalysisandfoundthatRIN regulatescarotenoidaccumulationviapositivelyregulatingPSY１ZISOandCRTISOinadirectmanneraswellaspositivelycontrollingZDSandnegativelyregulatingLYCBandLYCEbyanindirecteffectintomatofruit[４９]

VＧmybmyeloblastosisviraloncogenehomolog(MYB)proteinsbelongtoalargefamilyoftranscriptionfactorsinplantsThemajorityofMYBareR２R３ＧMYBsubfamilywithtworepeatsinitsMYBdomain

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TheR２R３ＧMYBTFsplaykeyrolesinregulatingplantＧspecificprocessesincludingprimaryandsecondarymetabolismgrowthanddevelopmentandresponsetoabioticandbioticstresses [５０]IncitrusCrMYB６８an R２R３ＧMYBtranscriptionalfactorcandirectlybindandnegativelyregulateCrBCH２resultinginthedelayinthetransformationofαＧandβＧcaroteneandtheinhibitionofpeeldeＧgreeningincitrus[５１]SimilarlySagawaetalidentifiedanR２R３ＧMYBtranscriptionfactorReducedCarotenoidPigmentation１(RCP１)whichpositivelyregulatescarotenoidbiosynthesisduringMimuluslewisiiflowerdevelopmentLossＧofＧfunctionmutationsinRCP１resultindownＧregulationofallcarotenoidbiosyntheticgenesandreducecarotenoidcontentwhileoverexpressionofthisgeneinthercp１ mutantbackgroundrestorescarotenoidproduction[５２]Thereforeinadditiontoregulatinganthocyanins[５３]R２R３ＧMYBisalsoinvolvedintheregulationofcarotenoidbiosynthesisinfruits

NAMATAF１２andCUC２ (NAC)transcriptionfactorsareoneofthelargestfamiliesofplantＧspecifictranscription factors which areimplicated in plant growth and developmentflavonoidbiosynthesiswoodformationandstressresponses [５４]TheroleofNACtranscriptionfactorsinregulatingfruitripeningandsenescencehasbeenreportedintomato[５５]banana[５６]andlitchi[５４]IntomatoSlNAC１and SlNAC４ positivelyregulatetomatofruitripeningbutexhibitdifferentialcharacteristicsAntisensesuppression ofSlNAC１ resultsin delayed ethylene production andfruitripeningbuthigherlevelsofethylenebiosynthesisandaccumulationoftotalcarotenoidandlycopeneaccompaniedbyupＧregulatedexpressionofgenesrelatedtolycopeneandethylenebiosynthesis [５５]DifferentfromSlNAC１reducedexpressionofSlNAC４byRNAinterference(RNAi)intomatodelayedfruitripeningdecreasedethylenesynthesisandreducedcarotenoidsbyalteringcarotenoidpathwayflux[５７]AdditionallyFuetalreportedthatpapayaCpNAC２actsasatranscriptionalactivatorofCpPDS２４CpZDSCpLCYＧeandCpCHYＧb by directly bindingtotheirpromotersand promotestheirtranscription[５８]

SomeothertranscriptionfactorshavealsobeenreportedtobeinvolvedinthetranscriptionalregulationofstructuregenesinthecarotenoidbiosynthesispathwayIntomatoSlSGR１aSTAYＧGREENproteinphysicallyinteracts with PSY１ to suppress PSY１ expressionthus negatively regulatinglycopeneproductionduringfruitripening[５９]PhytochromeＧinteractingfactor１downＧregulatetheaccumulationofcarotenoidbybindingtothepromoterofPSYandrepressingPSYexpressioninArabidopsisseedlings[６０]SimilarlyAtPAP２２amemberoftheAPETALA２ (AP２)ethyleneＧresponsiveelementＧbindingproteintranscriptionfactorfamilydirectlybinds withthepromotersofPSY andPDS toregulatecarotenoidbiosynthesisinArabidopsis [６１]PapayaCpEIN３aanethyleneresponsivefactordirectlybindswiththepromotersofCpPDS４andCpCHYＧbandpromotestheirtranscription[５８]InadditionoverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor(CrbHLH１)intomatolowerslycopeneaccumulationanddownＧregulatecarotenoidbiosyntheticgeneexpressionintomatofruit[６２]EctopicexpressionofanArabidopsisBZR１Ｇ１Dtranscriptionfactorinbrassinosteroidsignalingenhancescarotenoidaccumulationandfruitqualityattributesintomato[６３]４２　Epigeneticmodification

EpigeneticmodificationincludingthemethylationofDNACpGislandsandthemodificationofhistonesthatassociatedwithDNAinchromosomesplayaveryimportantroleinregulatinggeneexpressionEpigeneticmodification possiblyisimplicatedinregulation ofcarotenoid biosynthesis (Figure１)Cazzonellietalreportedahistonemethyltransferaseenzyme(SET DOMAIN GROUP８SDG８)thatmethylateshistoneH３onLys４andor３６(H３K４andH３K３６)inArabidopsisthalianawhichisrequiredforexpressionofCRTISOgeneMutationofSDG８resultsindownＧregulatedexpressionofCRTISOgeneimpairedlutein biosynthesis andincreased shoot branchingThis wasthefirstreportregardinginvolvementofepigeneticmodificationinregulationofcarotenoidbiosynthesis[６４]４３　AlternativeRNAsplicing

AlternativeRNAsplicingisanimportantregulationofgeneexpressioninhighereukaryotesRecentlyAlvarezetalfoundthatalternativesplicingofPSYisimplicatedinregulationofcarotenogenesisinArabidopsisArabidopsispredominantlypossessasinglePSYgenewithtwoalternativesplicevariants

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６１　　　

(ASV)inlength andintheexonintronretention oftheir５1049011UTRsASV１ with along ５1049011UTR(untranslatedregion)isinvolvedindevelopmentallyregulatedcarotenoidformationwhileASV２withashort５1049011UTRispreferentiallyinduced whenanimmediateincreaseinthecarotenoidpathwayfluxisrequired[６５]４４　microRNAs

MicroRNAs(miRNAs)arekeyregulatorsofgeneexpressionineukaryotesandplayapivotalroleintheregulationofvariousbiologicalaswellas metabolicprocessesInterestinglyanartificialmaturemicroRNAs (amiRNAs)successfullytargetedthe PSY mRNA andreduced PSY mRNA levelinPhaeodactylumtricornutumwhichfurtherreducedthelevelsofcarotenoidsinthePtricornutumamiRNAknockdownlines[６６]ItwasspeculatedthatmiRNApossiblyisinvolvedinthetranscriptionregulationofcarotenoidbiosynthesisinplants

５　PostＧtranscriptionalregulationofcarotenoidsbiosynthesis

　InadditiontotranscriptionregulationofstructuregenesinvolvedinthecarotenoidpathwayrecentstudieshaverevealedotherregulatorymechanismstocontrolbiosyntheticenzymelevelsandactivitiesinplantssuchaspostＧtranscriptionalregulation (Figure１)Theseregulatory mechanismspossiblyarepresentduringfruitdevelopmentandripening

ORANGE(OR)isaplastidＧlocalizedproteincarryingacysteineＧrichzincfingerdomainPreviousstudiedshowedthatORpromotescarotenoidaccumulationincalliofrice[６７]andsweetpotato [６８]FurtherZhouetalfoundthatArabidopsisORandPSYphysicallyinteractwitheachotherinplastidsresultingin minimaleffecton expression ofPSY gene [６９]Howeveroverexpression of AtORsignificantlyincreasedtheamountofenzymaticallyactivePSYwhereasanatoratorＧlikedoublemutantexhibitsadramaticallyreducedPSYlevelTheresultrevealedanovelmechanismunderlyingregulationofcarotenoidbiosynthesisviaposttranscriptionalmodificationofPSYinplants[６９]

Inanotherimportantliterature on postＧtranscriptionalregulation Welsch et alreported thatdegradationmodificationofproteinincarotenoidbiosynthesispathwayisimplicatedinregulationofcarotenoidbiosynthesisClpproteasesystemthemostabundantandcomplexsolubleproteasesystemintheplastidwasshowntotargetPSYTheabsenceofCLPC１CLPP４andCLPR１Ｇ２enhancedthelevelsofactivePSYandseveralothercarotenogenicenzymes[７０]ThereforeORproteincounterbalancesClpＧmediatedproteolysisinmaintainingPSYproteinhomeostasis

Theauthors1049011researchteamalsodiscoveredanindirectlypostＧtranscriptionalregulatorymechanismtoregulateexpressionofPSYgeneinbananafruitSulfoxidationofproteinsbyreactiveoxygenspeciescancauseconformationalalterationorfunctionalimpairmentswhichcouldbereversedby Metsulfoxidereductase(Msr)ItwasfoundthatCaM１isasubstrateofMaMsrA７anditssulforxidationisrepairedbyMaMsrA７MaHY５Ｇ１actingasatranscriptionalrepressorofMaPSY１MaPSY２andMaPSY３inbananafruitisa CaMＧbindingproteinSulfoxidationregulationof MaCaM１ by MaMsrA７altersexpressionofMaPSY１MaPSY２andMaPSY３genesbymodifyingMaHY５Ｇ１transcriptionalactivity(nopublisheddata)

TwootherproteinsalsohavebeenreportedtoberelatedtoposttranscriptionalregulationofcarotenoidbiosynthesisSlSGR１atomatoSTAYＧGREENproteinregulateslycopeneaccumulationduringtomatofruitripeningviadirectinteractionwithPSY１[５９]AnotherexampleisthepostＧtranslationalregulationofDXSJＧproteinJ２０ (chaperoneproteindnaJ２０)interactsdirectlywithDXSregulatingDXSproteinlevelandactivitybyidentifyingunfoldedormisfolded(damaged)formsofDXSandtargetingthemtotheHsp７０systemforproperfoldingundernormalconditionsordegradationuponstress[７１]

６　Hormonalregulationofcarotenoidbiosynthesis

　Fruitripeningisacomplexandgeneticallyprogrammedprocesswhichinvolvesaseriesoforganolepticphysiologicaland biochemical changesresulting in the development of edible quality [７２]

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６２　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

PhytohormonesplaycrucialrolesinfruitripeningwhichhasbeenshowntoaffectcarotenoidaccumulationinfruitsMajorprogressregardingtheinvolvementofphytohormonesinregulatingcarotenoidbiosynthesishasbeenachievedinfruits

Ethyleneplaysa centralrolein climactericfruitripeningTherole ofethylenein carotenoidaccumulationinclimactericfruitshasbeenwidelystudiedIntomatoethyleneinitiatesfruitripeningresultinginarapidcolorshiftfromgreentoredwithincreasedlycopeneaccumulationanddecreasedβＧxanthophyllsandchlorophyllscontentsTheroleofethyleneinregulatingcarotenoidbiosynthesisduringtomatofruitripeninginvolvesacomplexregulatorynetworkoftranscriptionfactorsRINasamasterregulatorbindstothepromotersofgenesinvolvedinfruitripeningprocessesincludingcarotenoidbiosynthesis[４８４９７３]APETALA２a(AP２a)isamemberofAP２ERFsuperfamilywhichregulatestomatofruitripeningbyregulatingethylenebiosynthesisandsignalingRepressionofAP２abyRNAinterference (RNAi)resultsin decreasedlevels ofphytoeneandlycopenebut higherβＧcaroteneaccumulationconsistentwithdownＧregulatedexpressionofPDSCtRＧb２andCtrlSOandupＧregulatedexpressionofZEP１MoreoverseveralripeningＧrelatedregulatorsRIPENINGＧINHIBITOR (RIN)NONＧRIPENING (NOR)andCOLORLESSNONＧRIPENING (CNR)functionupstreamofAP２aandpositivelyregulateitsexpression[７４]SlERF６anothermemberofAP２ERFsuperfamilyisanegativeregulatorofcarotenoidaccumulationReducedexpressionofSlERF６byRNAienhancedbothcarotenoidandethylenelevelsduringfruitripening[７５]InadditionthreeothertranscriptionfactorsarerelatedtotheethylenepathwayincludingTAGL１FRUITFULL１and２whichhavebeenreportedtopositivelyregulatecarotenoidaccumulationduringtomatoripening[７６mdash７８]

Auxinisinvolvedincellexpansionanddivisiontissuedifferentiationorgandevelopmentandarangeofphysiologicalprocess[７９]Recentlyincreasingevidencesshowthatauxinalsoplaysanimportantroleinregulatingfruitripening[８０]TheleveloffreeIAA (themostabundantauxin)tendstodeclinepriortotheonsetoftomatofruitripening[８１]AuxinnegativelycontrolscarotenoidaccumulationintomatofruitExogenousIAA treatmentsignificantlyreduceslycopeneaccumulationbutenhancesthelevelsofneoxanthinandviolaxanthinaccompaniedbydownＧregulatedexpressionofPsy１Psy３PdsZisoandCrtisoandupＧregulatedexpressionofβＧLcy１andCrtrＧβ１ [８２]Howeverwhetherauxindirectlyregulatesthegenesincarotenoidpathwayremainsunknown

Abscisicacid (ABA)isa key hormoneinvolvedintuningresponsestoabioticstressesLittleinformationisavailableabouttheinvolvementofABAinregulatingcarotenoidaccumulationduringtomatofruitripeningABA hasbeenreportedto beimplicatedinfruitripeningandinfluencecarotenoidaccumulationintomato[８３]andstrawberry[８４]fruit

JAssuchasmethyljasmonicacidjasmonicacidandotherderivativesareplantendogenoushormones[８５]JAsalsoplayimportantrolesinfruitripeningLietalreportedthatJAinduceethyleneproductionbyMdMYC２ＧmediatedandMdERF３ＧmediatedupregulationofMdACS１gene[８６]Applicationofmethyljasmonate(MeJA)increasestheaccumulationofanthocyaninβＧcarotenecontentsandseveralphenoliccompounds[８７]LiuetalfurtherilluminatedtheroleofJAinregulatingcarotenoidaccumulationduringtomatofruitripeningwithJAＧdeficientmutants(spr２anddef１)anda３５∷prosystransgenicline(３５∷prosyswithincreasedJAlevelsandconstitutiveJAsignaling)andfoundthatlycopeneaccumulationissignificantlyinhibitedinspr２anddef１fruitbutenhancedin３５S∷prosysfruitaccompaniedbyasimilartrendofexpressionoflycopenebiosyntheticgenes[８８]Inadditionethyleneproductionisdepressedinspr２anddef１fruitbutincreasedin３５S∷prosysfruitMoreovertheexogenousapplicationofMeJAtoNeverripe (Nr)an ethyleneＧinsensitive mutantresultsin enhancedlycopene accumulation andexpressionoflycopenebiosyntheticgenes [８８]TheseresultsindicatedthatJA promoteslycopenebiosynthesisinamannerindependentofethylene

７　Futureresearchdirections

　CarotenoidmetabolismandregulationhavebeenwidelyresearchedinplantsHoweverthecarotenoidＧ

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６３　　　

relatedstudieshavebeenmostlyfocusedonmodelspeciessuchasArabidopsisandtomatoThemolecularmechanismsunderlyingcarotenoid metabolism andregulationin otherfruitspeciesarestillpoorlyunderstoodConsideringthediversityofcarotenoidsinfruitsitisnecessarytoinvestigatethenovelgenesandregulationmechanismsrelatedtocarotenoidbiosynthesisinplants

Carotenoid accumulation is cooperatively controlled at multiple levelsincluding developmentalprogramsenvironmentalfactorsand metabolicsignalsTranscriptionfactorsplayimportantroleinregulatingcarotenoidbiosynthesisHoweveronlyafewtranscriptionfactorsinvolvedincarotenoidbiosynthesisareidentifiedandtranscriptionregulationismainlyrelatedtoexpressionofPSYMoreovermostofthesetranscriptionfactorsexerttheirinfluencesviaregulatingfruitripeningnotspecificcarotenoidbiosynthesisＧrelated genesTheinteracting partners oftranscriptionfactorsinvolvedincarotenoidmetabolicnetworkalsoremaintobeidentifiedPostＧtranscriptionalregulationalternativeRNAsplicingepigeneticmodificationandmiRNAareofimportanceinplantgrowthanddevelopmentandresponsetoabioticstressHoweverlittleinformationregardingtheinvolvementofthesemechanismsinregulating carotenoid metabolism in planteven in Arabidopsisis available Application ofphytohormonescontributestoregulatecarotenoidcontentand maintainfruitqualityinagricultureandpostharvesttreatmentThemechanismunderlyingregulationofcarotenoidmetabolismbyphytohormonesespeciallycrossＧtalkamongdifferentphytohormonesarestillfarfrombeingunderstoodInthefuturestudiesbetterunderstandingofcarotenoid metabolismandregulationinfruitswillnotonlyhaveanimportantimpactongeneticimprovementandpostharvesttreatmentbutalsowillstrengthenknowledgeofcarotenoidregulationinplants

Acknowledgements

ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(GrantNos３１７７２０４１３１３２２０４４and３１５０１５４５)ScienceandTechnologyPlanningProjectofGuangdongProvince(GrantNo２０１５B０９０９０１０５８)ScienceandTechnologyPlanningProjectofGuangzhou (GrantNo２０１６０４０２００４８)andTalentProgramofGuangdongProvince(No２０１４TX０１N０４９)

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[１１]Rodrigo MJCillaABarberaRetalCarotenoidbioaccessibilityinpulpandfreshjuicefromcarotenoidＧrichsweetorangesandmandarinsFoodampFunction２０１５６１９５０mdash１９５９

[１２]FuXFengCWangCetalInvolvementofmultiplephytoenesynthasegenesintissueＧandcultivarＧspecificaccumulationofcarotenoidsinloquatJournalofExperimentalBotany２０１４６５４６７９mdash４６８９

[１３]DelgadoＧPelayoRGallardoＧGuerreroLHorneroＧMendezDChlorophyllandcarotenoidpigmentsinthepeelandfleshofcommercialapplefruitvarietiesFoodResearchInternational２０１４６５２７２mdash２８１

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６４　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[１４]SinghBSinghJPKaurAetalBioactivecompoundsinbananaandtheirassociatedhealthbenefitsmdashAreviewFoodChemistry２０１６

２０６１mdash１１[１５]AubertCChalotGChemicalcompositionbioactivecompoundsandvolatilesofsixtablegrapevarieties(Vitisvinifera L)Food

Chemistry２０１８２４０５２４mdash５３３[１６]ZhengHZhangQQuanJetalDeterminationofsugarsorganicacidsaromacomponentsandcarotenoidsingrapefruitpulpsFood

Chemistry２０１６２０５１１２mdash１２１[１７]FanciullinoALDhuiqueＧMayerCLuroFetalCarotenoiddiversityincultivatedcitrusishighlyinfluencedbygeneticfactorsJournal

ofAgriculturalandFoodChemistry２００６５４４３９７mdash４４０６[１８]KatoMIkomaYMatsumotoHetalAccumulationofcarotenoidsandexpressionofcarotenoidbiosyntheticgenesduringmaturation

incitrusfruitPlantPhysiology２００４１３４８２４mdash８３７[１９]LuPJWangCYYinTTetalCytologicalandmolecularcharacterizationofcarotenoidaccumulationinnormalandhighＧlycopene

mutantorangesScientificReports２０１７７[２０]AmpomahＧDwamenaCMcGhieTWibisono RetalThekiwifruitlycopenebetaＧcyclaseplaysasignificantroleincarotenoid

accumulationinfruitJournalofExperimentalBotany２００９６０３７６５mdash３７７９[２１]AjilaCMRaoLJRaoUJSPCharacterizationofbioactivecompoundsfromrawandripeMangiferaindicaLpeelextractsFoodand

