Arch Microbiol DOI 10.1007/s00203-015-1130-3

MINI-REVIEW

An ecological role of fungal endophytes to ameliorate plants under biotic stress Neha Chadha1 · Manjita Mishra1 · Kartikeya Rajpal1 · Ruchika Bajaj1 · Devendra Kumar Choudhary1 · Ajit Varma1 

Received: 25 February 2015 / Revised: 19 June 2015 / Accepted: 22 June 2015 © Springer-Verlag Berlin Heidelberg 2015

Abstract  It is our consensus that plants survive and flourish in stressed ecosystems because of endosymbiotic organisms that have co-evolved and were essential for their adaptation to changing environments. Some of these microbial components are noncultivable and vertically transmitted from generation to generation. They represent a vast reservoir of heritable DNA that can enhance plant performance in changing environments and add genetic flexibility to adaptation of long-lived plants. If such endophytes can be identified that not only persist in progeny of novel hosts, but can confer benefits in mechanized, agricultural systems, they would be increasingly important in agricultural production and lead to a rapid and economical method of providing novel germplasms of native and crop plants. In the present review, authors advocate the deployment of fungal diversity and its role to overcome the biotic stress in plants. Endophytic fungal association with plants helps it to protect from various pathogen and pests and adapt to survive in harsh biotic and abiotic stress condition. Keywords  Endophytes · Biotic stress · Induced resistance · Mycorrhiza · Piriformospora indica

Communicated by Erko Stackebrandt. * Ajit Varma [email protected] 1



Amity Institute of Microbial Technology (AIMT), Block ‘E‑3’, 4th Floor, Amity University Campus, Sector‑125, Noida, Gautam Buddha Nagar 201313, UP, India

Introduction From the first observation taken by Darnel, Germany in 1904, microorganisms living within plant tissues for all or part of their life cycle without causing any visible symptoms of their presence are defined as endophytes. Plants benefit extensively by harboring these endophytic microbes; they promote plant growth and confer enhanced resistance to various pathogens by producing antibiotics. Endophytes also produce unusual secondary metabolites of plant importance under stress conditions together with some valuable pharmaceutical substances of biotechnological interest. Endophytes represent a huge diversity of microbial adaptations that have developed in special and sequestered environments, and their diversity and specialized habituation make them an exciting field of study in the search for new metabolites (Bacon and White 2000; Tan and Zou 2001). In view of their widespread application in plant and human health and environment, concerted efforts at endophytic diversity searches coupled with exploitation are necessary in the country on account of the varied and unique plant diversity (Nair and Padmavathy 2014). Tremendous diversity of bacteria and fungi that associated with plants does not affect its host in deleterious manner rather stimulate growth and induce disease resistance together with tolerance against adverse effect of environment. Interaction between plant and endophytes results in the promotion of plant health and reflects a significant application in low-input sustainable agriculture with high productivity (Mapelli et al. 2013; Aroca et al. 2013; Veneklaas et al. 2012; Li et al. 2012). In the present scenario, any change in climate reflects adverse effect on food security in sustainable agriculture. Some of these include the loss of usable land through

