Piriformospora indica: Sebacinales and Their Biotechnological Applications: 33 (Soil Biology)

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ARinfected grasses have broad pesticidal effects against five of the six major pasture pests present in New Zealand; however, the role of the epoxy-janthitrem compounds in insect resistance has not yet been fully elucidated Johnson et al. Because of the advantage these novel endophytes provide through improving ryegrass persistence but without causing significant detrimental animal effects, the uptake by farmers has been rapid Caradus, Lovatt and Belgrave A growing number of studies characterizing E.

The root-colonizing facultative endophyte Piriformospora indica forms beneficial symbioses with crop plants. Piriformospora indica was originally isolated by Verma et al. This filamentous fungus belongs to the order Sebacinales in Basidiomycota Weiss et al. Original inoculation experiments showed the ability of P.

Piriformospora indica

Plants colonized with P. The potential of P. Systemic resistance to different foliar pathogens via P. Fakhro et al. In hydroponics, P. Moreover, at high light densities it represses Pepino Mosaic Virus which has been found widely in tomato greenhouses in many European countries, in Morocco, South and North America, and in China Fakhro et al. Many other fungal endophytes have been shown to protect host plants from pathogenic fungi. The endophyte Epicoccum nigrum isolated from sugarcane is especially known for its biocontrol activity against pathogens, such as Sclerotinia sclerotiorum in sunflower, Pythium in cotton, phytoplasma bacteria in apple and Monilinia spp.

Murphy, Doohan and Hodkinson b isolated fungal endophytes from wild barley plants Hordeum murinum subsp. The tested seeds harbored some of the most devastating pathogens of barley, including species of Cochiolobus , Fusarium , Pyrenophora and Rhynchosporium.

In addition to suppressing seedborne pathogens, this strain also suppressed growth of the soil-borne pathogen Gaeumannomyces graminis var. Fungal endophytes isolated from healthy Theobroma cacao tissues have been screened in vitro for antagonism against major pathogens of cacao including Moniliophthora roreri causing frosty pod rot , Phytophthora palmivora causing black pod rot and M. Field trials have assessed the effects of these endophytic fungi and have shown that treatment with Colletotrichum gloeosporioides significantly decreased pod loss due to black pod rot and that treatment with Clonostachys rosea reduced the incidence of sporulating lesions of M.

Lastly, fungal entomopathogens are an important class of endophytes to consider for their anti-insect biocontrol properties Quesada Moraga, Herrero and Zabalgogeazcoa They have a unique ability to infect and colonize insects affecting insect survival and reproduction and many, if not all, have the ability to colonize plants Vidal and Jaber Interestingly, most of the commercially produced entomopathogenic fungi can be endophytic for part of their life cycle and include the species of Beauveria , Metarrhizium , Lecanicillium and Isaria Vidal and Jaber None of these commercial biocontrol products have made use of their endophytic mode of action however, but at least one such product is able to colonize plants endophytically reviewed in Vidal and Jaber Wagner and Lewis first described in detail the penetration and colonization of plant tissues by the entomopathogenic fungus, Beauveria bassiana.

Entomopathogenic fungi are effective against several root-feeding insects belonging to different orders, such as the root mealy bug, Cataenococcus ensete , the sugar beet root maggot, Tetanops myopaeformis , the diabroticine rootworms, and the white grubs Melolontha melolontha and Popillia japonica Li et al. The coffee berry borer Hypothenemus hampei is the most devastating pest of coffee throughout the world. Vega et al. They found various genera of fungal entomopathogens, including Acremonium, Beauveria, Cladosporium, Clonostachys and Paecilomyces.

Beauveria bassiana and Clonostachys rosea appeared to be pathogenic to the coffee berry borer Vega et al. These fungal entomopathogenic endophytes also play a role in soil nitrogen cycling. Behie, Zelisko and Bidochka tested the ability of Metarhizium robertsii to translocate insect-derived nitrogen to plants. They injected waxmoth larvae with 15 N-labeled nitrogen and placed the labeled insects on haricot bean Phaseolus vulgaris and switchgrass Panicum virgatum and observed incorporation of 15 N into amino acids of the plant, but only in the presence of Me.

