Endophytic Fungi for Pest and Disease Management

365 A. Ciancio & K. G. Mukerji (eds.), Integrated Management of Diseases Caused by Fungi, Phytoplasma and Bacteria, 365–387. © Springer Science+Business Media B.V. 2008

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SUSHEEL KUMAR 1, NUTAN KAUSHIK 1, RUANGELIE EDRADA-EBEL2, RAINER EBEL2 * AND PETER PROKSCH2

ENDOPHYTIC FUNGI FOR PEST AND DISEASE MANAGEMENT

1 TERI University, Habitat place, Lodi Road, New Delhi, India 2 Institut für Pharmazeutische Biologie und Biotechnologie,

Heinrich-Heine-Universität Düsseldorf, Germany 1

Abstract. Endophytes are microorganisms that inhabit the interior of a healthy plants. They offer great-untapped potentials, which can be exploited to maintain healthy crops. Many cultivated and wild type plants have been investigated for endophytic fungal metabolites which include guanidine and pyrrolizidine alkaloids, indole derivatives, sesquiterpenes, isocoumarin derivatives. These metabolites show beneficial effects to crop plants and many of them also have pesticidal and antimicrobial activity against plant and human pests and pathogens. Full potentials and efforts needed are herein discussed.

1. INTRODUCTION

The need for new and useful compounds to provide protection and relief to crop plants from pests and thereby sustainable food production for human consumption is ever growing. Pesticide consumption in India increased from 434 Metric Tones (MT) in 1954 to 70794 MT in 2002-03 (www.indiastat.com). However, a sharp reduction to 48350 MT during 2002-03 has been witnessed due to realization of the fact that the indiscriminate use of pesticides has created numerous problems, like the development of resistant strains in insects and plant pathogens, resurgence of pest species, direct toxicity to the applicator, destruction of parasites, predators, and other beneficial organisms, accumulation of pesticide residues in several agricultural commodities, water, air and soil (see http://www.ddsindia.com/www/npm.htm).

Animals intended for human food absorb pesticides from residues in their feed, water or during direct/indirect exposure in the course of pest control (Aulakh et al., 2006). Pesticide poisoning even causes more deaths than infectious diseases (Eddleston et al., 2002). A study of pesticide poisoning in South India demonstrated that two compounds, monocrotophos and endosulfan, accounted for majority of

* Present address: Department of Chemistry, University of Aberdeen, Meston Building, Meston Walk, Old Aberdeen, AB24 3UE, Scotland, UK

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deaths, of which two-thirds of the patients were less than 30 years old (Srinivasrao et al., 2005). Over 80% of women are found to be suffering from acute pesticide poisioning in the cotton growing areas, as they assist in mixing concentrated chemicals and refilling spraying tanks (Mancini et al., 2005). To cope with the stated problems there is a need to develop ecologically sound, environmentally safe and economically viable methodologies for plant disease and pest management.

Natural and biological control of pest and diseases affecting cultivated plants has gained considerable attention in the past decades as a way of reducing the use of chemical products in agriculture. Biological control has become an utmost important tool for Integrated Pest Management (IPM). Use of microorganisms that antagonize plant pathogens and insects as biological control agent results in enhancement of resident antagonist and is risk free. Antagonistic microorganisms most frequently are from the rhizosphere or the phyllosphere, while few are also endophytes. Endophytic fungi offer great-untapped potential, which can be exploited for the good crop health. The present review summarizes research work done on endophytic fungi from terrestrial plants, which are identified for pesticidal activity.

2. ENDOPHYTIC FUNGI

All microorganisms that inhabit the interior of a plant for at least one period of their life cycle are considered as endophytes (Arnold et al., 2003). It is noteworthy that, of the nearly 300,000-500,000 plant species that exist on the earth, each individual plant is host to one or more endophytes (Strobel, 2006). Endophytic fungi are widespread in all phyla of the kingdom Fungi. Most of the endophytic species belong to the phylum Ascomycota, and they are often closely related to fungi known to cause diseases, either in healthy tissue or as secondary invaders of damaged tissues (Schardl et al., 1997). This suggests that endophytes may have evolved from pathogens or vice-versa.

Figure 1. Endophytic and pathogenic interaction of fungi in a plant (adapted from Schulz et al., 2002)

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The fungal endophytes possess exoenzymes necessary to colonize their hosts and they grow well in the apoplastic washing fluid of their hosts. It has been suggested that fungal endophyte–plant host interactions are characterized by a finely tuned equilibrium between fungal virulence and plant defence, as depicted in Fig. 1 (Schulz et al., 2002).

