Endophytic Fungi Researches in Indonesia Dwi Hartantidigilib.ump.ac.id/files/disk1/23/jhptump-ump-gdl-dwihartant-1105-1-48_pdfsa-c.pdf · 202, Kembaran, Banyumas, Jawa Tengah, Indonesia

Proceeding of The 1st University of Muhammadiyah Purwokerto - Pharmacy International Conference

5-6 June 2015, Horison Hotel Purwokerto ISBN 978-602-73538-0-0

42

Endophytic Fungi Researches in Indonesia

Dwi Hartanti

Faculty of Pharmacy, University of Muhammadiyah of Purwokerto, Jl. Raya Dukuhwaluh, PO Box

202, Kembaran, Banyumas, Jawa Tengah, Indonesia 53182

(E-mail: [email protected])

ABSTRACT

Endophytic fungi are those grow intra- or intercelullarly in the tissues of higher plants without

causing overt symptoms of disease, They have been known to produce various bioactive

secondary metabolites and have been studied widely for biosynthesis, biotransformations,

bioremediations, and enzyme productions. In this review, a considerable amount of works that

have been published on the endophytic fungi isolated from host plants collected in Indonesia is

reported. This review give an overview of the reported studies from the selection of host plants,

the isolated fungi, the screened bioactivity, and the bioactive metabolites of endophytic fungi

derived from Indonesian host plants,

Key words: Bioactive metabolites, bioactivity, endophytic fungi, host plant, Indonesia.

INTRODUCTION

Endophytic fungi are those grow intra- or intercelullarly in the tissues of higher plants without

causing overt symptoms of disease (Schulz and Boyle, 2006). They are ubiquitous and have been

isolated from almost all plants grown elsewhere, from tropical to boreal ecosystems. The

relationship between endophytic fungi and their host can be obligate or facultative. They exhibit

complex interactions with their hosts, the insects and another microorganisms (Arnold et al.,

2007; Banerjee, 2011; Estrada et al., 2012; Kusari et al., 2013; Nair and Padmavathy, 2014;

Rodriguez et al., 2009; Schulz et al., 1999; Shipunov et al., 2008). Plants strictly control the

growth of endophytes and the endophytes gradually adapt to their living environments, In order

to maintain stable symbiosis, endophytes participate in plant protection against pathogens

through producing certain metabolites, promoting growth of plants and helping them adapt

better to the environment (Brakhage and Schroeckh, 2011; Das and Varma, 2009; Dudeja et al.,

2012; Gao et al., 2010; Kane, 2012).

Endophytic fungi have been known to produce various bioactive secondary metabolites (Abrahão

et al., 2013; Alvin et al., 2014; Aly et al., 2010; Jalgaonwala et al., 2011; Joseph and Priya, 2011;

Kaul et al., 2012; Radic and Strukelj, 2012; Suryanarayanan, 2013; Yu et al., 2010). They also have

been studied widely for biosynthesis, biotransformations, bioremidiations and enzyme

productions (Cook et al., 2014; Khan and Doty, 2011; Kumar and Ahmad, 2013; Luo et al., 2013;

Molina et al., 2012; Pimentel et al., 2011; Robl et al., 2013; Stępniewska and Kuźniar, 2013; Verza



43

et al., 2009; Wang and Dai, 2010; Ying et al., 2014). This review aims to take a comprehensive

look at the progress of endophytic fungi research in Indonesia as April 2015.

HOST PLANTS

A specific rationale for the selection of plant for endophyte isolation is performed in order to

widen the opportunity obtaining new endophytic fungi and new bioactive metabolites as well.

The prioritized host plants are those from unique environmental settings, have an ethnobotanical

history, that are endemic and grown in areas of great biodiversity (Strobel and Daisy, 2003). In

Indonesia, the most studied plant for isolation of endophytic fungi were medicinal plants,

followed by crops and mangroves (Figure 1). Most of medicinal plants studied for endophytic

fungi isolation were based one ethnomedicinal use by one or more of hundreds of Indonesian

tribes. The medicinal plants for endophytic fungi isolation reported in Indonesia were sambiloto

(Andrographis paniculata, Acanthaceae), sugar apple (Annona squamosa, Annonaceae), kepel

(Stelechocarpus burahol, Annonaceae), cananga (Cananga odorata, Annonaceae), pulasari (Alyxia

reinwardtii, Apocynaceae), keladi tikus (Typhonium divaricatum, Araceae), dahlia (Dahlia

viriabilis, Asteraceae), mangosteen (Garcinia mangostana, Clusiaceae), kandis gajah (G, griffithii,