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overuse, deforestation and poor irrigation practices, which have led to desertification and salinization of soils, especially in dry lands (Helldén and Tottrup 2008). Approaches currently being taken to face this situation come from the development of stress-tolerant crops, e.g., by genetic modification or breeding traits from wild plants. Genetic engineering has been proposed as the solution to these problems through a rapid improvement of crops. Crop genetic modification has generated a great public concern regarding their potential threats to the environmental and public health. As a consequence, legislation of several countries has restricted their use in agriculture. On the other hand, exotic libraries from wild plants for clever plant breeding could overcome the problem of narrowed genetic variability of today’s high-yield crops. Plant breeding driven by selection marker has also been a major breakthrough (Breithaupt 2003). However, these approaches have met limited success, probably because stress tolerance involves genetically complex processes and the ecological and evolutionary mechanisms responsible for stress tolerance in plants are poorly defined. New paradigms for sustainable crop improvement are currently arising. The above approaches do not consider the fact that plants in ecosystems have developed natural symbiotic associations for at least 400 million years with a broad diversity of microbial symbionts (Krings et al. 2007). The exploitation of plant–fungus symbiosis appear as a smart alternative for plant adaptation due to their great quantity, ubiquity, diversity, and broad range of ecological functions they play in natural ecosystem. Recent studies have shown that symbiotic endophytes are of crucial importance in the distribution of plant communities worldwide and are responsible of their adaptation to environments under highly selective pressure (Maciá-vicente et al. 2008a, b; Rodriguez and Redman 2008). These indicate that some endophytes confer tolerance to specific stresses and are responsible of the survival of plants to environments submitted to these particular conditions (Redman et al. 2002; Waller et al. 2005). A clear example of such adaptation specific from the habitat has been found in native grass species from coastal and geothermal habitats, which, respectively, require symbiotic fungi for their tolerance to salt or heat (Rodriguez et al. 2008). The stress tolerance conferred by the symbiosis is a habitat-specific phenomenon, which has been defined as habitat-adapted symbiosis (Redman et al. 2002; Rodriguez and Redman 2008), with endophytes from geothermal environments that confer tolerance to heat but not salt, and coastal endophytes conferring tolerance to salt, but not to heat. The same fungal species isolated from plants in habitats devoid of salt or heat stress did not appear to confer tolerance to these stresses. Moreover, fungal endophytes from agricultural crops confer resistance to disease, but no tolerance to salt or heat (Rodriguez et al.

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2008). In these studies, the endophytes from agricultural, coastal and geothermal ecosystems were able to colonize tomato and rice, conferring disease, salt and heat tolerance, respectively. Hence, these endophytes are capable to transfer their stress tolerance conferment to plants other than their original hosts. Interestingly, these endophytes also conferred drought tolerance irrespective of the habitat of origin (geothermal, coastal or agricultural), related with both a decrease in consumption of water by the plant and the modulation of the sensitivity/generation of reactive oxygen species. This could provide a mechanism for plants to make quantum evolutionary changes allowing for habitat expansion and survival in high-stress habitats (Rodriguez et al. 2005). It is currently thought that each plant in natural ecosystems comprises a community of organisms, including endophytes among others such as mycorrhizae and bacteria. The ability of the endophytic fungi to confer tolerance to stress may provide a new strategy to mitigate the impacts of global climate change on agriculture and natural plant communities (Rodriguez et al. 2008). Such symbiotic lifestyles suppose a potential source for the improvement of food crops, through adapting them to situations of increasing desertification and drought on global crop lands. It appears therefore as a sustainable alternative to the use of genetically modified organisms, which, on the other hand, did not yield the expected results. The characterization of endophytic species that confer tolerance to different stresses, both abiotic and biotic, depending on environmental conditions, as well as the detailed understanding of the mechanisms by which they occur, will be of great relevance in the following years, as environmental problems such as desertification of agro-ecosystems or damage to natural ecosystems aggravate. The plant–endophyte associations found were strongly influenced by the specific soil type where they took place, which was translated in an overall difference in species composition between communities from sand dunes and salt marshes. The major contribution to these differences was due to their dominant endophytes: Fusarium oxysporum for sand dunes or Aspergillus fumigatus and Alternaria chlamydospora for salt marshes (Rodriguez et al. 2008). The nature of plant–endophyte relationships may be affected by the addition of interacting species. The interaction between fungal endophyte and host is highly variable and transitory (Bacon and Yates 2006). Host endophyte interaction is termed as “balanced antagonist” an equilibrium state between fungal virulence and plant defense mechanism. Although change can occur through an imbalance in flow of nutrients, change in environmental and stress condition (Moricca and Ragazzi 2008). Along with mycorrhiza, the endophytes are well studied group of microorganisms, with the interest in latter gaining