Most of the plant species examined to date harbour endophytic fungi within their asymptomatic aerial tissues, such that the endophyte represents a ubiquitous, yet cryptic, component of terrestrial plant communities (Arnold et al., 2003). Detection of endophytic fungi inside the host tissue has been achieved by several techniques, including tissue print immunoassay (Hahn et al., 2003), transmission electron microscopy (Christensen et al., 2002), direct staining and aphid assay (Wilson, Clement & Kaiser, 1991). Antagonistic effects of endophytic fungi including Colletotrichum sp., Fusarium sp., Nectria sp., and Xylaria sp. isolated from cacao plants, has been reported against Phytophthora pathogens of cacao plant, in in vitro test. These fungi grow within their plant hosts without causing any apparent disease symptoms that involve continual metabolic interactions between fungus and host.

3. BIOACTIVITY OF ENDOPHYTIC FUNGI

Webber (1981) was the first researcher who noticed that the endophyte Phomopsis oblonga (Desmazieres) Traverso protected elm trees against the beetle Physocnemum brevilineum (Say). Later in the year 1985 bioactivity of this endophytic fungus was conclusively proven when it was shown that fungi belonging to the Xylariaceae family synthesize secondary metabolites which were found to be detrimental for beetle grubs (Clay, Hardy & Hammond, 1985). In another study, weight gain and survival of the insect-pest, Spodoptera frugiperda Smith, was found to be negatively affected by the endophytic fungus Balansia cyperi Edg., isolated from Cyperus sp. (Hardy, Clay & Hammond, 1985). Ahmad et al. (1985) verified similar effects of the same fungus over the grasshopper Acheta domesticus L.

In a choice assay Johnson et al. (1985), showed that aphids including Rhopalosiphum padi, Schizaphis graminum, Oncopeltus fasciatum would feed on endophyte-free Festuca plants rather than on infected samples. Methanol extracts of the tall fescue infected with Acremonium coenephialum were tested for toxicity against Oncopeltus fasciatum and found likewise to be effective. Since then a wide range of activities of endophytic fungi has been reported either by induction of host plant resistance or by production of secondary metabolites, which in turn protect the plant. Endophyte-grass interactions produce more metabolites useful for crop protection than endophyte-woody plant interactions (Saikkonen, 2004).

Fungal endophytes also impart enhanced tolerance to abiotic stresses (West, 1994; Siegel et al., 1990). Enhanced host plant resistance to insects has been reported in Acremonium endophyte host interactions (Breen, 1994).Increase in growth rate has been observed in tall fescue plants infected with Neotyphodium endophytic fungi, however, beneficial effects of endopohytic fungi on plant growth diminished with increased soil moisture and nutrients (Faeth & Fagan, 2002).

Root infection with endophytic fungi produces more phenolics and elicits greater plant defense reaction (Schulz et al., 1999). Endophytes and cell-free washings of their culture plates were reported to reduce the density and size of Puccinia pustules in a susceptible cultivar of wheat, when inoculated 3, 7, and 14 days prior to invasion of the pathogen. Interactions between endophytes and Puccinia are most probably mediated by defence mechanisms induced in the host plant (Dingle & McGee, 2003).

Birch trees with high frequencies of Melanconium sp. endophytes were less infected with pathogenic fungi Fusicladium sp. and birch rust fungus (Elamo et al., 1998). Induction of systemic resistance of Chinese cabbage to bacterial leaf spot and fungal leaf spot (caused by Alternaria), by inoculation of the endophytic fungus Heteroconium chaetospira, has been reported by Morita et al. (2003). The isolates were inoculated in the root zone and induced systemic resistance without migrating to foliage. In another experiment eggplant roots colonized by a sterile white mycelial endophyte were found to be highly resistant to Verticillium wilt (Narisawa et al., 2002). Table 1 provides a summary of endophytic fungi isolated from diverse plant species and their associated bioactivities.

4. ENDOPHYTIC METABOLITES AS SOURCE OF NEW PESTICIDES

Several metabolites showing pesticidal activity have been isolated and characterized from endophytic fungi. A summary is provided in Table 2. Endophytic fungi in the tribe Balansiae produce ergot alkaloids viz. ergonovine [1], ergotamine [2], ergocryptine [3], agroclavine [4] and elymoclavine [5] (Fig. 2) which caused reduction in larval weight and leaf area consumption of Spodoptera frugiperda at concentrations of 77 - 100 mg liter -1 (Clay & Cheplick, 1989).

Peramine [6] (Fig. 2), a pyrrolopyrazine alkaloid with insecticidal activity against argentine stem weevils (Rowan & Gaynor, 1986), has been isolated and characterized from several endophytic fungi present in the stem and leaf of tall fescue, ryegrass (Festuca arundinacea Schreb.) and other grasses (Schardl & Phillips, 1997). These endophytic fungi are Neotyphodium coenophialum (Morgan-Jones & Gams) Glenn, Bacon & Hanlin, N. lolli, Epichloe festucae and E. typhina (Fries.) Tulsane.