ChemicalToxicology２０１０４８３４０６mdash３４１１[２２]TuanPAKimJKParkNIetalCarotenoidcontentandexpressionofphytoenesynthaseandphytoenedesaturasegenesinbittermelon

(Momordicacharantia)FoodChemistry２０１１１２６１６８６mdash１６９２[２３]SchweiggertRMSteingassCBHellerAetalCharacterizationofchromoplastsandcarotenoidsofredＧandyellowＧfleshedpapaya

(CaricapapayaL)Planta２０１１２３４１０３１mdash１０４４[２４]AbushitaAADaoodHGBiacsPAChangeincarotenoidsandantioxidantvitaminsintomatoasafunctionofvarietalandtechnological

factorsJournalofAgriculturalandFoodChemistry２０００４８２０７５mdash２０８１[２５]LvPLiNLiuHetalChangesincarotenoidprofilesandintheexpressionpatternofthegenesincarotenoidmetabolismsduringfruit

developmentandripeninginfourwatermeloncultivarsFoodChemistry２０１５１７４５２mdash５９[２６]Liu CZhang HDaiZetalVolatilechemicalandcarotenoidprofilesin watermelonsCitrullusvulgaris (Thunb)Schrad

(Cucurbitaceae)withdifferentfleshcolorsFoodScienceandBiotechnology２０１２２１５３１mdash５４１[２７]AlquezarBRodrigoMJLadoJetalAcomparativephysiologicalandtranscriptionalstudyofcarotenoidbiosynthesisinwhiteandred

grapefruit(CitrusparadisiMacf)TreeGeneticsamp Genomes２０１３９１２５７mdash１２６９[２８]KatoMMechanismofcarotenoidaccumulationincitrusfruitJournaloftheJapaneseSocietyforHorticulturalScience２０１２８１２１９mdash

２３３[２９]IsaacsonTRonenGZamirDetalCloningoftangerinefromtomatorevealsacarotenoidisomeraseessentialfortheproductionofbetaＧ

caroteneandxanthophyllsinplantsPlantCell２００２１４３３３mdash３４２[３０]RonenGCohenMZamirDetalRegulationofcarotenoidbiosynthesisduringtomatofruitdevelopmentExpressionofthegenefor

lycopeneepsilonＧcyclaseisdownＧregulatedduringripeningandiselevatedinthemutantDeltaPlantJournal１９９９１７３４１mdash３５１[３１]RonenGCarmelＧGorenLZamirDetalAnalternativepathwaytobetaＧcaroteneformationinplantchromoplastsdiscoveredbymapＧ

basedcloningofBetaandoldＧgoldcolormutationsintomatoProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０００９７１１１０２mdash１１１０７

[３２]HorneroＧMendezDdeGuevaraRGLMinguezＧMosqueraMICarotenoidbiosynthesischangesinfiveredpepper(CapsicumannuumL)

cultivarsduringripeningCultivarselectionforbreedingJournalofAgriculturalandFoodChemistry２０００４８３８５７mdash３８６４[３３]GuzmanIHambySRomeroJetalVariabilityofcarotenoidbiosynthesisinorangecoloredCapsicumsppPlantScience２０１０１７９

４９mdash５９[３４]RodriguezＧUribeLGuzmanIRajapakseWetalCarotenoidaccumulationinorangeＧpigmentedCapsicumannuumfruitregulatedat

multiplelevelsJournalofExperimentalBotany２０１２６３５１７mdash５２６[３５]SunTYuanHCaoHetalCarotenoidmetabolisminplantstheroleofplastidsMolecularPlant２０１８１１５８mdash７４[３６]BramleyPMRegulationofcarotenoidformationduringtomatofruitripeninganddevelopmentJournalofExperimentalBotany２００２

５３２１０７mdash２１１３[３７]EstevezJMCanteroAReindlAetal１ＧdeoxyＧDＧxyluloseＧ５Ｇphosphatesynthasealimitingenzymeforplastidicisoprenoidbiosynthesis

inplantsJournalofBiologicalChemistry２００１２７６２２９０１mdash２２９０９[３８]BotellaＧPaviaPBesumbes OPhillips MAetalRegulationofcarotenoidbiosynthesisinplantsevidenceforakeyroleof

hydroxymethylbutenyldiphosphatereductaseincontrollingthesupplyofplastidialisoprenoidprecursorsPlantJournal２００４４０１８８mdash

１９９[３９]CazzonelliCIPogsonBJSourcetosinkregulationofcarotenoidbiosynthesisinplantsTrendsinPlantScience２０１０１５２６６mdash２７４[４０]FraserPDEnfissiEMAHalketJMetalManipulationofphytoenelevelsintomatofruiteffectsonisoprenoidsplastidsand

intermediarymetabolismPlantCell２００７１９３１９４mdash３２１１[４１]FraserPDRomerSKianoJWetalElevationofcarotenoidsintomatobygeneticmanipulationJournaloftheScienceofFoodand

Agriculture２００１８１８２２mdash８２７[４２]RayJMoureauPBirdCetalCloningandcharacterizaitonofageneinvolvedinphytoenesynthesisfromtomatoPlantMolecular

Biology１９９２１９４０１mdash４０４

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６５　　　

[４３]PengGWangCSongSetalTheroleof１ＧdeoxyＧDＧxyluloseＧ５ＧphosphatesynthaseandphytoenesynthasegenefamilyincitruscarotenoidaccumulationPlantPhysiologyandBiochemistry２０１３７１６７mdash７６

[４４]ZhaoDZhouCTaoJCarotenoidaccumulationandcarotenogenicgenesexpressionduringtwotypesofpersimmonfruit(DiospyroskakiL)developmentPlantMolecularBiologyReporter２０１１２９６４６mdash６５４

[４５]MlalaziBWelschRNamanyaPetalIsolationandfunctionalcharacterisationofbananaphytoenesynthasegenesaspotentialcisgenesPlanta２０１２２３６１５８５mdash１５９８

[４６]NeumanHGalpazNCunningham FXetalThetomatomutationnxd１revealsagenenecessaryforneoxanthinbiosynthesisanddemonstratesthatviolaxanthinisasufficientprecursorforabscisicacidbiosynthesisPlantJournal２０１４７８８０mdash９３

[４７]VrebalovJRuezinskyDPadmanabhanVetalA MADSＧboxgenenecessaryforfruitripeningatthetomatoripeningＧinhibitor(Rin)

locusScience２００２２９６３４３mdash３４６[４８]MartelCVrebalovJTafelmeyerPetalThetomato MADSＧBoxtranscriptionfactorRIPENINGINHIBITORinteractswith

promotersinvolvedinnumerousripeningprocessesinaCOLORLESSNONRIPENINGＧdependentmannerPlantPhysiology２０１１１５７

１５６８mdash１５７９[４９]Fujisawa MNakanoTShimaYetalAlargeＧscaleidentificationofdirecttargetsofthetomato MADSBoxtranscriptionfactor

RIPENINGINHIBITORrevealstheregulationoffruitripeningPlantCell２０１３２５３７１mdash３８６[５０]DubosCStrackeRGrotewoldEetalMYBtranscriptionfactorsinArabidopsisTrendsinPlantScience２０１０１５５７３mdash５８１[５１]ZhuFLuoTLiuCetalAnR２R３ＧMYBtranscriptionfactorrepressesthetransformationofalphaＧandbetaＧbranchcarotenoidsby

negativelyregulatingexpressionofCrBCH２andCrNCED５inflavedoofCitrusreticulateNewPhytologist２０１７２１６１７８mdash１９２[５２]SagawaJMStanleyLELaFountainAMetalAnR２R３ＧMYBtranscriptionfactorregulatescarotenoidpigmentationinMimuluslewisii

flowersNewPhytologist２０１６２０９１０４９mdash１０５７[５３]JaakolaLNewinsightsintotheregulationofanthocyaninbiosynthesisinfruitsTrendsinPlantScience２０１３１８４７７mdash４８２[５４]JiangGYanHWuFetalLitchifruitLcNAC１isatargetofLcMYC２andregulatoroffruitsenescencethroughitsinteractionwith

LcWRKY１PlantandCellPhysiology２０１７５８１０７５mdash１０８９[５５]MengCYangDMaXetalSuppressionoftomatoSlNAC１transcriptionfactordelaysfruitripeningJournalofPlantPhysiology

２０１６１９３８８mdash９６[５６]ShanWKuangJFChenLetalMolecularcharacterizationofbananaNACtranscriptionfactorsandtheirinteractionswithethylene

signallingcomponentEILduringfruitripeningJournalofExperimentalBotany２０１２６３５１７１mdash５１８７[５７]ZhuMChenGZhouSetalAnewtomatoNAC (NAMATAF１２CUC２)transcriptionfactorSlNAC４functionsasapositive

regulatoroffruitripeningandcarotenoidaccumulationPlantandCellPhysiology２０１４５５１１９mdash１３５[５８]FuCCHanYCKuangJFetalPapayaCpEIN３aandCpNAC２cooperativelyregulatecarotenoidbiosynthesisrelatedgenesCpPDS２

４CpLCYＧeandCpCHYＧbduringfruitripeningPlantandCellPhysiology２０１７５８２１５５mdash２１６５[５９]LuoZZhangJLiJetalASTAYＧGREENproteinSlSGR１regulateslycopeneandbetaＧcaroteneaccumulationbyinteractingdirectly

withSlPSY１duringripeningprocessesintomatoNewPhytologist２０１３１９８４４２mdash４５２[６０]ToledoＧOrtizGHuqERodriguezＧConcepcionMDirectregulationofphytoenesynthasegeneexpressionandcarotenoidbiosynthesisby

phytochromeＧinteractingfactorsProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１０１０７１１６２６mdash

１１６３１[６１]WelschRMaassDVoegelTetalTranscriptionfactorRAP２２anditsinteractingpartnerSINAT２Stableelementsinthe

carotenogenesisofArabidopsisleavesPlantPhysiology２００７１４５１０７３mdash１０８５[６２]EndoTFujiiHSugiyamaAetalOverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor (CubHLH１)whichis

homologoustoArabidopsisactivationＧtaggedbri１suppressor１interactingfactorgenesmodulatescarotenoidmetabolismintransgenictomatoPlantScience２０１６２４３３５mdash４８

[６３]LiuLJiaCZhang MetalEctopicexpressionofaBZR１Ｇ１DtranscriptionfactorinbrassinosteroidsignallingenhancescarotenoidaccumulationandfruitqualityattributesintomatoPlantBiotechnologyJournal２０１４１２１０５mdash１１５

[６４]CazzonelliCICuttrissAJCossettoSBetalRegulationofcarotenoidcompositionandshootbranchinginarabidopsisbyachromatinmodifyinghistonemethyltransferaseSDG８PlantCell２００９２１３９mdash５３

[６５]AlvarezDVossBMaassDetalCarotenogenesisisregulatedby５1049011UTRＧmediatedtranslationofphytoenesynthasesplicevariantsPlantPhysiology２０１６１７２２３１４mdash２３２６

[６６]KaurSSpillaneCReductionincarotenoidlevelsinthemarinediatomPhaeodactylumtricornutum byartificialmicroRNAstargetedagainsttheendogenousphytoenesynthasegeneMarineBiotechnology２０１５１７１mdash７

[６７]BaiCRiveraSMMedinaVetalAninvitrosystemfortherapidfunctionalcharacterizationofgenesinvolvedincarotenoidbiosynthesisandaccumulationPlantJournal２０１４７７４６４mdash４７５

[６８]KimSHAhnYOAhnMJetalCloningandcharacterizationofanOrangegenethatincreasescarotenoidaccumulationandsaltstresstoleranceintransgenicsweetpotatoculturesPlantPhysiologyandBiochemistry２０１３７０４４５mdash４５４

[６９]ZhouXWelschRYang YetalArabidopsisORproteinsarethemajorposttranscriptionalregulatorsofphytoenesynthaseincontrollingcarotenoidbiosynthesisProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１５１１２３５５８mdash

３５６３[７０]WelschRZhouXYuanHetalClpproteaseandORdirectlycontroltheproteostasisofphytoenesynthasethecrucialenzymefor

carotenoidbiosynthesisinArabidopsisMolecularPlant２０１８１１１４９mdash１６２

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６６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[７１]PulidoPToledoＧOrtizGPhillipsMAetalArabidopsisJＧProteinJ２０deliversthefirstenzymeoftheplastidialisoprenoidpathwaytoproteinqualitycontrolPlantCell２０１３２５４１８３mdash４１９４

[７２]PrasannaVPrabhaTNTharanathanRNFruitripeningphenomenamdashAnoverviewCriticalReviewsinFoodScienceandNutrition

２００７４７１mdash１９[７３]FujisawaMShimaYHiguchiNetalDirecttargetsofthetomatoＧripeningregulatorRINidentifiedbytranscriptomeandchromatin

immunoprecipitationanalysesPlanta２０１２２３５１１０７mdash１１２２[７４]KarlovaRRosinFMBusscherＧLangeJetalTranscriptomeandmetaboliteprofilingshowthatAPETALA２aisamajorregulatorof

tomatofruitripeningPlantCell２０１１２３９２３mdash９４１[７５]LeeJMJoungJGMcQuinnRetalCombinedtranscriptomegeneticdiversityandmetaboliteprofilingintomatofruitrevealsthatthe

ethyleneresponsefactorSlERF６playsanimportantroleinripeningandcarotenoidaccumulationPlantJournal２０１２７０１９１mdash２０４[７６]ShimaYFujisawaMKitagawaMetalTomatoFRUITFULLhomologsregulatefruitripeningviaethylenebiosynthesisBioscience

BiotechnologyandBiochemistry２０１４７８２３１mdash２３７[７７]VrebalovJPanILArroyoAJMetalFleshyfruitexpansionandripeningareregulatedbythetomatoSHATTERPROOFgene

TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ５９　　　

geranylgeranyldiphosphate(GGPP)synthase(GGPPS)[３９]ThecondensationoftwoGGPPmoleculescatalyzedbyphytoenesynthase(PSY)formsuncolored１５Ｇcis

phytoenethefirstcarotenoidproductThisstepisregardedasthemostimportantregulatorystepincarotenoidbiosynthesis[３９]TomatocontainsthreePSYgenesPSY１PSY２andPSY３whichexhibittissueＧspecificexpressionmainlyinfruitinpetalandinrootrespectivelyDuringtomatoripeningtheaccumulationofcarotenoidcorrelateswiththeexpressionofPSY１ [４０４１]TransgenictomatobyantisenseinhibitionofPSY１producesonly３ofthecarotenoidinwildtypewildtypefruit[４２]SimilarresultsregardingtherelationshipbetweenupregulatedexpressionofPSYgenesandincreasedcarotenoidaccumulationhavebeenreportedinalargenumberoffruitssuchascitrus[４３]pepper[３４]persimmon[４４]loquat[１２]watermelon [２５]andbanana[４５]Uncoloredphytoenethenundergoesaseriesofdesaturationandisomerizationreactionsto generateredＧcolored allＧtransＧlycopenethe predominatepigmentinredtomatoand watermelonfruitsThesereactionsaresequentiallycatalyzedbyphytoenedesaturase(PDS)ζＧcarotenedesaturase(ZDS)ζＧcaroteneisomerase(ZＧISO)andcarotenoidisomerase(CRTISO)[３９]

Downstreaminthecarotenoidbiosynthesispathwaythecyclizationoflycopeneislocatedatthebranchingpointofthepathwaywhichproduceaseriesofcarotene(Figure１)[６７３９]ThecyclizationoflycopeneinvolvestwoenzymeslycopeneβＧcyclase(LCYB)andlycopeneεＧcyclase(LCYE)LCYBcatalyzesatwoＧstepreactiontoproduceβＧcarotenewithtwoβＧringsAεＧringandaβＧringaresequentiallyaddedtolycopeneformingαＧcarotene(βεＧcarotene)whichiscatalyzedbyLCYEandLCYBFollowingthecyclizationoflycopeneαＧcaroteneandβＧcarotenearesubjectedtohydroxylationandepoxidationformingaseriesofxanthophylls[６７３９]TheαＧcaroteneissequentiallycatalyzedbytwohydroxylasesCYP９７A and CYP９７CgeneratingluteinthefinalproductofαＧbranchincarotenoid biosynthesispathwayβＧcaroteneundergoestwostepsofhydroxylationandtwostepsofepoxidationcatalyzedbyβＧcarotenehydroxylase (BCH)andzeaxanthinepoxidase (ZEP)sequentiallyformingβＧcryptoxanthinzeaxanthinantheraxanthinandviolaxanthin[６７３９]Theconversionofviolaxanthinintoneoxanthinbyneoxanthinsynthase(NXS)completesthecorebiosynthesispathway[４６]

４　Transcriptionalregulationofcarotenoidbiosynthesis

４１　TranscriptionfactorTranscriptionalregulationplaysavitalroleinfruitdevelopmentandripeningaswellasabioticstresses

ItiswellknownthattranscriptionfactorsareinvolvedintranscriptionregulationofstructureandfunctiongenesincarotenoidbiosynthesispathwayAlthoughthegenesinvolvedinthebiosynthesisofcarotenoidbiosynthesishavebeenidentifiedandcharacterizedfromvariousfruits(Figure１)onlyafewtranscriptionfactorshavebeendemonstratedtodirectlyregulatetheexpressionofthesefunctiongenesinthepathwayThetranscriptionalcontrolofcarotenoidaccumulationhasbeenmostlystudiedintomatoduringripeningThesetranscriptionfactorsinclude RINR２R３ＧMYBNACSGR１PIF１RAP２２EIN３etcHowevermostofthesetranscriptionfactorsexertbroadeffectsonfruitripeningieethylenesynthesisfruitsofteningcolorformationaromaandflavorproductionandareunlikelytobespecificregulatorsofcarotenoidbiosynthesis

RIPENINGＧINHIBITOR (RIN)isa memberoftranscriptionfactorfamilycontaining MADSＧboxwhichplaysanessentialroleinfruitripeningasaglobalmasterregulator[４７]MarteletalreportedthatRINinteractswithSlPSY１thespecificPSYgeneassociatedwithcarotenoidbiosynthesisintomato[４８]FujisawaetalidentifiedanumberofRINＧtargetedgenesincarotenoidbiosynthesispathwaybychromatinimmunoprecipitationcoupled with DNA microarrayanalysisandfoundthatRIN regulatescarotenoidaccumulationviapositivelyregulatingPSY１ZISOandCRTISOinadirectmanneraswellaspositivelycontrollingZDSandnegativelyregulatingLYCBandLYCEbyanindirecteffectintomatofruit[４９]

