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ppdb plant promoter database version 30Ayaka Hieno1 Hushna Ara Naznin1 Mitsuro Hyakumachi12 Tetsuya Sakurai3
Mututomo Tokizawa1 Hiroyuki Koyama12 Naoki Sato4 Tomoaki Nishiyama5
Mitsuyasu Hasebe67 Andreas D Zimmer8 Daniel Lang8 Ralf Reski8 Stefan
A Rensing9 Junichi Obokata10 and Yoshiharu Y Yamamoto123
1The United Graduate School of Agricultural Science Gifu University 1-1 Yanagido Gifu City Gifu 501-1193Japan 2Faculty of Applied Biological Sciences Gifu University 1-1 Yanagido Gifu City Gifu 501-1193 Japan3Center for Sustainable Resource Science RIKEN Yokohama Institute 1-7-22 Suehiro-cho Tsurumi-kuYokohama Kanagawa 230-0045 Japan 4Graduate School of Arts and Sciences The University of Tokyo 3-8-1Komaba Meguro-ku Tokyo 153-8902 Japan 5Advanced Science Research Center Kanazawa UniversityTakaramachi 13-1 Kanazawa City Ishikawa 920-0934 Japan 6National Institute for Basic Biology Nishigonaka38 Myodaiji Okazaki City Aichi 444-8585 Japan 7Department of Basic Biology School of Life ScienceGraduate University for Advanced Studies Okazaki 444-8585 Japan 8Faculty of Biology University ofFreiburg Schanzlestrasse 1 D79104 Freiburg Germany 9Plant Cell Biology Faculty of Biology University ofMarburg Karl-von-Frisch-Strasse 9 35043 Marburg Germany and 10Graduate School of Environmental LifeScience Kyoto Prefectural University 1-5 Hangi-cho Shimogamo Sakyo-ku Kyoto 606-8522 Japan
Received September 9 2013 Revised and Accepted October 8 2013
ABSTRACT
ppdb (httpppdbagrgifu-uacjp) is a plant pro-moter database that provides information on tran-scription start sites (TSSs) core promoter structure(TATA boxes Initiators Y Patches GA and CAelements) and regulatory element groups (REGs) asputative and comprehensive transcriptional regula-tory elements Since the last report in this journal thedatabase has been updated in three areas to version30 First new genomes have been included in thedatabase and now ppdb provides information onArabidopsis thaliana rice Physcomitrella patensand poplar Second new TSS tag data (34 million)from A thaliana determined by a high throughputsequencer has been added to give a 200-foldincrease in TSS data compared with version 10This results in a much higher coverage of 27 000A thaliana genes and finer positioning of promoterseven for genes with low expression levels Thirdmicroarray data-based predictions have beenappended as REG annotations which inform theirputative physiological roles
INTRODUCTION
Gene regulation is a central part of morphogenesis andenvironmental adaptation of higher plants and it iscontrolled by the promoter of each gene Therefore
understanding of promoter structure is crucial to under-stand these fundamental processes of plants
There are three aspects to promoter structure (i) theposition direction and strength of the transcription startsites (TSSs) that indicate actual promoter position (ii) thetype and position of the core promoter elements such asTATA boxes and Initiators (Inrs) that are thought to bethe major determinants of the direction and position ofpromoters and (iii) the type and position of transcriptionalregulatory elements that are involved in gene regulation
In our last report (1) we introduced the plant promoterdatabase (ppdb) which provided promoter informationabout TSS clusters core promoter elements [TATAboxes Inrs Y Patches GA and CA elements (23)] andregulatory element groups [REGs putative position-sensitive transcriptional regulatory elements that are ex-tracted by local distribution of short sequences (LDSS)analysis (2)] as putative and comprehensive sets of tran-scriptional regulatory elements The database of theoriginal version 10 contained information of two plantspecies Arabidopsis thaliana and rice
MAJOR EXTENSIONS FROM VERSION 10
The major amendment in version 30 is the addition ofthe Physcomitrella patens and poplar genomes to thedatabase The sources used for the information of thefour genomes including A thaliana and rice are shownin Table 1 The promoter elements of the moss genomehave been extracted by the LDSS method (2) During
To whom correspondence should be addressed Tel +81 58 293 2848 Email yyygifu-uacjp
D1188ndashD1192 Nucleic Acids Research 2014 Vol 42 Database issue Published online 4 November 2013doi101093nargkt1027
The Author(s) 2013 Published by Oxford University PressThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (httpcreativecommonsorglicensesby30) whichpermits unrestricted reuse distribution and reproduction in any medium provided the original work is properly cited
extraction we noticed that considerable numbers of mossgenes are driven by a similar type of promoter that islocated within long terminal repeats These promotersaffect the extraction process due to tight sequence conser-vation that is not related to promoter function and for thisreason they were excluded from the LDSS analysisA thaliana promoter elements have been applied to thepoplar genome because the Brassicaceae and Malpighialesare phylogenetically close
A new function called lsquoHomologue Gene Searchrsquo hasbeen added to facilitate the comparison of promoter struc-tures of orthologous genes within a species or betweendifferent species Orthologue groups have been determinedby Gclust a system that classifies orthologues accordingto the presence or absence of protein motifs (16)