A tetrameric acid analog, cryptocin [7] (Fig. 2), isolated from cultures of the endophytic fungus Cryptosporiopsis cf. quercina Petr. that is present in the inner bark of the stem of Tripterygium wilfordii Hook. F., has been found to be effective against Pyricularia oryzae Cav., and other phytopathogens (Li et al., 2000).

Indole derivatives like 6-isoprenylindole-3-carboxylic acid [8] (Fig. 2) have been isolated from the endophyte Colletotrichum sp. and showed growth inhibition properties against phytopathogenic fungi including Phytophthora capsici Leonian., Rhizoctonia cerealis Van der Hoeven., and Gaeumannomyces graminis (Sacc.) von Arx & Olivier var. tritici J. Walker (Lu et al., 2000).

Lolines [9] (Fig. 2) are saturated aminopyrrolizidine alkaloids occurring in Neotyphodium-Festucae endophyte host interactions. These compounds are broad-spectrum insecticides showing dual activity as metabolic toxins and feeding deterrents on specific insect species (Schardl & Phillips, 1997).

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Figure 2. Structure of metabolites 1 to 9.

During interactions of grasses from the genera Lolium and Festuca with the endophytic fungi Acremonium coenophialum and Epichloe typhina the secondary constituents loline [9], peramine [6], ergovaline [10] (Fig. 3), were produced. Loline and peramine were shown to have detrimental effects on aphids including Rhopalosiphum padi and Schizaphis graminum (Siegel et al., 1990).


Figure 3. Structure of metabolites 10 to 13. The cytotoxic alkaloid, cytochalasin [11] was isolated from Rhinocladiella sp.,

an endophytic fungus of Tripterygium wilfordii (Wagenaar et al., 2000). Phomapsichalasin [12] an antimicrobial agent was isolated from the endophytic fungus Phomopsis sp. fermented on shredded wheat (Horn et al., 1995). 1-N-methyl albonoursin [13], an antibiotic alkaloid is reported from Streptomyces sp. from perennial ryegrass (Gurney & Mantle, 1993) (Fig. 3).

Alkaloids from endophyte and grass interactions have been shown to be protective against several crop pests (Bush, Wilkinson & Schardl, 1997). Several steroids such as 3β-hydroxyergosta-5-ene; 3-oxoergosta-4,6,8(14),22-tetraene; 3β,5α-dihydroxy-6β-acetoxyergosta-7,22-diene and 3β,5α-dihydroxy-6β-phenyl-acetoxyergosta-7,22-diene have been reported as constituents of the liquid culture of Colletotrichum sp. isolated from Artemisia annua. They have shown antifungal activity against Phytophthora capsici Leonian., Rhizoctonia cerealis Van der Hoeven., Helminthosporium sativum Pamm., King and Bakke and Gaeumannomyces graminis (Sacc.) von Arx & Olivier var. tritici J. Walker (Lu et al., 2000).

Nodulisporic acid A [14], a novel and potent natural insecticide, has been isolated from Nodulisporium sp., an endophytic fungus of woody plants (Ondeyka et al., 1997). Insecticidal properties have been reported against Aedes mosquito larvae and larvae of the blowfly (Lucilia seracata). Furthermore, Hensen et al., (1999) elucidated the structure and relative stereochemistry by spectroscopic methods and X-ray diffraction analysis, which gave two stereoisomers A1 [14a] and

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A2 [14b], out of which A1 was more potent with regard to insecticidal activity than A2 (Fig. 4).

Figure 4. Structure of nodulisporic acid and its stereoisomers.

The sesquiterpene chokols A-G [15-21] (Fig. 5) have been isolated from

Epichloe typhina, an endophytic fungus of Phleum pratense, and found to be fungitoxic to the leaf spot disease pathogen Cladosporium phlei (Gregory) de Vries, (Koshino et al., 1989a). Mellein [22] (Fig. 6), an isocoumarin derivative isolated

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from the endophyte Pezicula sp. has been described to be strongly fungicidal, herbicidal and algicidal (Schulz et al., 1995).

Rugulosin [23] (Fig. 6), a fungal product showing insecticidal activity, has been

reported from Harmonema dematoides which is an endophytic fungus of balsam firs (Calhoun et al., 1992). Fungicidal molecules have also been isolated from Pezicula sp. (Schulz et al., 1995) and Epichloe typhina (host: Phleum pratense L.) (Koshino et al., 1989b).

Colletotric acid [24] (Fig. 6), a phenolic antifungal compound, has been isolated from liquid cultures of Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. which is an endophytic fungus of Artemisia mongolica Fisch., and was shown to be effective against Helminthosporium sativum Pammel, King & Bakke, (Zou et al., 2000). This compound was also found inhibitory to the bacteria Bacillus subtilis (Ehrenb.) Cohn, Staphylococcus aureus Rosenb. and Sarcina lutea.