Clusiaceae), G, forbessi, G, porrecta (Clusiaceae), paku simpai (Cibotium barometz,

Dicksoniaceae), red meranti (Shorea balarengan, Dipterocarpaceae), kumis kucing (Orthosiphon

stamineus, Lamiaceae), johor (Cassia siamea, Leguminosae), trengguli (C, fistula, Leguminosae),

kemladeyan (Loranthus parasiticus, Loranthaceae), neem (Azadirachta indica, Meliaceae), orchid

tree (Aglaia odorata, Meliaceae), mahagony (Swietania macrophylla, Meliaceae), brotowali

(Tinaspora crispa, Menispermaceae), yellow moonsheed (Archangelisia flava, Menispermaceae),

akar kuning (Fibraura chloroleuca, Menispermaceae), Java fig (Ficus benyamina, Moraceae),

Morus spp, (Moraceae), Indonesian laurel (Syzygium polyanthum, Myrtaceae), white gum

(Eucalypthus alba, Myrtaceae), guava (Psidium guajava, Myrtaceae), jasmine (Jasminum sambac,

Oleaceae), tunjuk langit (Helminthostachys zeylanica, Ophiogloseceae), pigeon orchid

(Dendrobium crumenatum, Orchidaceae), pandan (Pandanus amaryfolius, Pandanaceae), sirih

(Piper betle, Piperaceae), pepper (P, nigrum, Piperaceae), Celebes pepper ( P, crocatum,

Piperaceae), Indian mullberry (Morinda citrifolia, Rubiaceae), cinchona (Cinchona ledgeriana,

Rubiaceae), red cinchona (C, pubescens, Rubiaceae), catechu (Uncaria gambier, Rubiaceae),

honey bush (Murraya paniculata, Rutaceae), buah makasar (Brucea javanica, Simaroubaceae),

Chinese yew ( Taxus sumatrana, Taxaceae), tea (Camelia sinensis, Theaceae), mahkota dewa

(Phaleria macrocarpa, Thymelaeaceae), bengle hantu (Zingiber ottensii, Zingiberaceae), ginger

(Z, officinale, Zingiberaceae), white turmeric (Curcuma zedoaria, Zingiberaceae), galangal (Alpinia

galanga, Zingiberaceae), and ongkea (Mezzetia parviflora) (Agusta, 2007; Agusta et al., 2005;

Agusta et al., 2006b; Agusta et al., 2013; Artanti et al., 2014; Artanti et al., 2012; Artanti et al.,

Proceeding of The 1st University of Muhammadiyah Purwokerto

5-6 June 2015, Horison Hotel PurwokertoISBN 978-602-73538-0-0

2011; Astuti et al., 2014; Dompeipen

al., 2011a; Elfita et al., 2012b

al., 2013; Fitrya and Muharni

2014; Ilyas et al., 2009; Jamal

al., 2008; Kumala et al., 2010a

Kumala and Siswanto, 2007

Maehara et al., 2010; Mangunwardoyo

Muharni et al., 2014; Mun'im

2011; Praptiwi et al., 2013;

Ramdanis et al., 2012; Saraswaty

et al., 2007; Sugijanto et al.,

al., 2010; Sugijanto et al., 2004

Yunianto et al., 2012; Yunianto

The endophytic fungi from crops were also extensively studied in Indonesia

endophytic fungi obtained from crops were studied for their potency as bioagent for controlling

plant pathogenic insects, nematodes and fungi

oil (Elaeis guineensis, Arecaceae)

(Diospyros mabola, Ebenaceae)

(Dimocarpus longan, Sapindaceae)

University of Muhammadiyah Purwokerto - Pharmacy International Conference6 June 2015, Horison Hotel Purwokerto

Dompeipen et al., 2011; Elfina et al., 2014; Elfita et al., 2012a

2012b; Elfita et al., 2011b; Elfita et al., 2014; Elfita et al., 2013

Fitrya and Muharni, 2013; Ginting et al., 2013; Harni and Munif, 2012; Hermawati

Jamal et al., 2009; Kumala et al., 2007a; Kumala and Fitri, 2008

2010a; Kumala et al., 2011; Kumala et al., 2010b; Kumala

2007; Kumala et al., 2006; Kumala et al., 2007b; Lorenita

Mangunwardoyo et al., 2012; Margino, 2008; Mufidah et al.,

Mun'im et al., 2013; Noverita et al., 2009; Ola et al., 2014; Prabandari

; Prihatiningtias et al., 2007; Radji et al., 2009; Radji

Saraswaty et al., 2013; Shibuya et al., 2005; Sinaga et al., 2009

2011a; Sugijanto et al., 2009; Sugijanto and Dorra, 2012;

2004; Sugijanto et al., 2014; Winarno, 2006; Wulansari

Yunianto et al., 2014).