Fitness benefits conferred by mutualistic fungal endophytes contribute to, or are responsible for, plant adaptation to not only biotic stresses but also abiotic stress by increasing tolerance to drought and water stress, as well as tolerance to high temperature and high salinity Aly, Debbab and Proksch Habitat-adapted stress tolerance of plants conferred by habitat-specific symbionts is an intriguing phenomena hypothesized to be responsible for the establishment of plants in high stress environments Rodriguez et al.

A large number of class 2 endophytes have been found to be capable of habitat adaption providing tolerance to habitat-specific selective pressures such as soil pH, temperature and salinity Rodriguez et al. Leymus mollis dunegrass plants from several coastal beach habitats in the USA were shown to be symbiotic with the endophyte Fusarium culmorum which, when inoculated into salt-sensitive non-coastal plants, conferred salt tolerance to those plants Rodriguez et al. Similar experiments were carried out to demonstrate that endophytic fungi aid heat tolerance.

The tropical panic grass, Dichanthelium lanuginosum , found growing in geothermal soils in Yellowstone National Park forms a mutualistic symbiotic interaction with the class 2 endophyte, Curvularia protuberata which confers heat tolerance Redman et al. These habitat-specific symbionts also have a broad host range and have been shown to be able to confer habitat-specific tolerance to other plant species. For example, an endophyte from coastal plants can colonize the model monocot, rice, and confer salt tolerance, whereas endophytes from other habitats agricultural, coastal and geothermal can confer disease resistance but not salt or heat tolerance to the model dicot tomato Rodriguez et al.

Interestingly, all these endophytes conferred drought tolerance to plants regardless of the habitat of origin Rodriguez et al. Decreased water availability and increased soil salinization is a growing challenge to crop growth in many parts of the world Egamberdieva et al.

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The ability of fungal endophytes to confer stress tolerance to plants may provide a novel strategy for mitigating the impacts of global climate change on agricultural plant communities Rodriguez et al. Redman et al. They also conferred cold tolerance to growth chamber and greenhouse grown plants.

These findings indicate that the incorporation of fungal symbionts may be a useful strategy in both mitigating impacts of climate change on major crops and expanding agricultural production onto marginal lands Redman et al. Turning to endophytes that have the potential to promote plant growth, P. An extensive set of phytohormones and phytohormone signaling networks seem to be involved in mediating plant growth promotional activities which lead to increased early root growth promotion and finally to greater biomass.

Considerable research has been carried out on the mechanism of salt stress tolerance conferred to plants colonized with P. Piriformospora indica 's wide host benefits as well as its amenability for fundamental biological studies are attractive properties for research and its potential to transform the productivity of agricultural crops sustainably is exciting.

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With respect to barley, P. These results indicate that P. However, despite all of these described benefits, Franken states that it may be difficult to place P. Nonetheless, a powder formulation of P. There are also other endophytes of barley that have the potential to be advantageous in agricultural settings. Murphy, Doohan and Hodkinson a isolated endophytic fungi from wild barley H. The greatest impact one of these endophytic isolates had on grain yield and shoot dry weight was achieved under the lowest nutrient input.

Such strains may therefore be able to help by reducing fertilizer inputs while maintaining acceptable yields. Continuning with the theme of improving plant performance, the class 4 or DSE root-colonizing fungi, that are characterized by their darkly melanized septa, are an interesting group of endophytes that are present in a wide range of terrestrial ecosystems, but are especially common in polar and alpine habitats Rodriguez et al.

In these cold and water-stressed environments, arbuscular mycorrhizal fungi, the typical mutualists of grass roots at lower altitudes and latitudes, are essentially absent Newsham and it has been suggested that DSE species might act as surrogate mycorrhiza in these habitats Bledsoe, Klein and Bliss Inoculation of monocotyledonous and dicotyledonous plant species with these fungi increases root and shoot biomass, and shoot nitrogen and phosphorous contents. Meta-analyses performed by Newsham on data from 18 research articles, in which plants had been inoculated with DSE species, indicated that they can enhance plant performance under controlled conditions, particularly when most of the nitrogen is available in an organic form such as proteins, peptides and amino acids in the rhizosphere.