Arch Microbiol

importance lately because of their mutualistic association with the host plant and their possible role in enhancing the host’s deterrence against abiotic and biotic stresses (Varma et al. 1999; Faeth and Fagan 2002). Endophytic microorganisms that grow in the intercellular spaces of higher plants are recognized as one of the most chemically promising groups of microorganisms in terms of diversity and pharmaceutical potential (Wagenaar and Clardy 2001). Endophytic fungi that live inside the plant tissue are important element in plant symbiosis, and plant growth under stress environmental condition (Redman et al. 2002; Ernst et al. 2003; Rodriguez et al. 2004; Márquez et al. 2007), and help in plant defense (Omacini et al. 2001; Bailey et al. 2006). In most cases, diversity, geographical distribution, and host specificity of fungal endophytes are unknown (Otero et al. 2007; Arnold and Lutzoni 2007; Higgins et al. 2007). Recent estimates of fungal diversity implied that more than 90 % of fungal endophyte species are unknown (Hyde et al. 2007; Schmit and Mueller 2007). India constitutes one-third of fungal diversity in 1.5 million of fungi all over the world and only 50 % are identified and characterized till date. From them only 5–10 % of fungi can be cultured artificially. Fungi provide an infinite source of biological diversity and exploitation. Therefore, they can play an important role in the daily life of man and has wide in agriculture, industry, food industry, medicine, textiles, natural cycling, bioremediation, biofertilizers etc. hence, fungal biotechnology has become an essential part of the human well-being, Manoharachary et al. (2005). Fungal diversity has been intensively studied in different parts of India, which interprets the distribution patterns and conservation strategies. Only a small fraction of total fungal endophytes wealth has been used scientific scrutiny and mycologists have to reveal the unexplored the hidden properties. Researchers have explored various ecological habitats of India for studying fungal diversity, and the work being carried out predominantly on fungi inhabiting medicinal plant species (Raviraja 2005; Mohanta et al. 2008; Rajagopal et al. 2010). The fungi found associated with medicinal plants have been found to produce certain novel and pharmaceutically important secondary metabolites. There are more than one million species of endophytic fungi associated with plants worldwide which can provide a variety of secondary bioactive products such as alkaloid, benzopyranones, flavonoids, phenols, tannins, saponins, and steroids (Ganley et al. 2004). In mangrove ecosystem, fungal endophytes plays a key role in nutrient cycling and very less information is available about the fungal microbes association with decomposed leaves. The dominant fungal species from decomposing mangrove leaves belongs to the genus Aspergillus. The species are Aspergillusniger, A. fumigatus, A. verrucosa, A. candidus, A. flavus, and other species are Alternaria

alternata, Ophiobolus littoralis, Pontoporeia biturbinata, Spathulospora lanata, Fusarium spp., Penicillium spp., Mucor spp., and Curvularia spp. The assemblage of fungal endophytes constitutes a number of species such as Colletotrichum spp. Pestalotiopsis spp. Glomerella spp. Phyllosticta spp. and Phomopsis spp. Several strains that were isolated from twig xylem and bark was absent in roots, leaves and flowers. Therefore, the species composition and frequency of fungal endophyte species were solely dependent on the tissue type of host plant. The dominant fungi screened from different parts of host tissue indicate the degree of recurrence. Marine fungi that associated with macroorganisms like algae, sponges or tunicates produce secondary metabolites of having novel structures and potential pharmaceutical significance that helps in drug development. Nearly seven fungal isolates such as Stachylidium spp., Cadophora spp., are closely associated with marine algae and sponges which were cultivated during 40–60 days, and their extracts were tested for bioactivity. From higher marine fungi, 61 species were collected from the submerged wood blocks of Bruguiera gymnorhiza and Rhizophora mucronatain Mauritius water (Poonyth et al. 2001). Seventy-three and 67 fungal species were isolated from Godavari and Krishna estuaries of India from the decaying samples of Rhizophora and Avicennia (Venkateswara Sarma et al. 2001). Out of 78 fungal species, 45 belongs to genera of ascomycetes, one from basidiomycetes and 31 deuteromycetes were recorded from the dead woods of mangroves in different parts of India (Maria and Sridhar 2002). Zheng et al. (2003) recovered endophytic fungal strains were isolated from the inner barks of three kinds of mangrove plants. Pichavaram mangroves comprises 13 mangrove tree species (Avicennia marina, Rhizophora apiculata and R. mucronata) and 80 mangrove associates (trees, 24 spp.; shrubs, 21 spp.; herbs, 28 spp.; climbers, 7 spp.) (Kathiresan 2000). Pichavaram mangroves include bacteria (52 spp.), fungi (23 spp.). Kumar and Hyde (2004) reported the biodiversity and tissue recurrence of fungal endophytes in Tripterygium wilfordii. Almost 343 fungal endophytic were from 60 taxa with 30 morphotypes. Extreme environmental conditions are those areas where life conditions are detrimental or fatal to higher organisms with respect to its physicochemical properties. Thus, extreme environments differ in many aspects from those which humans consider as “normal,” moderate conditions with circumneutral pH, temperatures between 20 and 35 °C, pressures around 0.1 MPA (1 atm), and adequate concentrations of nutrient and saline. Extreme environments typically harbor specially adapted organisms, the so-called extremophiles. Most extremophiles are unicellular organisms that are, bacteria, and archaea. An extreme environment shows a low diversity of multicellular organisms, and only few animals are able to withstand the harsh