Fig 1. The nature of host plants.

The endophytic fungi from crops were also extensively studied in Indonesia. Most of the


nematodes and fungi. Mango (Mangifera indica, Anacardiaceae)

Arecaceae), water spinach (Ipomea reptans, Convolvulaceae)

Ebenaceae), candlenut (Aleuritas mollucana, Euphorbiaceae)

Sapindaceae), soy bean (Glycine max, Fabaceae), avocado (

Pharmacy International Conference

2012a; Elfita et

2013; Fitriyah et

Hermawati et al.,

2008; Kumala et

Kumala et al., 2009;

Lorenita et al., 203;

et al., 2013;

Prabandari et al.,

Radji et al., 2011;

2009; Srikandace

; Sugijanto et

Wulansari et al., 2014;

Most of the


Anacardiaceae), palm

Convolvulaceae), butter fruit

Euphorbiaceae), longan

avocado (Persea



45

gratissima, Lauraceae), cocoa (Theobroma cacao, Malvaceae), jackfruit (Artocarpus

heterophyllus, Moraceae), banana (Musa paradisiana, Musaceae), water cherry (S, aqueum,

Myrtaceae), vanilla (Vanilla planiflora, Orchidaceae), starfruit (Averhoa carambola, Oxalidaceae),

rice (Oriza sativa, Poaceae), corn (Zea mays, Poaceae), manilkara (Manilkara kauki, Sapotaceae),

citrus (Citrus sp,, Rutaceae), potato (Solanum tuberosum, Solanaceae) and chilli (Capsicum

annuum, Solanaceae) were the crops studied for their endophytic fungal diversity (Amin, 2013a;

Amin et al., 2013; Amin et al., 2014; Ariyanto et al., 2013; Ariyono et al., 2014; Delfita, 2011;

Hapsari et al., 2014; Hernawati et al., 2011; Legiastuti and Aminingsih, 2012; Manurung et al.,

2014; Margino, 2008; Nurzannah et al., 2014; Puspita et al., 2013; Rante et al., 2013; Sinaga et al.,

2013; Situmorang et al., 2013; Sriwati et al., 2011; Sudantha and Abadi, 2007b; Tirtana et al.,

2013; Tondok et al., 2012).

Mangroves are considered living in harsh environment (Kathiresan and Bingham, 2001), that they

meet the rationale for host plant selection. The studied mangroves for isolation of endophytic

fungi in Indonesia were Avicennia alba, A. marina (Acanthaceae), Sonneratia sp. (Lythraceae),

Bruguiera sp., Rhizophora mucronata, R. stylosa, R. apiculata, and Ceriops sp. (Rhizophoraceae)

(Kartika et al., 2013; Prihanto et al., 2011; Suciatmih and Rahmansyah, 2013; Sumampouw et al.,

2013; Tarman et al., 2013). Aside from the medicinal plants, crops, and mangroves, recently

studied host plant for endophytic fungi diversity are Gebang palm (Corypha utan, Arecaceae) and

sengon (Paracerianthes falcateria, Fabaceae) (Amin, 2013b; Margino, 2008).

THE ISOLATED ENDOPHYTIC FUNGI

The dominant endophytic fungi succesfully isolated from host plants are from Ascomycota

phylum, followed by Basidiomycota, Zygomycota, and Deuteromycota (Figure 2). The most often

isolated Ascomycota are Aspergillus spp. (Amin et al., 2013; Ariyanto et al., 2013; Elfina et al.,

2014; Elfita et al., 2011b; Ginting et al., 2013; Hapsari et al., 2014; Ilyas et al., 2009; Nurzannah et

al., 2014; Puspita et al., 2013; Suciatmih and Rahmansyah, 2013; Sudantha and Abadi, 2007a;