Figure 5. Structure of sesquiterpene chokols.


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Figure 6. Structure of metabolites 22 to 28.

Muscodor vitigenus Daisy, Strobel, Ezra, & W. M. Hess, an endophytic fungus isolated from Paullinia paullinioides Radlk., a liana growing in the Peruvian Amazon, has been shown to produce an insect repellent. The repellent has been

Muscodor albus an endophytic fungus from a rainforest plant has been proven to be a potent fumigant, which protected fruits and vegetables during storage. Fumigant property of endophytic fungus is due to the production of volatile organic compounds (VOCs). Most effective class of inhibitory compound were esters (1-butanol, 3-methyl-acetate). Other components of VOCs were alcohols, ketones, lipids, and acids. None of these compounds was effective individually. They rather acted due to synergistic effects. These compounds also prevented the growth of common agricultural pests, like smut, water mold and root rot (Strobel et al., 2001; Strobel, 2006).

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identified as naphthalene [25] (Fig. 6), and was demonstrated to exhibit insecticidal activity against the wheat stem sawfly, Cephus cinctus Norton. (Daisy et al., 2002). Production of griseofulvin [26] and dechlorogriseofulvin [27] (Fig. 6), from Xylaria sp., has been reported for the first time.

Xylaria sp. is an endophytic fungus of Abies holophylla. In vitro and in vivo tests of griseofulvin have shown antifungal activity against Magnaporthe grisea, Coryicium sasaki, Puccinia recondita, Blumeria graminis f. sp. hordei (Park et al., 2005). Other secondary metabolites occurring in different host endophyte interactions included quinones, peptides (cryptocandin) [28] (Fig. 6), pentaketides and phenols (Tan & Zou, 2001).

A nematicidal fungal metabolite (culture filtrate) has been isolated from an

Sm. & Swingle, showed efficacy against Meloidogyne incognita (Ko. & Wh.) Chit., wherein 98% of juveniles were killed within one hour of exposure to the culture filtrate (Hallmann & Sikora, 1996).

The culture filtrate of a F. oxysporum strain also reduced significantly the growth of Phytophthora cactorum (Lebert & Cohn) Schröt., Pythium ultimum Tro., and Rhizoctonia solani Kühn, in vitro. Dicanthelium lanuginosum plants inoculated with the endophytic fungus Curvularia sp. survived at a soil temperature of 65°C whereas plants lacking the fungi did not survive even at temperatures ≥ 40°C (Redman et al., 2002). Increased temperature resistance is advantageous to plants as they are able to grow concurrent with soil solarization where all soil-borne pathogens, pests and weeds would be killed at this temperature while crop plants will survive.

Fungal endophytes of the genera Neotyphodium and Acremonium isolated from wild wheat species served as a source of biological control agents against pests or abiotic stress factors in wheat (Marshall, Tunali & Nelson, 1999). Several endophytic fungi possessing insecticidal, antifungal and herbicidal activity have been reported from plants of diverse origin (Table 2). More recently, several endophytic species and their metabolites have been reported as plant protectants.

Endophytic fungi producing pesticidal compounds were frequently isolated from stargrass (Ji, Song & Tan, 2004); rice (Tian et al., 2004); Melia azedarach L. (Gries dos Santos et al., 2003); and Theobroma gileri L. (Evans et al., 2003). Pirttila et al. (2003) have isolated plant growth hormones from endophytic fungi of Pinus sylvestris. Many of the endophytes have so far remained underexplored for their metabolites. Endophytic fungi from wheat (Larren et al., 2002; 2006), rice (Fisher & Petrini, 1992; Tian et al., 2004), maize, coffee (Sette et al., 2006) and tea (Augusta et al., 2005), have also been described but analysis of their secondary metabolites has not yet been performed.

5. CONCLUSIONS

Endophytic fungi offer great potential in plant protection, imparting tolerance against several biotic and abiotic stress factors. However, endophyte-host interactions may turn to a pathogenic interaction, if susceptibility of host and/or virulence of the endophyte increase. However, if the metabolites responsible for the

endophytic fungus of tomato. The endophytic fungus Fusarium oxysporum E. F.


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beneficial effect can be isolated and exploited, then the risk of pathogenicity can be avoided. Structural elucidation of secondary metabolites will help in defining modes of action as well as in preparation of right formulations for field application. Standard protocols for isolation of bioactive molecules will be of great importance for production on large scale by fermentation technology. This will reduce the extra expenditure incurred in synthesis of chemical compounds. More plant species need to be explored for their endophytic fungi and their corresponding secondary metabolites. Endophytes that have not been investigated for their natural products so far should be studied for their bioactive metabolites in order to tap the rich biodiversity of endophytes.

ACKNOWLEDGEMENTS

N. K. and P. P. thank DST/DAAD for support and collaboration.

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