New A thaliana TSS data of 34 million tags whichcorresponds to a 200-fold increase in the previousdata have been added (Figure 1) REG annotationshave also been appended and show functional predictionsbased on microarray data of responses to plant hormones(AUX auxin BR brassinosteroid CK cytokinin ABAabscisic acid ET ethylene JA jasmonic acid SA salicylicacid) responses to a hormone-like chemical (H2O2) and
some environmental stress-related responses (droughtDREB1A overexpression) (7) Functional annotation of53 of 308 REGs is now available in version 30 (Figure 2)
BROWSING PROMOTER STRUCTURE
The major function of ppdb is to give an indication of apossible promoter structure for each gene in a genomebased on the established lists of LDSS-positive elementsThe information can be directly called by the gene ID(eg AT1G67090 or Os01g0791600) or selected from alist of lsquoKeyword Searchrsquo or lsquoHomologue Gene SearchrsquoPages for individual genes show the following informa-tion (i) DNA sequence (ii) TSS distribution (directionand strength at a 1-bp resolution) (iii) core promoterstructure and (iv) REG dataAt the sequence window promoter elements including
REGs and core elements are highlighted in a position-dependent manner as the default setting Care should betaken that promoters without any TSS information do notshow any elements as default For an indication of thepromoter elements of these genes the lsquoReliablersquo buttonshould be clicked which changes the state to lsquoAllrsquo
Table 1 Source of ppdb version 30
Specification Source Size
A thalianaGenome sequenceand gene annotation
TAIR9 httpwwwarabidopsisorg (4)
TSS information Selected RAFL cDNA httprargegscrikenjp (5) 62 108 (clonesa)Cap signature CT-MPSS tags (3) 158 237 (tagsb)Oligo-Cap Illumina data Tokizawa M Yamanaka H
Koyama H Sakurai TKurotani A Shinozaki K Suzuki YSugano S Obokata JYamamoto YY (unpublished data)
34 206 936 (tagsb)
Promoter elements A thaliana LDSS-positive octamers (23) 659 (octamersc)Annotation for LDSS elements PLACE httpwwwdnaaffrcgojpPLACE (6) 21 (only matched
motifsd)Annotation for LDSS elements
stress and hormonal responses(7) 53 (only matched
motifsc)Rice (Oryza sativa)
Genome sequenceand gene annotation
RGSP build 40 httprapdblabnigacjp (8) mdash
TSS information Carefully selected fl-cDNA (from KOME) httpcdna01dnaaffrcgojpcDNA (9) 17 286 (clonesa)Promoter elements Rice LDSS-positive octamers (210) 660 (octamersc)
Annotation for LDSS elements PLACE httpwwwdnaaffrcgojpPLACE (6) 4 (only matchedmotifsd)
Moss (P patens)Genome sequenceand gene annotation
JGI version 11 COSMOSS V16 httpwwwcosmosorg (1112) mdash
TSS information 50 CAGE (13) 1 122 382 (tagsb)Promoter elements P patens LDSS-positive octamers This work 198 (octamersc)
Poplar (Populus trichocarpa)Genome sequenceand gene annotation
Phytozome6 httpwwwphytozomenetpoplar (14) mdash
TSS information FL-cDNA info from GenBank (15) 15 256 (clonesaBP921855ndash937111)
36 103 (clonesaDB874873ndash910976)
Promoter elements A thaliana LDSS-positive octamers (23) 659 (octamersc)Orthologue gene
Orthologue group Gclust (16) 336 689 (familiese)
aclone number btag number cnumber of octamer sequences dnumber of motifs and enumber of orthologue families
Nucleic Acids Research 2014 Vol 42 Database issue D1189
(Figure 1 red arrow) This button is a toggle switchbetween lsquoReliablersquo and lsquoAllrsquo lsquoReliablersquo is a defaultsetting where only elements at appropriate positionsrelative to the peak TSS are detected The setting lsquoAllrsquoremoves the positional restriction as an indication ofpromoter elements allowing global detection The sensi-tive area in the lsquoReliablersquo mode for each element group isdescribed on the front page of the databaseThe lsquoTSS tag distributionrsquo columns in the lsquoFocused
viewrsquo provide the expressional strength of each TSS Theexpression is the sum of six TSS tag libraries that areprepared from leaves roots inflorescences etiolated seed-lings and shoots from low light-grown and high light-grown seedlings
The lsquoCore promoter informationrsquo table shows thepresence or absence of core promoter elements (TATAboxes Inrs Y Patches GA and CA elements)
The lsquoREG informationrsquo table shows a REG list togetherwith the corresponding PPDB motifs (23) and PLACEmotifs (6) REG sequences as well as PPDB and PLACEmotifs are linked to other pages containing biological in-formation New REG annotations forA thaliana obtainedfrom predicted cis-regulatory elements based on micro-array data (7) have been included (Figure 2)
Selection of the lsquoAllrsquo button (Figure 1) adds anothercategory lsquoNot Reliable Promoter Summaryrsquo belowlsquoOther Reliable Promoter Summaryrsquo This category canbe used when searching for regulatory elements (REGs)
Figure 1 Indication of individual promoters An Arabidopsis gene AT1G027801 is shown The information is composed of five panels lsquoSummaryof Genersquo lsquoOverviewrsquo lsquoFocused viewrsquo and also lsquoPromoter Summaryrsquo (not shown) and lsquoOther Reliable Promoter Summaryrsquo (not shown) The top TSS(TSS Peak) is shown in the second column of the lsquoFocused viewrsquo as white letters on a red background New TSS tag data (34 million) are shown atthe bottom of lsquoFocused viewrsquo highlighted in a red rectangle with rounded corners