Tarman et al., 2013; Tirtana et al., 2013). Fusarium spp. (Agusta et al., 2006b; Amin, 2013a; Amin

et al., 2014; Ariyono et al., 2014; Delfita, 2011; Elfina et al., 2014; Elfita et al., 2013; Hapsari et al.,

2014; Ilyas et al., 2009; Mangunwardoyo et al., 2012; Prihanto et al., 2011; Puspita et al., 2013;

Situmorang et al., 2013; Suciatmih and Rahmansyah, 2013; Sunariasih et al., 2014; Tirtana et al.,

2013; Yunianto et al., 2012). Penicillium spp. (Agusta, 2007; Ariyanto et al., 2013; Ariyono et al.,

2014; Hapsari et al., 2014; Maehara et al., 2010; Muharni et al., 2014; Radji et al., 2009;

Situmorang et al., 2013; Suciatmih and Rahmansyah, 2013; Sudantha and Abadi, 2007b;

Sunariasih et al., 2014; Tarman et al., 2013; Tirtana et al., 2013; Yunianto et al., 2014),

Colletotrichum spp. (Amin et al., 2014; Ariyono et al., 2014; Ginting et al., 2013; Hapsari et al.,

2014; Mangunwardoyo et al., 2012; Puspita et al., 2013; Radji et al., 2009; Suciatmih and



46

Rahmansyah, 2013; Tirtana et al., 2013). Cladosporium spp. (Ariyono et al., 2014; Ilyas et al.,

2009; Suada et al., 2012; Sudantha and Abadi, 2007b; Sugijanto and Dorra, 2012; Sunariasih et

al., 2014). Trichoderma spp. (Amin, 201.a; Elfina et al., 2014; Elfita et al., 2014; Hapsari et al.,

2014; Situmorang et al., 2013; Sudantha and Abadi, 2007b). Curvularia spp. (Amin et al., 2014;

Ariyanto et al., 2013; Ginting et al., 2013; Hapsari et al., 2014; Prabandari et al., 2012; Puspita et

al., 2013; Situmorang et al., 2013). Acremonium spp, (Amin, 2013a; Elfita et al., 2012b; Prihanto

et al., 2011; Puspita et al., 2013; Tirtana et al., 2013). Nigrospora spp. (Amin, 2013b; Ariyono et

al., 2014; Hapsari et al., 2014; Hernawati et al., 2011; Suada et al., 2012). Diaporthe spp. (Agusta,

2007; Agusta et al., 2005; Agusta et al., 2006a; Ilyas et al., 2009; Maehara et al., 2010; Ola et al.,

2014; Shibuya et al., 2005), and Altenaria spp. (Elfina et al., 2014; Situmorang et al., 2013;

Sunariasih et al., 2014; Tarman et al., 2013).

Another fungi living as endophytes from Ascomycota succesfully isolated are Ampelomyces sp.

(Prihanto et al., 2011), Arthrinium sp. (Maehara et al., 2010), Arthroascus sp., Cyniclomyces sp.,

Guillermondella sp., Hanseniaspora sp., Kluyveromyces sp. (Sugijanto et al., 2004), Aschersonia

sp., Pestalotia sp., Xylaria sp. (Tondok et al., 2012), Aureobasidium sp. (Lorenita et al., 203),

Beauveria sp. (Amin et al., 2013), Botryosporium sp., Clyndrophora spp., Humicola spp.,

Microsporium sp., Verticillium spp. (Puspita et al., 2013), Botrytis sp. (Puspita et al., 2013; Tirtana

et al., 2013), Cephalosporium sp. (Ariyono et al., 2014; Puspita et al., 2013), Cercospora piaropi,

C. nicotianae, Dothideomycete sp., Geomyces pannorum, Guignardia mangiferae, Pleosporaceae

sp. (Legiastuti and Aminingsih, 2012), G. endophyllicola (Mangunwardoyo et al., 2012; Suciatmih

and Rahmansyah, 2013), Ceriporia lacerate, Sordariomycetes sp. (Sunariasih et al., 2014),

Chochlibus lunatus (Fitrya and Muharni, 2013), Coniothyrium sp. (Hernawati et al., 2011),

Cylindrocephalum sp., Mastigosporium spp., Helicosporium sp., Paecylomyces sp., Passalora sp.

