Fungal growth promotor endophytes a pragmatic approach

Fungal growth promotor endophytes: a pragmatic approachtowards sustainable food and agriculture

Mahendra Rai & Dnyaneshwar Rathod & Gauravi Agarkar & Mudasir Dar &

Marian Brestic & Glaucia Maria Pastore & Mario Roberto Marostica Junior

Received: 23 July 2013 /Accepted: 17 February 2014# Springer Science+Business Media Dordrecht 2014

Abstract Agricultural productivity suffers a heavy loss dueto plant pathogens, insect pests and various abiotic stresses.Agriculture being the world’s largest economic sector, it is theneed of time to find and establish the ideal strategy for sus-tainable agriculture and improvement in crop growth.Endophytes are microorganisms that asymptomatically growwithin the plant tissues without causing any disease to thehost. Endophytic fungi live in symbiotic association withplants and play an important role in plant growth promotion,higher seed yield and plants resistant to various biotic, abioticstresses and diseases. Many are able to produce antimicrobialcompounds, plant growth hormones and various agrochemi-cal bioactive metabolites. These mycoendophytes hold enor-mous potential for the development of eco-friendly and eco-nomically viable agricultural products. In this review wefocused on the endophytic fungi recovered from differentmedicinal plants, their active principles involved in plantgrowth enhancement and the applications of fungal

endophytes in agriculture. Moreover, we also discussed aboutendophytic fungi and their pragmatic approach towards sus-tainable food and agriculture.

Keywords Agriculture . Antimicrobial . Endophytic fungi .

Medicinal plants . Plant growth

1 Introduction

Endophytes are microorganisms (bacterium, fungus, actino-mycetes) that live within the host plant tissues without causingany symptoms of disease (Vanessa and Christopher 2004).There has been a growing interest in the prospecting of thesemicroorganisms as a source of novel and bioactive naturalproducts. Some form a mutually beneficial relationship(symbiosis) with the host plants, while others are opportunis-tic pathogens. Petrini et al. (1992) reported that there may bemore than one type of fungal endophytes found within a singleplant. For example, 13 taxa of fungal endophytes were isolat-ed from the leaf, stem and root tissues ofCatharanthus roseus(Kharwar et al. 2008). These are relatively less studied andoffer tremendous potential of novel secondary metabolites forexploitation in medicine, pharmaceutical and agriculture in-dustry. Fungal endophytes have been found in healthy tissuesof all the plant taxa studied to date and it is their chemicaldiversity rather than biological diversity that is mainly respon-sible for the interest in these organisms. Endophytes reside inthe tissues between living plant cells, forming a mutuallybeneficial relationship with plants from symbiotic to border-ing pathogens. This kind of relationship may refer to asmutualism or symbiosis.

Karsten et al. (2007) reported herbicidal and algaecidalactivity in ethyl acetate extract of an endophytic Phoma sp.isolated from Fagonia cretica. Herre et al. (2007) claimed thatendophytic fungi play a potentially significant mutualistic role

M. Rai (*) :D. Rathod :G. Agarkar :M. DarDepartment of Biotechnology, Sant Gadge Baba AmravatiUniversity, Amravati 444 602, Maharashtra, Indiae-mail: [email protected]

M. Raie-mail: [email protected]

M. RaiInstitute of Chemistry, Biological Chemistry Laboratory,Universidade Estadual de Campinas, Campinas, SP, Brazil

M. BresticDepartment of Plant Physiology, Slovak University of Agriculture inNitra, Tr. A. Hlinku 2, 949 76 Nitra, Slovakia

G. M. Pastore :M. R. M. JuniorDEPAN – Faculdade de Engenharia de Alimentos (FEA),UNICAMP, Monteiro Lobato st., 80, Campinas, SP 13083-862,Brazil

SymbiosisDOI 10.1007/s13199-014-0273-3

by augmenting host defense responses against pathogens.Endophytes could contribute to host protection increasingthe expression of intrinsic host defense mechanisms and pro-viding additional sources of defense; extrinsic to those of thehost. The production of antibiotics from Pseudomonas such as2-4-diacethylphloroglucinol, phenazines, pyrrolnitrin,pyoluteorin and hydrogen cyanine antibiotics show antifun-gal, antibacterial, antihelminthic and phytotoxic activity..Endophytes have the ability to showmuch chemical diversity,including alkaloids, peptides, steroids, terpenoids,isocoumarins, quinones, phenylpropanoids and lignans, phe-nols, phenolic acids, aliphatic compounds, lactones, andothers. Among these compounds, the number of have inter-esting biological activity. After the discovery of Taxomycesandreanae, the producer of taxol from Taxus brevifolia, theinterest in endophyte research has increased with fast pace.Endophytic fungal diversity is higher in tropical and subtrop-ical plants than other climatic zones (Dreyfuss and Chapela1994; Bashyal et al. 1999; Arnold et al. 2000; Banerjee 2011).

Tenguria and Khan (2011) studied the diversity of endo-phytic fungi isolated from leaves of Azadirachta indica col-lected from Pachmarhi biosphere reserve of Madhya Pradeshstate, India. Wei et al. (2009) studied the colonization frequen-cies of endophytic Pestalotiopsis species diverse with hostplants, ages, tissues and sites. Ya-li et al. (2010) reported 49endophytic fungi which were recovered from Saussureainvolucrata.Among these fungiCylindrocarpon sp. was dom-inant followed by Phoma sp. and Fusarium species. Someendophytic fungi synthesize the same bioactive compounds astheir host plants (Mitchell et al. 2010; Zhao et al. 2011). Vieiraet al. (2012) reported diversity and antimicrobial activity ofendophytic fungi isolated from Solanum cernuum Vell. Theyrevealed that the most abundant taxa were closely related toArthrobotrys foliicola, Colletotrichum gloeosporioides,Colletotrichum sp. Coprinellus radians, Glomerella acutata,Diatrypella frostii, Mucor sp., Phoma glomerata, Phomamoricola, Phlebia subserialis and Phanerochaete sordida.These endophytes isolated from different medicinal plantsplay an important role to provide potent bioactive compounds.

2 Classes of fungal endophytes

Depending upon association and colonization of endophytesto host Rodriguez and his colleagues in 2009 classified theminto four classes. The endophytes belonging to Class 1 areclavicipitaceous while class 2–4 are non-clavicipitaceous.Those endophytes categorized in class 1 are reported fromgrasses by European investigators in the late 19th century inseeds of Lolium temulentum, L. arvense, L. linicolum andL. remotum. Further, they also hypothesized an associationto toxic syndromes experienced by animals that consumeinfected tissues. However, these hypotheses were largely

untested until Bacon et al. (1977) linked the endophyteNeotyphodium coenophialum to the widespread occurrenceof ‘summer syndrome’ toxicosis in cattle grazing tall fescue(Festuca arundinacea) pastures.

Non-clavicipitaceous endophytes which showed the poten-tial to colonize asymptomatically and confer habitat-adaptingfitness benefits to the different genetic host species includingmonocots and dicots. The maximum endophytic fungi belongto Ascomycota, and remaining are included in Basidiomycota.Class 2 endophytes are transmitted through seed coats orrhizomes having low abundance in the rhizosphere. Theseendophytes have conferred habitat-adapted fitness benefits inaddition to nonhabitat-adapted benefits; and typically havehigh infection frequencies in plants growing in high-stresshabitats (Rodriguez et al. 2009). The endophytes of class 3comprise the hyper diverse endophytic fungi colonized with theleaves of tropical trees (Rodrigues-Heerklotz et al. 2001).Moreover, the endophytes belonging to class 4 are mostly asco-mycetous fungi that form conidia or some time remain as sterileand form melanized structures such as inter- and intracellularhyphae and microsclerotia in the roots (Rodriguez et al. 2009).

The main aim of the present review is to discuss endo-phytes recovered from different medicinal plants and theirapplications in agriculture as growth promoters.

3Medicinal plants as treasure of fungal growth promoters

Endophytic fungi have been recognized as an important andnovel source of bioactive compounds. They produce a numberof important secondary metabolites, including gibberellins,anticancer, anti-fungal, antibacterial, anti-diabetic and immu-nosuppressant compounds. It has been suggested that someendophytes produce certain phytochemicals, originally char-acteristic of the host, might be related to a genetic combinationof the endophyte with the host that occurred in evolutionarytime (Tan and Zou 2000; Wiyakrutta et al. 2004). Stierle et al.1993 reported that an endophytic fungus, Taxomyces andreanaeisolated from the yew plant,Taxus brevifolia produced paclitaxol,an anti-cancer compound, same as their host yew plant.

A large number of medicinal plants produce growth en-hancer bioactive compounds like (GA3 (Gibberellin), IAA(Indoleacetic acid), ABA (Abscisic acid), Z (Zeatin), ZR(Zeatin riboside)). The endophytes isolated from medicinalplants can be applied for growth promotion activity for exam-ple Waqas et al. (2012a, b) studied the endophytic fungiPhoma glomerata and Penicillium sp. which significantlypromoted the shoot and allied growth attributes such as chlo-rophyll content, biomass of GAs-deficient dwarf mutantWaito-C and Dongjin-byeo rice. Thus, if endophytes, andespecially cultured endophytes, can produce the same rareand important bioactive compounds as their of host plants,this would not only reduce the need to harvest slow-growing

M. Rai et al.

and possibly rare plants, but also help to preserve the world’sever-diminishing biodiversity.

Nature has been a source of bioactive compounds forthousands of years and an impressive number ofmodern drugshave been isolated from natural resources. Traditionally usedmedicinal plants are important source of potentially usefulsecondary metabolites of great economic value all over theworld (Suryanarayanan et al. 2005; Prince and Prabakaran2011). Agriculture is the world’s largest economic sector andthe major population of the world is involved in this sector. Itplays an important role for the living of human beings as wellas animals. It is the only important means for the fulfillment ofhuman basic needs i.e. food, clothing and shelter. Greatercapacity for multiple crop production has been noticed in thetropical and sub-tropical regions of the world. In recent years,the demand for food crops has increased tremendously be-cause of the growing population. Agricultural productivitysuffers a heavy loss due to plant pathogens and insect pests.Major disease outbreaks have resulted in shortage of foodespecially in the developing countries. Loss of crops fromplant pathogens and insect pests result in hunger problems inless developed countries as the disease control methods arelimited in such countries (Varma et al. 2001).

India is a treasure of biodiversity, which hosts a largevariety of plants and has been identified as one of the eightimportant “Vavilorian” centres of origin and crop diversity.Although its total land area is only 2.4% of the total geograph-ical area of the world, the country accounts for eight percent ofthe total global biodiversity with an estimated 49,000 speciesof plants of which 4,900 are endemic (Kumar and Asija 2000).The medicinal qualities of plants are of course due to thepresence of bioactive chemicals. Plants synthesize many com-pounds known as primary metabolites that are critical to theirexistence. These include proteins, fats, and carbohydrates thatserve a variety of purposes indispensable for sustenance andreproduction, not only for the plants themselves, but also foranimals that feed on them and for their own growth. Plantsalso synthesize secondary metabolites many of which are“antibiotic” in a broad sense, protecting the plants againstfungi, bacteria, animals, and even other plants. Every plantspecies contains chemicals that can affect some animals ormicro-organisms negatively, strongly supporting the interpre-tation that secondarymetabolites play a vital role in combatingdiseases and herbivores. “Plants have been a rich source ofmedicines because they produce a host of bioactive molecules,most of which probably evolved as chemical defenses againstpredation or infection” (Cox and Balick 1994).