D1190 Nucleic Acids Research 2014 Vol 42 Database issue
Figure 2 REG information REG information of the AT5G523101 (RD29A) promoter is shown REG annotations added in version 30 arehighlighted in a red rectangle with rounded corners
Nucleic Acids Research 2014 Vol 42 Database issue D1191
from wider regions or when there is no TSS informationon the promoter of interest
ADDITIONAL PAGES
A whole list of REGs for each of the genomes can beviewed by selecting a cell in the table of lsquoIndex of Genesrsquoat the top of the page The lists present the relationshipsbetween REG ID sequence PPDB motifs PLACE motifsand also functional annotations Selection of a specificREG entry leads to lsquoSummary of the REGrsquo and lsquoEntrySequencesrsquo that show the whole gene lists containing thecorresponding REG together with gene annotations
ACKNOWLEDGEMENTS
We would like to acknowledge Mr Takeaki Taniguchi ofMitsubisi Research Institute for excellent technical assist-ance We also appreciate Dr Dong Nguyen Tien and MrHirokazu Murakami for maintenance of the database
FUNDING
Grant-in-Aid for Scientific Research on Priority AreaslsquoComparative Genomicsrsquo (in part) (to YYY and JO)Scientific Research on Priority Areas lsquoPerceptive Plantsrsquo(in part) (to YYY) Grant-in-Aid for Publication ofScientific Research Results lsquoDatabasesrsquo (in part) (to JOand YYY) from the Ministry of Education CultureSports Science and Technology of Japan AdvancedLow Carbon Technology Research and DevelopmentProgram from Japan Science and Technology Agency(JST ALCA) (in part) (to YYY) Funding for openaccess charge Ministry of Education Culture SportsScience and Technology Japan
Conflict of interest statement None declared
REFERENCES
1 YamamotoYY and ObokataJ (2008) ppdb a plant promoterdatabase Nucleic Acids Res 36 D977ndashD981
2 YamamotoYY IchidaH MatsuiM ObokataJ SakuraiTSatouM SekiM ShinozakiK and AbeT (2007) Identificationof plant promoter constituents by analysis of local distribution ofshort sequences BMC Genomics 8 67
3 YamamotoYY YoshitsuguT SakuraiT SekiMShinozakiK and ObokataJ (2009) Heterogeneity of Arabidopsis
core promoters revealed by high density TSS analysis Plant J60 350ndash362
4 LameschP BerardiniTZ LiD SwarbreckD WilksCSasidharanR MullerR DreherK AlexanderDL Garcia-HernandezM et al (2012) The Arabidopsis InformationResource (TAIR) improved gene annotation and new toolsNucleic Acids Res 40 D1202ndashD1210
5 SekiM NarusakaM KamiyaA IshidaJ SatouMSakuraiT NakajimaM EnjuA AkiyamaK OonoY et al(2002) Functional annotation of a full-length Arabidopsis cDNAcollection Science 296 141ndash145
6 HigoK UgawaY IwamotoM and KorenagaT (1999) Plantcis-acting regulatory DNA elements (PLACE) database 1999Nucleic Acids Res 27 297ndash300
7 YamamotoYY YoshiokaY HyakumachiM MaruyamaKYamaguchi-ShinozakiK TokizawaM and KoyamaH (2011)Prediction of transcriptional regulatory elements for planthormone responses based on microarray data BMC Plant Biol11 39
8 International_Rice_Genome_Sequencing_Project (2005) Themap-based sequence of the rice genome Nature 436 793ndash800
9 KikuchiS SatohK NagataT KawagashiraN DoiKKishimotoN YazakiJ IshikawaM YamadaH OokaHet al (2003) Collection mapping and annotation of over 28000cDNA clones from japonica rice Science 301 376ndash379
10 YamamotoYY IchidaH AbeT SuzukiY SuganoS andObokataJ (2007) Differentiation of core promoter architecturebetween plants and mammals revealed by LDSS analysis NucleicAcids Res 35 6219ndash6226
11 RensingSA LangD ZimmerAD TerryA SalamovAShapiroH NishiyamaT PerroudPF LindquistEA KamisugiYet al (2008) The Physcomitrella genome reveals evolutionary insightsinto the conquest of land by plants Science 319 64ndash69
12 ZimmerAD LangD BuchtaK RombautsS NishiyamaTHasebeM Van de PeerY RensingSA and ReskiR (2013)Reannotation and extended community resources for the genomeof the non-seed plant Physcomitrella patens provide insights intothe evolution of plant gene structures and functions BMCGenomics 14 498
13 NishiyamaT MiyawakiK OhshimaM ThompsonKNagashimaA HasebeM and KurataT (2012) Digital geneexpression profiling by 5rsquo-end sequencing of cDNAs duringreprogramming in the moss Physcomitrella patens PLoS ONE 7e36471
14 TuskanGA DifazioS JanssonS BohlmannJ GrigorievIHellstenU PutnamN RalphS RombautsS SalamovA et al(2006) The genome of black cottonwood Populus trichocarpa(Torr amp Gray) Science 313 1596ndash1604
15 NanjoT SakuraiT TotokiY ToyodaA NishiguchiMKadoT IgasakiT FutamuraN SekiM SakakiY et al(2007) Functional annotation of 19841 Populus nigra full-lengthenriched cDNA clones BMC Genomics 8 448
16 SatoN (2009) Gclust trans-kingdom classification of proteinsusing automatic individual threshold setting Bioinformatics 25599ndash605
D1192 Nucleic Acids Research 2014 Vol 42 Database issue
extraction we noticed that considerable numbers of mossgenes are driven by a similar type of promoter that islocated within long terminal repeats These promotersaffect the extraction process due to tight sequence conser-vation that is not related to promoter function and for thisreason they were excluded from the LDSS analysisA thaliana promoter elements have been applied to thepoplar genome because the Brassicaceae and Malpighialesare phylogenetically close