VＧmybmyeloblastosisviraloncogenehomolog(MYB)proteinsbelongtoalargefamilyoftranscriptionfactorsinplantsThemajorityofMYBareR２R３ＧMYBsubfamilywithtworepeatsinitsMYBdomain

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６０　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

TheR２R３ＧMYBTFsplaykeyrolesinregulatingplantＧspecificprocessesincludingprimaryandsecondarymetabolismgrowthanddevelopmentandresponsetoabioticandbioticstresses [５０]IncitrusCrMYB６８an R２R３ＧMYBtranscriptionalfactorcandirectlybindandnegativelyregulateCrBCH２resultinginthedelayinthetransformationofαＧandβＧcaroteneandtheinhibitionofpeeldeＧgreeningincitrus[５１]SimilarlySagawaetalidentifiedanR２R３ＧMYBtranscriptionfactorReducedCarotenoidPigmentation１(RCP１)whichpositivelyregulatescarotenoidbiosynthesisduringMimuluslewisiiflowerdevelopmentLossＧofＧfunctionmutationsinRCP１resultindownＧregulationofallcarotenoidbiosyntheticgenesandreducecarotenoidcontentwhileoverexpressionofthisgeneinthercp１ mutantbackgroundrestorescarotenoidproduction[５２]Thereforeinadditiontoregulatinganthocyanins[５３]R２R３ＧMYBisalsoinvolvedintheregulationofcarotenoidbiosynthesisinfruits

NAMATAF１２andCUC２ (NAC)transcriptionfactorsareoneofthelargestfamiliesofplantＧspecifictranscription factors which areimplicated in plant growth and developmentflavonoidbiosynthesiswoodformationandstressresponses [５４]TheroleofNACtranscriptionfactorsinregulatingfruitripeningandsenescencehasbeenreportedintomato[５５]banana[５６]andlitchi[５４]IntomatoSlNAC１and SlNAC４ positivelyregulatetomatofruitripeningbutexhibitdifferentialcharacteristicsAntisensesuppression ofSlNAC１ resultsin delayed ethylene production andfruitripeningbuthigherlevelsofethylenebiosynthesisandaccumulationoftotalcarotenoidandlycopeneaccompaniedbyupＧregulatedexpressionofgenesrelatedtolycopeneandethylenebiosynthesis [５５]DifferentfromSlNAC１reducedexpressionofSlNAC４byRNAinterference(RNAi)intomatodelayedfruitripeningdecreasedethylenesynthesisandreducedcarotenoidsbyalteringcarotenoidpathwayflux[５７]AdditionallyFuetalreportedthatpapayaCpNAC２actsasatranscriptionalactivatorofCpPDS２４CpZDSCpLCYＧeandCpCHYＧb by directly bindingtotheirpromotersand promotestheirtranscription[５８]

SomeothertranscriptionfactorshavealsobeenreportedtobeinvolvedinthetranscriptionalregulationofstructuregenesinthecarotenoidbiosynthesispathwayIntomatoSlSGR１aSTAYＧGREENproteinphysicallyinteracts with PSY１ to suppress PSY１ expressionthus negatively regulatinglycopeneproductionduringfruitripening[５９]PhytochromeＧinteractingfactor１downＧregulatetheaccumulationofcarotenoidbybindingtothepromoterofPSYandrepressingPSYexpressioninArabidopsisseedlings[６０]SimilarlyAtPAP２２amemberoftheAPETALA２ (AP２)ethyleneＧresponsiveelementＧbindingproteintranscriptionfactorfamilydirectlybinds withthepromotersofPSY andPDS toregulatecarotenoidbiosynthesisinArabidopsis [６１]PapayaCpEIN３aanethyleneresponsivefactordirectlybindswiththepromotersofCpPDS４andCpCHYＧbandpromotestheirtranscription[５８]InadditionoverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor(CrbHLH１)intomatolowerslycopeneaccumulationanddownＧregulatecarotenoidbiosyntheticgeneexpressionintomatofruit[６２]EctopicexpressionofanArabidopsisBZR１Ｇ１Dtranscriptionfactorinbrassinosteroidsignalingenhancescarotenoidaccumulationandfruitqualityattributesintomato[６３]４２　Epigeneticmodification

EpigeneticmodificationincludingthemethylationofDNACpGislandsandthemodificationofhistonesthatassociatedwithDNAinchromosomesplayaveryimportantroleinregulatinggeneexpressionEpigeneticmodification possiblyisimplicatedinregulation ofcarotenoid biosynthesis (Figure１)Cazzonellietalreportedahistonemethyltransferaseenzyme(SET DOMAIN GROUP８SDG８)thatmethylateshistoneH３onLys４andor３６(H３K４andH３K３６)inArabidopsisthalianawhichisrequiredforexpressionofCRTISOgeneMutationofSDG８resultsindownＧregulatedexpressionofCRTISOgeneimpairedlutein biosynthesis andincreased shoot branchingThis wasthefirstreportregardinginvolvementofepigeneticmodificationinregulationofcarotenoidbiosynthesis[６４]４３　AlternativeRNAsplicing

AlternativeRNAsplicingisanimportantregulationofgeneexpressioninhighereukaryotesRecentlyAlvarezetalfoundthatalternativesplicingofPSYisimplicatedinregulationofcarotenogenesisinArabidopsisArabidopsispredominantlypossessasinglePSYgenewithtwoalternativesplicevariants

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(ASV)inlength andintheexonintronretention oftheir５1049011UTRsASV１ with along ５1049011UTR(untranslatedregion)isinvolvedindevelopmentallyregulatedcarotenoidformationwhileASV２withashort５1049011UTRispreferentiallyinduced whenanimmediateincreaseinthecarotenoidpathwayfluxisrequired[６５]４４　microRNAs

MicroRNAs(miRNAs)arekeyregulatorsofgeneexpressionineukaryotesandplayapivotalroleintheregulationofvariousbiologicalaswellas metabolicprocessesInterestinglyanartificialmaturemicroRNAs (amiRNAs)successfullytargetedthe PSY mRNA andreduced PSY mRNA levelinPhaeodactylumtricornutumwhichfurtherreducedthelevelsofcarotenoidsinthePtricornutumamiRNAknockdownlines[６６]ItwasspeculatedthatmiRNApossiblyisinvolvedinthetranscriptionregulationofcarotenoidbiosynthesisinplants

５　PostＧtranscriptionalregulationofcarotenoidsbiosynthesis

　InadditiontotranscriptionregulationofstructuregenesinvolvedinthecarotenoidpathwayrecentstudieshaverevealedotherregulatorymechanismstocontrolbiosyntheticenzymelevelsandactivitiesinplantssuchaspostＧtranscriptionalregulation (Figure１)Theseregulatory mechanismspossiblyarepresentduringfruitdevelopmentandripening

ORANGE(OR)isaplastidＧlocalizedproteincarryingacysteineＧrichzincfingerdomainPreviousstudiedshowedthatORpromotescarotenoidaccumulationincalliofrice[６７]andsweetpotato [６８]FurtherZhouetalfoundthatArabidopsisORandPSYphysicallyinteractwitheachotherinplastidsresultingin minimaleffecton expression ofPSY gene [６９]Howeveroverexpression of AtORsignificantlyincreasedtheamountofenzymaticallyactivePSYwhereasanatoratorＧlikedoublemutantexhibitsadramaticallyreducedPSYlevelTheresultrevealedanovelmechanismunderlyingregulationofcarotenoidbiosynthesisviaposttranscriptionalmodificationofPSYinplants[６９]

Inanotherimportantliterature on postＧtranscriptionalregulation Welsch et alreported thatdegradationmodificationofproteinincarotenoidbiosynthesispathwayisimplicatedinregulationofcarotenoidbiosynthesisClpproteasesystemthemostabundantandcomplexsolubleproteasesystemintheplastidwasshowntotargetPSYTheabsenceofCLPC１CLPP４andCLPR１Ｇ２enhancedthelevelsofactivePSYandseveralothercarotenogenicenzymes[７０]ThereforeORproteincounterbalancesClpＧmediatedproteolysisinmaintainingPSYproteinhomeostasis

Theauthors1049011researchteamalsodiscoveredanindirectlypostＧtranscriptionalregulatorymechanismtoregulateexpressionofPSYgeneinbananafruitSulfoxidationofproteinsbyreactiveoxygenspeciescancauseconformationalalterationorfunctionalimpairmentswhichcouldbereversedby Metsulfoxidereductase(Msr)ItwasfoundthatCaM１isasubstrateofMaMsrA７anditssulforxidationisrepairedbyMaMsrA７MaHY５Ｇ１actingasatranscriptionalrepressorofMaPSY１MaPSY２andMaPSY３inbananafruitisa CaMＧbindingproteinSulfoxidationregulationof MaCaM１ by MaMsrA７altersexpressionofMaPSY１MaPSY２andMaPSY３genesbymodifyingMaHY５Ｇ１transcriptionalactivity(nopublisheddata)

TwootherproteinsalsohavebeenreportedtoberelatedtoposttranscriptionalregulationofcarotenoidbiosynthesisSlSGR１atomatoSTAYＧGREENproteinregulateslycopeneaccumulationduringtomatofruitripeningviadirectinteractionwithPSY１[５９]AnotherexampleisthepostＧtranslationalregulationofDXSJＧproteinJ２０ (chaperoneproteindnaJ２０)interactsdirectlywithDXSregulatingDXSproteinlevelandactivitybyidentifyingunfoldedormisfolded(damaged)formsofDXSandtargetingthemtotheHsp７０systemforproperfoldingundernormalconditionsordegradationuponstress[７１]

６　Hormonalregulationofcarotenoidbiosynthesis

　Fruitripeningisacomplexandgeneticallyprogrammedprocesswhichinvolvesaseriesoforganolepticphysiologicaland biochemical changesresulting in the development of edible quality [７２]

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PhytohormonesplaycrucialrolesinfruitripeningwhichhasbeenshowntoaffectcarotenoidaccumulationinfruitsMajorprogressregardingtheinvolvementofphytohormonesinregulatingcarotenoidbiosynthesishasbeenachievedinfruits

Ethyleneplaysa centralrolein climactericfruitripeningTherole ofethylenein carotenoidaccumulationinclimactericfruitshasbeenwidelystudiedIntomatoethyleneinitiatesfruitripeningresultinginarapidcolorshiftfromgreentoredwithincreasedlycopeneaccumulationanddecreasedβＧxanthophyllsandchlorophyllscontentsTheroleofethyleneinregulatingcarotenoidbiosynthesisduringtomatofruitripeninginvolvesacomplexregulatorynetworkoftranscriptionfactorsRINasamasterregulatorbindstothepromotersofgenesinvolvedinfruitripeningprocessesincludingcarotenoidbiosynthesis[４８４９７３]APETALA２a(AP２a)isamemberofAP２ERFsuperfamilywhichregulatestomatofruitripeningbyregulatingethylenebiosynthesisandsignalingRepressionofAP２abyRNAinterference (RNAi)resultsin decreasedlevels ofphytoeneandlycopenebut higherβＧcaroteneaccumulationconsistentwithdownＧregulatedexpressionofPDSCtRＧb２andCtrlSOandupＧregulatedexpressionofZEP１MoreoverseveralripeningＧrelatedregulatorsRIPENINGＧINHIBITOR (RIN)NONＧRIPENING (NOR)andCOLORLESSNONＧRIPENING (CNR)functionupstreamofAP２aandpositivelyregulateitsexpression[７４]SlERF６anothermemberofAP２ERFsuperfamilyisanegativeregulatorofcarotenoidaccumulationReducedexpressionofSlERF６byRNAienhancedbothcarotenoidandethylenelevelsduringfruitripening[７５]InadditionthreeothertranscriptionfactorsarerelatedtotheethylenepathwayincludingTAGL１FRUITFULL１and２whichhavebeenreportedtopositivelyregulatecarotenoidaccumulationduringtomatoripening[７６mdash７８]

Auxinisinvolvedincellexpansionanddivisiontissuedifferentiationorgandevelopmentandarangeofphysiologicalprocess[７９]Recentlyincreasingevidencesshowthatauxinalsoplaysanimportantroleinregulatingfruitripening[８０]TheleveloffreeIAA (themostabundantauxin)tendstodeclinepriortotheonsetoftomatofruitripening[８１]AuxinnegativelycontrolscarotenoidaccumulationintomatofruitExogenousIAA treatmentsignificantlyreduceslycopeneaccumulationbutenhancesthelevelsofneoxanthinandviolaxanthinaccompaniedbydownＧregulatedexpressionofPsy１Psy３PdsZisoandCrtisoandupＧregulatedexpressionofβＧLcy１andCrtrＧβ１ [８２]Howeverwhetherauxindirectlyregulatesthegenesincarotenoidpathwayremainsunknown

Abscisicacid (ABA)isa key hormoneinvolvedintuningresponsestoabioticstressesLittleinformationisavailableabouttheinvolvementofABAinregulatingcarotenoidaccumulationduringtomatofruitripeningABA hasbeenreportedto beimplicatedinfruitripeningandinfluencecarotenoidaccumulationintomato[８３]andstrawberry[８４]fruit

JAssuchasmethyljasmonicacidjasmonicacidandotherderivativesareplantendogenoushormones[８５]JAsalsoplayimportantrolesinfruitripeningLietalreportedthatJAinduceethyleneproductionbyMdMYC２ＧmediatedandMdERF３ＧmediatedupregulationofMdACS１gene[８６]Applicationofmethyljasmonate(MeJA)increasestheaccumulationofanthocyaninβＧcarotenecontentsandseveralphenoliccompounds[８７]LiuetalfurtherilluminatedtheroleofJAinregulatingcarotenoidaccumulationduringtomatofruitripeningwithJAＧdeficientmutants(spr２anddef１)anda３５∷prosystransgenicline(３５∷prosyswithincreasedJAlevelsandconstitutiveJAsignaling)andfoundthatlycopeneaccumulationissignificantlyinhibitedinspr２anddef１fruitbutenhancedin３５S∷prosysfruitaccompaniedbyasimilartrendofexpressionoflycopenebiosyntheticgenes[８８]Inadditionethyleneproductionisdepressedinspr２anddef１fruitbutincreasedin３５S∷prosysfruitMoreovertheexogenousapplicationofMeJAtoNeverripe (Nr)an ethyleneＧinsensitive mutantresultsin enhancedlycopene accumulation andexpressionoflycopenebiosyntheticgenes [８８]TheseresultsindicatedthatJA promoteslycopenebiosynthesisinamannerindependentofethylene

７　Futureresearchdirections

　CarotenoidmetabolismandregulationhavebeenwidelyresearchedinplantsHoweverthecarotenoidＧ

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６３　　　

relatedstudieshavebeenmostlyfocusedonmodelspeciessuchasArabidopsisandtomatoThemolecularmechanismsunderlyingcarotenoid metabolism andregulationin otherfruitspeciesarestillpoorlyunderstoodConsideringthediversityofcarotenoidsinfruitsitisnecessarytoinvestigatethenovelgenesandregulationmechanismsrelatedtocarotenoidbiosynthesisinplants

Carotenoid accumulation is cooperatively controlled at multiple levelsincluding developmentalprogramsenvironmentalfactorsand metabolicsignalsTranscriptionfactorsplayimportantroleinregulatingcarotenoidbiosynthesisHoweveronlyafewtranscriptionfactorsinvolvedincarotenoidbiosynthesisareidentifiedandtranscriptionregulationismainlyrelatedtoexpressionofPSYMoreovermostofthesetranscriptionfactorsexerttheirinfluencesviaregulatingfruitripeningnotspecificcarotenoidbiosynthesisＧrelated genesTheinteracting partners oftranscriptionfactorsinvolvedincarotenoidmetabolicnetworkalsoremaintobeidentifiedPostＧtranscriptionalregulationalternativeRNAsplicingepigeneticmodificationandmiRNAareofimportanceinplantgrowthanddevelopmentandresponsetoabioticstressHoweverlittleinformationregardingtheinvolvementofthesemechanismsinregulating carotenoid metabolism in planteven in Arabidopsisis available Application ofphytohormonescontributestoregulatecarotenoidcontentand maintainfruitqualityinagricultureandpostharvesttreatmentThemechanismunderlyingregulationofcarotenoidmetabolismbyphytohormonesespeciallycrossＧtalkamongdifferentphytohormonesarestillfarfrombeingunderstoodInthefuturestudiesbetterunderstandingofcarotenoid metabolismandregulationinfruitswillnotonlyhaveanimportantimpactongeneticimprovementandpostharvesttreatmentbutalsowillstrengthenknowledgeofcarotenoidregulationinplants

Acknowledgements

ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(GrantNos３１７７２０４１３１３２２０４４and３１５０１５４５)ScienceandTechnologyPlanningProjectofGuangdongProvince(GrantNo２０１５B０９０９０１０５８)ScienceandTechnologyPlanningProjectofGuangzhou (GrantNo２０１６０４０２００４８)andTalentProgramofGuangdongProvince(No２０１４TX０１N０４９)

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promotersinvolvedinnumerousripeningprocessesinaCOLORLESSNONRIPENINGＧdependentmannerPlantPhysiology２０１１１５７

１５６８mdash１５７９[４９]Fujisawa MNakanoTShimaYetalAlargeＧscaleidentificationofdirecttargetsofthetomato MADSBoxtranscriptionfactor

RIPENINGINHIBITORrevealstheregulationoffruitripeningPlantCell２０１３２５３７１mdash３８６[５０]DubosCStrackeRGrotewoldEetalMYBtranscriptionfactorsinArabidopsisTrendsinPlantScience２０１０１５５７３mdash５８１[５１]ZhuFLuoTLiuCetalAnR２R３ＧMYBtranscriptionfactorrepressesthetransformationofalphaＧandbetaＧbranchcarotenoidsby

negativelyregulatingexpressionofCrBCH２andCrNCED５inflavedoofCitrusreticulateNewPhytologist２０１７２１６１７８mdash１９２[５２]SagawaJMStanleyLELaFountainAMetalAnR２R３ＧMYBtranscriptionfactorregulatescarotenoidpigmentationinMimuluslewisii

flowersNewPhytologist２０１６２０９１０４９mdash１０５７[５３]JaakolaLNewinsightsintotheregulationofanthocyaninbiosynthesisinfruitsTrendsinPlantScience２０１３１８４７７mdash４８２[５４]JiangGYanHWuFetalLitchifruitLcNAC１isatargetofLcMYC２andregulatoroffruitsenescencethroughitsinteractionwith

LcWRKY１PlantandCellPhysiology２０１７５８１０７５mdash１０８９[５５]MengCYangDMaXetalSuppressionoftomatoSlNAC１transcriptionfactordelaysfruitripeningJournalofPlantPhysiology

２０１６１９３８８mdash９６[５６]ShanWKuangJFChenLetalMolecularcharacterizationofbananaNACtranscriptionfactorsandtheirinteractionswithethylene

signallingcomponentEILduringfruitripeningJournalofExperimentalBotany２０１２６３５１７１mdash５１８７[５７]ZhuMChenGZhouSetalAnewtomatoNAC (NAMATAF１２CUC２)transcriptionfactorSlNAC４functionsasapositive

regulatoroffruitripeningandcarotenoidaccumulationPlantandCellPhysiology２０１４５５１１９mdash１３５[５８]FuCCHanYCKuangJFetalPapayaCpEIN３aandCpNAC２cooperativelyregulatecarotenoidbiosynthesisrelatedgenesCpPDS２