Plants apparently do not benefit from DSE species when roots can readily access inorganic nitrogen Newsham These asexual species do not manifest symptoms of disease and are characterized by their vertical transmission of hyphae via host seeds. In Australia, the collective condition is referred to as perennial ryegrass toxicosis which can result in sheep deaths estimated to be in the hundreds of thousands in some years Reed and Lean Indeed, grazing on endophyte-free grass did not cause the disease anymore but a new problem appeared.

In New Zealand, ryegrass persistence was seriously affected by damage caused by invertebrate pests, especially by the Argentine stem weevil Listronotus bonariensis Prestidge, Pottinger and Barker Fig. Due to the extraordinary biodiversity of fungal endophytes, they provide a largely untapped opportunity to discover novel natural products with unique chemical structures that have been optimized by co- evolution with higher plants.

The recent development of screening technologies has revealed the great potential of fungal endophytes for producing novel biologically active compounds with promising medicinal or agricultural applications Zhang, Song and Tan ; Aly, Debbab and Proksch ; Wu et al. These molecules can play an important role in communication between organisms, in plant protection and plant adaptation to habitat and environmental changes.

For reasons of safety and environmental problems, many synthetic agricultural agents have been, and will be, removed from the market. Secondary metabolites produced by fungal endophytes provide novel opportunities to control pests and pathogens Strobel and Daisy Discovering plants that harbor these microbes capable of producing novel bioactive metabolites is the first step.

Schulz described that certain microbial metabolites are characteristic of certain biotopes, on both an environmental and a taxonomic level. This study indicated that organisms living in unique biotopes or habitats that are subjected to constant metabolic and environmental interactions will yield even more secondary metabolites than organisms that are not Schulz Therefore, the search for novel secondary metabolites should primarily center on organisms that inhabit unique biotopes.

Successful collection of plants harboring endophytes which produce novel and unique natural bioactives requires the identification of plants i from unique environmental settings, especially those with an unusual biology, and possessing novel strategies for survival; ii that have an ethnobotanical history used by indigenous peoples and that are related to the specific uses or applications of interest; iii that are endemic, that have an unusual longevity or that have occupied a certain ancient land mass; and iv that grow in areas of great biodiversity Strobel and Daisy Expeditions to the Amazonian rain forest have led to the discovery of a wide range of secondary metabolites produced by endophytic fungi Strobel and Strobel There are many examples of secondary metabolites from endophytic fungi which are being used, or have promise to be used, against pathogens and pests of horticultural and agricultural plants.

This includes fungal endophytes which produce promising but so far unidentified compounds through to well understood and described anti-microbial secondary metabolites. An overview of metabolites produced by plant-associated microbial strains, including many fungal endophytes, was published by Gunatilaka Examples of some well-characterized anti-microbial secondary metabolites from endophytic fungi are presented below in alphabetical order.

Several of these compounds have been described by Strobel and Daisy The chemical structures of selected compounds are shown in Fig. Some anti-microbial compounds produced by the sugarcane endophyte Epicoccum nigrum Brown, Finlay and Ward have been characterized, such as epicorazines A-B Baute et al. Especially the compounds flavipin and epicorazines A-B have been associated with E. Ambuic acid is an antifungal and anti-oomycete agent from the endophytic fungus Pestalotiopsis microspora , isolates of which have been found in many of the world's rainforests.

It is active against several Fusarium species and against Pythium ultimum Li et al.

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It also appears to be a quorum-sensing as defined by Fuqua, Winans and Greenberg inhibitor Gary Strobel, pers. Colletonoic acid Bills et al. It shows good anti-bacterial, anti-fungal and anti-algal activities Hussain et al. Colletotric acid is a metabolite of Colletotrichum gloeosporioides , an endophytic fungus from A. It displays antimicrobial activity against bacteria as well as against the fungus Helminthosporium sativum Zou et al.

Cordycepsidone A was isolated from the endophytic fungus Cordyceps dipterigena and has strong antifungal activity against the plant pathogenic fungus Gibberella fujikuroi Varughese et al. Cryptocandin is a lipopeptide isolated from Cryptosporiopsis quercina , a fungus commonly associated with hardwood species in Europe. It is active against a number of plant-pathogenic fungi, including Sclerotinia sclerotiorum and Botrytis cinerea Strobel et al. It is related to known antimycotic compounds: the echinocandins and the pneumocandins Walsh Cryptocin is produced by Cr.