A new function called lsquoHomologue Gene Searchrsquo hasbeen added to facilitate the comparison of promoter struc-tures of orthologous genes within a species or betweendifferent species Orthologue groups have been determinedby Gclust a system that classifies orthologues accordingto the presence or absence of protein motifs (16)
New A thaliana TSS data of 34 million tags whichcorresponds to a 200-fold increase in the previousdata have been added (Figure 1) REG annotationshave also been appended and show functional predictionsbased on microarray data of responses to plant hormones(AUX auxin BR brassinosteroid CK cytokinin ABAabscisic acid ET ethylene JA jasmonic acid SA salicylicacid) responses to a hormone-like chemical (H2O2) and
some environmental stress-related responses (droughtDREB1A overexpression) (7) Functional annotation of53 of 308 REGs is now available in version 30 (Figure 2)
BROWSING PROMOTER STRUCTURE
The major function of ppdb is to give an indication of apossible promoter structure for each gene in a genomebased on the established lists of LDSS-positive elementsThe information can be directly called by the gene ID(eg AT1G67090 or Os01g0791600) or selected from alist of lsquoKeyword Searchrsquo or lsquoHomologue Gene SearchrsquoPages for individual genes show the following informa-tion (i) DNA sequence (ii) TSS distribution (directionand strength at a 1-bp resolution) (iii) core promoterstructure and (iv) REG dataAt the sequence window promoter elements including
REGs and core elements are highlighted in a position-dependent manner as the default setting Care should betaken that promoters without any TSS information do notshow any elements as default For an indication of thepromoter elements of these genes the lsquoReliablersquo buttonshould be clicked which changes the state to lsquoAllrsquo
Table 1 Source of ppdb version 30
Specification Source Size
A thalianaGenome sequenceand gene annotation
TAIR9 httpwwwarabidopsisorg (4)
TSS information Selected RAFL cDNA httprargegscrikenjp (5) 62 108 (clonesa)Cap signature CT-MPSS tags (3) 158 237 (tagsb)Oligo-Cap Illumina data Tokizawa M Yamanaka H
Koyama H Sakurai TKurotani A Shinozaki K Suzuki YSugano S Obokata JYamamoto YY (unpublished data)
34 206 936 (tagsb)
Promoter elements A thaliana LDSS-positive octamers (23) 659 (octamersc)Annotation for LDSS elements PLACE httpwwwdnaaffrcgojpPLACE (6) 21 (only matched
motifsd)Annotation for LDSS elements
stress and hormonal responses(7) 53 (only matched
motifsc)Rice (Oryza sativa)
Genome sequenceand gene annotation
RGSP build 40 httprapdblabnigacjp (8) mdash
TSS information Carefully selected fl-cDNA (from KOME) httpcdna01dnaaffrcgojpcDNA (9) 17 286 (clonesa)Promoter elements Rice LDSS-positive octamers (210) 660 (octamersc)
Annotation for LDSS elements PLACE httpwwwdnaaffrcgojpPLACE (6) 4 (only matchedmotifsd)
Moss (P patens)Genome sequenceand gene annotation
JGI version 11 COSMOSS V16 httpwwwcosmosorg (1112) mdash
TSS information 50 CAGE (13) 1 122 382 (tagsb)Promoter elements P patens LDSS-positive octamers This work 198 (octamersc)
Poplar (Populus trichocarpa)Genome sequenceand gene annotation
Phytozome6 httpwwwphytozomenetpoplar (14) mdash
TSS information FL-cDNA info from GenBank (15) 15 256 (clonesaBP921855ndash937111)
36 103 (clonesaDB874873ndash910976)
Promoter elements A thaliana LDSS-positive octamers (23) 659 (octamersc)Orthologue gene
Orthologue group Gclust (16) 336 689 (familiese)
aclone number btag number cnumber of octamer sequences dnumber of motifs and enumber of orthologue families
Nucleic Acids Research 2014 Vol 42 Database issue D1189
(Figure 1 red arrow) This button is a toggle switchbetween lsquoReliablersquo and lsquoAllrsquo lsquoReliablersquo is a defaultsetting where only elements at appropriate positionsrelative to the peak TSS are detected The setting lsquoAllrsquoremoves the positional restriction as an indication ofpromoter elements allowing global detection The sensi-tive area in the lsquoReliablersquo mode for each element group isdescribed on the front page of the databaseThe lsquoTSS tag distributionrsquo columns in the lsquoFocused
viewrsquo provide the expressional strength of each TSS Theexpression is the sum of six TSS tag libraries that areprepared from leaves roots inflorescences etiolated seed-lings and shoots from low light-grown and high light-grown seedlings
The lsquoCore promoter informationrsquo table shows thepresence or absence of core promoter elements (TATAboxes Inrs Y Patches GA and CA elements)
The lsquoREG informationrsquo table shows a REG list togetherwith the corresponding PPDB motifs (23) and PLACEmotifs (6) REG sequences as well as PPDB and PLACEmotifs are linked to other pages containing biological in-formation New REG annotations forA thaliana obtainedfrom predicted cis-regulatory elements based on micro-array data (7) have been included (Figure 2)
Selection of the lsquoAllrsquo button (Figure 1) adds anothercategory lsquoNot Reliable Promoter Summaryrsquo belowlsquoOther Reliable Promoter Summaryrsquo This category canbe used when searching for regulatory elements (REGs)