４CpLCYＧeandCpCHYＧbduringfruitripeningPlantandCellPhysiology２０１７５８２１５５mdash２１６５[５９]LuoZZhangJLiJetalASTAYＧGREENproteinSlSGR１regulateslycopeneandbetaＧcaroteneaccumulationbyinteractingdirectly

withSlPSY１duringripeningprocessesintomatoNewPhytologist２０１３１９８４４２mdash４５２[６０]ToledoＧOrtizGHuqERodriguezＧConcepcionMDirectregulationofphytoenesynthasegeneexpressionandcarotenoidbiosynthesisby

phytochromeＧinteractingfactorsProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１０１０７１１６２６mdash

１１６３１[６１]WelschRMaassDVoegelTetalTranscriptionfactorRAP２２anditsinteractingpartnerSINAT２Stableelementsinthe

carotenogenesisofArabidopsisleavesPlantPhysiology２００７１４５１０７３mdash１０８５[６２]EndoTFujiiHSugiyamaAetalOverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor (CubHLH１)whichis

homologoustoArabidopsisactivationＧtaggedbri１suppressor１interactingfactorgenesmodulatescarotenoidmetabolismintransgenictomatoPlantScience２０１６２４３３５mdash４８

[６３]LiuLJiaCZhang MetalEctopicexpressionofaBZR１Ｇ１DtranscriptionfactorinbrassinosteroidsignallingenhancescarotenoidaccumulationandfruitqualityattributesintomatoPlantBiotechnologyJournal２０１４１２１０５mdash１１５

[６４]CazzonelliCICuttrissAJCossettoSBetalRegulationofcarotenoidcompositionandshootbranchinginarabidopsisbyachromatinmodifyinghistonemethyltransferaseSDG８PlantCell２００９２１３９mdash５３

[６５]AlvarezDVossBMaassDetalCarotenogenesisisregulatedby５1049011UTRＧmediatedtranslationofphytoenesynthasesplicevariantsPlantPhysiology２０１６１７２２３１４mdash２３２６

[６６]KaurSSpillaneCReductionincarotenoidlevelsinthemarinediatomPhaeodactylumtricornutum byartificialmicroRNAstargetedagainsttheendogenousphytoenesynthasegeneMarineBiotechnology２０１５１７１mdash７

[６７]BaiCRiveraSMMedinaVetalAninvitrosystemfortherapidfunctionalcharacterizationofgenesinvolvedincarotenoidbiosynthesisandaccumulationPlantJournal２０１４７７４６４mdash４７５

[６８]KimSHAhnYOAhnMJetalCloningandcharacterizationofanOrangegenethatincreasescarotenoidaccumulationandsaltstresstoleranceintransgenicsweetpotatoculturesPlantPhysiologyandBiochemistry２０１３７０４４５mdash４５４

[６９]ZhouXWelschRYang YetalArabidopsisORproteinsarethemajorposttranscriptionalregulatorsofphytoenesynthaseincontrollingcarotenoidbiosynthesisProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１５１１２３５５８mdash

３５６３[７０]WelschRZhouXYuanHetalClpproteaseandORdirectlycontroltheproteostasisofphytoenesynthasethecrucialenzymefor

carotenoidbiosynthesisinArabidopsisMolecularPlant２０１８１１１４９mdash１６２

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６６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[７１]PulidoPToledoＧOrtizGPhillipsMAetalArabidopsisJＧProteinJ２０deliversthefirstenzymeoftheplastidialisoprenoidpathwaytoproteinqualitycontrolPlantCell２０１３２５４１８３mdash４１９４

[７２]PrasannaVPrabhaTNTharanathanRNFruitripeningphenomenamdashAnoverviewCriticalReviewsinFoodScienceandNutrition

２００７４７１mdash１９[７３]FujisawaMShimaYHiguchiNetalDirecttargetsofthetomatoＧripeningregulatorRINidentifiedbytranscriptomeandchromatin

immunoprecipitationanalysesPlanta２０１２２３５１１０７mdash１１２２[７４]KarlovaRRosinFMBusscherＧLangeJetalTranscriptomeandmetaboliteprofilingshowthatAPETALA２aisamajorregulatorof

tomatofruitripeningPlantCell２０１１２３９２３mdash９４１[７５]LeeJMJoungJGMcQuinnRetalCombinedtranscriptomegeneticdiversityandmetaboliteprofilingintomatofruitrevealsthatthe

ethyleneresponsefactorSlERF６playsanimportantroleinripeningandcarotenoidaccumulationPlantJournal２０１２７０１９１mdash２０４[７６]ShimaYFujisawaMKitagawaMetalTomatoFRUITFULLhomologsregulatefruitripeningviaethylenebiosynthesisBioscience

BiotechnologyandBiochemistry２０１４７８２３１mdash２３７[７７]VrebalovJPanILArroyoAJMetalFleshyfruitexpansionandripeningareregulatedbythetomatoSHATTERPROOFgene

TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

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６０　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

TheR２R３ＧMYBTFsplaykeyrolesinregulatingplantＧspecificprocessesincludingprimaryandsecondarymetabolismgrowthanddevelopmentandresponsetoabioticandbioticstresses [５０]IncitrusCrMYB６８an R２R３ＧMYBtranscriptionalfactorcandirectlybindandnegativelyregulateCrBCH２resultinginthedelayinthetransformationofαＧandβＧcaroteneandtheinhibitionofpeeldeＧgreeningincitrus[５１]SimilarlySagawaetalidentifiedanR２R３ＧMYBtranscriptionfactorReducedCarotenoidPigmentation１(RCP１)whichpositivelyregulatescarotenoidbiosynthesisduringMimuluslewisiiflowerdevelopmentLossＧofＧfunctionmutationsinRCP１resultindownＧregulationofallcarotenoidbiosyntheticgenesandreducecarotenoidcontentwhileoverexpressionofthisgeneinthercp１ mutantbackgroundrestorescarotenoidproduction[５２]Thereforeinadditiontoregulatinganthocyanins[５３]R２R３ＧMYBisalsoinvolvedintheregulationofcarotenoidbiosynthesisinfruits

NAMATAF１２andCUC２ (NAC)transcriptionfactorsareoneofthelargestfamiliesofplantＧspecifictranscription factors which areimplicated in plant growth and developmentflavonoidbiosynthesiswoodformationandstressresponses [５４]TheroleofNACtranscriptionfactorsinregulatingfruitripeningandsenescencehasbeenreportedintomato[５５]banana[５６]andlitchi[５４]IntomatoSlNAC１and SlNAC４ positivelyregulatetomatofruitripeningbutexhibitdifferentialcharacteristicsAntisensesuppression ofSlNAC１ resultsin delayed ethylene production andfruitripeningbuthigherlevelsofethylenebiosynthesisandaccumulationoftotalcarotenoidandlycopeneaccompaniedbyupＧregulatedexpressionofgenesrelatedtolycopeneandethylenebiosynthesis [５５]DifferentfromSlNAC１reducedexpressionofSlNAC４byRNAinterference(RNAi)intomatodelayedfruitripeningdecreasedethylenesynthesisandreducedcarotenoidsbyalteringcarotenoidpathwayflux[５７]AdditionallyFuetalreportedthatpapayaCpNAC２actsasatranscriptionalactivatorofCpPDS２４CpZDSCpLCYＧeandCpCHYＧb by directly bindingtotheirpromotersand promotestheirtranscription[５８]

SomeothertranscriptionfactorshavealsobeenreportedtobeinvolvedinthetranscriptionalregulationofstructuregenesinthecarotenoidbiosynthesispathwayIntomatoSlSGR１aSTAYＧGREENproteinphysicallyinteracts with PSY１ to suppress PSY１ expressionthus negatively regulatinglycopeneproductionduringfruitripening[５９]PhytochromeＧinteractingfactor１downＧregulatetheaccumulationofcarotenoidbybindingtothepromoterofPSYandrepressingPSYexpressioninArabidopsisseedlings[６０]SimilarlyAtPAP２２amemberoftheAPETALA２ (AP２)ethyleneＧresponsiveelementＧbindingproteintranscriptionfactorfamilydirectlybinds withthepromotersofPSY andPDS toregulatecarotenoidbiosynthesisinArabidopsis [６１]PapayaCpEIN３aanethyleneresponsivefactordirectlybindswiththepromotersofCpPDS４andCpCHYＧbandpromotestheirtranscription[５８]InadditionoverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor(CrbHLH１)intomatolowerslycopeneaccumulationanddownＧregulatecarotenoidbiosyntheticgeneexpressionintomatofruit[６２]EctopicexpressionofanArabidopsisBZR１Ｇ１Dtranscriptionfactorinbrassinosteroidsignalingenhancescarotenoidaccumulationandfruitqualityattributesintomato[６３]４２　Epigeneticmodification

EpigeneticmodificationincludingthemethylationofDNACpGislandsandthemodificationofhistonesthatassociatedwithDNAinchromosomesplayaveryimportantroleinregulatinggeneexpressionEpigeneticmodification possiblyisimplicatedinregulation ofcarotenoid biosynthesis (Figure１)Cazzonellietalreportedahistonemethyltransferaseenzyme(SET DOMAIN GROUP８SDG８)thatmethylateshistoneH３onLys４andor３６(H３K４andH３K３６)inArabidopsisthalianawhichisrequiredforexpressionofCRTISOgeneMutationofSDG８resultsindownＧregulatedexpressionofCRTISOgeneimpairedlutein biosynthesis andincreased shoot branchingThis wasthefirstreportregardinginvolvementofepigeneticmodificationinregulationofcarotenoidbiosynthesis[６４]４３　AlternativeRNAsplicing

AlternativeRNAsplicingisanimportantregulationofgeneexpressioninhighereukaryotesRecentlyAlvarezetalfoundthatalternativesplicingofPSYisimplicatedinregulationofcarotenogenesisinArabidopsisArabidopsispredominantlypossessasinglePSYgenewithtwoalternativesplicevariants

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６１　　　

(ASV)inlength andintheexonintronretention oftheir５1049011UTRsASV１ with along ５1049011UTR(untranslatedregion)isinvolvedindevelopmentallyregulatedcarotenoidformationwhileASV２withashort５1049011UTRispreferentiallyinduced whenanimmediateincreaseinthecarotenoidpathwayfluxisrequired[６５]４４　microRNAs

MicroRNAs(miRNAs)arekeyregulatorsofgeneexpressionineukaryotesandplayapivotalroleintheregulationofvariousbiologicalaswellas metabolicprocessesInterestinglyanartificialmaturemicroRNAs (amiRNAs)successfullytargetedthe PSY mRNA andreduced PSY mRNA levelinPhaeodactylumtricornutumwhichfurtherreducedthelevelsofcarotenoidsinthePtricornutumamiRNAknockdownlines[６６]ItwasspeculatedthatmiRNApossiblyisinvolvedinthetranscriptionregulationofcarotenoidbiosynthesisinplants

５　PostＧtranscriptionalregulationofcarotenoidsbiosynthesis

　InadditiontotranscriptionregulationofstructuregenesinvolvedinthecarotenoidpathwayrecentstudieshaverevealedotherregulatorymechanismstocontrolbiosyntheticenzymelevelsandactivitiesinplantssuchaspostＧtranscriptionalregulation (Figure１)Theseregulatory mechanismspossiblyarepresentduringfruitdevelopmentandripening

ORANGE(OR)isaplastidＧlocalizedproteincarryingacysteineＧrichzincfingerdomainPreviousstudiedshowedthatORpromotescarotenoidaccumulationincalliofrice[６７]andsweetpotato [６８]FurtherZhouetalfoundthatArabidopsisORandPSYphysicallyinteractwitheachotherinplastidsresultingin minimaleffecton expression ofPSY gene [６９]Howeveroverexpression of AtORsignificantlyincreasedtheamountofenzymaticallyactivePSYwhereasanatoratorＧlikedoublemutantexhibitsadramaticallyreducedPSYlevelTheresultrevealedanovelmechanismunderlyingregulationofcarotenoidbiosynthesisviaposttranscriptionalmodificationofPSYinplants[６９]

Inanotherimportantliterature on postＧtranscriptionalregulation Welsch et alreported thatdegradationmodificationofproteinincarotenoidbiosynthesispathwayisimplicatedinregulationofcarotenoidbiosynthesisClpproteasesystemthemostabundantandcomplexsolubleproteasesystemintheplastidwasshowntotargetPSYTheabsenceofCLPC１CLPP４andCLPR１Ｇ２enhancedthelevelsofactivePSYandseveralothercarotenogenicenzymes[７０]ThereforeORproteincounterbalancesClpＧmediatedproteolysisinmaintainingPSYproteinhomeostasis

Theauthors1049011researchteamalsodiscoveredanindirectlypostＧtranscriptionalregulatorymechanismtoregulateexpressionofPSYgeneinbananafruitSulfoxidationofproteinsbyreactiveoxygenspeciescancauseconformationalalterationorfunctionalimpairmentswhichcouldbereversedby Metsulfoxidereductase(Msr)ItwasfoundthatCaM１isasubstrateofMaMsrA７anditssulforxidationisrepairedbyMaMsrA７MaHY５Ｇ１actingasatranscriptionalrepressorofMaPSY１MaPSY２andMaPSY３inbananafruitisa CaMＧbindingproteinSulfoxidationregulationof MaCaM１ by MaMsrA７altersexpressionofMaPSY１MaPSY２andMaPSY３genesbymodifyingMaHY５Ｇ１transcriptionalactivity(nopublisheddata)

TwootherproteinsalsohavebeenreportedtoberelatedtoposttranscriptionalregulationofcarotenoidbiosynthesisSlSGR１atomatoSTAYＧGREENproteinregulateslycopeneaccumulationduringtomatofruitripeningviadirectinteractionwithPSY１[５９]AnotherexampleisthepostＧtranslationalregulationofDXSJＧproteinJ２０ (chaperoneproteindnaJ２０)interactsdirectlywithDXSregulatingDXSproteinlevelandactivitybyidentifyingunfoldedormisfolded(damaged)formsofDXSandtargetingthemtotheHsp７０systemforproperfoldingundernormalconditionsordegradationuponstress[７１]

６　Hormonalregulationofcarotenoidbiosynthesis

　Fruitripeningisacomplexandgeneticallyprogrammedprocesswhichinvolvesaseriesoforganolepticphysiologicaland biochemical changesresulting in the development of edible quality [７２]

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６２　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

PhytohormonesplaycrucialrolesinfruitripeningwhichhasbeenshowntoaffectcarotenoidaccumulationinfruitsMajorprogressregardingtheinvolvementofphytohormonesinregulatingcarotenoidbiosynthesishasbeenachievedinfruits

Ethyleneplaysa centralrolein climactericfruitripeningTherole ofethylenein carotenoidaccumulationinclimactericfruitshasbeenwidelystudiedIntomatoethyleneinitiatesfruitripeningresultinginarapidcolorshiftfromgreentoredwithincreasedlycopeneaccumulationanddecreasedβＧxanthophyllsandchlorophyllscontentsTheroleofethyleneinregulatingcarotenoidbiosynthesisduringtomatofruitripeninginvolvesacomplexregulatorynetworkoftranscriptionfactorsRINasamasterregulatorbindstothepromotersofgenesinvolvedinfruitripeningprocessesincludingcarotenoidbiosynthesis[４８４９７３]APETALA２a(AP２a)isamemberofAP２ERFsuperfamilywhichregulatestomatofruitripeningbyregulatingethylenebiosynthesisandsignalingRepressionofAP２abyRNAinterference (RNAi)resultsin decreasedlevels ofphytoeneandlycopenebut higherβＧcaroteneaccumulationconsistentwithdownＧregulatedexpressionofPDSCtRＧb２andCtrlSOandupＧregulatedexpressionofZEP１MoreoverseveralripeningＧrelatedregulatorsRIPENINGＧINHIBITOR (RIN)NONＧRIPENING (NOR)andCOLORLESSNONＧRIPENING (CNR)functionupstreamofAP２aandpositivelyregulateitsexpression[７４]SlERF６anothermemberofAP２ERFsuperfamilyisanegativeregulatorofcarotenoidaccumulationReducedexpressionofSlERF６byRNAienhancedbothcarotenoidandethylenelevelsduringfruitripening[７５]InadditionthreeothertranscriptionfactorsarerelatedtotheethylenepathwayincludingTAGL１FRUITFULL１and２whichhavebeenreportedtopositivelyregulatecarotenoidaccumulationduringtomatoripening[７６mdash７８]

Auxinisinvolvedincellexpansionanddivisiontissuedifferentiationorgandevelopmentandarangeofphysiologicalprocess[７９]Recentlyincreasingevidencesshowthatauxinalsoplaysanimportantroleinregulatingfruitripening[８０]TheleveloffreeIAA (themostabundantauxin)tendstodeclinepriortotheonsetoftomatofruitripening[８１]AuxinnegativelycontrolscarotenoidaccumulationintomatofruitExogenousIAA treatmentsignificantlyreduceslycopeneaccumulationbutenhancesthelevelsofneoxanthinandviolaxanthinaccompaniedbydownＧregulatedexpressionofPsy１Psy３PdsZisoandCrtisoandupＧregulatedexpressionofβＧLcy１andCrtrＧβ１ [８２]Howeverwhetherauxindirectlyregulatesthegenesincarotenoidpathwayremainsunknown

Abscisicacid (ABA)isa key hormoneinvolvedintuningresponsestoabioticstressesLittleinformationisavailableabouttheinvolvementofABAinregulatingcarotenoidaccumulationduringtomatofruitripeningABA hasbeenreportedto beimplicatedinfruitripeningandinfluencecarotenoidaccumulationintomato[８３]andstrawberry[８４]fruit

JAssuchasmethyljasmonicacidjasmonicacidandotherderivativesareplantendogenoushormones[８５]JAsalsoplayimportantrolesinfruitripeningLietalreportedthatJAinduceethyleneproductionbyMdMYC２ＧmediatedandMdERF３ＧmediatedupregulationofMdACS１gene[８６]Applicationofmethyljasmonate(MeJA)increasestheaccumulationofanthocyaninβＧcarotenecontentsandseveralphenoliccompounds[８７]LiuetalfurtherilluminatedtheroleofJAinregulatingcarotenoidaccumulationduringtomatofruitripeningwithJAＧdeficientmutants(spr２anddef１)anda３５∷prosystransgenicline(３５∷prosyswithincreasedJAlevelsandconstitutiveJAsignaling)andfoundthatlycopeneaccumulationissignificantlyinhibitedinspr２anddef１fruitbutenhancedin３５S∷prosysfruitaccompaniedbyasimilartrendofexpressionoflycopenebiosyntheticgenes[８８]Inadditionethyleneproductionisdepressedinspr２anddef１fruitbutincreasedin３５S∷prosysfruitMoreovertheexogenousapplicationofMeJAtoNeverripe (Nr)an ethyleneＧinsensitive mutantresultsin enhancedlycopene accumulation andexpressionoflycopenebiosyntheticgenes [８８]TheseresultsindicatedthatJA promoteslycopenebiosynthesisinamannerindependentofethylene