There are a few reports on the use of medicinal plants forthe control of pest and pathogens in agriculture. The antifun-gal activity of different medicinal plants such as Aloe vera,Ocimum sanctum, Centella asiatica, Piper betle, Calotropisgigantea, Vitex negundo, Ocimum basilicum and Azadirachtaindica were screened against plant pathogenic fungus

Colletotrichum falcatum (Prince and Prabakaran 2011).Pandey et al. (2002) compared the antifungal potential of leafextracts of 49 angiosperms with commercial fungicides byscreening them againstHelminthosporium sativum.A numberof medicinal plants have been used for the control of plantpathogens, and some for growth enhancement, and thus, theyplay an important role in agriculture.

4 Active principles involved in growth enhancement

Endophytic fungi live in symbiotic association with plants andplay an important role in plant growth (You et al. 2012). Rootcolonization by endophytic fungi is accompanied by the pro-motion of growth, higher seed yield and the plants are moreresistant to various biotic and abiotic stresses (Varma et al.2001; Oelmüller et al. 2004; Rai et al. 2004;Waller et al. 2005;Sherameti et al. 2008a, b). Baker et al. (1984) reported in-creased biomass in perennial ryegrass infected with endophyt-ic Lolium perenne, while Latch et al. (1985) reported a signif-icant increase in leaf area of perennial ryegrass inoculatedwith endophytic fungus Neotyphodium lolii. Clay andSchardl (2002) illustrated that endophyte infected plants ofLolium multiforum had more vegetative tillers and allocatedmore biomass to roots and seeds than endophyte-free plants.Schardl and Phillips (1997) demonstrated enhanced tilleringand root growth in tall fescue inoculated with endophyticNeotyphodium coenaphialum. Pocasangre (2000) and Niere(2001) revealed similar results showing increased biomass oftissue-cultured plants treated with endophytic F. oxysporumwhen compared to control plants. Similarly, the positive ef-fects of endophytes on growth of bananas were observed byTing et al. in 2007. Further, they also reported an increase inheight, pseudo-stem diameter, and number of leaves in plantsinoculated with endophytic F. oxysporum. Increase in heightup to 50 % was achieved in cotton inoculated with the rootendophytic fungus Cladorrhinum foecundissimum (Gasoniand De Gurfinkel 1997). A plant root colonizing fungusPiriformospora indica isolated from rhizosphere of Prosopisjuliflora and Zizyphus nummularia has shown to providestrong growth promoting activity during its symbiosis with abroad spectrum of plants (Verma et al. 1998; Varma et al.1999). Inoculation with P. indica resulted in 50 % freshbiomass increase in Artemisia annua L. (Franken et al.1998; Varma et al. 1999), better growth of Brassica oleraceavar. capitata (Kumari et al. 2003) and profuse proliferation ofroots and fast growth of A. vasica was observed (Rai andVarma 2005). Recently, Prasad et al. (2013) reported enhance-ment of biomass and antioxidant activity in Bacopa monnierawhen co-cultivated with P. indica.

A large number of bacterial endophytes have been isolatedfrom all kinds of plants such as monocotyledonous and dico-tyledonous (Posada and Vega 2005; Robert et al. 2008) and

Fungal growth promotor endophytes

from different tissue of several plant species (Kobayashi andPalumbo 2000). It is reported that the bacterial endophytesshows the similar mechanisms for plant growth promotion asrhizospheric PGPB (plant growth promoting bacteria) (Ali2013). Similarly, Ali (2013), reported that the bacterial endo-phytes provide more efficient and prompted defense to theirhosts as compared to the rhizospheric PGPB that bind exclu-sively to the plant’s rhizosphere and also promotes host plantgrowth under a wide range of environmental conditions.

Several researchers endeavored to reveal the active princi-ple which is involved in growth enhancement of the plants byendophytes. The endophyte mediated stimulation of plantgrowth can be elucidated by improved plant nutrition andincreased tolerance to biotic and abiotic stresses (Machungoet al. 2009). Improved plant nutrition occurs through increas-ing the uptake and concentration of a variety of nutrients fromsoil such as phosphorus as in case of Festuca rubra inoculatedwith the fungal endophyte Epichloe festucae (Zabalgogeazcoaet al. 2006), solubilising certain plant nutrients which areunavailable to plants in certain soils (e.g. rock phosphate)and fixing the atmospheric nitrogen (Pineda et al. 2010).The root endophyte Heteroconium chaetospira, significantlyincreased the biomass of Chinese cabbage due to nitrogentransfer (Usuki and Narisawa 2007). Rai et al. (2001) reportedsignificant increase in growth and yield of Spilanthes calvaand Withania somnifera inoculated with an endophyteP. indica caused by greater absorption of water and mineralnutrients due to extensive colonization of roots by P. indica.Sudha et al. (1998) found active translocation of phosphate inrice and transformed carrot roots on inoculation withP. indica.Enhancement of growth by endophytes may be a result ofproduction of phytohormones by the fungal endophytes as inmaize (Nassar et al. 2005). Some endophytes synthesize plantgrowth hormones such as indole-3-acetic acid, cytokininesand gibberellins that promote plant growth (Van Loon 2007;Contreras-Cornejo 2009) and can also increase abovegroundphotosynthesis through the modulation of endogenous sugarand abscisic acid (ABA) signaling (Zhang 2008).

Studies on P. indica illustrated the fungal-mediated uptakeof radiolabelled phosphorus from the medium and its translo-cation to the host in an energy-dependent process, evidencedby a sharp increase in its content in the shoot. Transfer ofPhosphorus by P. indica to host plant has significant effecton plant growth particularly at phosphorus-deprived condi-tion, therefore, helping the plant to overcome the phosphorusstress condition (Kumar et al. 2011). Growth responses bymicrobial inoculated seedlings over the control strengthensthe view that the interactions between host and microbesleads to physiological changes and translocation of sugarsresulting in changes in photosynthetic rates of infectedleaves and their metabolic activities (Bacon and White2000). Hill et al. (1990) found that infection with endophytesresulted in augmented leaf area of Festuca arundinacea and

that increase was correlated with higher concentrations ofsecondary compounds such as alkaloids. However, growthresponses may change in different atmospheric conditionsand edaphic factors and also genotype of the host and micro-bial inoculants. Hence, more work is needed to utilize theseendophytic fungi for better crop production and to minimizethe use of chemical fertilizers (Naik et al. 2008).

The endophytic fungi provides benefit to the host plant byincreasing uptake of water or nutrient and protection frominsects, birds or mammals (Lekberg and Koide 2005). Theendophytic fungi enhance nutrient content of the plant alongwith increasing production of secondary metabolites (Dighton2003). The defense due to endophyte is also effective againstplant pathogens (Arnold et al. 2003).

Endophytic fungi have their effect on plants, right from theseed germination stages. During seed germination, the sym-biotically associated endophytic fungi degrade cuticle cellu-lose and make available carbon for seedling which improvesgermination, vigour and establishment (Jerry 1994). The en-dophytic fungi may have the metabolic machinery to produceplant growth regulators and thereby promote seed germinationin crop plants (Bhagobaty and Joshi 2009). To obtain betterseeds germination and afterward improved plant growth, sev-eral studies have elucidated the seed priming with plantgrowth regulators (Weihong 2004; Wen-guang et al. 2009).Among phytohormones, gibberellic acid (GA) is mostly re-sponsible for cell division and elongation, activation of em-bryo, weakening of endosperm layer and mobilization ofendosperm food reserves (Waqas et al. 2012a). While germi-nation, GA counteracts the effects of abscisic acid (ABA) andthus releasing the seed dormancy which positively regulatesthe germination (Taiz and Zeiger 2002; Davies 2004; Kuceraet al. 2005; Rodríguez-Gacio et al. 2009). In seed germinationprocess, expression of genes are induced via GA signalingthus encoding enzymes which are responsible for mobilizationof food reserves including starch, lipids and proteins stored inendosperm (Peng and Harberd 2002).

Fungi produce a wide variety of phytohormones includinggibberellins (GAs), abscisic acid (ABA) and auxin (IAA)(You et al. 2012). Hamayun et al. (2009d)) reported that theendophytic Aspergillus fumigatus produce significant amountof bioactive GA3, GA4 and GA7 along with inactive GA7,GA19 and GA24 in its culture filtrate (Table 2). The soybeanseeds treated with the culture filtrate of A. fumigatus signifi-cantly improved the speed of germination and higher shootlength was observed as compared to control (Hamayun et al.2009d). Similar results were also observed for the culturefi l t rate of Chrysosporium pseudomerdarium andPaecilomyces sp. which improved the speed of germination(Waqas et al. 2012a). Khan et al. (2011c) also depicted anal-ogous results with culture filtrate of Penicillium funiculosumwhich showed highest speed of germination in soybean seeds.In addition, the germination percentage of seeds treated with

M. Rai et al.

fungal culture filtrate was significantly higher as compared tocontrol (Khan et al. 2011c; Waqas et al. 2012a). These allameliorated effects on host plants were due to GAs which wasprobably produced by endophytic fungi.

Many bacterial endophytes have reported in vitro produc-tion of IAA and its possible involvement in plant growthpromotion (Amna et al. 2006; Govindarajan et al. 2008;Rothballer et al. 2008; Jha and Kumar 2009; Malfanova et al.2011). Other phytohormones produced by bacterial endophytesinclude ABA (Cohen et al. 2008), cytokinins (Sgroy et al.2009) and GAs (Malfanova et al. 2011). Inoculation of maizeplants with a GAs producing endophytic Azospirillum sp.resulted in increased level of GA3 in plant roots and therebypromoted plant growth (Lucangeli and Bottini 1997).

Gibberellic acid (GA) is a phytohormone, a diterpenoidcomplex, which controls the growth of plants and promotesflowering, stem elongation, seed germination, and ripening(Yamaguchi 2008; Hamayun et al. 2009d). Gibberellafujikuroi is a known pathogen of rice plants which causesbakanae, was discovered in the 1920s and its active compo-nent, GA was isolated in 1935 (Mander 2003). So far onehundred thirty-six kinds of GAs have been identified as sec-ondary metabolites of which GA1, GA3, GA4, and GA7 haveshown plant growth promoting activity (Kawaide and Sassa1993; Bottini et al. 2004; Choi et al. 2005; Khan et al. 2008;Khan et al. 2009a; Hamayun et al. 2009a; Khan et al. 2011b;You et al. 2012). GAs are involved in every aspect of plantgrowth and development, but their most typical and spectac-ular property is the enhancement of stem growth (Nishijimaet al. 1995). GAs can modify the sex expression of flowers,induce the parthenocarpic development of fruit and delaysenescence (Nadeem et al. 2010). GAs prevent the need forexposure to red light in the germination of seeds and spores,and the need for vernalisation in the growth of bulbs andtubers (Nadeem et al. 2010). GAs are also associated withthe breaking of winter dormancy and stimulate the formationof hydrolytic enzymes during seed germination (Martin1983).

Endophytic fungi are a little known for the production ofplant growth stimulating hormones, especially gibberellins(Hamayun et al. 2009c). Number of researchers have studiedplant growth activities of GAs (Yamaguchi 2008; Hwang et al.2011) (Table 1). You et al. (2012) confirmed the plant growthpromoting activity of endophytic fungus Penicillium sp. iso-lated from the roots of halophytes using Waito-c rice (WR)seedlings. WR, a dwarf rice mutant with reduced GA biosyn-thesis, were treated with uniconazol as a GA biosynthesisretardant (Khan et al. 2008; Hamayun et al. 2009d; Khanet al. 2012a).

In addition, the orchid associated with Fusariumproliferatum (Tsavkelova et al. 2008), more and more hiddenendophytic fungi, mostly isolates from roots of apparentlyhealthy plants, are being discovered as GA producers

(Table 2). An endophytic Penicillium citrinum showed thegrowth promotion activity on dune plants due to the presenceof bioactive GAs in the filtrate of fungi (Khan et al. 2008).Hasan (2002) studied the growth promotion activity of endo-phy t i c Phoma he r ba r um a nd Chr y s o s po r i umpseudomerdarium on Soybean isolated from Soybean andproved that some endophytes are host specific. Nadeemet al. (2010) evaluated the plant promoting activity of endo-phytic Penicillium sp. and Aspergillus sp. which secretesphysiologically active GA3, GA4, and GA7. Further, theyalso studied stress resistance capability of endophytes.