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conditions of particular extreme environments. In India, several fungal strains recovered from saline soils of Gujarat. Fungal endophytes help the host plants to withstand and tolerate the unfavorable environmental conditions such as drought, high temperatures, and salts (Malinowski and Belesky 2000). Dichanthelium lanuginosum, the herbal plant growing in soil where temperatures reach to 57 °C, because of presence of Curvularia spp. an endophytic fungus. The colonized plants can survive in high temperature and water stressed areas than uncolonized plants. These beneficial effects were observed by systemically alternation in distal leaves, with increasing anti-oxidative capacity because of activation of glutathione ascorbate cycle in plants and results in grain yield. Therefore, such symbioses are required as they can help the plants to adapt in global climate changing atmosphere (Rodriguez et al. 2004). In addition, Piriformospora indica, a root endophyte, effectively helps the plants to enhance the tolerance against abiotic stress condition like drought in Chinese cabbage (Brassica campestris L. sp. Chinensis) and Arabidopsis thaliana (Sherameti et al. 2008; Vadassery et al. 2009; Sun et al. 2010). Under drought condition, colonized host plants had more chlorophyll content and photosynthetic efficiency compared to noncolonized plants (Sherameti et al. 2008; Strasser et al. 2007). Arnold et al. (2000) studied on fungal endophytes from tropical forests in Central Panama. Different studies were done like colonization patterns, host preference, richness, and spatial variation in leaves of tree species—Ouratealucens and Heisteriaconcinna, 418 fungal endophyte species were isolated from 83 leaves and most of were identified by a single isolate (59 %). These studies suggested the example of host preference and spatial heterogeneity. Arnold et al. (2001) reviewed extensively on fungal endophytes in tropical trees about their abundance, diversity and their ecological implications. Tropical fungi are traditionally not well studied. Fungal endophytes may represent a very ubiquitous, cryptic and ecologically interesting component of tropical forests. Endophytes seem to be both ubiquitous and highly diverse in tropical forests. Further investigation of tropical endophytes will help to easily clarify the fungal diversity. The study on tropical fungal endophytes is very promising to enrich our understandings on plant– fungus interactions in tropical forests, tropical biodiversity, and tropical ecology. Gangadevi and Muthumary (2007) reported endophytic fungal diversity in young, old, and senescent leaves of a medicinal plant Ocimum basilicum L. Not much is studied on the temporal and spatial variation of fungal endophytes which inhabit the foliage of medicinally important plants. This study was to be done first time on endophytic fungi diversity of medicinal plants from Chennai city, Southern India. Phyllosticta spp. were found to produce secondary metabolites, i.e., taxol in artificial