７　Futureresearchdirections

　CarotenoidmetabolismandregulationhavebeenwidelyresearchedinplantsHoweverthecarotenoidＧ

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６３　　　

relatedstudieshavebeenmostlyfocusedonmodelspeciessuchasArabidopsisandtomatoThemolecularmechanismsunderlyingcarotenoid metabolism andregulationin otherfruitspeciesarestillpoorlyunderstoodConsideringthediversityofcarotenoidsinfruitsitisnecessarytoinvestigatethenovelgenesandregulationmechanismsrelatedtocarotenoidbiosynthesisinplants

Carotenoid accumulation is cooperatively controlled at multiple levelsincluding developmentalprogramsenvironmentalfactorsand metabolicsignalsTranscriptionfactorsplayimportantroleinregulatingcarotenoidbiosynthesisHoweveronlyafewtranscriptionfactorsinvolvedincarotenoidbiosynthesisareidentifiedandtranscriptionregulationismainlyrelatedtoexpressionofPSYMoreovermostofthesetranscriptionfactorsexerttheirinfluencesviaregulatingfruitripeningnotspecificcarotenoidbiosynthesisＧrelated genesTheinteracting partners oftranscriptionfactorsinvolvedincarotenoidmetabolicnetworkalsoremaintobeidentifiedPostＧtranscriptionalregulationalternativeRNAsplicingepigeneticmodificationandmiRNAareofimportanceinplantgrowthanddevelopmentandresponsetoabioticstressHoweverlittleinformationregardingtheinvolvementofthesemechanismsinregulating carotenoid metabolism in planteven in Arabidopsisis available Application ofphytohormonescontributestoregulatecarotenoidcontentand maintainfruitqualityinagricultureandpostharvesttreatmentThemechanismunderlyingregulationofcarotenoidmetabolismbyphytohormonesespeciallycrossＧtalkamongdifferentphytohormonesarestillfarfrombeingunderstoodInthefuturestudiesbetterunderstandingofcarotenoid metabolismandregulationinfruitswillnotonlyhaveanimportantimpactongeneticimprovementandpostharvesttreatmentbutalsowillstrengthenknowledgeofcarotenoidregulationinplants

Acknowledgements

ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(GrantNos３１７７２０４１３１３２２０４４and３１５０１５４５)ScienceandTechnologyPlanningProjectofGuangdongProvince(GrantNo２０１５B０９０９０１０５８)ScienceandTechnologyPlanningProjectofGuangzhou (GrantNo２０１６０４０２００４８)andTalentProgramofGuangdongProvince(No２０１４TX０１N０４９)

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５２５３９mdash５６１[３]RollandNCurienGFinazziGetalThebiosyntheticcapacitiesoftheplastidsandintegrationbetweencytoplasmicandchloroplast

processesAnnualReviewofGenetics２０１２４６２３３mdash２６４[４]OdorissiXavierAAPerezＧGalvezACarotenoidsasasourceofantioxidantsinthedietSubcellularBiochemistry２０１６７９３５９mdash３７５[５]KrinskyNIJohnsonEJCarotenoidactionsandtheirrelationtohealthanddiseaseMolecularAspectsofMedicine２００５２６４５９mdash５１６[６]YuanHZhangJNageswaranDetalCarotenoidmetabolismandregulationinhorticulturalcropsHorticultureResearch２０１５２[７]LadoJZacariasLJesusRodrigoMRegulationofcarotenoidbiosynthesisduringfruitdevelopmentSubcellularBiochemistry２０１６７９

１６１mdash１９８[８]ZhuHChen MWen QetalIsolationandcharacterizationofthecarotenoidbiosyntheticgenesLCYBLCYEandCHXBfrom

strawberryandtheirrelationtocarotenoidaccumulationScientiaHorticulturae２０１５１８２１３４mdash１４４[９]BrandiFBarEMourguesFetalStudyoflsquoRedhavenrsquopeachanditswhiteＧfleshedmutantsuggestsakeyroleofCCD４carotenoid

dioxygenaseincarotenoidandnorisoprenoidvolatilemetabolismBMCPlantBiology２０１１１１[１０]HaSHKimJBParkJSetalAcomparisonofthecarotenoidaccumulationinCapsicumvarietiesthatshowdifferentripeningcolours

deletionofthecapsanthinＧcapsorubinsynthasegeneisnotaprerequisitefortheformationofayellowpepperJournalofExperimentalBotany２００７５８３１３５mdash３１４４

[１１]Rodrigo MJCillaABarberaRetalCarotenoidbioaccessibilityinpulpandfreshjuicefromcarotenoidＧrichsweetorangesandmandarinsFoodampFunction２０１５６１９５０mdash１９５９

[１２]FuXFengCWangCetalInvolvementofmultiplephytoenesynthasegenesintissueＧandcultivarＧspecificaccumulationofcarotenoidsinloquatJournalofExperimentalBotany２０１４６５４６７９mdash４６８９

[１３]DelgadoＧPelayoRGallardoＧGuerreroLHorneroＧMendezDChlorophyllandcarotenoidpigmentsinthepeelandfleshofcommercialapplefruitvarietiesFoodResearchInternational２０１４６５２７２mdash２８１

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６４　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[１４]SinghBSinghJPKaurAetalBioactivecompoundsinbananaandtheirassociatedhealthbenefitsmdashAreviewFoodChemistry２０１６

２０６１mdash１１[１５]AubertCChalotGChemicalcompositionbioactivecompoundsandvolatilesofsixtablegrapevarieties(Vitisvinifera L)Food

Chemistry２０１８２４０５２４mdash５３３[１６]ZhengHZhangQQuanJetalDeterminationofsugarsorganicacidsaromacomponentsandcarotenoidsingrapefruitpulpsFood

Chemistry２０１６２０５１１２mdash１２１[１７]FanciullinoALDhuiqueＧMayerCLuroFetalCarotenoiddiversityincultivatedcitrusishighlyinfluencedbygeneticfactorsJournal

ofAgriculturalandFoodChemistry２００６５４４３９７mdash４４０６[１８]KatoMIkomaYMatsumotoHetalAccumulationofcarotenoidsandexpressionofcarotenoidbiosyntheticgenesduringmaturation

incitrusfruitPlantPhysiology２００４１３４８２４mdash８３７[１９]LuPJWangCYYinTTetalCytologicalandmolecularcharacterizationofcarotenoidaccumulationinnormalandhighＧlycopene

mutantorangesScientificReports２０１７７[２０]AmpomahＧDwamenaCMcGhieTWibisono RetalThekiwifruitlycopenebetaＧcyclaseplaysasignificantroleincarotenoid

accumulationinfruitJournalofExperimentalBotany２００９６０３７６５mdash３７７９[２１]AjilaCMRaoLJRaoUJSPCharacterizationofbioactivecompoundsfromrawandripeMangiferaindicaLpeelextractsFoodand

ChemicalToxicology２０１０４８３４０６mdash３４１１[２２]TuanPAKimJKParkNIetalCarotenoidcontentandexpressionofphytoenesynthaseandphytoenedesaturasegenesinbittermelon

(Momordicacharantia)FoodChemistry２０１１１２６１６８６mdash１６９２[２３]SchweiggertRMSteingassCBHellerAetalCharacterizationofchromoplastsandcarotenoidsofredＧandyellowＧfleshedpapaya

(CaricapapayaL)Planta２０１１２３４１０３１mdash１０４４[２４]AbushitaAADaoodHGBiacsPAChangeincarotenoidsandantioxidantvitaminsintomatoasafunctionofvarietalandtechnological

factorsJournalofAgriculturalandFoodChemistry２０００４８２０７５mdash２０８１[２５]LvPLiNLiuHetalChangesincarotenoidprofilesandintheexpressionpatternofthegenesincarotenoidmetabolismsduringfruit

developmentandripeninginfourwatermeloncultivarsFoodChemistry２０１５１７４５２mdash５９[２６]Liu CZhang HDaiZetalVolatilechemicalandcarotenoidprofilesin watermelonsCitrullusvulgaris (Thunb)Schrad

(Cucurbitaceae)withdifferentfleshcolorsFoodScienceandBiotechnology２０１２２１５３１mdash５４１[２７]AlquezarBRodrigoMJLadoJetalAcomparativephysiologicalandtranscriptionalstudyofcarotenoidbiosynthesisinwhiteandred

grapefruit(CitrusparadisiMacf)TreeGeneticsamp Genomes２０１３９１２５７mdash１２６９[２８]KatoMMechanismofcarotenoidaccumulationincitrusfruitJournaloftheJapaneseSocietyforHorticulturalScience２０１２８１２１９mdash

２３３[２９]IsaacsonTRonenGZamirDetalCloningoftangerinefromtomatorevealsacarotenoidisomeraseessentialfortheproductionofbetaＧ

caroteneandxanthophyllsinplantsPlantCell２００２１４３３３mdash３４２[３０]RonenGCohenMZamirDetalRegulationofcarotenoidbiosynthesisduringtomatofruitdevelopmentExpressionofthegenefor

lycopeneepsilonＧcyclaseisdownＧregulatedduringripeningandiselevatedinthemutantDeltaPlantJournal１９９９１７３４１mdash３５１[３１]RonenGCarmelＧGorenLZamirDetalAnalternativepathwaytobetaＧcaroteneformationinplantchromoplastsdiscoveredbymapＧ

basedcloningofBetaandoldＧgoldcolormutationsintomatoProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０００９７１１１０２mdash１１１０７

[３２]HorneroＧMendezDdeGuevaraRGLMinguezＧMosqueraMICarotenoidbiosynthesischangesinfiveredpepper(CapsicumannuumL)

cultivarsduringripeningCultivarselectionforbreedingJournalofAgriculturalandFoodChemistry２０００４８３８５７mdash３８６４[３３]GuzmanIHambySRomeroJetalVariabilityofcarotenoidbiosynthesisinorangecoloredCapsicumsppPlantScience２０１０１７９

４９mdash５９[３４]RodriguezＧUribeLGuzmanIRajapakseWetalCarotenoidaccumulationinorangeＧpigmentedCapsicumannuumfruitregulatedat

multiplelevelsJournalofExperimentalBotany２０１２６３５１７mdash５２６[３５]SunTYuanHCaoHetalCarotenoidmetabolisminplantstheroleofplastidsMolecularPlant２０１８１１５８mdash７４[３６]BramleyPMRegulationofcarotenoidformationduringtomatofruitripeninganddevelopmentJournalofExperimentalBotany２００２

５３２１０７mdash２１１３[３７]EstevezJMCanteroAReindlAetal１ＧdeoxyＧDＧxyluloseＧ５Ｇphosphatesynthasealimitingenzymeforplastidicisoprenoidbiosynthesis

inplantsJournalofBiologicalChemistry２００１２７６２２９０１mdash２２９０９[３８]BotellaＧPaviaPBesumbes OPhillips MAetalRegulationofcarotenoidbiosynthesisinplantsevidenceforakeyroleof

hydroxymethylbutenyldiphosphatereductaseincontrollingthesupplyofplastidialisoprenoidprecursorsPlantJournal２００４４０１８８mdash

１９９[３９]CazzonelliCIPogsonBJSourcetosinkregulationofcarotenoidbiosynthesisinplantsTrendsinPlantScience２０１０１５２６６mdash２７４[４０]FraserPDEnfissiEMAHalketJMetalManipulationofphytoenelevelsintomatofruiteffectsonisoprenoidsplastidsand

intermediarymetabolismPlantCell２００７１９３１９４mdash３２１１[４１]FraserPDRomerSKianoJWetalElevationofcarotenoidsintomatobygeneticmanipulationJournaloftheScienceofFoodand

Agriculture２００１８１８２２mdash８２７[４２]RayJMoureauPBirdCetalCloningandcharacterizaitonofageneinvolvedinphytoenesynthesisfromtomatoPlantMolecular

Biology１９９２１９４０１mdash４０４

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６５　　　

[４３]PengGWangCSongSetalTheroleof１ＧdeoxyＧDＧxyluloseＧ５ＧphosphatesynthaseandphytoenesynthasegenefamilyincitruscarotenoidaccumulationPlantPhysiologyandBiochemistry２０１３７１６７mdash７６

[４４]ZhaoDZhouCTaoJCarotenoidaccumulationandcarotenogenicgenesexpressionduringtwotypesofpersimmonfruit(DiospyroskakiL)developmentPlantMolecularBiologyReporter２０１１２９６４６mdash６５４

[４５]MlalaziBWelschRNamanyaPetalIsolationandfunctionalcharacterisationofbananaphytoenesynthasegenesaspotentialcisgenesPlanta２０１２２３６１５８５mdash１５９８

[４６]NeumanHGalpazNCunningham FXetalThetomatomutationnxd１revealsagenenecessaryforneoxanthinbiosynthesisanddemonstratesthatviolaxanthinisasufficientprecursorforabscisicacidbiosynthesisPlantJournal２０１４７８８０mdash９３

[４７]VrebalovJRuezinskyDPadmanabhanVetalA MADSＧboxgenenecessaryforfruitripeningatthetomatoripeningＧinhibitor(Rin)

locusScience２００２２９６３４３mdash３４６[４８]MartelCVrebalovJTafelmeyerPetalThetomato MADSＧBoxtranscriptionfactorRIPENINGINHIBITORinteractswith

promotersinvolvedinnumerousripeningprocessesinaCOLORLESSNONRIPENINGＧdependentmannerPlantPhysiology２０１１１５７

１５６８mdash１５７９[４９]Fujisawa MNakanoTShimaYetalAlargeＧscaleidentificationofdirecttargetsofthetomato MADSBoxtranscriptionfactor

RIPENINGINHIBITORrevealstheregulationoffruitripeningPlantCell２０１３２５３７１mdash３８６[５０]DubosCStrackeRGrotewoldEetalMYBtranscriptionfactorsinArabidopsisTrendsinPlantScience２０１０１５５７３mdash５８１[５１]ZhuFLuoTLiuCetalAnR２R３ＧMYBtranscriptionfactorrepressesthetransformationofalphaＧandbetaＧbranchcarotenoidsby

negativelyregulatingexpressionofCrBCH２andCrNCED５inflavedoofCitrusreticulateNewPhytologist２０１７２１６１７８mdash１９２[５２]SagawaJMStanleyLELaFountainAMetalAnR２R３ＧMYBtranscriptionfactorregulatescarotenoidpigmentationinMimuluslewisii

flowersNewPhytologist２０１６２０９１０４９mdash１０５７[５３]JaakolaLNewinsightsintotheregulationofanthocyaninbiosynthesisinfruitsTrendsinPlantScience２０１３１８４７７mdash４８２[５４]JiangGYanHWuFetalLitchifruitLcNAC１isatargetofLcMYC２andregulatoroffruitsenescencethroughitsinteractionwith

LcWRKY１PlantandCellPhysiology２０１７５８１０７５mdash１０８９[５５]MengCYangDMaXetalSuppressionoftomatoSlNAC１transcriptionfactordelaysfruitripeningJournalofPlantPhysiology

２０１６１９３８８mdash９６[５６]ShanWKuangJFChenLetalMolecularcharacterizationofbananaNACtranscriptionfactorsandtheirinteractionswithethylene

signallingcomponentEILduringfruitripeningJournalofExperimentalBotany２０１２６３５１７１mdash５１８７[５７]ZhuMChenGZhouSetalAnewtomatoNAC (NAMATAF１２CUC２)transcriptionfactorSlNAC４functionsasapositive

regulatoroffruitripeningandcarotenoidaccumulationPlantandCellPhysiology２０１４５５１１９mdash１３５[５８]FuCCHanYCKuangJFetalPapayaCpEIN３aandCpNAC２cooperativelyregulatecarotenoidbiosynthesisrelatedgenesCpPDS２

４CpLCYＧeandCpCHYＧbduringfruitripeningPlantandCellPhysiology２０１７５８２１５５mdash２１６５[５９]LuoZZhangJLiJetalASTAYＧGREENproteinSlSGR１regulateslycopeneandbetaＧcaroteneaccumulationbyinteractingdirectly

withSlPSY１duringripeningprocessesintomatoNewPhytologist２０１３１９８４４２mdash４５２[６０]ToledoＧOrtizGHuqERodriguezＧConcepcionMDirectregulationofphytoenesynthasegeneexpressionandcarotenoidbiosynthesisby

phytochromeＧinteractingfactorsProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１０１０７１１６２６mdash

１１６３１[６１]WelschRMaassDVoegelTetalTranscriptionfactorRAP２２anditsinteractingpartnerSINAT２Stableelementsinthe

carotenogenesisofArabidopsisleavesPlantPhysiology２００７１４５１０７３mdash１０８５[６２]EndoTFujiiHSugiyamaAetalOverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor (CubHLH１)whichis

homologoustoArabidopsisactivationＧtaggedbri１suppressor１interactingfactorgenesmodulatescarotenoidmetabolismintransgenictomatoPlantScience２０１６２４３３５mdash４８

[６３]LiuLJiaCZhang MetalEctopicexpressionofaBZR１Ｇ１DtranscriptionfactorinbrassinosteroidsignallingenhancescarotenoidaccumulationandfruitqualityattributesintomatoPlantBiotechnologyJournal２０１４１２１０５mdash１１５

[６４]CazzonelliCICuttrissAJCossettoSBetalRegulationofcarotenoidcompositionandshootbranchinginarabidopsisbyachromatinmodifyinghistonemethyltransferaseSDG８PlantCell２００９２１３９mdash５３

[６５]AlvarezDVossBMaassDetalCarotenogenesisisregulatedby５1049011UTRＧmediatedtranslationofphytoenesynthasesplicevariantsPlantPhysiology２０１６１７２２３１４mdash２３２６

[６６]KaurSSpillaneCReductionincarotenoidlevelsinthemarinediatomPhaeodactylumtricornutum byartificialmicroRNAstargetedagainsttheendogenousphytoenesynthasegeneMarineBiotechnology２０１５１７１mdash７

[６７]BaiCRiveraSMMedinaVetalAninvitrosystemfortherapidfunctionalcharacterizationofgenesinvolvedincarotenoidbiosynthesisandaccumulationPlantJournal２０１４７７４６４mdash４７５

[６８]KimSHAhnYOAhnMJetalCloningandcharacterizationofanOrangegenethatincreasescarotenoidaccumulationandsaltstresstoleranceintransgenicsweetpotatoculturesPlantPhysiologyandBiochemistry２０１３７０４４５mdash４５４

[６９]ZhouXWelschRYang YetalArabidopsisORproteinsarethemajorposttranscriptionalregulatorsofphytoenesynthaseincontrollingcarotenoidbiosynthesisProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１５１１２３５５８mdash

３５６３[７０]WelschRZhouXYuanHetalClpproteaseandORdirectlycontroltheproteostasisofphytoenesynthasethecrucialenzymefor

carotenoidbiosynthesisinArabidopsisMolecularPlant２０１８１１１４９mdash１６２

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６６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[７１]PulidoPToledoＧOrtizGPhillipsMAetalArabidopsisJＧProteinJ２０deliversthefirstenzymeoftheplastidialisoprenoidpathwaytoproteinqualitycontrolPlantCell２０１３２５４１８３mdash４１９４