(Hapsari et al., 2014), Fennelia nivea (Saraswaty et al., 2013), Geotrichum sp. (Amin et al., 2014),

Gliocladium spp. (Amin et al., 2014; Situmorang et al., 2013), Gloesporium sp., Helminthosporium

sp., Monocillium sp., Nodulsporium sp. (Ariyono et al., 2014), Cochliobolus geniculatus,

Glomerella cingulata, Lecanicillium kalimantanense, Neonectria punicea, Periconia macrospinosa,

Rhizopycnis vagum, Talaromyces assiutensis, Myrothecium verrucaria (Ginting et al., 2013),

Hyalodendron sp. (Hapsari et al., 2014; Tirtana et al., 2013), Lecythophora sp. (Sugijanto et al.,

2011b; Sugijanto et al., 2010), Monilia sp. (Fitriyah et al., 2013), Nectria rigidiuscula (Yunianto et

al., 2012), Pestalotiopsis spp. (Ilyas et al., 2009; Mangunwardoyo et al., 2012; Suciatmih and

Rahmansyah, 2013), Nodulisporium sp., Phaeosphaeriopsis musae, Phialemonium curvatum,

Sarocladium oryzae, Sordariomycetes sp. (Suada et al., 2012), Phoma spp. (Ilyas et al., 2009;

Situmorang et al., 2013), Phomopsis spp. (Ilyas et al., 2009; Maehara et al., 2010; Suciatmih and

Rahmansyah, 2013), Sarocladium oryzae (Suada et al., 2012; Sunariasih et al., 2014),

Scolecobasidium sp., Westerdikella sp., Xylohypha sp. (Mangunwardoyo et al., 2012),



47

Talaromyces spp. (Ginting et al., 2013; Hermawati et al., 2014; Suciatmih and Rahmansyah,

2013), and Thievalia polygonoperda (Prihatiningtias et al., 2007).

Fig 2. The phyllum of isolated endophytic fungi.

Calocybe gambosa (Tondok et al., 2012), Fomitopsis cf. maliae (Sunariasih et al., 2014),

Fomitopsis pinicola (Maehara et al., 2010), Moniliella sp. (Lorenita et al., 203), Resinicium friabile

(Tondok et al., 2012), Rhizoctonia spp. (Marlida et al., 2010a; Sudantha and Abadi, 2007b),

Schizophyllum spp. (Maehara et al., 2010; Sunariasih et al., 2014), and Zygodesmus spp. (Puspita

et al., 2013) were the endophytic fungi from Basidiomycota. From Zygomycota phylum,

endophytic Cunninghamella sp. (Tirtana et al., 2013), Martensiomyces sp. (Ariyono et al., 2014),

Mucor spp. (Puspita et al., 2013), and Mycotypha sp. (Hapsari et al., 2014) were succesfully

isolated. It has been reported that endophytic Coelomycetes sp. (Jamal et al., 2009; Wulansari et

al., 2014) and Zasmidium cellare (Radji et al., 2009) from Deuteromycota phylum have been

reported previously.

THE SCREENED BIOACTIVITY OF ENDOPHYTIC FUNGI

The first of the steps needed for discovery of new biaoctive metabolites from endophytic fungi is

to determine the bioactivity of a crude extract of their culture broth or mycelium. The

identification and structure elucidation of the most potent metabolite is the next step to develop

the new drugs that would potentially be used in therapy (Radic and Strukelj, 2012). Bioactivity

guided isolation is commonly performed in order to obtain bioactive compounds from



48

endophytic fungi (Strobel and Daisy, 2003). The selection of the screened bioactivity of

endophytic fungi based on the bioactivity of their respective host plant. The most often studied

bioactivity of endophytic fungi in Indonesia is antimicrobial, followed by inhibition of enzymes,

production of metabolites, citotoxicity, biotransformation, antinematodic, antioxidant, and

antimalarial (Figure 3).

There are two main purposes of studying antimicrobial activity of endophytic fungi, they are

producing antibiotic for human disease or developing bioagent to combat plant pathogenic fungi.