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culture media. The endophytic fungus is thus good source of natural bioactive agent. Antimicrobial potentials of fungal endophytes inhabit the three ethnomedicinal plants of Similipal Biosphere Reserve, India (Mohanta et al. 2008). Sixty fungal endophytes belongs to fourteen genera were isolated out of which thirtyone endophytes (51.66 %) were found as filamentous forms and twenty-nine of them (48.33 %) as yeast colonies. Dominant and host-specific endophytes were from Curvularia, Fusarium, Alternaria, and Penicillium. Among the potent strains of thirteen isolates, 19.3 % showed both antibacterial and antifungal activity and 6.4 % strain showed antimicrobial activity against all the test pathogens. The study suggested that fungal endophytes of ethnomedicinal plants could be a promising source of antimicrobial substances. Fungal endophytic organisms have been isolated from different parts of plant like scale primordia, meristem and resin ducts (Pirttilä et al. 2000, 2003), leaf segments and roots (Hata et al. 2002) and from bark, leaf blade, petiole (Hata and Sone 2008), and buds (Table 4). Only 16 endophytic isolates were obtained from 800 surface-sterilized seeds. Endophytic fungi classified into two broad groups based on phylogeny and life history traits as clavicipitaceous (C) which infect some grasses and the nonclavicipitaceous endophytes (NC endophytes), which infects the nonvascular tissue of some plants ferns and allies, conifers, and angiosperms (Rodriguez et al. 2009). NC endophytes further represent three distinct functional classes based on host colonization and transmission, in planta biodiversity and fitness benefits conferred to hosts. Plant tissues are multilayered, spatially and diverse microbial habitats, and support a rich and varied endophytic microorganisms. Endophytic fungi have been associated with plants for over 400 million years (Krings et al. 2007) and have been studied in various geographical and climatic zones. They are ubiquitous and occur within all known plants, which includes a broad range of host orders, families, genera and species, (Davey and Currah 2006), deciduous and coniferous trees (Guo et al. 2008; Albrectsen et al. 2010; Mohamed et al. 2010; Sun et al. 2011), grasses (Müller and Krauss 2005; Su et al. 2010), and lichens (Suryanarayanan et al. 2005; Li et al. 2007a, b). Endophytic fungi basically consist of members of the Ascomycota or their mitosporic fungi, some taxa of the Basidiomycota, Zygomycota and Oomycota (Guo et al. 2008), which produces various bioactive chemicals (Liu et al. 2008, 2009, 2010, 2011; Aly et al. 2010; Xu et al. 2010; Tejesvi et al. 2011), promote plant host growth and resistance to environmental stress condition (Ting et al. 2008; Saikkonen et al. 2010), and decompose litter (Purahong and Hyde 2011; Sun et al. 2011). Therefore, endophytic fungi play an important component of natural ecosystems, material and energy recycle.

Arch Microbiol

Fungal endophyte and biotic stress Fungal endophyte plays an important role in plant pathogen. Its use in pest control or resistance against biotic pressures has received a great attention, but little is known about their physiology and the regulation processes of the plant–endophyte interaction. Endophyte–pathogen

interactions can be broadly classified on the basis of the pathogen involved. These can be endophyte–nematode interaction, endophyte–plant pathogenic fungi interaction and interaction of endophytes with other plant pathogens. The competition of ecological niche and nutrition between pathogen–endophyte protects plant by rapid colonization and thereby exhausting the limited available substrates so

Table 1  Common plant diseases occurring globally and their causative agents Host

Disease

 Acidovorax citrulli

Cucurbits

Bacterial fruit blotch

 Agrobacterium tumefaciens

Walnuts, grape vines

Crown gall disease

 Erwinia tracheiphila

Cucurbits

Bacterial wilt

 Pectobacterium carotovorum

Fodder beets, sugar beet

Beet vascular necrosis

 Burkholderia glumae

Rice plant

Panicle blight

 Clavibacter michiganesis sub-sp. sepidonicus

Solanum tuberosum

Ring rot

 Pectobacterium atrosepticum

Black leg

 Pseudomonas amygdali pv. Lachrymans

Solanum tuberosum Cucumber

 Pseudomonas glycinea

Soybean

Bacterial blight

 Ralstonia solanacearum

Solanum tuberosum

Wilting

 Agrobacterium tumefaciens

Juglan sregia

Crown gall disease

 Xanthomonaso ryzae pv. Oryzae

Bacterial blight

 Xanthomonas campestris pv. Hederae

Cenchru sciliaris English ivy

 Xylella fastidiosa

Grapes

Leaf scorch, stunting

 Dickeya (dadantii and solani)

Solanaceae Banana, beans, cabbage

Necrosis, blight and soft rot

 Acrocalym mamedicaginis

Alfalfa

Root and crown rot

 Alternaria brassicae

Brassica sp.

Damping off, leaf spot

 Athelia rolfsii

Southern blight

 Bionectria ochroleuca

Juniperus virginiana L Oil seed rape

 Bipolaris incurvata

Coconut

Blight and leaf spots

 Blumeria graminis

Cereals

Powdery mildew

 Cadophora malonum

Apple, pear

Side rot

 Cytospora palmarum

Coconut

Leaf blight

 Diplodia phoenicum

Date palm

Diplodia

 Erysiphecichora cearum

Cucurbits

Powdery mildew

 F. culmorum

Cereals

Seedling blight, foot rot

 Guignardia philoprina

Araliaceae sp.