[７２]PrasannaVPrabhaTNTharanathanRNFruitripeningphenomenamdashAnoverviewCriticalReviewsinFoodScienceandNutrition

２００７４７１mdash１９[７３]FujisawaMShimaYHiguchiNetalDirecttargetsofthetomatoＧripeningregulatorRINidentifiedbytranscriptomeandchromatin

immunoprecipitationanalysesPlanta２０１２２３５１１０７mdash１１２２[７４]KarlovaRRosinFMBusscherＧLangeJetalTranscriptomeandmetaboliteprofilingshowthatAPETALA２aisamajorregulatorof

tomatofruitripeningPlantCell２０１１２３９２３mdash９４１[７５]LeeJMJoungJGMcQuinnRetalCombinedtranscriptomegeneticdiversityandmetaboliteprofilingintomatofruitrevealsthatthe

ethyleneresponsefactorSlERF６playsanimportantroleinripeningandcarotenoidaccumulationPlantJournal２０１２７０１９１mdash２０４[７６]ShimaYFujisawaMKitagawaMetalTomatoFRUITFULLhomologsregulatefruitripeningviaethylenebiosynthesisBioscience

BiotechnologyandBiochemistry２０１４７８２３１mdash２３７[７７]VrebalovJPanILArroyoAJMetalFleshyfruitexpansionandripeningareregulatedbythetomatoSHATTERPROOFgene

TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６１　　　

(ASV)inlength andintheexonintronretention oftheir５1049011UTRsASV１ with along ５1049011UTR(untranslatedregion)isinvolvedindevelopmentallyregulatedcarotenoidformationwhileASV２withashort５1049011UTRispreferentiallyinduced whenanimmediateincreaseinthecarotenoidpathwayfluxisrequired[６５]４４　microRNAs

MicroRNAs(miRNAs)arekeyregulatorsofgeneexpressionineukaryotesandplayapivotalroleintheregulationofvariousbiologicalaswellas metabolicprocessesInterestinglyanartificialmaturemicroRNAs (amiRNAs)successfullytargetedthe PSY mRNA andreduced PSY mRNA levelinPhaeodactylumtricornutumwhichfurtherreducedthelevelsofcarotenoidsinthePtricornutumamiRNAknockdownlines[６６]ItwasspeculatedthatmiRNApossiblyisinvolvedinthetranscriptionregulationofcarotenoidbiosynthesisinplants

５　PostＧtranscriptionalregulationofcarotenoidsbiosynthesis

　InadditiontotranscriptionregulationofstructuregenesinvolvedinthecarotenoidpathwayrecentstudieshaverevealedotherregulatorymechanismstocontrolbiosyntheticenzymelevelsandactivitiesinplantssuchaspostＧtranscriptionalregulation (Figure１)Theseregulatory mechanismspossiblyarepresentduringfruitdevelopmentandripening

ORANGE(OR)isaplastidＧlocalizedproteincarryingacysteineＧrichzincfingerdomainPreviousstudiedshowedthatORpromotescarotenoidaccumulationincalliofrice[６７]andsweetpotato [６８]FurtherZhouetalfoundthatArabidopsisORandPSYphysicallyinteractwitheachotherinplastidsresultingin minimaleffecton expression ofPSY gene [６９]Howeveroverexpression of AtORsignificantlyincreasedtheamountofenzymaticallyactivePSYwhereasanatoratorＧlikedoublemutantexhibitsadramaticallyreducedPSYlevelTheresultrevealedanovelmechanismunderlyingregulationofcarotenoidbiosynthesisviaposttranscriptionalmodificationofPSYinplants[６９]

Inanotherimportantliterature on postＧtranscriptionalregulation Welsch et alreported thatdegradationmodificationofproteinincarotenoidbiosynthesispathwayisimplicatedinregulationofcarotenoidbiosynthesisClpproteasesystemthemostabundantandcomplexsolubleproteasesystemintheplastidwasshowntotargetPSYTheabsenceofCLPC１CLPP４andCLPR１Ｇ２enhancedthelevelsofactivePSYandseveralothercarotenogenicenzymes[７０]ThereforeORproteincounterbalancesClpＧmediatedproteolysisinmaintainingPSYproteinhomeostasis

Theauthors1049011researchteamalsodiscoveredanindirectlypostＧtranscriptionalregulatorymechanismtoregulateexpressionofPSYgeneinbananafruitSulfoxidationofproteinsbyreactiveoxygenspeciescancauseconformationalalterationorfunctionalimpairmentswhichcouldbereversedby Metsulfoxidereductase(Msr)ItwasfoundthatCaM１isasubstrateofMaMsrA７anditssulforxidationisrepairedbyMaMsrA７MaHY５Ｇ１actingasatranscriptionalrepressorofMaPSY１MaPSY２andMaPSY３inbananafruitisa CaMＧbindingproteinSulfoxidationregulationof MaCaM１ by MaMsrA７altersexpressionofMaPSY１MaPSY２andMaPSY３genesbymodifyingMaHY５Ｇ１transcriptionalactivity(nopublisheddata)

TwootherproteinsalsohavebeenreportedtoberelatedtoposttranscriptionalregulationofcarotenoidbiosynthesisSlSGR１atomatoSTAYＧGREENproteinregulateslycopeneaccumulationduringtomatofruitripeningviadirectinteractionwithPSY１[５９]AnotherexampleisthepostＧtranslationalregulationofDXSJＧproteinJ２０ (chaperoneproteindnaJ２０)interactsdirectlywithDXSregulatingDXSproteinlevelandactivitybyidentifyingunfoldedormisfolded(damaged)formsofDXSandtargetingthemtotheHsp７０systemforproperfoldingundernormalconditionsordegradationuponstress[７１]

６　Hormonalregulationofcarotenoidbiosynthesis

　Fruitripeningisacomplexandgeneticallyprogrammedprocesswhichinvolvesaseriesoforganolepticphysiologicaland biochemical changesresulting in the development of edible quality [７２]

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PhytohormonesplaycrucialrolesinfruitripeningwhichhasbeenshowntoaffectcarotenoidaccumulationinfruitsMajorprogressregardingtheinvolvementofphytohormonesinregulatingcarotenoidbiosynthesishasbeenachievedinfruits

Ethyleneplaysa centralrolein climactericfruitripeningTherole ofethylenein carotenoidaccumulationinclimactericfruitshasbeenwidelystudiedIntomatoethyleneinitiatesfruitripeningresultinginarapidcolorshiftfromgreentoredwithincreasedlycopeneaccumulationanddecreasedβＧxanthophyllsandchlorophyllscontentsTheroleofethyleneinregulatingcarotenoidbiosynthesisduringtomatofruitripeninginvolvesacomplexregulatorynetworkoftranscriptionfactorsRINasamasterregulatorbindstothepromotersofgenesinvolvedinfruitripeningprocessesincludingcarotenoidbiosynthesis[４８４９７３]APETALA２a(AP２a)isamemberofAP２ERFsuperfamilywhichregulatestomatofruitripeningbyregulatingethylenebiosynthesisandsignalingRepressionofAP２abyRNAinterference (RNAi)resultsin decreasedlevels ofphytoeneandlycopenebut higherβＧcaroteneaccumulationconsistentwithdownＧregulatedexpressionofPDSCtRＧb２andCtrlSOandupＧregulatedexpressionofZEP１MoreoverseveralripeningＧrelatedregulatorsRIPENINGＧINHIBITOR (RIN)NONＧRIPENING (NOR)andCOLORLESSNONＧRIPENING (CNR)functionupstreamofAP２aandpositivelyregulateitsexpression[７４]SlERF６anothermemberofAP２ERFsuperfamilyisanegativeregulatorofcarotenoidaccumulationReducedexpressionofSlERF６byRNAienhancedbothcarotenoidandethylenelevelsduringfruitripening[７５]InadditionthreeothertranscriptionfactorsarerelatedtotheethylenepathwayincludingTAGL１FRUITFULL１and２whichhavebeenreportedtopositivelyregulatecarotenoidaccumulationduringtomatoripening[７６mdash７８]

Auxinisinvolvedincellexpansionanddivisiontissuedifferentiationorgandevelopmentandarangeofphysiologicalprocess[７９]Recentlyincreasingevidencesshowthatauxinalsoplaysanimportantroleinregulatingfruitripening[８０]TheleveloffreeIAA (themostabundantauxin)tendstodeclinepriortotheonsetoftomatofruitripening[８１]AuxinnegativelycontrolscarotenoidaccumulationintomatofruitExogenousIAA treatmentsignificantlyreduceslycopeneaccumulationbutenhancesthelevelsofneoxanthinandviolaxanthinaccompaniedbydownＧregulatedexpressionofPsy１Psy３PdsZisoandCrtisoandupＧregulatedexpressionofβＧLcy１andCrtrＧβ１ [８２]Howeverwhetherauxindirectlyregulatesthegenesincarotenoidpathwayremainsunknown

Abscisicacid (ABA)isa key hormoneinvolvedintuningresponsestoabioticstressesLittleinformationisavailableabouttheinvolvementofABAinregulatingcarotenoidaccumulationduringtomatofruitripeningABA hasbeenreportedto beimplicatedinfruitripeningandinfluencecarotenoidaccumulationintomato[８３]andstrawberry[８４]fruit

JAssuchasmethyljasmonicacidjasmonicacidandotherderivativesareplantendogenoushormones[８５]JAsalsoplayimportantrolesinfruitripeningLietalreportedthatJAinduceethyleneproductionbyMdMYC２ＧmediatedandMdERF３ＧmediatedupregulationofMdACS１gene[８６]Applicationofmethyljasmonate(MeJA)increasestheaccumulationofanthocyaninβＧcarotenecontentsandseveralphenoliccompounds[８７]LiuetalfurtherilluminatedtheroleofJAinregulatingcarotenoidaccumulationduringtomatofruitripeningwithJAＧdeficientmutants(spr２anddef１)anda３５∷prosystransgenicline(３５∷prosyswithincreasedJAlevelsandconstitutiveJAsignaling)andfoundthatlycopeneaccumulationissignificantlyinhibitedinspr２anddef１fruitbutenhancedin３５S∷prosysfruitaccompaniedbyasimilartrendofexpressionoflycopenebiosyntheticgenes[８８]Inadditionethyleneproductionisdepressedinspr２anddef１fruitbutincreasedin３５S∷prosysfruitMoreovertheexogenousapplicationofMeJAtoNeverripe (Nr)an ethyleneＧinsensitive mutantresultsin enhancedlycopene accumulation andexpressionoflycopenebiosyntheticgenes [８８]TheseresultsindicatedthatJA promoteslycopenebiosynthesisinamannerindependentofethylene

７　Futureresearchdirections

　CarotenoidmetabolismandregulationhavebeenwidelyresearchedinplantsHoweverthecarotenoidＧ

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６３　　　

relatedstudieshavebeenmostlyfocusedonmodelspeciessuchasArabidopsisandtomatoThemolecularmechanismsunderlyingcarotenoid metabolism andregulationin otherfruitspeciesarestillpoorlyunderstoodConsideringthediversityofcarotenoidsinfruitsitisnecessarytoinvestigatethenovelgenesandregulationmechanismsrelatedtocarotenoidbiosynthesisinplants

Carotenoid accumulation is cooperatively controlled at multiple levelsincluding developmentalprogramsenvironmentalfactorsand metabolicsignalsTranscriptionfactorsplayimportantroleinregulatingcarotenoidbiosynthesisHoweveronlyafewtranscriptionfactorsinvolvedincarotenoidbiosynthesisareidentifiedandtranscriptionregulationismainlyrelatedtoexpressionofPSYMoreovermostofthesetranscriptionfactorsexerttheirinfluencesviaregulatingfruitripeningnotspecificcarotenoidbiosynthesisＧrelated genesTheinteracting partners oftranscriptionfactorsinvolvedincarotenoidmetabolicnetworkalsoremaintobeidentifiedPostＧtranscriptionalregulationalternativeRNAsplicingepigeneticmodificationandmiRNAareofimportanceinplantgrowthanddevelopmentandresponsetoabioticstressHoweverlittleinformationregardingtheinvolvementofthesemechanismsinregulating carotenoid metabolism in planteven in Arabidopsisis available Application ofphytohormonescontributestoregulatecarotenoidcontentand maintainfruitqualityinagricultureandpostharvesttreatmentThemechanismunderlyingregulationofcarotenoidmetabolismbyphytohormonesespeciallycrossＧtalkamongdifferentphytohormonesarestillfarfrombeingunderstoodInthefuturestudiesbetterunderstandingofcarotenoid metabolismandregulationinfruitswillnotonlyhaveanimportantimpactongeneticimprovementandpostharvesttreatmentbutalsowillstrengthenknowledgeofcarotenoidregulationinplants

Acknowledgements

ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(GrantNos３１７７２０４１３１３２２０４４and３１５０１５４５)ScienceandTechnologyPlanningProjectofGuangdongProvince(GrantNo２０１５B０９０９０１０５８)ScienceandTechnologyPlanningProjectofGuangzhou (GrantNo２０１６０４０２００４８)andTalentProgramofGuangdongProvince(No２０１４TX０１N０４９)

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TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

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６２　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

PhytohormonesplaycrucialrolesinfruitripeningwhichhasbeenshowntoaffectcarotenoidaccumulationinfruitsMajorprogressregardingtheinvolvementofphytohormonesinregulatingcarotenoidbiosynthesishasbeenachievedinfruits

Ethyleneplaysa centralrolein climactericfruitripeningTherole ofethylenein carotenoidaccumulationinclimactericfruitshasbeenwidelystudiedIntomatoethyleneinitiatesfruitripeningresultinginarapidcolorshiftfromgreentoredwithincreasedlycopeneaccumulationanddecreasedβＧxanthophyllsandchlorophyllscontentsTheroleofethyleneinregulatingcarotenoidbiosynthesisduringtomatofruitripeninginvolvesacomplexregulatorynetworkoftranscriptionfactorsRINasamasterregulatorbindstothepromotersofgenesinvolvedinfruitripeningprocessesincludingcarotenoidbiosynthesis[４８４９７３]APETALA２a(AP２a)isamemberofAP２ERFsuperfamilywhichregulatestomatofruitripeningbyregulatingethylenebiosynthesisandsignalingRepressionofAP２abyRNAinterference (RNAi)resultsin decreasedlevels ofphytoeneandlycopenebut higherβＧcaroteneaccumulationconsistentwithdownＧregulatedexpressionofPDSCtRＧb２andCtrlSOandupＧregulatedexpressionofZEP１MoreoverseveralripeningＧrelatedregulatorsRIPENINGＧINHIBITOR (RIN)NONＧRIPENING (NOR)andCOLORLESSNONＧRIPENING (CNR)functionupstreamofAP２aandpositivelyregulateitsexpression[７４]SlERF６anothermemberofAP２ERFsuperfamilyisanegativeregulatorofcarotenoidaccumulationReducedexpressionofSlERF６byRNAienhancedbothcarotenoidandethylenelevelsduringfruitripening[７５]InadditionthreeothertranscriptionfactorsarerelatedtotheethylenepathwayincludingTAGL１FRUITFULL１and２whichhavebeenreportedtopositivelyregulatecarotenoidaccumulationduringtomatoripening[７６mdash７８]

Auxinisinvolvedincellexpansionanddivisiontissuedifferentiationorgandevelopmentandarangeofphysiologicalprocess[７９]Recentlyincreasingevidencesshowthatauxinalsoplaysanimportantroleinregulatingfruitripening[８０]TheleveloffreeIAA (themostabundantauxin)tendstodeclinepriortotheonsetoftomatofruitripening[８１]AuxinnegativelycontrolscarotenoidaccumulationintomatofruitExogenousIAA treatmentsignificantlyreduceslycopeneaccumulationbutenhancesthelevelsofneoxanthinandviolaxanthinaccompaniedbydownＧregulatedexpressionofPsy１Psy３PdsZisoandCrtisoandupＧregulatedexpressionofβＧLcy１andCrtrＧβ１ [８２]Howeverwhetherauxindirectlyregulatesthegenesincarotenoidpathwayremainsunknown

Abscisicacid (ABA)isa key hormoneinvolvedintuningresponsestoabioticstressesLittleinformationisavailableabouttheinvolvementofABAinregulatingcarotenoidaccumulationduringtomatofruitripeningABA hasbeenreportedto beimplicatedinfruitripeningandinfluencecarotenoidaccumulationintomato[８３]andstrawberry[８４]fruit

JAssuchasmethyljasmonicacidjasmonicacidandotherderivativesareplantendogenoushormones[８５]JAsalsoplayimportantrolesinfruitripeningLietalreportedthatJAinduceethyleneproductionbyMdMYC２ＧmediatedandMdERF３ＧmediatedupregulationofMdACS１gene[８６]Applicationofmethyljasmonate(MeJA)increasestheaccumulationofanthocyaninβＧcarotenecontentsandseveralphenoliccompounds[８７]LiuetalfurtherilluminatedtheroleofJAinregulatingcarotenoidaccumulationduringtomatofruitripeningwithJAＧdeficientmutants(spr２anddef１)anda３５∷prosystransgenicline(３５∷prosyswithincreasedJAlevelsandconstitutiveJAsignaling)andfoundthatlycopeneaccumulationissignificantlyinhibitedinspr２anddef１fruitbutenhancedin３５S∷prosysfruitaccompaniedbyasimilartrendofexpressionoflycopenebiosyntheticgenes[８８]Inadditionethyleneproductionisdepressedinspr２anddef１fruitbutincreasedin３５S∷prosysfruitMoreovertheexogenousapplicationofMeJAtoNeverripe (Nr)an ethyleneＧinsensitive mutantresultsin enhancedlycopene accumulation andexpressionoflycopenebiosyntheticgenes [８８]TheseresultsindicatedthatJA promoteslycopenebiosynthesisinamannerindependentofethylene

７　Futureresearchdirections

　CarotenoidmetabolismandregulationhavebeenwidelyresearchedinplantsHoweverthecarotenoidＧ

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SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６３　　　

relatedstudieshavebeenmostlyfocusedonmodelspeciessuchasArabidopsisandtomatoThemolecularmechanismsunderlyingcarotenoid metabolism andregulationin otherfruitspeciesarestillpoorlyunderstoodConsideringthediversityofcarotenoidsinfruitsitisnecessarytoinvestigatethenovelgenesandregulationmechanismsrelatedtocarotenoidbiosynthesisinplants