Figure 1 Indication of individual promoters An Arabidopsis gene AT1G027801 is shown The information is composed of five panels lsquoSummaryof Genersquo lsquoOverviewrsquo lsquoFocused viewrsquo and also lsquoPromoter Summaryrsquo (not shown) and lsquoOther Reliable Promoter Summaryrsquo (not shown) The top TSS(TSS Peak) is shown in the second column of the lsquoFocused viewrsquo as white letters on a red background New TSS tag data (34 million) are shown atthe bottom of lsquoFocused viewrsquo highlighted in a red rectangle with rounded corners
D1190 Nucleic Acids Research 2014 Vol 42 Database issue
Figure 2 REG information REG information of the AT5G523101 (RD29A) promoter is shown REG annotations added in version 30 arehighlighted in a red rectangle with rounded corners
Nucleic Acids Research 2014 Vol 42 Database issue D1191
from wider regions or when there is no TSS informationon the promoter of interest
ADDITIONAL PAGES
A whole list of REGs for each of the genomes can beviewed by selecting a cell in the table of lsquoIndex of Genesrsquoat the top of the page The lists present the relationshipsbetween REG ID sequence PPDB motifs PLACE motifsand also functional annotations Selection of a specificREG entry leads to lsquoSummary of the REGrsquo and lsquoEntrySequencesrsquo that show the whole gene lists containing thecorresponding REG together with gene annotations
ACKNOWLEDGEMENTS
We would like to acknowledge Mr Takeaki Taniguchi ofMitsubisi Research Institute for excellent technical assist-ance We also appreciate Dr Dong Nguyen Tien and MrHirokazu Murakami for maintenance of the database
FUNDING
Grant-in-Aid for Scientific Research on Priority AreaslsquoComparative Genomicsrsquo (in part) (to YYY and JO)Scientific Research on Priority Areas lsquoPerceptive Plantsrsquo(in part) (to YYY) Grant-in-Aid for Publication ofScientific Research Results lsquoDatabasesrsquo (in part) (to JOand YYY) from the Ministry of Education CultureSports Science and Technology of Japan AdvancedLow Carbon Technology Research and DevelopmentProgram from Japan Science and Technology Agency(JST ALCA) (in part) (to YYY) Funding for openaccess charge Ministry of Education Culture SportsScience and Technology Japan
Conflict of interest statement None declared
REFERENCES
1 YamamotoYY and ObokataJ (2008) ppdb a plant promoterdatabase Nucleic Acids Res 36 D977ndashD981
2 YamamotoYY IchidaH MatsuiM ObokataJ SakuraiTSatouM SekiM ShinozakiK and AbeT (2007) Identificationof plant promoter constituents by analysis of local distribution ofshort sequences BMC Genomics 8 67
3 YamamotoYY YoshitsuguT SakuraiT SekiMShinozakiK and ObokataJ (2009) Heterogeneity of Arabidopsis
core promoters revealed by high density TSS analysis Plant J60 350ndash362
4 LameschP BerardiniTZ LiD SwarbreckD WilksCSasidharanR MullerR DreherK AlexanderDL Garcia-HernandezM et al (2012) The Arabidopsis InformationResource (TAIR) improved gene annotation and new toolsNucleic Acids Res 40 D1202ndashD1210
5 SekiM NarusakaM KamiyaA IshidaJ SatouMSakuraiT NakajimaM EnjuA AkiyamaK OonoY et al(2002) Functional annotation of a full-length Arabidopsis cDNAcollection Science 296 141ndash145
6 HigoK UgawaY IwamotoM and KorenagaT (1999) Plantcis-acting regulatory DNA elements (PLACE) database 1999Nucleic Acids Res 27 297ndash300
7 YamamotoYY YoshiokaY HyakumachiM MaruyamaKYamaguchi-ShinozakiK TokizawaM and KoyamaH (2011)Prediction of transcriptional regulatory elements for planthormone responses based on microarray data BMC Plant Biol11 39
8 International_Rice_Genome_Sequencing_Project (2005) Themap-based sequence of the rice genome Nature 436 793ndash800
9 KikuchiS SatohK NagataT KawagashiraN DoiKKishimotoN YazakiJ IshikawaM YamadaH OokaHet al (2003) Collection mapping and annotation of over 28000cDNA clones from japonica rice Science 301 376ndash379
10 YamamotoYY IchidaH AbeT SuzukiY SuganoS andObokataJ (2007) Differentiation of core promoter architecturebetween plants and mammals revealed by LDSS analysis NucleicAcids Res 35 6219ndash6226
11 RensingSA LangD ZimmerAD TerryA SalamovAShapiroH NishiyamaT PerroudPF LindquistEA KamisugiYet al (2008) The Physcomitrella genome reveals evolutionary insightsinto the conquest of land by plants Science 319 64ndash69
12 ZimmerAD LangD BuchtaK RombautsS NishiyamaTHasebeM Van de PeerY RensingSA and ReskiR (2013)Reannotation and extended community resources for the genomeof the non-seed plant Physcomitrella patens provide insights intothe evolution of plant gene structures and functions BMCGenomics 14 498
13 NishiyamaT MiyawakiK OhshimaM ThompsonKNagashimaA HasebeM and KurataT (2012) Digital geneexpression profiling by 5rsquo-end sequencing of cDNAs duringreprogramming in the moss Physcomitrella patens PLoS ONE 7e36471
14 TuskanGA DifazioS JanssonS BohlmannJ GrigorievIHellstenU PutnamN RalphS RombautsS SalamovA et al(2006) The genome of black cottonwood Populus trichocarpa(Torr amp Gray) Science 313 1596ndash1604
15 NanjoT SakuraiT TotokiY ToyodaA NishiguchiMKadoT IgasakiT FutamuraN SekiM SakakiY et al(2007) Functional annotation of 19841 Populus nigra full-lengthenriched cDNA clones BMC Genomics 8 448
16 SatoN (2009) Gclust trans-kingdom classification of proteinsusing automatic individual threshold setting Bioinformatics 25599ndash605
D1192 Nucleic Acids Research 2014 Vol 42 Database issue