Khan et al. (2012c) found that endophytic Chaetomiumglobosum produces various physiologically active and inac-tive GAs as well as IAA in its culture medium. Its culturefiltrate significantly enhanced the shoot growth and alliedgrowth characteristics of the host pepper plants and mutantrice Waito-C. The presence of IAA in C. globosum clearlysuggested the existence of IAA biosynthesis pathway as re-ported for some other classes of fungi by Tuomi et al. (1993).Waqas et al. (2012b) studied the endophytic fungi Phomaglomerata and Penicillium sp. which significantly promotedthe shoot and allied growth attributes such as chlorophyllcontent, biomass of GAs-deficient dwarf mutant Waito-Cand Dongjin-byeo rice (normal cultivar). Analysis of the purecultures of these endophytes showed biologically active GAs(GA1, GA3, GA4 and GA7) in various quantities and alsoproduced varying levels of IAA in their culture filtrate (Waqaset al. 2012b). When the effect of these endophytic fungi wasevaluated on cucumber plants under salinity and droughtconditions, the plant height and biomass was increased as wellas higher assimilation of essential nutrients like potassium,calcium and magnesium was also observed as compared tocontrol plants during salinity stress (Waqas et al. 2012b). Asimilar behavior of an endophyte producing auxin was alsoreported by Mei and Flinn (2010) in which indole acetic acidproducing endophytic fungi enhanced rice plant growth undersalinity, drought and temperature stress. According to Waqaset al. (2012b) the greater salt tolerance in the presence ofendophytes may be due the improvement in plant nutritionbalance under stress. The endophytes might inhibit the uptakeof Na + or prevent its transport to other plant parts whilstproducing phytohormones (Waqas et al. 2012b).

Many fungal endophytes have been reported to eithersecrete GAs in their culture medium or have an active GAsbiosynthesis pathway. These include Fusarium fujikuroi,Sphaceloma manihoticola (Bomke et al. 2008; Shweta et al.2010), Phaeosphaeria sp. (Kawaide 2006), Phaeosphaeriasp., Neurospora crassa (Rademacher 1994), Sesamumindicum (Choi et al. 2005), Cladosporium sphaerospermum(Hamayun et al. 2009c), Cladosporium sp. (Hamayun et al.2009c), Penicillium sp. (Hamayun et al. 2010a), Gliomastixmurorum (Khan et al. 2009b), Arthrinium phaeospermum(Khan et al. 2009a), Aspergillus fumigatus (Khan et al.


2011a), Penicillium funiculosum (Khan et al. 2011c),Exophiala sp. (Khan et al. 2011b), Penicillium citrinum(Khan et al. 2008), Chrysosporium pseudomerdarium(Hamayun et al. 2009b) and Scolecobasidium tshawytschae(Hamayun et al. 2009a) have been reported as GAs producers.Hasan (2002) also demonstrated GA production byAspergillus flavus, A. niger, Penicillium corylophilum,P. cyclopium, P. funiculosum and Rhizopus stolonifer whileFusarium oxysporum could secrete both GAs and IAA. GAsalong with other plant hormones like indole acetic acid (IAA)

secreted by rhizosphere fungi can improve plant growth andcrop productivity (Hasan 2002; Yuan et al. 2010).

Auxins, cytokinins and gibberellins are the most citedgrowth promoters associated with the induced growth ofplants as a response to endophytic association (Shi et al.2009). Auxins are known to stimulate cell division, resultinginto increase in root mass and accelerated formation of roothairs, while cytokinins induce root elongation, thereby alsoincreasing root mass (Daly and Inman 1958). Cytokinins arealso apparently responsible for enhancing nutrient

Table 1 Endophytic fungi and their plant growth promotion activity

Sr. No. Host plant Explants Fungal endophytes Plant growth promotion host References

1 Dendrobium loddigesii Leaves, Stems and Roots Fusarium sp.,Pyrenochaeta sp.

Dendrobium loddigesii Chen et al., 2010

2 Euphorbia pekinensis Leaves, Stems and Roots Fusarium sp. Euphorbia pekinensis Dai et al., 2008

3 Sorghum bicolor Leaves, Stems and Roots Helminthosporium velutinum Sorghum bicolor Diene et al., 2010

4 Glycine max Roots Cladosporium sphaerospermum waito-c rice, Glycine max Hamayun et al. 2009c

5 Glycine max Roots Phoma herbarum waito-c rice, Glycine max Hamayun et al. 2009d

6 Cucumis sativus Roots Cladosporium sp. waito-c rice, Cucumis sativus Hamayun et al., 2010c

7 Ipomea batatas Leaves, Stems and Roots Fusarium oxysporum,Emericella nidulans

paclobutrazol treated rice Hipol, 2012

8 Ixeris repenes Roots Penicillium citrinum waito-c rice, Atriplex gemelinii Khan et al. 2008

9 Elymus mollis Roots Gliomastix murorum waito-c rice, Atriplex gemelinii Khan et al. 2009b

10 Cucumis sativus Roots Paecilomyces formosus waito-c rice, Dongjin-byeo rice Khan et al. 2012a

11 Solanum tuberosum Tuber Aspergillus ustus Solanum tuberosum,Arabidopsis thaliana

Marina et al. 2011

12 Cucumis sativus Roots Phoma glomerata, Penicillium sp. waito-c rice, Dongjin-byeo rice Waqas et al. 2012b

13 Suaeda japonica Roots Penicillium sp. waito-c rice, Suaeda japonica You et al. 2012

14 Monochoria Vaginalis Roots Penicillium sp., Aspergillus sp. waito-c rice, Echinocloa crusgalli Nadeem et al. 2010

15 Potentilla fulgens Roots Penicillium verruculosum Vigna radiata, Cicer arietinum Bhagobaty andJoshi 2009

16 Capsicum annuum Roots Chaetomium globosum waito-c rice, Capsicum annuum Khan et al., 2012c

17 Medicinal plants Leaves, Stems and Roots Chaetomium globosum,Aureobasidium pullulans,Gliocladium roseum

Oryza sativa,Sorghum vulgare,Arachis hypogea,Eleusine coracana

Naik et al. 2008

18 Musa sp. Roots and Corm Fusarium oxysporum Musa sp. Machungo et al. 2009

19 Glycine max Roots Scolecobasidium tshawytschae waito-c rice,Glycine max

Hamayun et al. 2009a

20 Chrysanthemumcoronarium

Roots Penicillium sp. waito-c rice,Chrysanthemum coronarium


21 Cucumis sativus Roots Phoma sp. waito-c rice, Cucumis sativus Hamayun et al. 2010b

22 Glycine max Roots Aspergillus fumigatus waito-c rice, Glycine max Khan et al. 2011a

23 Sesamum indicum,Glycine max

Root tips Fusarium oxysporum Vicia faba, Glycine maxSesamum indicum,

Hasan 2002

24 Zoysia tenuifolia Roots Penicillium simplicissimum Arabidopsis thaliana Hossain et al., 2007

25 Prosopis juliflora,Zizyphus nummularia

Roots Piriformospora indica,Sebacina vermifera

Mentha piperita,Thymus vulgaris

Dolatabadi et al., 2012

26 Glycine max Roots Chrysosporium pseudomerdarium waito-c rice, Glycine max Hamayun et al. 2009b

27 Cucumis sativus Roots Exophiala sp. waito-c rice, Dongjin-byeo riceCucumis sativus

Khan et al. 2011b

28 Glycine max Roots Metarhizium anisopliae LHL07 waito-c rice,Dongjin-byeo riceGlycine max

Khan et al., 2012d

29 Theobroma gileri Pod Trichoderma hamatum Theobroma cacao Bae et al. 2009

Note: Waito-c rice (WR) - a dwarf rice mutant with reduced GA biosynthesis

M. Rai et al.

Table 2 Various types of phytohormones extracted from fungal endophytes occurring in medicinal plants

Sr. No. Host plant Endophytic fungi Types of phytohormones produced References

1 Euphorbia pekinensis Fusarium sp. IAA, GA Dai et al., 2008

2 B. polycarpam Phomopsis sp. IAA, Abscisic acid Dai et al., 2008

3 Potentilla fulgens Penicillium verruculosum IAA Bhagobaty and Joshi 2009

4 Glycine max Scolecobasidiumtshawytschae

physiologically activeGA1, GA3, GA4, GA7physiologically inactiveGA15, GA24


5 Glycine max Chrysosporiumpseudomerdarium

physiologically activeGA1, GA3, GA4, GA7physiologically inactiveGA5, GA9, GA15, GA19, GA24

Hamayun et al. 2009b

6 Glycine max Cladosporiumsphaerospermum

physiologically activeGA3, GA4, GA7physiologically inactiveGA5, GA15, GA19, GA24

Hamayun et al. 2009c

7 Glycine max Aspergillus fumigatus physiologically activeGA3, GA4, GA7physiologically inactiveGA5, GA19, GA24

Hamayun et al. 2009d

8 Cucumis sativus Phoma sp. physiologically activeGA1, GA3, GA4physiologically inactive GA9, GA15,

GA19, GA20

Hamayun et al. 2010b

9 Glycine max Phoma herbarum physiologically activeGA1, GA3, GA4, GA7physiologically inactive GA9, GA12,

GA15, GA19, GA20

Hamayun et al. 2009d

10 Cucumis sativus Cladosporium sp. physiologically activeGA1, GA3, GA4, GA7physiologically inactive GA9, GA12,

GA15, GA19, GA20

Hamayun et al., 2010c

11 Chrysanthemum coronarium Penicillium sp. physiologically activeGA1, GA3, GA4, GA7physiologically inactive GA9, GA12,

GA15, GA19, GA20


12 Vicia faba,Corchorus olitorius,Sesamum indicum,Glycine max

Aspergillus flavus,A. niger,Penicilliumcorylophilum,P. cyclopium,P. funiculosum, Rhizopus

stolonifer

GA Hasan 2002

13 Sesamum indicum,Glycine max

Fusarium oxysporum GA and IAA Hasan 2002

14 Ixeris repenes Penicillium citrinum physiologically activeGA1, GA3, GA4, GA7physiologically inactive GA5, GA9,

GA12, GA15, GA19, GA20, GA24

Khan et al. 2008

15 Carex kobomugi Arthrinium phaeospermum physiologically activeGA1, GA3, GA4, GA7physiologically inactive GA5, GA9,

GA12, GA15, GA19, GA24

Khan et al. 2009a

16 Elymus mollis Gliomastix murorum physiologically activeGA1, GA3, GA4, GA7physiologically inactive GA5, GA9,

GA20, GA24

Khan et al. 2009b

17 Glycine max Aspergillus fumigatus GA4, GA9 and GA12 Khan et al. 2011a

18 Cucumis sativus Paecilomyces formosus physiologically activeGA1, GA3, GA4physiologically inactive GA5, GA8,

GA9, GA12, GA20, GA24and IAA

Khan et al. 2012a

19 Capsicum annuum Chaetomium globosum physiologically activeGA1, GA4

Khan et al. 2011c


accumulation and transportation, thus contributing to overallimproved plant growth (Fig. 1). (Kiraly et al. 1967;Dekhuijzen and Overeem 1971; Sziraki et al. 1975;Vizarova 1979). Inoculation of Arabidopsis plants with anendophyte Aspergillus ustus affected the root system byinhibiting primary root growth and increased the lateral-rootnumber, lateral-root growth, and root hairs length suggestingthe role of phytohormones (Marina et al. 2011). Moreover,Marina et al. (2011) demonstrated that A. ustus synthesizesIAA-related indoles (auxins) and GAs in liquid cultures.Sirrenberg et al. (2007) reported the production of IAA inliquid culture of P. indica which when colonized Arabidopsisthaliana caused changes in root growth, leading to stunted andhighly branched root systems. Plants treated with endophytesare often healthier than those lacking such interactions (Baconand White 2000; Schulz 2002; Strobel 2003; Schulz andBoyle 2005; Waller et al. 2005; Arnold 2008; Hyde andDoytong 2008; Khan et al. 2008), which may be attributedto the endophyte secretion of growth hormones such as IAA(Kawaguchi and Sydn 1996; Khan et al. 2011c) and GAs(Hasan 2002; Kawaide 2006; Khan et al. 2008; Bomke et al.2008; Hamayun et al. 2009a; Hamayun et al. 2009b; Khanet al. 2011a; Khan et al. 2011c).