Carotenoid accumulation is cooperatively controlled at multiple levelsincluding developmentalprogramsenvironmentalfactorsand metabolicsignalsTranscriptionfactorsplayimportantroleinregulatingcarotenoidbiosynthesisHoweveronlyafewtranscriptionfactorsinvolvedincarotenoidbiosynthesisareidentifiedandtranscriptionregulationismainlyrelatedtoexpressionofPSYMoreovermostofthesetranscriptionfactorsexerttheirinfluencesviaregulatingfruitripeningnotspecificcarotenoidbiosynthesisＧrelated genesTheinteracting partners oftranscriptionfactorsinvolvedincarotenoidmetabolicnetworkalsoremaintobeidentifiedPostＧtranscriptionalregulationalternativeRNAsplicingepigeneticmodificationandmiRNAareofimportanceinplantgrowthanddevelopmentandresponsetoabioticstressHoweverlittleinformationregardingtheinvolvementofthesemechanismsinregulating carotenoid metabolism in planteven in Arabidopsisis available Application ofphytohormonescontributestoregulatecarotenoidcontentand maintainfruitqualityinagricultureandpostharvesttreatmentThemechanismunderlyingregulationofcarotenoidmetabolismbyphytohormonesespeciallycrossＧtalkamongdifferentphytohormonesarestillfarfrombeingunderstoodInthefuturestudiesbetterunderstandingofcarotenoid metabolismandregulationinfruitswillnotonlyhaveanimportantimpactongeneticimprovementandpostharvesttreatmentbutalsowillstrengthenknowledgeofcarotenoidregulationinplants

Acknowledgements

ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(GrantNos３１７７２０４１３１３２２０４４and３１５０１５４５)ScienceandTechnologyPlanningProjectofGuangdongProvince(GrantNo２０１５B０９０９０１０５８)ScienceandTechnologyPlanningProjectofGuangzhou (GrantNo２０１６０４０２００４８)andTalentProgramofGuangdongProvince(No２０１４TX０１N０４９)

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[６５]AlvarezDVossBMaassDetalCarotenogenesisisregulatedby５1049011UTRＧmediatedtranslationofphytoenesynthasesplicevariantsPlantPhysiology２０１６１７２２３１４mdash２３２６

[６６]KaurSSpillaneCReductionincarotenoidlevelsinthemarinediatomPhaeodactylumtricornutum byartificialmicroRNAstargetedagainsttheendogenousphytoenesynthasegeneMarineBiotechnology２０１５１７１mdash７

[６７]BaiCRiveraSMMedinaVetalAninvitrosystemfortherapidfunctionalcharacterizationofgenesinvolvedincarotenoidbiosynthesisandaccumulationPlantJournal２０１４７７４６４mdash４７５

[６８]KimSHAhnYOAhnMJetalCloningandcharacterizationofanOrangegenethatincreasescarotenoidaccumulationandsaltstresstoleranceintransgenicsweetpotatoculturesPlantPhysiologyandBiochemistry２０１３７０４４５mdash４５４

[６９]ZhouXWelschRYang YetalArabidopsisORproteinsarethemajorposttranscriptionalregulatorsofphytoenesynthaseincontrollingcarotenoidbiosynthesisProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１５１１２３５５８mdash

３５６３[７０]WelschRZhouXYuanHetalClpproteaseandORdirectlycontroltheproteostasisofphytoenesynthasethecrucialenzymefor

carotenoidbiosynthesisinArabidopsisMolecularPlant２０１８１１１４９mdash１６２

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６６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[７１]PulidoPToledoＧOrtizGPhillipsMAetalArabidopsisJＧProteinJ２０deliversthefirstenzymeoftheplastidialisoprenoidpathwaytoproteinqualitycontrolPlantCell２０１３２５４１８３mdash４１９４

[７２]PrasannaVPrabhaTNTharanathanRNFruitripeningphenomenamdashAnoverviewCriticalReviewsinFoodScienceandNutrition

２００７４７１mdash１９[７３]FujisawaMShimaYHiguchiNetalDirecttargetsofthetomatoＧripeningregulatorRINidentifiedbytranscriptomeandchromatin

immunoprecipitationanalysesPlanta２０１２２３５１１０７mdash１１２２[７４]KarlovaRRosinFMBusscherＧLangeJetalTranscriptomeandmetaboliteprofilingshowthatAPETALA２aisamajorregulatorof

tomatofruitripeningPlantCell２０１１２３９２３mdash９４１[７５]LeeJMJoungJGMcQuinnRetalCombinedtranscriptomegeneticdiversityandmetaboliteprofilingintomatofruitrevealsthatthe

ethyleneresponsefactorSlERF６playsanimportantroleinripeningandcarotenoidaccumulationPlantJournal２０１２７０１９１mdash２０４[７６]ShimaYFujisawaMKitagawaMetalTomatoFRUITFULLhomologsregulatefruitripeningviaethylenebiosynthesisBioscience

BiotechnologyandBiochemistry２０１４７８２３１mdash２３７[７７]VrebalovJPanILArroyoAJMetalFleshyfruitexpansionandripeningareregulatedbythetomatoSHATTERPROOFgene

TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

bullReviewsbull

SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６３　　　

relatedstudieshavebeenmostlyfocusedonmodelspeciessuchasArabidopsisandtomatoThemolecularmechanismsunderlyingcarotenoid metabolism andregulationin otherfruitspeciesarestillpoorlyunderstoodConsideringthediversityofcarotenoidsinfruitsitisnecessarytoinvestigatethenovelgenesandregulationmechanismsrelatedtocarotenoidbiosynthesisinplants

Carotenoid accumulation is cooperatively controlled at multiple levelsincluding developmentalprogramsenvironmentalfactorsand metabolicsignalsTranscriptionfactorsplayimportantroleinregulatingcarotenoidbiosynthesisHoweveronlyafewtranscriptionfactorsinvolvedincarotenoidbiosynthesisareidentifiedandtranscriptionregulationismainlyrelatedtoexpressionofPSYMoreovermostofthesetranscriptionfactorsexerttheirinfluencesviaregulatingfruitripeningnotspecificcarotenoidbiosynthesisＧrelated genesTheinteracting partners oftranscriptionfactorsinvolvedincarotenoidmetabolicnetworkalsoremaintobeidentifiedPostＧtranscriptionalregulationalternativeRNAsplicingepigeneticmodificationandmiRNAareofimportanceinplantgrowthanddevelopmentandresponsetoabioticstressHoweverlittleinformationregardingtheinvolvementofthesemechanismsinregulating carotenoid metabolism in planteven in Arabidopsisis available Application ofphytohormonescontributestoregulatecarotenoidcontentand maintainfruitqualityinagricultureandpostharvesttreatmentThemechanismunderlyingregulationofcarotenoidmetabolismbyphytohormonesespeciallycrossＧtalkamongdifferentphytohormonesarestillfarfrombeingunderstoodInthefuturestudiesbetterunderstandingofcarotenoid metabolismandregulationinfruitswillnotonlyhaveanimportantimpactongeneticimprovementandpostharvesttreatmentbutalsowillstrengthenknowledgeofcarotenoidregulationinplants

Acknowledgements

ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(GrantNos３１７７２０４１３１３２２０４４and３１５０１５４５)ScienceandTechnologyPlanningProjectofGuangdongProvince(GrantNo２０１５B０９０９０１０５８)ScienceandTechnologyPlanningProjectofGuangzhou (GrantNo２０１６０４０２００４８)andTalentProgramofGuangdongProvince(No２０１４TX０１N０４９)

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[６９]ZhouXWelschRYang YetalArabidopsisORproteinsarethemajorposttranscriptionalregulatorsofphytoenesynthaseincontrollingcarotenoidbiosynthesisProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１５１１２３５５８mdash

３５６３[７０]WelschRZhouXYuanHetalClpproteaseandORdirectlycontroltheproteostasisofphytoenesynthasethecrucialenzymefor

carotenoidbiosynthesisinArabidopsisMolecularPlant２０１８１１１４９mdash１６２

bullReviewsbull

６６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[７１]PulidoPToledoＧOrtizGPhillipsMAetalArabidopsisJＧProteinJ２０deliversthefirstenzymeoftheplastidialisoprenoidpathwaytoproteinqualitycontrolPlantCell２０１３２５４１８３mdash４１９４

[７２]PrasannaVPrabhaTNTharanathanRNFruitripeningphenomenamdashAnoverviewCriticalReviewsinFoodScienceandNutrition

２００７４７１mdash１９[７３]FujisawaMShimaYHiguchiNetalDirecttargetsofthetomatoＧripeningregulatorRINidentifiedbytranscriptomeandchromatin

immunoprecipitationanalysesPlanta２０１２２３５１１０７mdash１１２２[７４]KarlovaRRosinFMBusscherＧLangeJetalTranscriptomeandmetaboliteprofilingshowthatAPETALA２aisamajorregulatorof

tomatofruitripeningPlantCell２０１１２３９２３mdash９４１[７５]LeeJMJoungJGMcQuinnRetalCombinedtranscriptomegeneticdiversityandmetaboliteprofilingintomatofruitrevealsthatthe

ethyleneresponsefactorSlERF６playsanimportantroleinripeningandcarotenoidaccumulationPlantJournal２０１２７０１９１mdash２０４[７６]ShimaYFujisawaMKitagawaMetalTomatoFRUITFULLhomologsregulatefruitripeningviaethylenebiosynthesisBioscience

BiotechnologyandBiochemistry２０１４７８２３１mdash２３７[７７]VrebalovJPanILArroyoAJMetalFleshyfruitexpansionandripeningareregulatedbythetomatoSHATTERPROOFgene

TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

bullReviewsbull

６４　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[１４]SinghBSinghJPKaurAetalBioactivecompoundsinbananaandtheirassociatedhealthbenefitsmdashAreviewFoodChemistry２０１６

２０６１mdash１１[１５]AubertCChalotGChemicalcompositionbioactivecompoundsandvolatilesofsixtablegrapevarieties(Vitisvinifera L)Food

Chemistry２０１８２４０５２４mdash５３３[１６]ZhengHZhangQQuanJetalDeterminationofsugarsorganicacidsaromacomponentsandcarotenoidsingrapefruitpulpsFood

Chemistry２０１６２０５１１２mdash１２１[１７]FanciullinoALDhuiqueＧMayerCLuroFetalCarotenoiddiversityincultivatedcitrusishighlyinfluencedbygeneticfactorsJournal

ofAgriculturalandFoodChemistry２００６５４４３９７mdash４４０６[１８]KatoMIkomaYMatsumotoHetalAccumulationofcarotenoidsandexpressionofcarotenoidbiosyntheticgenesduringmaturation

incitrusfruitPlantPhysiology２００４１３４８２４mdash８３７[１９]LuPJWangCYYinTTetalCytologicalandmolecularcharacterizationofcarotenoidaccumulationinnormalandhighＧlycopene

mutantorangesScientificReports２０１７７[２０]AmpomahＧDwamenaCMcGhieTWibisono RetalThekiwifruitlycopenebetaＧcyclaseplaysasignificantroleincarotenoid

accumulationinfruitJournalofExperimentalBotany２００９６０３７６５mdash３７７９[２１]AjilaCMRaoLJRaoUJSPCharacterizationofbioactivecompoundsfromrawandripeMangiferaindicaLpeelextractsFoodand

ChemicalToxicology２０１０４８３４０６mdash３４１１[２２]TuanPAKimJKParkNIetalCarotenoidcontentandexpressionofphytoenesynthaseandphytoenedesaturasegenesinbittermelon

(Momordicacharantia)FoodChemistry２０１１１２６１６８６mdash１６９２[２３]SchweiggertRMSteingassCBHellerAetalCharacterizationofchromoplastsandcarotenoidsofredＧandyellowＧfleshedpapaya

(CaricapapayaL)Planta２０１１２３４１０３１mdash１０４４[２４]AbushitaAADaoodHGBiacsPAChangeincarotenoidsandantioxidantvitaminsintomatoasafunctionofvarietalandtechnological

factorsJournalofAgriculturalandFoodChemistry２０００４８２０７５mdash２０８１[２５]LvPLiNLiuHetalChangesincarotenoidprofilesandintheexpressionpatternofthegenesincarotenoidmetabolismsduringfruit

developmentandripeninginfourwatermeloncultivarsFoodChemistry２０１５１７４５２mdash５９[２６]Liu CZhang HDaiZetalVolatilechemicalandcarotenoidprofilesin watermelonsCitrullusvulgaris (Thunb)Schrad

(Cucurbitaceae)withdifferentfleshcolorsFoodScienceandBiotechnology２０１２２１５３１mdash５４１[２７]AlquezarBRodrigoMJLadoJetalAcomparativephysiologicalandtranscriptionalstudyofcarotenoidbiosynthesisinwhiteandred

grapefruit(CitrusparadisiMacf)TreeGeneticsamp Genomes２０１３９１２５７mdash１２６９[２８]KatoMMechanismofcarotenoidaccumulationincitrusfruitJournaloftheJapaneseSocietyforHorticulturalScience２０１２８１２１９mdash

２３３[２９]IsaacsonTRonenGZamirDetalCloningoftangerinefromtomatorevealsacarotenoidisomeraseessentialfortheproductionofbetaＧ

caroteneandxanthophyllsinplantsPlantCell２００２１４３３３mdash３４２[３０]RonenGCohenMZamirDetalRegulationofcarotenoidbiosynthesisduringtomatofruitdevelopmentExpressionofthegenefor

lycopeneepsilonＧcyclaseisdownＧregulatedduringripeningandiselevatedinthemutantDeltaPlantJournal１９９９１７３４１mdash３５１[３１]RonenGCarmelＧGorenLZamirDetalAnalternativepathwaytobetaＧcaroteneformationinplantchromoplastsdiscoveredbymapＧ

basedcloningofBetaandoldＧgoldcolormutationsintomatoProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０００９７１１１０２mdash１１１０７

[３２]HorneroＧMendezDdeGuevaraRGLMinguezＧMosqueraMICarotenoidbiosynthesischangesinfiveredpepper(CapsicumannuumL)

cultivarsduringripeningCultivarselectionforbreedingJournalofAgriculturalandFoodChemistry２０００４８３８５７mdash３８６４[３３]GuzmanIHambySRomeroJetalVariabilityofcarotenoidbiosynthesisinorangecoloredCapsicumsppPlantScience２０１０１７９

４９mdash５９[３４]RodriguezＧUribeLGuzmanIRajapakseWetalCarotenoidaccumulationinorangeＧpigmentedCapsicumannuumfruitregulatedat

multiplelevelsJournalofExperimentalBotany２０１２６３５１７mdash５２６[３５]SunTYuanHCaoHetalCarotenoidmetabolisminplantstheroleofplastidsMolecularPlant２０１８１１５８mdash７４[３６]BramleyPMRegulationofcarotenoidformationduringtomatofruitripeninganddevelopmentJournalofExperimentalBotany２００２

５３２１０７mdash２１１３[３７]EstevezJMCanteroAReindlAetal１ＧdeoxyＧDＧxyluloseＧ５Ｇphosphatesynthasealimitingenzymeforplastidicisoprenoidbiosynthesis

inplantsJournalofBiologicalChemistry２００１２７６２２９０１mdash２２９０９[３８]BotellaＧPaviaPBesumbes OPhillips MAetalRegulationofcarotenoidbiosynthesisinplantsevidenceforakeyroleof

hydroxymethylbutenyldiphosphatereductaseincontrollingthesupplyofplastidialisoprenoidprecursorsPlantJournal２００４４０１８８mdash

１９９[３９]CazzonelliCIPogsonBJSourcetosinkregulationofcarotenoidbiosynthesisinplantsTrendsinPlantScience２０１０１５２６６mdash２７４[４０]FraserPDEnfissiEMAHalketJMetalManipulationofphytoenelevelsintomatofruiteffectsonisoprenoidsplastidsand

intermediarymetabolismPlantCell２００７１９３１９４mdash３２１１[４１]FraserPDRomerSKianoJWetalElevationofcarotenoidsintomatobygeneticmanipulationJournaloftheScienceofFoodand

Agriculture２００１８１８２２mdash８２７[４２]RayJMoureauPBirdCetalCloningandcharacterizaitonofageneinvolvedinphytoenesynthesisfromtomatoPlantMolecular

Biology１９９２１９４０１mdash４０４

bullReviewsbull

SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６５　　　

[４３]PengGWangCSongSetalTheroleof１ＧdeoxyＧDＧxyluloseＧ５ＧphosphatesynthaseandphytoenesynthasegenefamilyincitruscarotenoidaccumulationPlantPhysiologyandBiochemistry２０１３７１６７mdash７６

[４４]ZhaoDZhouCTaoJCarotenoidaccumulationandcarotenogenicgenesexpressionduringtwotypesofpersimmonfruit(DiospyroskakiL)developmentPlantMolecularBiologyReporter２０１１２９６４６mdash６５４

[４５]MlalaziBWelschRNamanyaPetalIsolationandfunctionalcharacterisationofbananaphytoenesynthasegenesaspotentialcisgenesPlanta２０１２２３６１５８５mdash１５９８

[４６]NeumanHGalpazNCunningham FXetalThetomatomutationnxd１revealsagenenecessaryforneoxanthinbiosynthesisanddemonstratesthatviolaxanthinisasufficientprecursorforabscisicacidbiosynthesisPlantJournal２０１４７８８０mdash９３

[４７]VrebalovJRuezinskyDPadmanabhanVetalA MADSＧboxgenenecessaryforfruitripeningatthetomatoripeningＧinhibitor(Rin)

locusScience２００２２９６３４３mdash３４６[４８]MartelCVrebalovJTafelmeyerPetalThetomato MADSＧBoxtranscriptionfactorRIPENINGINHIBITORinteractswith

promotersinvolvedinnumerousripeningprocessesinaCOLORLESSNONRIPENINGＧdependentmannerPlantPhysiology２０１１１５７

１５６８mdash１５７９[４９]Fujisawa MNakanoTShimaYetalAlargeＧscaleidentificationofdirecttargetsofthetomato MADSBoxtranscriptionfactor

RIPENINGINHIBITORrevealstheregulationoffruitripeningPlantCell２０１３２５３７１mdash３８６[５０]DubosCStrackeRGrotewoldEetalMYBtranscriptionfactorsinArabidopsisTrendsinPlantScience２０１０１５５７３mdash５８１[５１]ZhuFLuoTLiuCetalAnR２R３ＧMYBtranscriptionfactorrepressesthetransformationofalphaＧandbetaＧbranchcarotenoidsby

negativelyregulatingexpressionofCrBCH２andCrNCED５inflavedoofCitrusreticulateNewPhytologist２０１７２１６１７８mdash１９２[５２]SagawaJMStanleyLELaFountainAMetalAnR２R３ＧMYBtranscriptionfactorregulatescarotenoidpigmentationinMimuluslewisii

flowersNewPhytologist２０１６２０９１０４９mdash１０５７[５３]JaakolaLNewinsightsintotheregulationofanthocyaninbiosynthesisinfruitsTrendsinPlantScience２０１３１８４７７mdash４８２[５４]JiangGYanHWuFetalLitchifruitLcNAC１isatargetofLcMYC２andregulatoroffruitsenescencethroughitsinteractionwith

LcWRKY１PlantandCellPhysiology２０１７５８１０７５mdash１０８９[５５]MengCYangDMaXetalSuppressionoftomatoSlNAC１transcriptionfactordelaysfruitripeningJournalofPlantPhysiology

２０１６１９３８８mdash９６[５６]ShanWKuangJFChenLetalMolecularcharacterizationofbananaNACtranscriptionfactorsandtheirinteractionswithethylene

signallingcomponentEILduringfruitripeningJournalofExperimentalBotany２０１２６３５１７１mdash５１８７[５７]ZhuMChenGZhouSetalAnewtomatoNAC (NAMATAF１２CUC２)transcriptionfactorSlNAC４functionsasapositive

regulatoroffruitripeningandcarotenoidaccumulationPlantandCellPhysiology２０１４５５１１９mdash１３５[５８]FuCCHanYCKuangJFetalPapayaCpEIN３aandCpNAC２cooperativelyregulatecarotenoidbiosynthesisrelatedgenesCpPDS２