(Figure 1 red arrow) This button is a toggle switchbetween lsquoReliablersquo and lsquoAllrsquo lsquoReliablersquo is a defaultsetting where only elements at appropriate positionsrelative to the peak TSS are detected The setting lsquoAllrsquoremoves the positional restriction as an indication ofpromoter elements allowing global detection The sensi-tive area in the lsquoReliablersquo mode for each element group isdescribed on the front page of the databaseThe lsquoTSS tag distributionrsquo columns in the lsquoFocused
viewrsquo provide the expressional strength of each TSS Theexpression is the sum of six TSS tag libraries that areprepared from leaves roots inflorescences etiolated seed-lings and shoots from low light-grown and high light-grown seedlings
The lsquoCore promoter informationrsquo table shows thepresence or absence of core promoter elements (TATAboxes Inrs Y Patches GA and CA elements)
The lsquoREG informationrsquo table shows a REG list togetherwith the corresponding PPDB motifs (23) and PLACEmotifs (6) REG sequences as well as PPDB and PLACEmotifs are linked to other pages containing biological in-formation New REG annotations forA thaliana obtainedfrom predicted cis-regulatory elements based on micro-array data (7) have been included (Figure 2)
Selection of the lsquoAllrsquo button (Figure 1) adds anothercategory lsquoNot Reliable Promoter Summaryrsquo belowlsquoOther Reliable Promoter Summaryrsquo This category canbe used when searching for regulatory elements (REGs)
Figure 1 Indication of individual promoters An Arabidopsis gene AT1G027801 is shown The information is composed of five panels lsquoSummaryof Genersquo lsquoOverviewrsquo lsquoFocused viewrsquo and also lsquoPromoter Summaryrsquo (not shown) and lsquoOther Reliable Promoter Summaryrsquo (not shown) The top TSS(TSS Peak) is shown in the second column of the lsquoFocused viewrsquo as white letters on a red background New TSS tag data (34 million) are shown atthe bottom of lsquoFocused viewrsquo highlighted in a red rectangle with rounded corners
D1190 Nucleic Acids Research 2014 Vol 42 Database issue
Figure 2 REG information REG information of the AT5G523101 (RD29A) promoter is shown REG annotations added in version 30 arehighlighted in a red rectangle with rounded corners
Nucleic Acids Research 2014 Vol 42 Database issue D1191
from wider regions or when there is no TSS informationon the promoter of interest
ADDITIONAL PAGES
A whole list of REGs for each of the genomes can beviewed by selecting a cell in the table of lsquoIndex of Genesrsquoat the top of the page The lists present the relationshipsbetween REG ID sequence PPDB motifs PLACE motifsand also functional annotations Selection of a specificREG entry leads to lsquoSummary of the REGrsquo and lsquoEntrySequencesrsquo that show the whole gene lists containing thecorresponding REG together with gene annotations
ACKNOWLEDGEMENTS
We would like to acknowledge Mr Takeaki Taniguchi ofMitsubisi Research Institute for excellent technical assist-ance We also appreciate Dr Dong Nguyen Tien and MrHirokazu Murakami for maintenance of the database
FUNDING
Grant-in-Aid for Scientific Research on Priority AreaslsquoComparative Genomicsrsquo (in part) (to YYY and JO)Scientific Research on Priority Areas lsquoPerceptive Plantsrsquo(in part) (to YYY) Grant-in-Aid for Publication ofScientific Research Results lsquoDatabasesrsquo (in part) (to JOand YYY) from the Ministry of Education CultureSports Science and Technology of Japan AdvancedLow Carbon Technology Research and DevelopmentProgram from Japan Science and Technology Agency(JST ALCA) (in part) (to YYY) Funding for openaccess charge Ministry of Education Culture SportsScience and Technology Japan
Conflict of interest statement None declared
REFERENCES
1 YamamotoYY and ObokataJ (2008) ppdb a plant promoterdatabase Nucleic Acids Res 36 D977ndashD981
2 YamamotoYY IchidaH MatsuiM ObokataJ SakuraiTSatouM SekiM ShinozakiK and AbeT (2007) Identificationof plant promoter constituents by analysis of local distribution ofshort sequences BMC Genomics 8 67
3 YamamotoYY YoshitsuguT SakuraiT SekiMShinozakiK and ObokataJ (2009) Heterogeneity of Arabidopsis
core promoters revealed by high density TSS analysis Plant J60 350ndash362
4 LameschP BerardiniTZ LiD SwarbreckD WilksCSasidharanR MullerR DreherK AlexanderDL Garcia-HernandezM et al (2012) The Arabidopsis InformationResource (TAIR) improved gene annotation and new toolsNucleic Acids Res 40 D1202ndashD1210
5 SekiM NarusakaM KamiyaA IshidaJ SatouMSakuraiT NakajimaM EnjuA AkiyamaK OonoY et al(2002) Functional annotation of a full-length Arabidopsis cDNAcollection Science 296 141ndash145
6 HigoK UgawaY IwamotoM and KorenagaT (1999) Plantcis-acting regulatory DNA elements (PLACE) database 1999Nucleic Acids Res 27 297ndash300
7 YamamotoYY YoshiokaY HyakumachiM MaruyamaKYamaguchi-ShinozakiK TokizawaM and KoyamaH (2011)Prediction of transcriptional regulatory elements for planthormone responses based on microarray data BMC Plant Biol11 39
8 International_Rice_Genome_Sequencing_Project (2005) Themap-based sequence of the rice genome Nature 436 793ndash800
9 KikuchiS SatohK NagataT KawagashiraN DoiKKishimotoN YazakiJ IshikawaM YamadaH OokaHet al (2003) Collection mapping and annotation of over 28000cDNA clones from japonica rice Science 301 376ndash379
10 YamamotoYY IchidaH AbeT SuzukiY SuganoS andObokataJ (2007) Differentiation of core promoter architecturebetween plants and mammals revealed by LDSS analysis NucleicAcids Res 35 6219ndash6226