Bacterial endophytes also enhance the growth of their hostplants in various ways, for example, by secretion of plantgrowth regulators, such as indole-3-acetic acid (IAA) (Leeet al. 2004; Ryan et al. 2008), solubilization of minerals such

as phosphorus (Wakelin et al. 2004; Ryan et al. 2008), pro-duction of siderophores that chelate iron and make it availableto the plant roots (Ryan et al. 2008) and fixation of atmospher-ic nitrogen that is supplied to the plant (Ryan et al. 2008).Moreover, the bacterial endophytes provide the essential vita-mins to plants (Bandara et al. 2006). Similarly, the bacterialendophytes affects positively on growth of the host plants byosmotic adjustment, stomatal regulation, modification of rootmorphology, enhanced uptake of minerals, alteration of nitro-gen accumulation and metabolism (Belesky and Malinowski2000). Miliūtė and Buzaitė (2011) reported that the bacterialendophytes influence the plant promotion activity by compet-ing with plant pathogens and producing a broad range ofvarious compounds, which protect the host against pathogens.

In their natural surroundings, plants have to deal with awhole range of environmental changes that determine plantgrowth and development. Hormones and many endogenoussignals regulate plant growth and development in combinationwith the genetic information (Marina et al. 2011). Khan et al.(2011a) quantified isoflavones through HPLC analysis whichshowed that A. fumigatus inoculated plants with /without saltstress contained higher isoflavones than non-inoculatedplants. Thus, under extreme environmental conditions, thesephytohormone producing endophytic fungi can affect theproduction of several secondary metabolites like flavonoidsalong with phytohormones to help the plant to tolerate/avoidstress (Schulz 2002; Waller et al. 2005; Khan et al. 2011c).

Table 2 (continued)

Sr. No. Host plant Endophytic fungi Types of phytohormones produced References

physiologically inactive GA9,GA12, GA20

and IAA20 Monochoria

VaginalisPenicillium sp. physiologically active

GA3, GA4, GA7physiologically inactive GA9,GA24

Nadeem et al. 2010

21 MonochoriaVaginalis

Aspergillus sp. physiologically activeGA3, GA4, GA7physiologically inactive

GA9, GA12, GA24

Nadeem et al. 2010

22 Cucumis sativus Phoma glomerata physiologically activeGA1, GA3, GA4physiologically inactive GA7and IAA

Waqas et al. 2012b

23 Cucumis sativus Penicillium sp. physiologically activeGA1, GA3and IAA

Waqas et al. 2012b

24 Suaeda japonica Penicillium sp. physiologically activeGA1, GA3, GA4, GA7physiologically inactive GA9, GA12,

GA19, GA20, GA24, GA34

You et al. 2012

25 Glycine max Penicillium funiculosum GA1, GA4, GA8, GA9and IAA

Khan and Lee (2013)

26 Cucumis sativus Exophiala sp. physiologically activeGA1, GA3, GA4, GA7physiologically inactive GA5, GA8,

GA9, GA12, GA20

Khan et al. 2011b

27 Salvia miltiorrhiza Trichoderma atroviride Tanshinone Ming et al. 2013

M. Rai et al.

Yet, little is known about GAs production by endophytic fungiand their role in abiotic stress (Khan et al. 2012a). Redmanet al. (2011) reported that the IAA producing endophytic fungican enhance rice plant growth under salinity, drought andtemperature stress. A majority (80.7 %) of fungal endophytesfrom the sand dune flora of Korean coastal region, promotedgrowth of Waito-C rice thus indicating the production of plantgrowth promoting hormones by these fungi (Khan et al.2012b) (Table 2).

Now a days, endophytic fungi residing in root tissues andsecreting plant growth regulating compounds are of greatinterest to enhance crop yield and quality. Such growth regu-lating compounds can influence plant development and rescueplant growth in stressful environments (Marina et al. 2011).Abscisic acid (ABA) is involved in several stress signalingpathways and promotes seed dormancy (Asselbergh et al.2008). Normal response of a plant to stress is to reduce growthby increasing ABA content and reducing GAs (Shinozaki andYamaguchi-Shinozaki 1997; Ueguchi et al. 2007). GA defi-cient plants are more susceptible to stress than those withhigher levels of this hormone (Shinozaki and Yamaguchi-Shinozaki 1997). The higher amount of GA12 in endophytetreated plants under salinity stress elucidated the activation ofGAs biosynthesis pathway, while higher production of GA3and GA4 confirm plant growth maintenance during stresscondition (Khan et al. 2012a). The cucumber plants inoculated

with endophytic P. formosus ameliorated their growth bypossessing lower levels of stress responsive endogenousABA and elevated GAs contents (Khan et al. 2012a).

There are some plant hormones which act as defense sig-naling substance. These include abscisic acid (ABA),jasmonic acid (JA) and salicylic acid (SA) which respond toabiotic stress stimuli (Shinozaki and Yamaguchi-Shinozaki2007). Jasmonic acid induces the biosynthesis of defenserelated-proteins and protective secondary metabolites In re-sponse to biotic and abiotic stresses (Brodersen et al. 2006;Balbi and Devoto 2008).

Many physiological phenomenon, such as resistance topathogens and insects, development of pollen, root growthand senescence can be modulated by Jasmonates (Lorenzoet al. 2004). Salicylic acid (SA) plays a key role in flowering ,growth and development, stomatal behavior, ethylene biosyn-thesis, and respiration (Raskin 1992).

Recently, Ming and his collaborators (2013) reported thatTrichoderma atroviride D16, an endophytic fungus isolatedfrom the root of Salvia miltiorrhiza, previously reported toproduce tanshinone I (T-I) and tanshinone IIA (T-IIA) havebeen found to promote the growth and secondary metabolismof S. miltiorrhiza hairy roots. Similarly, Mahmoud andNarisawa (2013) also reported a new fungal endophyte,Scolecobasidium humicola which promotes growth of tomatoby increasing biomass. S. humicola is a dark septate

Fig. 1 Different mechanisms ofplant growth promotion byendophytic fungi


endophyte and was isolated from the roots of tomatoEpicoccum nigrum P16 strain is an endophyte isolated fromsugarcane. E. nigrum colonizes the root system, increasesbiomass and produce compounds that inhibit the growth ofFusarium verticillioides, Colletotrichum falcatum,Ceratocystis paradoxa, and Xanthomomas albilineans whichusually attack sugarcane. The growth inhibition is assumed tobe due to epicorazines A–B, epirodines A–B, flavipin,epicoccines A–D, epipiridones compounds (Fávaro et al.2012).

Very little information is available about the molecularbasis of root growth promotion by beneficial microbes orfungi (Pieterse and Dicke 2007). Although the molecularmechanisms of beneficial endophyte-host plant interactionsare not known yet, several studies have revealed that thebacterial endophytes can promote plant growth by enhancingthe plant’s capacity for nutrient acquisition, better water man-agement and resistance to abiotic and biotic stresses via reg-ulation of different hormones (Sturz et al. 2000; Berg 2009;Mei and Flinn 2010; Welbaum et al. 2004; Compant et al.2005). Lee et al. (2011) studied the molecular mechanisms bywhich the endophyte P. indica promotes growth and biomassproduction of various plant species. The authors further dem-onstrated two-fold increase in fresh weight of the seedlings ofChinese cabbage inoculated with P. indica and the auxin levelin the roots was also two-fold higher as compared touncolonized controls, but there was no detectable auxin inan exudate fraction from P. indica. It is clear that microbe-induced stimulation of root growth or changes in root archi-tecture involves auxins or interferes with the auxin metabo-lism or signaling in the roots (Sirrenberg et al. 2007;Contreras-Cornejo 2009; Schäfer et al. 2009). Lee et al.(2011) claimed that activation of auxin biosynthesis or itsrelease from conjugates and signaling in the roots might bethe cause for the P. indica-mediated growth phenotype inChinese cabbage. Moreover, Schäfer et al. (2009) observedstage-specific up-regulation of genes involved in phytohor-mones metabolism, mainly encompassing gibberellin, auxinand abscisic acid. Thus, microbes can support plant growth bymany ways such as by elevating auxin synthesis, releasingauxin from stores or conjugates, stimulating its transport, oractivating auxin-induced genes in various tissues which arerequired for cell growth or proliferation (Ludwig-Müller1999; 2000; Ludwig-Müller et al. 2005).

5 Potential benefits from endophytes in agriculture

Although the endophytes were discovered in early 19th centu-ry, they were studied inmore detail only from the 80’s onwards.Soon after 90’s endophytes were accepted as being of greatimportance for the hosts, protecting the plants against plantpathogenic fungi, bacteria, pests, insects, nematodes, etc.

From the potential benefit point of view, the microbial endo-phytes are much attractive in all fields of life, as they are liableto contain new genes in presumption and held promising novelproducts, thus the chance of finding new and novel bioactivecompounds from endophytic microorganisms is considerable(Qin et al. 2011). The endophytic microorganisms associatedwith traditionally medicinal plants are considered to be a richsource of bioactive functional metabolites (Strobel and Daisy2003; Rai et al. 2012). The growing interest in endophytic fungiand their beneficial activities is apparent from the researchcontinuously carried out throughout the globe, to combat cur-rent biological crises and demand in various field of life espe-cially medicine and agriculture (Qin et al. 2011; Rai et al. 2012;Varma et al. 2012). Recent studies of the culturable endophyticmicroorganisms resulted in the extraction and identification ofmany novel chemical compounds with potentially diverse bio-logical activities (Qin et al. 2011; Gangwar et al. 2012).

The endophytes are considered as the gold mines of life,because these organisms produce vast number of biologicallyactive compounds, as well as are beneficial for growth anddevelopment of host plants (Rai 2003; Gangwar et al. 2012). Apotential beneficial use of microbial endophytes is growth anddevelopment of the host plants. In 1998, Varma and colleaguesdiscovered Piriformospora indica in the desert soil of Rajasthan,India, which belongs to Basidiomycotina (Verma et al. 1998).P. indica is an endophyte and has tremendous capacity to en-hance growth of host plant through its root-colonization (Raiet al. 2001, 2012; Prasad et al. 2013). Gangwar et al. (2012)isolated endophytic actinomycetes from healthy wheat plantsand analyzed their role in pathogen defense and growth regula-tion for their hosts. These endophytic actinomycetes showedvarious abilities for the growth promotion and development ofhost wheat plant. The endophytes helped in phosphate solubili-zation and produced good concentrations of plant growth hor-mone IAA (Indole Acetic Acid). Some of these actinomycetesalso produce catechol and hydroxamate type of siderophore,indicating that healthy tissues of plants harbor diversity of endo-phytic actinomycetes with functional diversity (Verma et al.2009; Gangwar et al. 2012). There is a big list of endophyticmicroorganisms which are capable of synthesizing variouschemicals for the growth of development of the host plants(Taechowisan et al., 2003: Verma et al. 2009). If practiced, thesemicrobial endophytes can become a boon for future agriculture.