４CpLCYＧeandCpCHYＧbduringfruitripeningPlantandCellPhysiology２０１７５８２１５５mdash２１６５[５９]LuoZZhangJLiJetalASTAYＧGREENproteinSlSGR１regulateslycopeneandbetaＧcaroteneaccumulationbyinteractingdirectly

withSlPSY１duringripeningprocessesintomatoNewPhytologist２０１３１９８４４２mdash４５２[６０]ToledoＧOrtizGHuqERodriguezＧConcepcionMDirectregulationofphytoenesynthasegeneexpressionandcarotenoidbiosynthesisby

phytochromeＧinteractingfactorsProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１０１０７１１６２６mdash

１１６３１[６１]WelschRMaassDVoegelTetalTranscriptionfactorRAP２２anditsinteractingpartnerSINAT２Stableelementsinthe

carotenogenesisofArabidopsisleavesPlantPhysiology２００７１４５１０７３mdash１０８５[６２]EndoTFujiiHSugiyamaAetalOverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor (CubHLH１)whichis

homologoustoArabidopsisactivationＧtaggedbri１suppressor１interactingfactorgenesmodulatescarotenoidmetabolismintransgenictomatoPlantScience２０１６２４３３５mdash４８

[６３]LiuLJiaCZhang MetalEctopicexpressionofaBZR１Ｇ１DtranscriptionfactorinbrassinosteroidsignallingenhancescarotenoidaccumulationandfruitqualityattributesintomatoPlantBiotechnologyJournal２０１４１２１０５mdash１１５

[６４]CazzonelliCICuttrissAJCossettoSBetalRegulationofcarotenoidcompositionandshootbranchinginarabidopsisbyachromatinmodifyinghistonemethyltransferaseSDG８PlantCell２００９２１３９mdash５３

[６５]AlvarezDVossBMaassDetalCarotenogenesisisregulatedby５1049011UTRＧmediatedtranslationofphytoenesynthasesplicevariantsPlantPhysiology２０１６１７２２３１４mdash２３２６

[６６]KaurSSpillaneCReductionincarotenoidlevelsinthemarinediatomPhaeodactylumtricornutum byartificialmicroRNAstargetedagainsttheendogenousphytoenesynthasegeneMarineBiotechnology２０１５１７１mdash７

[６７]BaiCRiveraSMMedinaVetalAninvitrosystemfortherapidfunctionalcharacterizationofgenesinvolvedincarotenoidbiosynthesisandaccumulationPlantJournal２０１４７７４６４mdash４７５

[６８]KimSHAhnYOAhnMJetalCloningandcharacterizationofanOrangegenethatincreasescarotenoidaccumulationandsaltstresstoleranceintransgenicsweetpotatoculturesPlantPhysiologyandBiochemistry２０１３７０４４５mdash４５４

[６９]ZhouXWelschRYang YetalArabidopsisORproteinsarethemajorposttranscriptionalregulatorsofphytoenesynthaseincontrollingcarotenoidbiosynthesisProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１５１１２３５５８mdash

３５６３[７０]WelschRZhouXYuanHetalClpproteaseandORdirectlycontroltheproteostasisofphytoenesynthasethecrucialenzymefor

carotenoidbiosynthesisinArabidopsisMolecularPlant２０１８１１１４９mdash１６２

bullReviewsbull

６６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[７１]PulidoPToledoＧOrtizGPhillipsMAetalArabidopsisJＧProteinJ２０deliversthefirstenzymeoftheplastidialisoprenoidpathwaytoproteinqualitycontrolPlantCell２０１３２５４１８３mdash４１９４

[７２]PrasannaVPrabhaTNTharanathanRNFruitripeningphenomenamdashAnoverviewCriticalReviewsinFoodScienceandNutrition

２００７４７１mdash１９[７３]FujisawaMShimaYHiguchiNetalDirecttargetsofthetomatoＧripeningregulatorRINidentifiedbytranscriptomeandchromatin

immunoprecipitationanalysesPlanta２０１２２３５１１０７mdash１１２２[７４]KarlovaRRosinFMBusscherＧLangeJetalTranscriptomeandmetaboliteprofilingshowthatAPETALA２aisamajorregulatorof

tomatofruitripeningPlantCell２０１１２３９２３mdash９４１[７５]LeeJMJoungJGMcQuinnRetalCombinedtranscriptomegeneticdiversityandmetaboliteprofilingintomatofruitrevealsthatthe

ethyleneresponsefactorSlERF６playsanimportantroleinripeningandcarotenoidaccumulationPlantJournal２０１２７０１９１mdash２０４[７６]ShimaYFujisawaMKitagawaMetalTomatoFRUITFULLhomologsregulatefruitripeningviaethylenebiosynthesisBioscience

BiotechnologyandBiochemistry２０１４７８２３１mdash２３７[７７]VrebalovJPanILArroyoAJMetalFleshyfruitexpansionandripeningareregulatedbythetomatoSHATTERPROOFgene

TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

bullReviewsbull

SCIENCEFOUNDATIONINCHINA　　Vol２６No１２０１８ ６５　　　

[４３]PengGWangCSongSetalTheroleof１ＧdeoxyＧDＧxyluloseＧ５ＧphosphatesynthaseandphytoenesynthasegenefamilyincitruscarotenoidaccumulationPlantPhysiologyandBiochemistry２０１３７１６７mdash７６

[４４]ZhaoDZhouCTaoJCarotenoidaccumulationandcarotenogenicgenesexpressionduringtwotypesofpersimmonfruit(DiospyroskakiL)developmentPlantMolecularBiologyReporter２０１１２９６４６mdash６５４

[４５]MlalaziBWelschRNamanyaPetalIsolationandfunctionalcharacterisationofbananaphytoenesynthasegenesaspotentialcisgenesPlanta２０１２２３６１５８５mdash１５９８

[４６]NeumanHGalpazNCunningham FXetalThetomatomutationnxd１revealsagenenecessaryforneoxanthinbiosynthesisanddemonstratesthatviolaxanthinisasufficientprecursorforabscisicacidbiosynthesisPlantJournal２０１４７８８０mdash９３

[４７]VrebalovJRuezinskyDPadmanabhanVetalA MADSＧboxgenenecessaryforfruitripeningatthetomatoripeningＧinhibitor(Rin)

locusScience２００２２９６３４３mdash３４６[４８]MartelCVrebalovJTafelmeyerPetalThetomato MADSＧBoxtranscriptionfactorRIPENINGINHIBITORinteractswith

promotersinvolvedinnumerousripeningprocessesinaCOLORLESSNONRIPENINGＧdependentmannerPlantPhysiology２０１１１５７

１５６８mdash１５７９[４９]Fujisawa MNakanoTShimaYetalAlargeＧscaleidentificationofdirecttargetsofthetomato MADSBoxtranscriptionfactor

RIPENINGINHIBITORrevealstheregulationoffruitripeningPlantCell２０１３２５３７１mdash３８６[５０]DubosCStrackeRGrotewoldEetalMYBtranscriptionfactorsinArabidopsisTrendsinPlantScience２０１０１５５７３mdash５８１[５１]ZhuFLuoTLiuCetalAnR２R３ＧMYBtranscriptionfactorrepressesthetransformationofalphaＧandbetaＧbranchcarotenoidsby

negativelyregulatingexpressionofCrBCH２andCrNCED５inflavedoofCitrusreticulateNewPhytologist２０１７２１６１７８mdash１９２[５２]SagawaJMStanleyLELaFountainAMetalAnR２R３ＧMYBtranscriptionfactorregulatescarotenoidpigmentationinMimuluslewisii

flowersNewPhytologist２０１６２０９１０４９mdash１０５７[５３]JaakolaLNewinsightsintotheregulationofanthocyaninbiosynthesisinfruitsTrendsinPlantScience２０１３１８４７７mdash４８２[５４]JiangGYanHWuFetalLitchifruitLcNAC１isatargetofLcMYC２andregulatoroffruitsenescencethroughitsinteractionwith

LcWRKY１PlantandCellPhysiology２０１７５８１０７５mdash１０８９[５５]MengCYangDMaXetalSuppressionoftomatoSlNAC１transcriptionfactordelaysfruitripeningJournalofPlantPhysiology

２０１６１９３８８mdash９６[５６]ShanWKuangJFChenLetalMolecularcharacterizationofbananaNACtranscriptionfactorsandtheirinteractionswithethylene

signallingcomponentEILduringfruitripeningJournalofExperimentalBotany２０１２６３５１７１mdash５１８７[５７]ZhuMChenGZhouSetalAnewtomatoNAC (NAMATAF１２CUC２)transcriptionfactorSlNAC４functionsasapositive

regulatoroffruitripeningandcarotenoidaccumulationPlantandCellPhysiology２０１４５５１１９mdash１３５[５８]FuCCHanYCKuangJFetalPapayaCpEIN３aandCpNAC２cooperativelyregulatecarotenoidbiosynthesisrelatedgenesCpPDS２

４CpLCYＧeandCpCHYＧbduringfruitripeningPlantandCellPhysiology２０１７５８２１５５mdash２１６５[５９]LuoZZhangJLiJetalASTAYＧGREENproteinSlSGR１regulateslycopeneandbetaＧcaroteneaccumulationbyinteractingdirectly

withSlPSY１duringripeningprocessesintomatoNewPhytologist２０１３１９８４４２mdash４５２[６０]ToledoＧOrtizGHuqERodriguezＧConcepcionMDirectregulationofphytoenesynthasegeneexpressionandcarotenoidbiosynthesisby

phytochromeＧinteractingfactorsProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１０１０７１１６２６mdash

１１６３１[６１]WelschRMaassDVoegelTetalTranscriptionfactorRAP２２anditsinteractingpartnerSINAT２Stableelementsinthe

carotenogenesisofArabidopsisleavesPlantPhysiology２００７１４５１０７３mdash１０８５[６２]EndoTFujiiHSugiyamaAetalOverexpressionofacitrusbasichelixＧloopＧhelixtranscriptionfactor (CubHLH１)whichis

homologoustoArabidopsisactivationＧtaggedbri１suppressor１interactingfactorgenesmodulatescarotenoidmetabolismintransgenictomatoPlantScience２０１６２４３３５mdash４８

[６３]LiuLJiaCZhang MetalEctopicexpressionofaBZR１Ｇ１DtranscriptionfactorinbrassinosteroidsignallingenhancescarotenoidaccumulationandfruitqualityattributesintomatoPlantBiotechnologyJournal２０１４１２１０５mdash１１５

[６４]CazzonelliCICuttrissAJCossettoSBetalRegulationofcarotenoidcompositionandshootbranchinginarabidopsisbyachromatinmodifyinghistonemethyltransferaseSDG８PlantCell２００９２１３９mdash５３

[６５]AlvarezDVossBMaassDetalCarotenogenesisisregulatedby５1049011UTRＧmediatedtranslationofphytoenesynthasesplicevariantsPlantPhysiology２０１６１７２２３１４mdash２３２６

[６６]KaurSSpillaneCReductionincarotenoidlevelsinthemarinediatomPhaeodactylumtricornutum byartificialmicroRNAstargetedagainsttheendogenousphytoenesynthasegeneMarineBiotechnology２０１５１７１mdash７

[６７]BaiCRiveraSMMedinaVetalAninvitrosystemfortherapidfunctionalcharacterizationofgenesinvolvedincarotenoidbiosynthesisandaccumulationPlantJournal２０１４７７４６４mdash４７５

[６８]KimSHAhnYOAhnMJetalCloningandcharacterizationofanOrangegenethatincreasescarotenoidaccumulationandsaltstresstoleranceintransgenicsweetpotatoculturesPlantPhysiologyandBiochemistry２０１３７０４４５mdash４５４

[６９]ZhouXWelschRYang YetalArabidopsisORproteinsarethemajorposttranscriptionalregulatorsofphytoenesynthaseincontrollingcarotenoidbiosynthesisProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica２０１５１１２３５５８mdash

３５６３[７０]WelschRZhouXYuanHetalClpproteaseandORdirectlycontroltheproteostasisofphytoenesynthasethecrucialenzymefor

carotenoidbiosynthesisinArabidopsisMolecularPlant２０１８１１１４９mdash１６２

bullReviewsbull

６６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[７１]PulidoPToledoＧOrtizGPhillipsMAetalArabidopsisJＧProteinJ２０deliversthefirstenzymeoftheplastidialisoprenoidpathwaytoproteinqualitycontrolPlantCell２０１３２５４１８３mdash４１９４

[７２]PrasannaVPrabhaTNTharanathanRNFruitripeningphenomenamdashAnoverviewCriticalReviewsinFoodScienceandNutrition

２００７４７１mdash１９[７３]FujisawaMShimaYHiguchiNetalDirecttargetsofthetomatoＧripeningregulatorRINidentifiedbytranscriptomeandchromatin

immunoprecipitationanalysesPlanta２０１２２３５１１０７mdash１１２２[７４]KarlovaRRosinFMBusscherＧLangeJetalTranscriptomeandmetaboliteprofilingshowthatAPETALA２aisamajorregulatorof

tomatofruitripeningPlantCell２０１１２３９２３mdash９４１[７５]LeeJMJoungJGMcQuinnRetalCombinedtranscriptomegeneticdiversityandmetaboliteprofilingintomatofruitrevealsthatthe

ethyleneresponsefactorSlERF６playsanimportantroleinripeningandcarotenoidaccumulationPlantJournal２０１２７０１９１mdash２０４[７６]ShimaYFujisawaMKitagawaMetalTomatoFRUITFULLhomologsregulatefruitripeningviaethylenebiosynthesisBioscience

BiotechnologyandBiochemistry２０１４７８２３１mdash２３７[７７]VrebalovJPanILArroyoAJMetalFleshyfruitexpansionandripeningareregulatedbythetomatoSHATTERPROOFgene

TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent

bullReviewsbull

６６　　　 Vol２６No１２０１８　　SCIENCEFOUNDATIONINCHINA

[７１]PulidoPToledoＧOrtizGPhillipsMAetalArabidopsisJＧProteinJ２０deliversthefirstenzymeoftheplastidialisoprenoidpathwaytoproteinqualitycontrolPlantCell２０１３２５４１８３mdash４１９４

[７２]PrasannaVPrabhaTNTharanathanRNFruitripeningphenomenamdashAnoverviewCriticalReviewsinFoodScienceandNutrition

２００７４７１mdash１９[７３]FujisawaMShimaYHiguchiNetalDirecttargetsofthetomatoＧripeningregulatorRINidentifiedbytranscriptomeandchromatin

immunoprecipitationanalysesPlanta２０１２２３５１１０７mdash１１２２[７４]KarlovaRRosinFMBusscherＧLangeJetalTranscriptomeandmetaboliteprofilingshowthatAPETALA２aisamajorregulatorof

tomatofruitripeningPlantCell２０１１２３９２３mdash９４１[７５]LeeJMJoungJGMcQuinnRetalCombinedtranscriptomegeneticdiversityandmetaboliteprofilingintomatofruitrevealsthatthe

ethyleneresponsefactorSlERF６playsanimportantroleinripeningandcarotenoidaccumulationPlantJournal２０１２７０１９１mdash２０４[７６]ShimaYFujisawaMKitagawaMetalTomatoFRUITFULLhomologsregulatefruitripeningviaethylenebiosynthesisBioscience

BiotechnologyandBiochemistry２０１４７８２３１mdash２３７[７７]VrebalovJPanILArroyoAJMetalFleshyfruitexpansionandripeningareregulatedbythetomatoSHATTERPROOFgene

TAGL１PlantCell２００９２１３０４１mdash３０６２[７８]WangSLuGHouZetalMembersofthetomatoFRUITFULL MADSＧboxfamilyregulatestyleabscissionandfruitripening

JournalofExperimentalBotany２０１４６５３００５mdash３０１４[７９]HagenGAuxinsignaltransductionEssaysinBiochemistry２０１５５８１mdash１２[８０]PanLZengWNiuLetalPpYUC１１astrongcandidategeneforthestonyhardphenotypeinpeach(PrunuspersicaLBatsch)

participatesinIAAbiosynthesisduringfruitripeningJournalofExperimentalBotany２０１５６６７０３１mdash７０４４[８１]BoettcherCKeyzersRABossPKetalSequestrationofauxinbytheindoleＧ３ＧaceticacidＧamidosynthetaseGH３Ｇ１ingrapeberry(Vitis

viniferaL)andtheproposedroleofauxinconjugationduringripeningJournalofExperimentalBotany２０１０６１３６１５mdash３６２５[８２]SuLDirettoGPurgattoEetalCarotenoidaccumulationduringtomatofruitripeningismodulatedbytheauxinＧethylenebalance

BMCPlantBiology２０１５１５[８３]WengLZhaoFLiRetalThezincfingertranscriptionfactorSlZFP２negativelyregulatesabscisicacidbiosynthesisandfruitripening

intomatoPlantPhysiology２０１５１６７９３１mdash９４９[８４]JiaHFChaiYMLiCLetalAbscisicacidplaysanimportantroleintheregulationofstrawberryfruitripeningPlantPhysiology

２０１１１５７１８８mdash１９９[８５]CreelmanRAMulletJEBiosynthesisandactionofjasmonatesinplantsAnnualReviewofPlantPhysiologyandPlantMolecular

Biology１９９７４８３５５mdash３８１[８６]LiTXuYZhangLetalThejasmonateＧactivatedtranscriptionfactorMdMYC２regulatesETHYLENERESPONSEFACTORand

ethylenebiosyntheticgenestopromoteethylenebiosynthesisduringapplefruitripeningPlantCell２０１７２９１３１６mdash１３３４[８７]RudellDRMattheisJPFanXetalMethyljasmonateenhancesanthocyaninaccumulationandmodifiesproductionofphenolicsand

pigmentsinlsquoFujirsquoapplesJournaloftheAmericanSocietyforHorticulturalScience２００２１２７４３５mdash４４１[８８]LiuLWeiJZhang MetalEthyleneindependentinductionoflycopenebiosynthesisintomatofruitsbyjasmonatesJournalof

ExperimentalBotany２０１２６３５７５１mdash５７６１

DuanXuewu

ProfDuanXuewureceivedhisPhDdegreefromtheGraduateSchoolof

ChineseAcademyofSciencesin２００４Heiscurrentlyaprofessorof

South China Botanical GardenChinese Academy ofSciencesHis

researchinterestsincludebiochemistryandmolecularbiologyinrelation

to ripeningsenescence and deterioration of postharvestfruits and

vegetablesespeciallytranscriptionalregulationandposttranscriptional

modificationanddevelopmentofstorageandhandlingtechniquesin

subtropicalandtropicalfruitHewasthePrincipalInvestigatorofmore

than２０projectsfromthegovernmentUptonowhehaspublishedmorethan９０papersandhasbeen

patented２９inventionpatentsincludinganUSApatent