11 RensingSA LangD ZimmerAD TerryA SalamovAShapiroH NishiyamaT PerroudPF LindquistEA KamisugiYet al (2008) The Physcomitrella genome reveals evolutionary insightsinto the conquest of land by plants Science 319 64ndash69
12 ZimmerAD LangD BuchtaK RombautsS NishiyamaTHasebeM Van de PeerY RensingSA and ReskiR (2013)Reannotation and extended community resources for the genomeof the non-seed plant Physcomitrella patens provide insights intothe evolution of plant gene structures and functions BMCGenomics 14 498
13 NishiyamaT MiyawakiK OhshimaM ThompsonKNagashimaA HasebeM and KurataT (2012) Digital geneexpression profiling by 5rsquo-end sequencing of cDNAs duringreprogramming in the moss Physcomitrella patens PLoS ONE 7e36471
14 TuskanGA DifazioS JanssonS BohlmannJ GrigorievIHellstenU PutnamN RalphS RombautsS SalamovA et al(2006) The genome of black cottonwood Populus trichocarpa(Torr amp Gray) Science 313 1596ndash1604
15 NanjoT SakuraiT TotokiY ToyodaA NishiguchiMKadoT IgasakiT FutamuraN SekiM SakakiY et al(2007) Functional annotation of 19841 Populus nigra full-lengthenriched cDNA clones BMC Genomics 8 448
16 SatoN (2009) Gclust trans-kingdom classification of proteinsusing automatic individual threshold setting Bioinformatics 25599ndash605
D1192 Nucleic Acids Research 2014 Vol 42 Database issue
Figure 2 REG information REG information of the AT5G523101 (RD29A) promoter is shown REG annotations added in version 30 arehighlighted in a red rectangle with rounded corners
Nucleic Acids Research 2014 Vol 42 Database issue D1191
from wider regions or when there is no TSS informationon the promoter of interest
ADDITIONAL PAGES
A whole list of REGs for each of the genomes can beviewed by selecting a cell in the table of lsquoIndex of Genesrsquoat the top of the page The lists present the relationshipsbetween REG ID sequence PPDB motifs PLACE motifsand also functional annotations Selection of a specificREG entry leads to lsquoSummary of the REGrsquo and lsquoEntrySequencesrsquo that show the whole gene lists containing thecorresponding REG together with gene annotations
ACKNOWLEDGEMENTS
We would like to acknowledge Mr Takeaki Taniguchi ofMitsubisi Research Institute for excellent technical assist-ance We also appreciate Dr Dong Nguyen Tien and MrHirokazu Murakami for maintenance of the database
FUNDING
Grant-in-Aid for Scientific Research on Priority AreaslsquoComparative Genomicsrsquo (in part) (to YYY and JO)Scientific Research on Priority Areas lsquoPerceptive Plantsrsquo(in part) (to YYY) Grant-in-Aid for Publication ofScientific Research Results lsquoDatabasesrsquo (in part) (to JOand YYY) from the Ministry of Education CultureSports Science and Technology of Japan AdvancedLow Carbon Technology Research and DevelopmentProgram from Japan Science and Technology Agency(JST ALCA) (in part) (to YYY) Funding for openaccess charge Ministry of Education Culture SportsScience and Technology Japan
Conflict of interest statement None declared
REFERENCES
1 YamamotoYY and ObokataJ (2008) ppdb a plant promoterdatabase Nucleic Acids Res 36 D977ndashD981
2 YamamotoYY IchidaH MatsuiM ObokataJ SakuraiTSatouM SekiM ShinozakiK and AbeT (2007) Identificationof plant promoter constituents by analysis of local distribution ofshort sequences BMC Genomics 8 67
3 YamamotoYY YoshitsuguT SakuraiT SekiMShinozakiK and ObokataJ (2009) Heterogeneity of Arabidopsis
core promoters revealed by high density TSS analysis Plant J60 350ndash362
4 LameschP BerardiniTZ LiD SwarbreckD WilksCSasidharanR MullerR DreherK AlexanderDL Garcia-HernandezM et al (2012) The Arabidopsis InformationResource (TAIR) improved gene annotation and new toolsNucleic Acids Res 40 D1202ndashD1210
5 SekiM NarusakaM KamiyaA IshidaJ SatouMSakuraiT NakajimaM EnjuA AkiyamaK OonoY et al(2002) Functional annotation of a full-length Arabidopsis cDNAcollection Science 296 141ndash145
6 HigoK UgawaY IwamotoM and KorenagaT (1999) Plantcis-acting regulatory DNA elements (PLACE) database 1999Nucleic Acids Res 27 297ndash300
7 YamamotoYY YoshiokaY HyakumachiM MaruyamaKYamaguchi-ShinozakiK TokizawaM and KoyamaH (2011)Prediction of transcriptional regulatory elements for planthormone responses based on microarray data BMC Plant Biol11 39
8 International_Rice_Genome_Sequencing_Project (2005) Themap-based sequence of the rice genome Nature 436 793ndash800
9 KikuchiS SatohK NagataT KawagashiraN DoiKKishimotoN YazakiJ IshikawaM YamadaH OokaHet al (2003) Collection mapping and annotation of over 28000cDNA clones from japonica rice Science 301 376ndash379
10 YamamotoYY IchidaH AbeT SuzukiY SuganoS andObokataJ (2007) Differentiation of core promoter architecturebetween plants and mammals revealed by LDSS analysis NucleicAcids Res 35 6219ndash6226
11 RensingSA LangD ZimmerAD TerryA SalamovAShapiroH NishiyamaT PerroudPF LindquistEA KamisugiYet al (2008) The Physcomitrella genome reveals evolutionary insightsinto the conquest of land by plants Science 319 64ndash69
12 ZimmerAD LangD BuchtaK RombautsS NishiyamaTHasebeM Van de PeerY RensingSA and ReskiR (2013)Reannotation and extended community resources for the genomeof the non-seed plant Physcomitrella patens provide insights intothe evolution of plant gene structures and functions BMCGenomics 14 498