Endophytes promote the growth and developments incrops and plants through different ways which includes theproduction of phytohormones like Auxins (IAA) (Lee et al.2004; Verma et al. 2009; Gangwar et al. 2012) andGebberillins (Khan and Lee 2013), solubilisation of phos-phates and the production of a siderophore (Wakelin et al.2004; Verma et al. 2009; Gangwar et al. 2012). There are alsoreports that endophytic organisms able to help plants in os-motic adjustments, stomatal regulation supply of essentialvitamins (Pirttilä et al. 2004; Leite et al. 2012), modification

M. Rai et al.

of root morphology, uptake of minerals like nitrogen accumu-lation (Compant et al. 2005).

Endophytes synthesize biocontrol agents, used to protect thecrops and plants from microbial infection (Fungi and Bacteria),insects (Nematodes) and viral infections. Kloepper and Ryu(2006) studied the role of endophytes in plant systemic acquiredresistance (SAR). The Endophytes isolated from leaves ofcucumber were observed for effective control of Botrytiscinerea, inhibiting the spore germination and germ tube elon-gation of these deadly pathogenic fungi (Kloepper and Ryu2006). The chemical derivatives of endophytic fungiAspergillus clavatonanicus from Torreya mairei synthesizingclavatol, Phomopsis sp. (YM 311483) and Xylaria sp. produc-ing lactones, the glucoside derivatives (Xularosides A) pro-duced by Xylaria sp., Pestalotiopsis jesteri synthesizingJesterone, the Chloridium sp producing Javanicin and the me-tabo l i t e s Phomoenamide , Phomoni t roes te r andDeacetylphomoxanthone B synthesized by endophytic fungusPhomopsis sp. (PSU D), all exhibit the strong antifungal activ-ities both against plant and animal pathogenic fungi(Jalgaonwala et al. 2011).

This was also presumed that endophytes are helpful inphytoremediation of contaminated soil and water bodies,along with forest regeneration and agricultural crops produc-tion. Some endophytic microorganisms also exhibit xenobi-otics degrading abilities, most of these endophytes are hostedby plants growing in soil contaminated with xenobiotics. Thegenome of these organisms gifted with contaminant degradinggenes (Siciliano et al., 2001). It was seen in endophytic strainsof Methyl-bacterium isolated from hybrid poplar trees, har-boring the property of biodegradation of nitro-aromatic com-pounds such as 2,4,6- trinitrotoluene (Van et al. 2004). Theseendophytes have the potential for phytoremediation bydegrading xenobiotic components of soil and thus decreasingsoil and water toxicity (Barac et al. 2004).

The ideal strategy for sustainable agriculture, improvementin crop growth and reduction in effects of toxic metals is theprimary demand of present world. The resilience shown by theendophytes (fungal endophytes) mainly associated with cropplants in contaminated fields of agriculture will be an impor-tant step towards reduced agrochemical pollutions. Khan andLee (2013) studied the metal resistant endophytes Penicilliumfuniculosum LHL06 and revealed its role in rescuing cropplants and their metabolism during metal stresses of Copperand Cadmium. The Endophyte saves the host-plant by mini-mizing electrolytic leakage and lipid peroxidation induced byCopper and also reduces glutathione action to evade oxidativestress. The symbiont also synthesizes large amounts of prolineand glutamate used to reduce stress. The production ofabscisic acid a stress phytohormone is also down-regulatedduring plant-metal-microbe association (Khan and Lee 2013).Such stress tolerance mediating and growth promoting endo-phytic organisms can be practiced at field levels to enhance

the bioremediation of the chemical and metal polluted agri-cultural fields. The endophytic fungi also play important rolein the resistance of host plant against its insect herbivores, byproducing large number of varied defensive compounds in thedifferent tissues of host or through change in nutritional qual-ities of plants. Two endophytic fungi Nigrospora sp. andCladosporium sp. isolated from Tinospora cordifolia(Thunb.) Miers when inoculated in the cauliflower (Brassicaolereaceae L.) showed the resistance against the Spodopteralitura (Fab.), a polyphagous pest. Endophyte infected cauli-flower plants harbored the resistance against the pests bylarval and pupal mortality in the presence of endophyticorganisms (Thakur et al. 2013).

The balanced antagonism and high variability of endo-phytes can be generally characterized with endophyte-hostinteractions, which confirm the symbiotic interactions cangrow within a scale ranging from mutualism to commensal-ism, and ultimately results in pathogenicity. Even though, thissystem of fungal endophytes really donates the host with anabsolute phenotype for its survival. Demonstrating a numberof activities in favor of host plant like, metabolism, stresstolerance and nutrition acquisition are strengthened or adaptedby fungal endophyte (Yuan et al. 2010). Awell known fungalendophyte Piriformospora indica, belonging to orderSebacinales, determines the resistance of host to biotic andabiotic stress, simultaneously (Verma et al. 1998; Rai et al.2001). The fungal organisms including foliar endophytes androot endophytes are also being deeply exploited to producebiologically active compounds, resulting in over expression ofstress-related enzymes, inducing resistance in hosts uponstress. This fungal colonization of endophytes is responsiblefor beneficial effects to hosts directly or indirectly (Yuan et al.2010). Moreover more study is needed for enhancement ofhost performance and fitness by endophyte colonization. Thiswill offer valuable approach for plant cultivation and breed-ing. For now, the discovery of indigenously novel endophytes(Fungi and Bacteria) from natural habitats is urgently neededto avoid extraordinary loss of biodiversity.

Endophytes provide an inbuilt systemic resistance for thehost plants against pests and Insects. A variety of defensivepesticide chemicals in the form of alkaloids are synthesized byendophytes or by host plants itself in response to endophyte(Easton et al. 2009). These alkaloids are generally distastefuland poisonous to chinch bugs, webworms, billbugs and sev-eral other surface-feeding insects. Though the endophytesproducing alkaloids are more efficient against above-groundinsect and pests, they also have an impact on below-groundplant parasitic nematodes. Generally, the endophytic fungusand production of alkaloids are concentrated in abovegroundplant parts, but it has also been seen that as much as 15 % ofthe lolines (N-formyl loline, N-acetyl loline and N-acetylnorloline) and smaller amounts of ergot alkaloids occur inroots. Ergot alkaloids are strong deterrents against insects like


beetle gurbs and are helpful to reduced their survival andweight. Also in the vicinity of endophyte containing grasses;the parasitic root nematodes in the soil have been found to besmaller (Bush et al. 1997). These ergot alkaloids have anaction on vaso-constriction in mammals. Contraction of smallblood vessels in brain organs etc. can result in con-vulsions,dementia and gangrene. Also the bitter tastes of alkaloids deterherbivores, insects and pests (Clay 1998).

Aside from the direct toxic effect of endophyte-infectedplants have on many surface feeding insects, endophytes alsoalter insect foraging behavior. Insects such as chinch bugs andsod webworms spend more time moving and less time feedingin stands of turf grass containing even moderate proportions ofendophyte-infected plants. This increase in movement makesthe insects much more vulnerable to predators and pathogens(Clay 1998).

6 Key area for research

The researchers all over the world are engaged in searchingand developing new ways for sustainable agriculture that have

a minor environmental impact with high affectivity and lowtoxicity. This search is the response against the chal-lenges posed by agrochemicals used in agricultureresulting into environmental pollution. The study ofendophytic microorganisms is a broad field of investi-gation and is entirely open to new findings and discov-eries. The results presented in this review show that,great diversity has been found among fungal endophytesisolated from various hosts. These play important rolesfor protecting plants against pests, diseases, herbivores,environmental stresses and help them to gear up growthand development by providing those minerals etc. Thus,it is predictable that new ways of relations and interac-tions between endophytes and their hosts will beestablished for convenience. This will boost the studiesfocusing on these microorganisms, to synthesize thechemicals of interest. Much more work is needed tounderstand the physiology, biochemical pathways, de-fensive role, secondary metabolite production, relatedto endophytes and their host. There is a pressing needto study the role of endophytes in production of sec-ondary metabolites both in vivo and in vitro.

Fig. 2 Future approach forproduction and application ofendophytic fungal inoculants

M. Rai et al.

The biotechnological approaches can be applied for ad-vancement of chemical synthesis by endophytes, use of ge-netic engineering tools to develop the methods of gene trans-fer and cloning techniques so that the new generation oforganisms can be developed to combat the upcoming crisesin present day agriculture. Further, growing endophytes inlarge scale, modifying culture conditions like changing pH,changing growth media and supplying some stimulants mighthelp in getting better production of the particular bioactivecompound for agricultural purpose (Fig. 2). Finally, a numberof synthetic agricultural products have been removed from themarket due to safety and environmental problems so there isalso a need to discover an alternative to control crop pests andpathogens to increase in growth of crops. To overcome thechemical use and pathogens attack on crops, there is need for avariety of novel agrochemical bioactive compounds of bio-logical origin.

7 Conclusions

Plant endophytic fungi, as a novel and abundant microorgan-ism resource, owning the special ability to produce the sameor similar compounds originated from their host plants, as wellas other bioactive compounds, have increased manyinvestigators interesting in both basic research and appliedfields. Many novel and valuable bioactive compounds withantimicrobial, insecticidal and growth promoting activitieshave been successfully obtained from the endophytic fungi.During the long period of co-evolution, the endophytic fungihave adapted themselves to their special microenvironmentsgradually by genetic variation, including uptake of plant DNAsegments into their own genomes, as well as insertion of theirDNA segments into the host genomes. This could have led tocertain endophytes own the ability to biosynthesize somephytochemicals originated from their host plants.The need for new bioactive compounds to overcome the

growing problems of agriculture pathogen attack on crop plantis of increasing importance. The capability of fungi to producebioactive fungal metabolites have encouraged researchers toisolate and screen fungi from diverse habitat and environ-ments to search for novel bio-active metabolites. Many areable to produce quite a good amount of antimicrobial com-pounds tested in preliminary test. If endophytes produce thegrowth hormones as their host it would reduce the use ofchemical fertilizer also. Furthermore, a microbial source of ahigh-value product is an economical way to produce a metab-olite in a bulk quantity and thus reducing its market price. Thefungal endophytes hold enormous potential as sources ofagrochemical bioactive compounds. These endophytes mayopen up new vistas for the development of eco-friendly andeconomically viable agricultural products.