The endophytic fungi screened for producing antibiotics were mainly isolated from antimicrobial

medicinal plant such as A. squamosa, S. burahol, C. odorata, D. variabilis, L. parasiticus, A.

reinwardtii, G. mangostana, C. fistula, F. benyamina, A. indica, A. odorata, A. flava, F. chloroleuca,

J. sambac, M. citrifolia, S. polyanthum, D. crumenatum, P. betle, P. crocatum, P. macrocarpa, Z.

officinale, Z. ottensii, A. galanga, C. zedoaria and M. parviflora. For this purpose, the extract of

selected endophytic fungi were tested against common human pathogenic microorganisms such

as Bacillus subtilis, Staphylococcus aureus, Micrococcus luteus, Escherichia coli, Shigella dysentri,

Streptomyces pneumoniae, Salmonella typhiimurium, Pseudomonas aeruginosa,Candida

albicans, C. kruzei and Malassezia furfur (Fitriyah et al., 2013; Ginting et al., 2013; Kumala et al.,

2007a; Kumala and Siswanto, 2007; Margino, 2008; Mufidah et al., 2013; Muharni et al., 2014;

Noverita et al., 2009; Ola et al., 2014; Prihatiningtias et al., 2007; Radji et al., 2011; Sinaga et al.,

2009; Sugijanto et al., 2011a; Sugijanto et al., 2009; Sugijanto et al., 2011b; Sugijanto and Dorra,

2012; Sugijanto et al., 2010; Sugijanto et al., 2014; Wulansari et al., 2014).

In order to obtain biocontrol agents against plant pathogenic fungi, endophytic fungi were

isolated from crops such as M. indica, D. mabola, A. mollucana, P. guajava, P. gratissima, T.

cacao, A. heterophyllus, M. paradisiana, S. aqueum, V. planiflora, A. carambola, O. sativa, Z.

mays, M. kauki, D. longan, S. tuberosum and C. annuum. The tested organisms for finding new

biocontrol agents against plant pathogenic fungi are Fusarium spp., Phytophthora spp.,

Curvularia spp., Helminthosporium maydis, and Botryodiplodia theobromae (Amin et al., 2013;

Manurung et al., 2014; Margino, 2008; Nurzannah et al., 2014; Puspita et al., 2013; Sinaga et al.,

2013; Suada et al., 2012; Sudantha and Abadi, 2007b; Sunariasih et al., 2014; Tirtana et al., 2013).

Antidiabetic activity of endophytic fungi was studied using inhibition of α-glucosidase model. The

fungi were isolated from medicinal plants traditionally used as antidiabetic such as S. mahagoni,

A. paniculata, O. spicatus, M. citrifolia, P. crocatum, P. ornatum, C. siamea, and T. sumatrana.

Endophytic fungi isolated from A. paniculata, O. spicatus, P. crocatum and C. siamea exhibited a

potent α-glucosidase inhibition activity. The similar results were also shown by endophytic fungi

Collelotricum sp. isolated from T. sumatrana (Artanti et al., 2012; Dompeipen et al., 2011;

Mun'im et al., 2013).



49

It has been reported that endophytic fungi undergo a sophisticated communication with their

host plants and resulted their capability to produce the same or similar metabolites produced by

their respective host plants (Kusari et al., 2012). Piperine, gingkolide B, taxol, podophyllotoxin,

camptothecin, vincristin, vinblastin, and huperzine A were the metabolites produced by both

endophytic fungi and the host plant where they live (Chithra et al., 2014; Cui et al., 2012;

Eyberger et al., 2006; Liu et al., 2010; Shweta et al., 2013). This approach was used to screen the

endophytic fungi isolated from their respective host plant. The capability of producing kinin and

sinkonin, that were the major metabolites produced by Cinchona plant, was used as the

screening method to choose the endophytic fungi isolated from C. ledgeriana and C. pubescens

(Winarno, 2006). The screening of endophytic fungi based on their capability of producing

phytase has been reported also. Phytase was produced by Rhizoctonia sp. and F. verticillioides

derived from G. max (Delfita, 2011; Marlida et al., 2010b).

Fig 3. The screened bioactivity of endophytic fungi.

Citotoxic activities of endophytic fungi have been reported. Fusarium spp. and Nectria

rigidiuscula residing in A. squamosa exhibited citotoxicity effect against MCF-7 brest cancer cells

(Yunianto et al., 2012). 19,20-epoxycytochalasin Q was a compound isolated from endophytic

Xylaria sp. residing in Morus sp. that possessing cytotoxic effect with IC50<0.1 μg/mL against

murine leukemia P-388 (Hermawati et al., 2014). An endophytic fungi isolated from P. crocatum

was reported inhibiting the growth of WiDr and T47D cell lines (Astuti et al., 2014). Endophytic F.

chlamydosporum isolated from B. javanica possesses citotoxicy against L1210, while metabolites

of B. parva isolated from the same host plant inhbits the growth of T47D and MCF-7. Endophytic



50

fungi 1.3.11, also isolated from B. javanica, shows a synergyc effect to that of doxorubicin

against MCF-7 (Kumala et al., 2010b; Kumala et al., 2009; Kumala et al., 2006; Kumala et al.,

2007b).