13 NishiyamaT MiyawakiK OhshimaM ThompsonKNagashimaA HasebeM and KurataT (2012) Digital geneexpression profiling by 5rsquo-end sequencing of cDNAs duringreprogramming in the moss Physcomitrella patens PLoS ONE 7e36471
14 TuskanGA DifazioS JanssonS BohlmannJ GrigorievIHellstenU PutnamN RalphS RombautsS SalamovA et al(2006) The genome of black cottonwood Populus trichocarpa(Torr amp Gray) Science 313 1596ndash1604
15 NanjoT SakuraiT TotokiY ToyodaA NishiguchiMKadoT IgasakiT FutamuraN SekiM SakakiY et al(2007) Functional annotation of 19841 Populus nigra full-lengthenriched cDNA clones BMC Genomics 8 448
16 SatoN (2009) Gclust trans-kingdom classification of proteinsusing automatic individual threshold setting Bioinformatics 25599ndash605
D1192 Nucleic Acids Research 2014 Vol 42 Database issue
from wider regions or when there is no TSS informationon the promoter of interest
ADDITIONAL PAGES
A whole list of REGs for each of the genomes can beviewed by selecting a cell in the table of lsquoIndex of Genesrsquoat the top of the page The lists present the relationshipsbetween REG ID sequence PPDB motifs PLACE motifsand also functional annotations Selection of a specificREG entry leads to lsquoSummary of the REGrsquo and lsquoEntrySequencesrsquo that show the whole gene lists containing thecorresponding REG together with gene annotations
ACKNOWLEDGEMENTS
We would like to acknowledge Mr Takeaki Taniguchi ofMitsubisi Research Institute for excellent technical assist-ance We also appreciate Dr Dong Nguyen Tien and MrHirokazu Murakami for maintenance of the database
FUNDING
Grant-in-Aid for Scientific Research on Priority AreaslsquoComparative Genomicsrsquo (in part) (to YYY and JO)Scientific Research on Priority Areas lsquoPerceptive Plantsrsquo(in part) (to YYY) Grant-in-Aid for Publication ofScientific Research Results lsquoDatabasesrsquo (in part) (to JOand YYY) from the Ministry of Education CultureSports Science and Technology of Japan AdvancedLow Carbon Technology Research and DevelopmentProgram from Japan Science and Technology Agency(JST ALCA) (in part) (to YYY) Funding for openaccess charge Ministry of Education Culture SportsScience and Technology Japan
Conflict of interest statement None declared
REFERENCES
1 YamamotoYY and ObokataJ (2008) ppdb a plant promoterdatabase Nucleic Acids Res 36 D977ndashD981
2 YamamotoYY IchidaH MatsuiM ObokataJ SakuraiTSatouM SekiM ShinozakiK and AbeT (2007) Identificationof plant promoter constituents by analysis of local distribution ofshort sequences BMC Genomics 8 67
3 YamamotoYY YoshitsuguT SakuraiT SekiMShinozakiK and ObokataJ (2009) Heterogeneity of Arabidopsis
core promoters revealed by high density TSS analysis Plant J60 350ndash362
4 LameschP BerardiniTZ LiD SwarbreckD WilksCSasidharanR MullerR DreherK AlexanderDL Garcia-HernandezM et al (2012) The Arabidopsis InformationResource (TAIR) improved gene annotation and new toolsNucleic Acids Res 40 D1202ndashD1210
5 SekiM NarusakaM KamiyaA IshidaJ SatouMSakuraiT NakajimaM EnjuA AkiyamaK OonoY et al(2002) Functional annotation of a full-length Arabidopsis cDNAcollection Science 296 141ndash145
6 HigoK UgawaY IwamotoM and KorenagaT (1999) Plantcis-acting regulatory DNA elements (PLACE) database 1999Nucleic Acids Res 27 297ndash300
7 YamamotoYY YoshiokaY HyakumachiM MaruyamaKYamaguchi-ShinozakiK TokizawaM and KoyamaH (2011)Prediction of transcriptional regulatory elements for planthormone responses based on microarray data BMC Plant Biol11 39
8 International_Rice_Genome_Sequencing_Project (2005) Themap-based sequence of the rice genome Nature 436 793ndash800
9 KikuchiS SatohK NagataT KawagashiraN DoiKKishimotoN YazakiJ IshikawaM YamadaH OokaHet al (2003) Collection mapping and annotation of over 28000cDNA clones from japonica rice Science 301 376ndash379
10 YamamotoYY IchidaH AbeT SuzukiY SuganoS andObokataJ (2007) Differentiation of core promoter architecturebetween plants and mammals revealed by LDSS analysis NucleicAcids Res 35 6219ndash6226
11 RensingSA LangD ZimmerAD TerryA SalamovAShapiroH NishiyamaT PerroudPF LindquistEA KamisugiYet al (2008) The Physcomitrella genome reveals evolutionary insightsinto the conquest of land by plants Science 319 64ndash69
12 ZimmerAD LangD BuchtaK RombautsS NishiyamaTHasebeM Van de PeerY RensingSA and ReskiR (2013)Reannotation and extended community resources for the genomeof the non-seed plant Physcomitrella patens provide insights intothe evolution of plant gene structures and functions BMCGenomics 14 498
13 NishiyamaT MiyawakiK OhshimaM ThompsonKNagashimaA HasebeM and KurataT (2012) Digital geneexpression profiling by 5rsquo-end sequencing of cDNAs duringreprogramming in the moss Physcomitrella patens PLoS ONE 7e36471
14 TuskanGA DifazioS JanssonS BohlmannJ GrigorievIHellstenU PutnamN RalphS RombautsS SalamovA et al(2006) The genome of black cottonwood Populus trichocarpa(Torr amp Gray) Science 313 1596ndash1604
15 NanjoT SakuraiT TotokiY ToyodaA NishiguchiMKadoT IgasakiT FutamuraN SekiM SakakiY et al(2007) Functional annotation of 19841 Populus nigra full-lengthenriched cDNA clones BMC Genomics 8 448
16 SatoN (2009) Gclust trans-kingdom classification of proteinsusing automatic individual threshold setting Bioinformatics 25599ndash605
D1192 Nucleic Acids Research 2014 Vol 42 Database issue