References

Ali S. (2013) Plant growth-promoting bacterial endophytes that containacc deaminase: isolation, characterization, and use. Thesis,University of Waterloo. Waterloo, Ontario, Canada

Amna T, Khajuria RK, Puri SC, Verma V, Qazi GN (2006) Determinationand quantification of camptothecin in an endophytic fungus byliquid chromatography positive mode electrospray ionization tan-dem mass spectrometry. Curr Sci 91(2):208–212

Arnold AE (2008) Endophytic fungi: hidden components of tropicalcommunity ecology. In: Carson WP, Schnitzer SA (eds) Tropicalforest community ecology. Blackwell Publishing Ltd, West Sussex,pp 178–188

Arnold A, Maynard Z, Gilbert G, Coley P, Kursar T (2000) Are tropicalendophytes hyperdiverse? Ecol Lett 3(4):267–274

Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, HerreEA (2003) Fungal endophytes limit pathogen damage in a tropicaltree. Proc Natl Acad Sci U S A 100(26):15649–15654

Asselbergh B, De Vleesschauwer D, HöfteM (2008) Global switches andfine-tuning-ABA modulates plant pathogen defense. Mol PlantMicrobe Interact 21:709–719

Bacon CW, White JF (2000) Microbial endophytes. Marcel Deker Inc,New York, pp 99–101

Bacon CW, Porter JK, Robins JD, Luttrell ES (1977) Epichloë typhi fromtoxic tall fescue grasses. Appl Environ Microbiol 34:576–581

Bae H, Sicher RC, Kim MS, Kim SH, Strem MD, Melnick RL, BaileyBA (2009) The beneficial endophyte Trichoderma hamatum isolateDIS 219b promotes growth and delays the onset of the droughtresponse in Theobroma cacao. J Exp Bot 60(11):3279–3295

Baker GM, Pottinger RP, Addison PJ, Prestidge R (1984) Effect ofLolium endophyte fungus infections on behaviour of argentine stemweevil. N Z J Agric Res 27:271–277

Balbi V, Devoto A (2008) Jasmonate signaling network in Arabidopsisthaliana: crucial regulatory nodes and new physiological scenarios.New Phytol 177:301–318

Bandara WMMS, Seneviratne G, Kulasooriya SA (2006) Interactionsamong endophytic bacteria and fungi: effects and potentials. J Biosci31:645–650

Banerjee D (2011) Endophytic fungal diversity in tropical and subtropicalplants. Res J Microbiol 6:54–62

Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV,Vangronsveld J, van der Lelie D (2004) Engineered endophyticbacteria improve phytoremediation of water-soluble, volatile, orga-nic pollutants. Nat Biotechnol 22:583–588

Bashyal B, Li JY, Strobel GA, Hess WM (1999) Seimatoantleriumnepalense, an endophytic taxol producing coelomycete fromHimalayan yew (Taxus wallichiana). Mycotaxon 72:33

Belesky DP, Malinowski DP (2000) Abiotic stresses and morphologicalplasticity and chemical adaptations of Neotyphodium-infected tallfescue plants. In: Bacon CW, Jr. White JF (eds) Microbial endo-phytes. Marcel Dekker, New York, pp 455–484

Berg G (2009) Plant-micro interactions promoting plant growth andhealth: perspectives for controlled use of microorganisms in agri-culture. Appl Microbiol Biotechnol 84:11–18

Bhagobaty RK, Joshi SR (2009) Promotion of seed germination of Greengram and Chick pea by Penicillium verruculosum RS7PF, a rootendophytic fungus of Potentilla fulgens L. Adv Biotechnol 16–18

Bomke C, Rojas MC, Gong F, Hedden P, Tudzynski B (2008) Isolationand characterization of the gibberellin biosynthetic gene cluster inSphaceloma manihoticola. Appl Environ Microbiol 74:5325–5339

Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteriaand its involvement in plant growth promotion and yield increase.Appl Microbiol Biotechnol 65:497–503

Brodersen P, Petersen M, Nielsen HB, Zhu S, NewmanMA, Shokat KM,Rietz S, Parker J, Mundy J (2006) Arabidopsis MAP kinase 4


regulates salicylic acid- and jasmonic acid/ethylene-dependent re-sponses via EDS1 and PAD4. Plant J 47:532–546

Bush LP, Wilkinson HH, Schard CL (1997) Bioprotective alkaloids ofgrass-fungal endophyte symbioses. Plant Physiol 114:1–7

Choi WY, Rim SO, Lee JH, Lee JM, Lee IJ, Cho KJ (2005) Isolation ofgibberellins-producing fungi from the root of several Sesamumindicum plants. J Microbiol Biotechnol 15:22–28

Clay K (1998) Fungal endophytes of grasses: a defensive mutualismbetween plants and fungi. Ecology 69(1):10–16

Clay K, Schardl C (2002) Evolutionary origins and ecological conse-quence of endophyte symbiosis with grasses. Am Nat 160:99–127

Cohen AC, Bottini R, Piccoli P (2008) Azospirillum brasilense Sp 245produces ABA in chemically-defined culture medium and increasesABA content in Arabidopsis plants. Plant Growth Regul 54:97–103

Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plantgrowth promoting bacteria for biocontrol of plant diseases: princi-ples, mechanisms of action and future prospects. Appl EnvironMicrobiol 71:4951–4959

Contreras-Cornejo HA (2009) Trichoderma virens, a plant beneficialfungus, enhances biomass production and promotes lateral rootgrowth through an auxin-dependent mechanism in Arabidopsis.Plant Physiol 149:1579–1592

Cox PA, Balick MJ (1994) The Ethnobotanical approach to drug discov-ery. Sci Am 270(6):82–87

Daly JM, Inman RE (1958) Changes in auxin levels in safflower hypo-cotyls infected with Puccinia carthami. Phytopathology 48:91–97

Davies PJ (2004).The plant hormones: their nature, occurrence, andfunctions. Chapter A. Davies PJ (eds) Plant Hormones biosynthesis,signal transduction, action. 3rd edition. Kluwer Academic Publisher

Dekhuijzen HM, Overeem JC (1971) The role of cytokinins in clubrootformation. Physiol Plant Pathol 1:151–161

Dighton J (2003) Fungi in ecosystem processes. Marcel Dekker, NewYork. ISBN 978-0-8247-4244-7

Dreyfuss M, Chapela I (1994) Potential of fungi in the discovery of novel,low-molecular weight pharmaceuticals. The discovery of natural prod-ucts with therapeutic potential (Gullo VP, ed), 26(5) pp 26(5):49–80

Easton HS, Lyons TB, Cooper BM, MaceWJ (2009) Loline alkaloids forbetter protection of pastures from insect pests. Proc N Z GrasslAssoc 71:151–154

Fávaro LC, Sebastianes FL, AraújoWL (2012)Epicoccum nigrum P16, asugarcane endophyte, produces antifungal compounds andinducesroot growth. PLoS One 7(6):e36826. doi:10.1371/journal.pone.0036826

Franken P, Butehorn B, Verma A (1998) Piriformospora indica, a culti-vable root cell-infecting fungus promotes the growth of a broadrange of plant species. p. 65. In Ahonen-Jonnarth U, Danell E,Fransson P, Kårén O, Lindahl B, Rangel I, and R

Gangwar M, Rani S, Sharma N (2012) Diversity of endophyticactinomyetes fromwheat and its potential as plant growth promotingand biocontrol agents. J Adv Lab Res Biol 3(1):18–23

Gasoni L, De Gurfinkel BS (1997) The endophyte Cladorrhinumforcundissimum in cotton roots: phosphorus uptake and host growth.Mycol Res 101:867–870

Govinda ra j an M, Ba landreau J , Kwon SW, Weon HY,Lakshminarasimhan C (2008) Effects of the inoculation ofBurkholderia vietnamensis and related endophytic diazotrophic bac-teria on grain yield of rice. Microb Ecol 55:21–37

Hamayun M, Khan SA, Ahmad N, Tang DS, Kang SM, Na CI, Sohn EY,Hwang YH, Shin DH, Lee BH, Kim JG, Lee IJ (2009a)Cladosporium sphaerospermum as a new plant growth-promotingendophyte from the roots of Glycine max (L.) Merr. World JMicrobiol Biotechnol 25:627–632

Hamayun M, Khan SA, Iqbal I, Hwang YH, Shin DH, Sohn EY, LeeBH, Na CI, Lee IJ (2009b) Chrysosporium pseudomerdariumproduces gibberellins and promotes plant growth. J Microbiol47:425–430

Hamayun M, Khan SA, Khan MA, Khan AL, Kang SM, Kim SK, JooGJ, Lee IJ (2009c) Gibberellin production by pure cultures of a newstrain of Aspergillus fumigates. World J Microbiol Biotechnol 25:1785–1792

Hamayun M, Khan SA, Kim HY, Chaudhary MF, Hwang YH, Shin DH,Kim IK, Lee BH, Lee IJ (2009d) Gibberellin production and plantgrowth enhancement by newly isolated strain of Scolecobasidiumtshawytschae. J Microbiol Biotechnol 19(6):560–565

Hamayun M, Khan SA, Iqbal I, Ahmad B, Lee IJ (2010a) Isolation of agibberellin-producing fungus (Penicillium sp. MH7) and growthpromotion of Crown Daisy (Chrysanthemum coronarium). JMicrobiol Biotechnol 20(1):202–207

Hamayun M, Khan SA, Khan AL, Rehman G, Kim YH, Iqbal I, HussainJ, Sohn EY, Lee IJ (2010b) Gibberellin production and plant growthpromotion from pure cultures of Cladosporium sp. MH-6 isolatedfrom cucumber (Cucumis sativus L.). Mycologia 102(5):989–995

Hasan HAH (2002) Gibberellin and auxin production by plant root fungiand their biosynthesis under salinity-calcium interaction. RostlinnáVýroba 48:101–106

Herre EA, Mejia LC, Kyllo DA, Rojas E, Maynard Z, Butler A,Van Bael SA (2007) Ecological implications of anti-pathogeneffects of tropical fungal endophytes and mycorrhizae.Ecology 88(3):550–558

Hill NS, Belesky DP, Stringer WC (1990) Competitiveness of tall fescueas influenced by Acremonium coenophialum. Crop Sci 31:185–190

Hwang JS, You YH, Bae JJ, Khan SA, Kim JG, Choo YS (2011) Effectsof endophytic fungal secondary metabolites on the growth andphysiological response of Carex kobomugi Ohwi. J Coastal Res27:544–548

Hyde KD, Doytong K (2008) The fungal endophyte dilemma. FungalDiv 33:163–173

Jalgaonwala RE, Mohite BV, Mahajan RT (2011) A review: naturalproducts from plant associated endophytic fungi. J MicrobiolBiotech Res 1(2):21–32

Jerry B (1994) A role of endophytic fungi in regulating nutrients andenergy in plants within a desert ecosystem. International symposiumand workshop on desertification in developed countries. Accessedon 2011/10/25

Jha P, Kumar A (2009) Characterization of novel plant growth promotingendophytic bacterium Achromobacter xylosoxidans from wheatplant. Microb Ecol 58:179–188

Karsten K, Umar F, Ulrich F, Barbara S, Siegfried D, Gennaro P, Piero S,Sándor A, Tibor K (2007) Secondary metabolites isolated from anendophytic phoma sp.absolute configuration of tetrahydropyrenophorolusing the solid-state TDDFT CD methodology. Eur J Org Chem 19:3206–3211

Kawaguchi M, Sydn K (1996) The excessive production of indole-3-acetic acid and its significance in studies of the biosynthesis of thisregulator of plant growth and development. Plant Cell Physiol 37:1043–1048

Kawaide H (2006) Biochemical and molecular analysis of gibberellinsbiosynthesis in fungi. Biosci Biotech Biochem 70:583–590

Kawaide H, Sassa T (1993) Accumulation of gibberellins A1 and themetabolism of gibberellin A9 to gibberellin A1 in a Phaeosphaeriasp. L 487 culture. Biosci Biotech Biochem 57:1403–1405

Khan AL, Lee IJ (2013) Endophytic Penicillium funiculosum LHL06secretes gibberellin that reprograms Glycine max L. growth duringcopper stress. BMC Plant Biol 13(1):86

Khan SA, HamayunM, Yoon HJ, KimHY, Suh SJ, Hwang SK, Kim JM,Lee IJ, Choo YS, Yoon UH, Kong WS, Lee BM, Kim JG (2008)Plant growth promotion and Penicillium citrinum. BMC Microbiol8:231

Khan SA, Hamayun M, Kim HY, Yoon HJ, Seo JC, Choo YS (2009a) Anew strain of Arthrinium phaeospermum isolated from Carexkobomugi Ohwi is capable of gibberellins production. BiotechnolLett 31:283–287

M. Rai et al.

http://dx.doi.org/10.1371/journal.pone.0036826


Khan SA, Hamayun M, Kim HY, Yoon HJ, Lee IJ, Kim JG (2009b)Gibberellin production and plant growth promotion by a newlyisolated strain of Gliomastix murorum. World J MicrobiolBiotechnol 25:829–833

Khan AL, HamayunM, Ahmad N,Waqas M, Kang SM, Kim YH, Lee IJ(2011a)Exophiala sp. LHL08 reprogramsCucumis sativus to highergrowth under abiotic stresses. Physiol Plant 143(4):329–343

Khan AL, HamayunM,KimYH,Kang SM, Lee IJ (2011b) Ameliorativesymbiosis of endophyte (Penicillium funiculosum sp. LHL06) undersalt stress elevated plant growth of Glycine max L. Plant PhysiolBiochem 49(8):852–862