Endophytic fungi also has been used in biotransformation process. Coelomycetes AFKR-3 isolated

from A. flava has shown the capability to transform berberine into its 7-N-oxide derivative and

palmatine into a new derivative palmatine 7-N-oxide (Agusta et al., 2013). Diaporthe sp. isolated

from C. sinensis oxidized stereoselectively at C-4 position of (+)-catechin and (-)-epicatechin to

give the correspondent 3,4-cis-dihydroxyflavan derivatives, respectively. (-)-Epicatechin 3-O-

gallate and (-)-epigallocatechin 3-O-gallate were also oxidized by the fungus into 3,4-

dihydroxyflavan derivatives (Shibuya et al., 2005). The endophytic fungus Diaporthe sp. E isolate

obtained from C. sinensis showed their capability to biotransform (-)-epigallocatechin-3-O-

gallate into (-)-2R,3S-dihydromyricetin (Agusta, 2007).

The endophytic fungi have been studied for antinematodic and biopesticide activity. Endophytic

Nigrospora sp. isolated from P. falcateria showed antinematodic activity against the motile

juvenile stage 2 of the root knot Meloidogyne spp. (Amin, 2013b). The endophytic fungus isolated

from M. paradisiana also showed the potency as biocontrol agent in controlling Radopholus

similis (Sinaga et al., 2013). Trichoderma sp. isolated from P. nigrum was reported exhibiting the

biocontrol activity against nematode M. incognita and R. similis (Harni and Munif, 2012).

The antimalarial activity screening was performed using endophytic A. flavus isolated from A.

paniculata. This fungi produced 7-hydroxypiranopiridin-4-on, an antimalarial metabolites (Elfita

et al., 2011b). Two alkaloid compounds isolated from endophytic fungi residing in brotowali also

active as antimalarial (Elfita et al., 2011a). Antioxidant activity of endophytic fungi was shown by

F. nivea residing in T. divaricatum (Saraswaty et al., 2013) and Acremonium sp. residing in G.

griffithii (Elfita et al., 2012a).

METABOLITES OF ENDOPHYTIC FUNGI

Linear with the extensive screening of antimicrobial activity of endophytic fungi, some of the

isolated metabolites were active as antimicrobial agents. Two new metabolites, diaporthemins A

and B, together with the known flavomannin-6,6’-di-O-methyl ether were isolated from D.

melonis residing in A. squamosa collected in Kupang. Flavomannin-6,6’-di-O-methyl ether was

active as antimicrobial against S. aureus ATCC 29213 and S. pneumoniae ATCC 49619 with MIC of

2 and 32 µg/mL, respectively (Ola et al., 2014). Coelomycetes sp. AFKR-18 derived from the young

stems of a A. flava produced pachybasin when cultured in a liquid medium. Pachybasin inhibited

the growth of E. coli, B. subtilis, M. luteus, S. cerevisiae, C. albicans, A. niger, A. flavus, S. aureus

and F. oxysporum with MIC values of 16.0-64.0 μg/mL (Wulansari et al., 2014). The 3-acetyl -



51

2,5,7-trihydroxy-1,4-naphtalenedione, a compound isolated from endophytic fungi TCBP4

obtained from T. crispa, possessed a better antifungal activity compared to commercial

antifungal nystatin and cabisidin against C. albicans (Praptiwi et al., 2013). A new compound

lecythomycin and known compounds (2R)-3-(2-hydroxypropyl)-benzene-1,2-diol, kojic acid, 7-O-

acetyl-kojic acid, p-hydroxybenzoic acid, emodine, 7-chloroemodine and ergosterol-5,8-peroxide

were isolated from Lecythophora sp. residing in A. reinwardtii. Lecytomycin displayed antifungal

activity against A. fumigatus and C. kruzei at MIC of 62.5-125 μg /mL (Sugijanto et al., 2009;

Sugijanto et al., 2011b). Methyl eugenol was the main metabolite of ethyl acetate extracts of

Colletotricum sp. PWD2 dan Coelomycetes sp. PWA1 isolated from P. amarylifolius that inhibited

the growth of Saccaromyces cerevisae (Jamal et al., 2009). Two alkaloids, meleagrine and

chrysogine, are isolated from Penicillium sp. from A. squamosa. Both compounds were not

exhibited antimicrobial and cytotoxic activity (Yunianto et al., 2014). The structure of bioactive

metabolites from endophytic fungi is shown in figure 4.