It also shows strong activity against the plant-pathogenic fungi Fusarium oxysporum , Geotrichum candidum , Rhizoctonia solarum and S. Jesterone is produced by Pe. As anticipated, the compound has anti-oomycete activity Li and Strobel Pestacin and isopestacin Fig. Both also have anti-microbial activity Strobel and Daisy Phomopsichalasin is a secondary metabolite from the fungal endophyte Phomopsis sp.

Scandenin was isolated from a Derris scandens plant from Pakistan and has strong anti-bacterial activity against B. Examples of anti-oxidant secondary metabolites from endophytic fungi with anti-microbial activity. Although the topic of volatile antibiotics would perfectly fit into the previous section, they have been put it under a separate heading because special techniques are required to detect these compounds. Their anti-microbial activity is detected using air contact between the volatile-producing fungus and the target pathogen see Fig. The volatile mixture can subsequently be separated and identified using a combination of chemical profiles built by LC-HRMS liquid chromatography-high resolution mass spectrometry or NMR nuclear magnetic resonance and multivariate data analysis Wu et al.

Prevention from rotting of dried fruits by volatiles produced by the endophytic fungus Daldinia concentrica. The volatile mixture consists of at least 28 compounds. The endophytic fungus Muscodor albus , isolated from small branches of Cinnamomum zeylanicum cinnamon tree Worapong et al.

Several individual compounds had some inhibitory effect against the test fungi and bacteria, but none was lethal. However, a strong synergistic effect was found and collectively they caused death of a broad range of plant- and human-pathogenic fungi and bacteria. Five classes of compounds were detected, namely alcohols, esters, ketones, acids and lipids.

Initial studies showed that the most effective class of inhibitory compounds was the esters, of which isoamyl acetate was the most biologically active compound Strobel et al. Subsequently, seven new Mu. However, none of the new isolates produced any of the esters known from the original Mu.

All together, they produce 50 different volatiles with an impressive range of biological activities, such as growth inhibition of Gram-positive and Gram-negative bacteria and of plant-pathogenic fungi and oomycetes Ezra, Hess and Strobel Interestingly, all isolates of Mu. Muscodor crispans is an endophytic fungus of Ananas ananassoides wild pineapple growing in the Bolivian Amazon Basin.


The fungus produces a mixture of antifungal and antibacterial volatile organic compounds. Pythium ultimum appeared to be the most sensitive organism of the fungal and oomycete plant pathogens tested towards the volatile mixture of Mu. Other sensitive plant fungal and oomycete pathogens include Alternaria helianthi , Botrytis cinerea , Fusarium culmorum , F. Also the plant-pathogenic bacterium Xanthomonas axonopodis pv. Interestingly, in contrast to the situation with Mu. For instance, no azulene or naphthalene derivatives were detected in the volatile mixture of Mu.

As a result, this mixture was suggested to have potential utility in applications ranging from food preservation to agricultural, household and industrial uses Mitchell et al. A Gliocladium sp. Of particular interest was that its most abundant volatile inhibitor was identified as [8]annulene Fig. The endophytic fungus Daldinia concentrica , isolated from an olive tree in Israel, produces at least 28 volatile organic compounds which are very promising for post-harvest control. These volatiles protect dried fruits of apricot, plum and raisin from rotting.

Moreover, they protect peanuts against Aspergillus niger , oranges and tomato paste against Penicillium digitatum and grapes against Botrytis cinerea. Artificial mixtures of selected volatiles have great promise for application in food industry and agriculture David Ezra and Orna Liarzi, pers.

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The association of synthetic pesticides with ecological damage has led to research to discover powerful, selective and safe alternatives Strobel and Daisy Until now, biopesticides are only a small part of the pesticide market but their impact is increasing. Several endophytes are known to produce secondary metabolites that have anti-insect properties. Some of their chemical structures are shown in Fig. Examples of some well-characterized anti-insect secondary metabolites from endophytic fungi. See Fig. The structure of epoxy-janthitrem I is from Johnson et al.

Nodulisporic acids Fig. They act by activating insect glutamate-gated chloride channels. The first nodulisporic compounds were isolated from the endophyte Nodulisporium sp.