Khan AL, Hamayun M, Kim YH, Kang SM, Lee JH, Lee IJ (2011c)Gibberellins producing endophytic Aspergillus fumigatus sp. LH02influenced endogenous phytohormonal levels, isoflavonoids pro-duction and plant growth in salinity stress. Process Biochem 46:440–447

Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, Lee IJ(2012a) Endophytic fungal association via gibberellins and indoleacetic acid can improve plant growth under abiotic stress: an exam-ple of paecilomyces formosus LHL10. BMC Microbiol 12:3

Khan SA, HamayunM, Khan AL, Lee IJ, Shinwari ZK, Kim JG (2012b)Isolation of plant growth promoting endophytic fungi from dicotsinhabiting coastal sand dunes of Korea. Pak J Bot 44(4):1453–1460

Kharwar RN, Verma VC, Strobel G, Ezra D (2008) The endophyticfungal complex of Catharanthus roseus (L.) G. Don. Curr Sci95(2):228–233

Kiraly Z, El-Hammady M, Pozsar BI (1967) Increased cytokinin activityof rust infected bean and broad bean leaves. Phytopathology 57:93–94

Kloepper JW, Ryu CM (2006) Bacterial endophytes as elicitors of in-duced systemic resistance. Soil Biol 9:33–52

Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effectson plants and uses in agriculture. In: Bacon CW, White JF (eds)Microbial endophytes. Marcel Dekker, Inc., New York, pp 199–233

Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interac-tions during seed dormancy release and germination. Seed Sci Res15:281–307

Kumar V, Asija (2000) Biodiversity conservation in: biodiversity-principles and conservation. Agrobiosis (India), Jodhpur

Kumar M, Yadav V, Kumar H, Sharma R, Singh A, Tuteja N, Johri AK(2011) Piriformospora indica enhances plant growth by transferringphosphate. Plant Signal Behav 6(5):723–725

Kumari R, Kishan H, Bhoon YK, Varma A (2003) Colonization ofcruciferous plants by Piriformospora indica. Curr Sci 85(12):1672–1674

Latch GCM, Hunt WF, Musgrave DR (1985) Endophytic fungi affectgrowth of perennial ryegrass. N Z J Agric Res 28:165–168

Lee S, Flores-Encarnacion M, Contreras-Zentella M, Garcia-Flores L,Escamilla JE, Kennedy C (2004) Indole-3-acetic acid biosynthesis isdeficient in Glucon acetobacter diazotrophicus strains with muta-tions in cytochrome C biogenesis genes. J Bacteriol 186:5384–5391

Lee YC, Johnson JM, Chien CT, Sun C, Cai D, Lou B, Oelmuller R, YehKW (2011) Growth promotion of Chinese cabbage and Arabidopsisby Piriformospora indica is not stimulated by mycelium-synthe-sized auxin. Mol Plant-Microbe Interactions 24:421–431

Lekberg Y, Koide RT (2005) Is plant performance limited by abundanceof arbuscular mycorrhizal fungi? a metaanalysis of studies publishedbetween 1988 and 2003. New Phytol 168(1):189–204

Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R (2004)JASMONATE-INSENSITIVE encodes a MYC transcriptionfactor essential to discriminate between different jasmonate-regulated defence responses in Arabidopsis. Plant Cell 16:1938–1950

Lucangeli C, Bottini R (1997) Effects of Azospirillum spp. on endoge-nous gibberellin content and growth of maize (Zea mays L.) treatedwith uniconazole. Symbiosis 23:63–72

Ludwig-Müller J (1999) The biosynthesis of auxins. Curr Top Plant Biol1:77–88

Ludwig-Müller J (2000) Hormonal balance in plants during colonizationby mycorrhizal fungi. In: Douds DD, Kapulnik Y (eds) Arbuscularmycorrhizas: physiology and function. Kluwer AcademicPublishers, Dordrecht, pp 263–285

Ludwig-Müller J, Vertocnik A, Town CD (2005) Analysis of indole-3-butyric acid-induced adventitious root formation on Arabidopsisstem segments. J Exp Bot 56:2095–2105

Machungo C, Losenge T, Kahangi E, Coyne D, Dubois T, Kimenju J(2009) Effect of endophytic Fusarium oxysporum on growth oftissue-cultured Banana plants. Afr J Hort Sci 2:160–167

Mahmoud RS, Narisawa K (2013) A new fungal endophyte,Scolecobasidium humicola, promotes tomato growth under organicnitrogen conditions. PLoS One 8(11):e78746. doi:10.1371/journal.pone.0078746

Malfanova N, Kamilova F, Validov S, Shcherbakov A, Chebotar V,Tikhonovich I, Lugtenberg B (2011) Characterization of Bacillussubtilis HC8, a novel plant-beneficial endophytic strain from gianthogweed. Microb Biotech 4:523–532

Mander LN (2003) Twenty years of gibberellin research. Nat Prod Rep20:49–69

Marina S, Angel M, Silva-Flores MA, Cervantes-Badillo MG, Rosales-Saavedra MT, Islas-Osuna MA, Casas-Flores S (2011) The plantgrowth-promoting fungus Aspergillus ustus promotes growth andinduces resistance against different lifestyle pathogens inArabidopsis thaliana. J Microbiol Biotechnol 21(7):686–696

Martin GC (1983) The Biochemistry and Physiology of Gibberellins, A.Crozier (ed.). Praeger, New York. 2: 395–444

Mei C, Flinn BS (2010) The use of beneficial microbial endophytes forplant biomass and stress tolerance improvement. Recent PatentsBiotechnol 4:81–95

Miliūtė I, Buzaitė O (2011) IAA production and other plant growthpromoting traits of endophytic bacteria from apple tree.Biogeosciences 57(2):98–102

Ming Q, Su C, Zheng C, Jia M, Zhang Q, Zhang H, Rahman K, Han Tand Qin L, (2013) Elicitors fromthe endophytic fungus Trichodermaatroviride promote Salvia miltiorrhiza hairy root growth andtanshinone biosynthesis. J Exp Bot. (Epub ahead of print)

Mitchell AM, Strobel GA, Moore E, Robison R, Sears J (2010) Volatileantimicrobials fromMuscodor crispans, a novel endophytic fungus.Microbiology 156:270–277

Nadeem A, Hamayun M, Khan SA, Khan AL, Lee IJ, Shin DH (2010)Gibberellin-producing endophytic fungi isolated from Monochoriavaginalis. J Microbiol Biotechnol 20(12):1744–1749

Naik BS, Shashikala J, Krishnamurthy YL (2008) Host growth charac-teristics influenced by seed inoculation with microorganisms. WorldJ Agric Sci 4(S):891–895

Nassar HA, El-Tarabily KA, Sivasithamparam K (2005) Promotion ofplant growth by an auxin-producing isolate of the yeast Williopsissaturnus endophytic in maize (Zea mays) roots. J Biol Fertil Soils42:2

Niere B (2001) Significance of non-pathogenic isolates of Fusariumoxysporum Schlecht, Fries for the biological control of theburrowing nematode Radopholus similis (Cobb) Thorne on tissue-cultured bananas. PhD Thesis, University of Bonn, Germany.

Nishijima T, Koshioka M, Yamazaki H, Mander LN (1995) Endogenousgibberellins and bolting in cultivars of Japanese radish. Acta Hortic394:199–206

Oelmüller R, Shahollari B, Peškan-Berghöfer T, Trebicka A, Giong PH,Sherameti I, Oudhoff M, Venus Y, Altschmied L, Varma A (2004)Molecular analyses of the interaction between Arabidopsis roots andthe growth-promoting fungus Piriformospora indica .Endocytobiosis Cell Res 15:504–517

Pandey MK, Singh AK, Singh RB (2002) Mycotoxic potential ofsomehigher plants. Plant Dis Res 17:51–56




Peng J, Harberd NP (2002) The role of GA-mediated signalling in thecontrol of seed germination. Curr Opin Plant Biol 5:376–381

Petrini OTN, Sieber LT, Viret O (1992) Ecology metabolite productionand substrate utilization in endophytic fungi. Natl Toxin 1:185–196

Pieterse CM, Dicke M (2007) Plant interactions with microbes andinsects: from molecular mechanisms to ecology. Trends Plant Sci12:564–569

Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M (2010)Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514

Pirttilä AM, Joensuu P, Pospiech H, Jalonen J, Hohtola A (2004) Budendophytes of Scots pine produce adenine derivatives and othercompounds that affect morphology and mitigate browning of calluscultures. Physiol Plant 121:305–312

Pocasangre L (2000) Biological enhancement of tissue culture plantletswith endophytic fungi for the control of the burrowing nematodeRadopholus similis and the panama disease (Fusarium oxysporum f.sp. cubense). PhD Thesis, University of Bonn, Germany

Posada F, Vega FE (2005) Establishment of the fungalentomopathogen Beauveria bass iana (Ascomycota:Hypocreales) as an endophyte in cocoa seedl ings(Theobroma cacao). Mycologia 97:1195–1200

Prasad R, Kamal S, Sharma PK, Oelmüller R, Varma A (2013) Rootendophyte Piriformospora indicaDSM 11827 alters plant morphol-ogy, enhances biomass and antioxidant activity of medicinal plantBacopa monniera. J BasicMicrobiol. doi:10.1002/jobm.201200367

Prince L, Prabakaran P (2011) Antifungal activity of medicinal plantsagainst plant pathogenic fungus Colletotrichum falcatum. Asian JPlant Sci Res 1(1):84–87

Qin S, Xing K, Jiang J, Xu L, Li W (2011) Biodiversity, bioactive naturalproducts and biotechnological potential of plant-associated endo-phytic actinobacteria. Appl Microbiol Biotechnol 89:457–473

Rademacher W (1994) Gibberellin formation in microorganisms. PlantGrowth Reg 15:303–314

RaiMK (2003) Plant-DerivedAntimycotics. Haworth Press, BinghamtonRai M, Varma A (2005) Arbuscular mycorrhiza-like biotechnolog-

ical potential of Piriformospora indica, which promotes thegrowth of Adhatoda vasica Nees. Electron J Biotechnol 8(1):107–112

RaiMK, Acharya D, Singh A, Varma A (2001) Positive growth responsesof the medicinal plants Spilanthes calva and Withania sonmifera toinoculation by Piriformospora indica in a field trial. Mycorrhiza 11:123–128

Rai MK, Varma A, Pandey AK (2004) Antifungal potential of Spilanthescalva after inoculation of Piriformospora indica. Mycoses 47:479–481

Rai M, Gade A, Rathod D, Dar M, Varma A (2012) Review:mycoendophytes in medicinal plants: diversity and bioactivities.Nusantara Biosci 4(2):86–96

Raskin I (1992) Role of salicylic acid in plants. Annu Rev Plant PhysiolPlant Mol Biol 43:439–463

Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L (2011)Increased fitness of rice plants to abiotic stress via habitat adaptedsymbiosis: a strategy formitigating impacts of climate change. PLoSONE 6:e14823

Robert PR, Kieran G, Ashley F, David JR, David ND (2008) Bacterialendophytes: recent developments and applications. FEMSMicrobiol Lett 278:1–9

Rodrigues-Heerklotz KF, Drandarov K, Heerklotz J, Hesse M,Werner C (2001) Guignardic acid, a novel type of secondarymetabolite produced by the endophytic fungus guignardia sp.:isolation, structure elucidation, and asymmetric synthesis.Helv Chim Aca 84:3766

Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungalendophytes: diversity and functional roles. New Phytol 182(2):314–30

Rodríguez-Gacio MDC, Matilla-Vázquez MA, Matilla AJ (2009) Seeddormancy and ABA signaling: the breakthrough goes on. PlantSignal Behav 4(11):1035–1048