Fig 4. Structure of bioactive metabolites produced by endophytic fungi.

Endophytic T. wortmanii, Xylaria sp., and an unidentified fungus were obtained from host plant

M. cathayana and M. macroura. Wortmin and skyrin are two known compounds isolated from T.

wortmanii, while 19,20-epoxycytochalasin Q, 18-deoxy-19,20-epoxycytochalasin Q, and 19,20-

epoxycytochalasin C were isolated from Xylaria sp. On the other hand, two arthrinone derivatives

and a presilphiperfoliane sesquiterpene were isolated from an unidentified fungus. 19,20-



52

epoxycytochalasin Q exhibited the most active cytotoxicity against murine leukemia P-388 with

IC50<0.1 μg/mL (Hermawati et al., 2014). An antioxidant metabolite, 3,5-dihydroxy-2,5-

dimethyltrideca-2,9,11-triene-4,8-dione, was isolated from Acremonium sp. residing in G. griffithii

(Elfita et al., 2012b).

The 7-hydroxypiranopiridin-4-on was an antimalarial metabolites of A. flavus isolated from A.

paniculata with MIC of 0,201 μM against Plasmodium falciparum 3D7 (Elfita et al., 2011b).

Another antimalarial metabolites produced by endophytic fungi were 7- hydroxy-3,4,5-trimethyl-

6-on-2,3,4,6-tetrahydroisoquinoline-8-carboxylic acid and 2,5-dihydroxy-1-

(hydroxymethyl)pyridin-4-on. Those alkaloids was produced by endophytic fungi BB3 and BB4

isolated from T. crispa (Elfita et al., 2011a). Table 1 summarizes the metabolites isolated from

endophytic fungi that were untested for their bioactivity.

Table 1. The bioactivity-untested metabolites of endophytic fungi

Metabolites Endophitic

Fungi

Host plants References

di-(2-ethylhexyl)phthalate and 5-(4’-

ethoxy-2’-hydroxy-5’-methyl-2’,3’-

dihydrofuran-3’-il (hydroxy) methyl-4-

isopropyl-3-methyl-2-pyran-2-on

Penicillium

sp.

C. zedoaria (Muharni et al.,

2014)

arugosin J, xylarugosin, resacetophenone Xylaria sp. C.

xanthorrhiza

(Hammerschmidt

et al., 2014)

5-hydroxy-4-hydroxymethyl-2H-pyran-2-

one (1) and (5-hydroxy-2-oxo-2H pyran-4-

yl)

methyl acetate

Trichoderma

sp.

T. crispa (Elfita et al., 2014)

(7R,8S)-7,8-dihydroxy-3,7-dimethyl-6-oxo-

7,8-dihydro6H-isochromene -carbaldehyde

Fusarium sp. T. crispa (Elfita et al., 2013)

11,12,13-trimethylheksyl-2-methylhexa-

2,4-dienoat

C. lunatus H. zaylanica (Fitrya and

Muharni, 2013)

8,10,12-trihydroxy-9-methoxy-7a-methyl-

7,7a,12a,13-tetrahydrobenzocyclohepta

oxocin-6-one

A. niger G. griffithii (Elfita et al.,

2012a)

8-hydroxy-9,12-octadecadienoic acid C. lunata C. barometz (Prabandari et al.,

2011)

kinin and sinkonin unidentified C.

ledgeriana

(Winarno, 2006)

(+)-epicytoskyrin and (+)-1,1’-bislunatin D.

phaseolorum

C. sinensis (Agusta et al.,

2006a)

CONCLUSIONS

It is believed that searching for natural products produced by endophytes could be a promising

way to discover highly effective, low toxicity, and minimal environmental impact bioactive

metabolites. In Indonesia, the rationale for plant selection have been followed, resulted in the

variety of host plants and their respective isolated endophytic fungi. Bioactivities of endophytic



53

fungi have been reported, and many bioactive metabolites have been isolated from those fungi

through bioactivity-guided isolation.

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Endophytic Fungi Researches in Indonesia Dwi Hartantidigilib.ump.ac.id/files/disk1/23/jhptump-ump-gdl-dwihartant-1105-1-48_pdfsa-c.pdf · 202, Kembaran, Banyumas, Jawa Tengah, Indonesia