Rothballer M, Eckert B, Schmid M, Fekete A, Schloter M, Lehner A,Pollmann S, Hartmann A (2008) Endophytic root colonization ofgramineous plants by Herbaspirillum frisingense. FEMS MicrobiolEcol 66:85–95

Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterialendophytes: recent developments and applications. FEMSMicrobiol Lett 278(1):1–9

Schäfer P, Pfiffi S, Voll LM, Zajic D, Chandler PM, Waller F, Scholz U,Pons-Kühnemann J, Sonnewald S, Sonnewald U, Kogel KH (2009)Manipulation of plant innate immunity and gibberellins as factor ofcompatibility in the mutualistic association of barley roots withPiriformospora indica. Plant J 59:461–474

Schardl CL, Phillips TD (1997) Grass endophytes. Plant Dis 81:5Schulz B (2002) Endophytic fungi: a source of novel biologically active

secondary metabolites. Mycolog Res 106:996–1004Schulz B, Boyle C (2005) The endophytic continuum. Mycolog Res 109:

661–686Sgroy V, Cassán F, Masciarelli O, Del Papa MF, Lagares A, Luna V

(2009) Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacte-ria associated to the halophyte Prosopis strombulifera. ApplMicrobiol Biotechnol 85:371–381

Sherameti I, Tripathi S, Varma A, Oelmüller R (2008a) The root coloniz-ing endophyte Pirifomospora indica confers drought tolerance inArabidopsis by stimulating the expression of drought stress–relatedgenes in leaves. Mol Plant-Microbe Interact 21:799–807

Sherameti I, Venus Y, Drzewiecki C, Tripathi S, Dan VM, Nitz I, VarmaA, Grundler FM, Oelmüller R (2008b) PYK10, a β-glucosidaselocated in the endoplasmatic reticulum, is crucial for the beneficialinteraction between Arabidopsis thaliana and the endophytic fungusPiriformospora indica. Plant J 21:799–807

Shi Y, Lou K, Li C (2009) Isolation, quantity distribution and character-ization of Shinozaki, K. and Yamaguchi, S. K. (1997) Gene expres-sion and signal transduction in water-stress response. Plant Physiol.115: 327–334

Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signaltransduction in water-stress response. Plant Physiol 115:327–334

Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved indrought stress response and tolerance. J Exp Bot 58:221–227

Shweta S, Zuehlke S, Ramesha BT, Priti V, Mohana Kumar P, RavikanthG, Spiteller M, Vasudeva R, Uma SR (2010) Endophytic fungalstrains of Fusarium solani, from Apodytes dimidiata E.Mey. ex Arn(Icacinaceae) produce camptothecin, 10-hydroxycamptothecin and9-methoxycamptothecin. Phytochemistry 71(1):117–122

Sirrenberg A, Göbel C, Grond S, Czempinski N, Ratzinger A, KarlovskyP, Santos P, Feussner I, Pawlowski K (2007) Piriformospora indicaaffects plant growth by auxin production. Physiol Plant 131(4):581–589

Stierle A, Strobel GA, Stierle D (1993) Taxol and taxane production byTaxomyces andreanae, an endophytic fungus of Pacifi c Yew.Science 260:214–216

Strobel GA (2003) Endophytes as sources of bioactive products. MicrobInfect 5:535–544

Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes andtheir natural products. Microbiol Mol Biol Rev 67(4):491–502

Sturz AV, Christie B, Nowak J (2000) Bacterial endophytes: potential rolein developing sustainable system of crop production. Crit Rev PlantSci 19:1–30

Sudha, Hurek T, Varma A (1998) Active translocation of phosphate (P32)to rice and carrot by Piriformospora indica. In: Ahonen-Jonnarth U,Danell E, Fransson P, Karen O, Lindahl B, Rangel I, Finlay R (eds)Second International Congress onMycorrhiza. Uppsala, Sweden, pp5–10

M. Rai et al.

http://dx.doi.org/10.1002/jobm.201200367

Suryanarayanan TS, Wittlinger SK, Faeth SH (2005) Endophytic fungiassociated with cacti in Arizona. Mycol Res 109(5):635–639

Sziraki I, Balazs E, Kiraly Z (1975) Increased levels of cytokinin andindole-acetic acid peach leaves infected with Taphrina deformans.Physiol Plant Pathol 5:45–50

Taiz L, Zeiger E (2002) Plant Physiology.3rd edition. Sinauer Associates,Inc., Publishers, Massachusettes

Tan RX, Zou WX (2001) Endophytes: a rich source of functional meta-bolites. Nat Prod Rep 18:448–459

Tenguria RK, Khan FN (2011) Distribution of endophytic fungi in leavesof Azadirachta indica A. Juss. (Neem) of Panchmarhi BiosphereReserve. Curr Bot 2(2):27–29

Thakur A, Kaur S, Kaur A, Singh V (2013) Enhanced resistance toSpodoptera litura in endophyte infected cauliflower plants.Environ Entomol 42(2):240–246

Ting ASY, Meon S, Kadir J, Radu S, Singh G (2007) Endophyticmicroorganisms as potential growth promoters of banana. JBiocontrol 53:541–553

Tsavkelova EA, Bömke C, Netrusov AI, Weiner J, Tudzynski B(2008) Production of gibberellic acids by an orchid-associated Fusarium proliferatum strain. Fungal Genet Biol45:1393–1403

Tuomi T, Ilvesoksa J, Laakso S, Rosenqvist H (1993) Interaction ofabscisic acid and indole-3-acetic acid producing fungi with salixleaves. J Plant Growth Regul 12:149–156

Ueguchi TM, NakajimaM,Motoyuki A,MatsuokaM (2007) Gibberellinreceptor and its role in gibberellin signaling in plants. Annu RevPlant Biol 58:183–198

Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark,septate endophytic fungus, Heteroconium chaetospira and a non-mycorrhizal plant, Chinese cabbage. Mycologia 99:175–184

Van AB, Peres CM, Doty SL, Yoon JM, Schnoor JL (2004)Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented,facultatively methylotrophic, methane-utilizing bacterium isolatedfrom poplar trees (Populus deltoides x nigra DN34) 54:1191–1196

Van Loon LC (2007) Plant responses to plant growth-promotingrhizobacteria. Eur J Plant Pathol 119:243–254

Vanessa MC, Christopher MMF (2004) Analysis of the endophyticactinobacterial population in the roots of wheat (Triticum aestivumL) by terminal restriction fragment length polymorphism and sequenc-ing of 16S rRNA clones. Appl Environ Microbiol 70:31787–31794

Varma A, Verma S, Sudha SN, Bütehorn B, Franken P (1999)Piriformospora indica, a cultivable plant-growth-promoting rootendophyte. Appl Environ Microbiol 65(6):2741–2744

VarmaA, SinghA, Sudha S, Sahay N, Sharma J, RoyA, KumariM, RanaD, Thakran S, Deka D, Bharti K, Franken P, Hurek T, Blechert O,Rexer KH, Kost G, Hahn A, Hock B, Maier W, Walter M, Strack D,Kranner I (2001) Piriformospora indica: A cultivable mycorrhiza-like endosymbiotic fungus. In: Bock B (ed) Mycota IX. SpringerSeries, Springer-Verlag, Berlin, pp 123–150

Varma A, Hartmann A, Bakshi M, Oelmueller R, Lou B (2012)Piriformospora indica: a novel plant growth-promoting mycorrhizalfungus. Agric Res 1(2):117–131

Verma S, Varma A, Rexer K, Hassel A, Kost G, Sarbhoy A, Bisen P,Butehorn B, Franken P (1998) Piriformaspora indica, gen. et sp.nov., a new root-colonizing fungus. Mycologia 90:896–903

Verma VC, Gond SK, Kumar A, Mishra A, Kharwar RN, Gange A(2009) Endophytic actinomycetes from Azadirachta indica A.Juss.: isolation, diversity, and anti-microbial activity. Microb Ecol57:749–756

Vieira ML, Hughes AF, Gil VB, Vaz AB, Alves TM, Zani CL, Rosa CA,Rosa LH (2012) Diversity and antimicrobial activities of the fungalendophyte community associated with the traditional Brazilian me-dicinal plant Solanum cernuum Vell. (Solanaceae). Can J Microbiol58(1):54–66

Vizarova G (1979) Changes in the level of endogenous cytokinins ofbarley during the development of powdery mildews. PhytopatholZool 95:314–329

Wakelin SA, Warren RA, Harvey PR, Ryder MH (2004) Phosphatesolubilization by Penicillium spp. closely associated with wheatroots. Biol Fertil Soils 40(1):36–43

Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, FischerM, Heier T,Huckelhoven R, Neumann C, Von Wettstein D, Franken P, KogelKH (2005) The endophytic fungus Piriformospora indica repro-grams barley to salt-stress tolerance, disease resistance and higheryield. PNAS 102:13386–13391

Waqas M, Khan AL, Hamayun M, Kamran M, Kang SM, Kim YH, LeeIJ (2012a) Assessment of endophytic fungi cultural filtrate on soy-bean seed germination. Afr J Biotechnol 11(85):15135–15143

Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, LeeIJ (2012b) Endophytic fungi produce gibberellins and indole-aceticacid and promotes host-plant growth during stress. Molecules 17:10754–10773

Wei J, Xu T, Guo L, Liu A, Zhang Y, Pan X (2009) EndophyticPestalotiopsis species associated with plants of PodocarpaceaeTheaceae and Taxaceae in southern China. Fun Div 24:55–74

Weihong Z (2004) Effects of Gibberellin on seed germination and seed-ling growth of Lilac. For Sci Technol 2004:4

Welbaum G, Sturz AV, Dong Z, Nowak J (2004) Managing soil micro-organisms to improve productivity of agroecosystems. Crit RevPlant Sci 23:175–193

Wen-guang MA, Zheng Y, Wen-long S, Bi-qing S, Yong-zhi N (2009)Gibberellin priming treatment improve vigour of pelleted seed andseedling quality in tobacco. Acta Agric Zhejiangensis 2009:3

Wiyakrutta S, Sriubolmas N, Panphut W, Thongon N, DanwisetkanjanaK, Ruangrungsi N, Meevootisom V (2004) Endophytic fungi withanti-microbial, anti-cancer and anti-malarial activities isolated fromThai medicinal plants. World J Microbiol Biotechnol 20:265–272

Ya-li LV, Fu-sheng Z, Juan C, Jin-long C, Yong-mei X, Xiang-dong L,Shun-xing G (2010) Diversity and antimicrobial activity of endo-phytic fungi associated with the Alpine plant Saussurea involucrate.Biol Pharm Bull 33(8):1300–1306

Yamaguchi S (2008) Gibberellin metabolism and its regulation. AnnuRev Plant Biol 59:225–251

You YH, Yoon H, Kang SM, Shin JH, Choo YS, Lee IJ, Lee JM, Kim JG(2012) Fungal diversity and plant growth promotion of endophyticfungi from six halophytes in Suncheon Bay. J Microbiol Biotechnol22(11):1549–1556

Yuan ZL, Zhang CL, Lin FC (2010) Role of diverse non-systemic fungalendophytes in plant performance and response to stress: progressand approaches. J Plant Growth Regul 29:116–126

Zabalgogeazcoa I, Ciudad AG, Vázquez de Aldana BR, Criado BG (2006)Effects of the infection by the fungal endophyteEpichloë festucae in thegrowth and nutrient content of Festuca rubra. Eur J Agron 24:374–384

Zhang HM (2008) Soil bacteria augment Arabidopsis photosynthesis bydecreasing glucose sensing and abscisic acid levels in planta. Plant J56:264–273

Zhao J, Shan T, Mou Y, Zhou L (2011) Plant-derived bioactive com-pounds produced by endophytic fungi. Mini-Rev Med Chem 11:159–168


Fungal growth promotor endophytes a pragmatic approach

Documents

Transcript of Fungal growth promotor endophytes a pragmatic approach