Leaf spot

 Helicobasidium purpureum

Brassica rapa, Beta vulgaris Cotton, pepper, onion

Violet root rot

a. Bacterial pathogen

 Pectobacterium carotovorum

Angular leaf spot

Leaf spot

Bacterial soft rots

b. Fungal pathogen

 Leveillulata urica c. Viral pathogen  Alfalfa mosaic virus

Seed rot

Powdery mildew

Pisum sativum, Solanum tuberosum

Wilting, white flecks, ringspots

 Barley yellow mosaic virus  Cymbidium mosaic virus  Sunn-hemp mosaic virus  Lettuce mosaic virus  Papaya mosaic virus

Barley Orchids Cannabis Lettuce Papaya

Yellow mosaic disease Chlorotic and necrotic lesions Spotting, discoloration Spotting, discoloration, distortion Stunting, mosaic symptoms on leaf

 Tobacco mosaic virus

Tobacco, tomato, pepper

Mosaic pattern on leaves

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that none would be available for pathogens to grow (Pal and Gardener 2006). Moreover, plants produce lignin to limit the growth of endophytes and cause it to be a virulent (Harman et al. 2004). As a result, the cell wall becomes rereinforced after endophytic colonization; thus, it becomes difficult for pathogens to infest. Hyperparasites and predation are another ecological strategy that endophytes provide to suppress plant pathogens and protect host plant. In hyper parasitism, the pathogen is directly attacked by a specific endophyte that kills it or its propagules, e.g., Trichoderma are able to parasitize hyphae of plant pathogen Rhizoctonia solani and many of these observations are linked with biocontrol (Grosch et al. 2006; Tripathi et al. 2008). A very interesting connection exists among endophytes and viruses. Curvularia endophyte isolated from Dichantelium lanuginosum (Elliott) Gould would confer heat tolerance in plants. Later it was discovered that the virus infecting the endophyte was contributing to the heat tolerance observed in the plants. Furthermore, the virus-infected endophyte could be used to confer heat tolerance to tomato plants (Márquez et al. 2007). Another example of virus infecting the endophyte is of Epichloëfestucae virus 1 (EfV1) which asymptomatically infects the grass endophyte Epichloë festucae, but in this case it is unknown that the presence of the virus in the endophyte affects the plant host (Romo et al. 2007). Plants may acquire protection against pathogen through constitutive and induced resistance (Bultman and Murphy 2000). The timing of this defense response is critical and reflects on the difference between coping and succumbing to such biotic challenge of pathogens. Systemic acquired resistance (SAR) and induced systemic resistance (ISR) are two forms of induced resistance wherein plant defenses are preconditioned by prior infection or treatment that results in resistance (tolerance) against subsequent challenge by a pathogen or parasite (Vallad and Goodman 2004; Király et al. 2007; Tripathi et al. 2008; Choudhary et al. 2011). It has been reported that fungal endophytes have the ability to protect host from diseases and limit the damage caused by pathogen microorganism (Arnold et al. 2003; Ganley et al. 2008; Mejıa et al. 2008). In vitro co-culture with pathogens and endophytes or comparison of the survival rate of plant inoculated with fungal endophytes are the two most common methods of endophyte limiting the pathogen damage. Bacteria and fungi exhibit biotrophic and necrotrophic strategies. Pathogens can also be classified based on the environment in which they occur and the tissues which they infect. Pathogens secrete complex chemical compounds such as enzymes, toxins, growth regulators, and polysaccharides. These compounds interfere with the natural metabolic processes of the host plant, thereby leading to occurrence of diseases. The compounds secreted by different pathogens

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Arch Microbiol

have been summarized (Table 1a–c). Plants have evolved their own set of defense mechanisms to prevent invasion and colonization by pathogens. Plants detect the presence of pathogenic microorganisms by recognizing elicitors and pathogen-associated molecular patterns (PAMPs), leading to flux of ions, proteins phosphorylation/dephosphorylation, production of signaling molecules such as salicylic acid and ethylene, and activation of reactive oxygen species. These compounds, in turn, regulate gene expression and the activation of defense responses, for example, cell wall strengthening and the accumulation of phytoalexins and pathogenesis-related (PR) proteins. The recognition of the avirulent strains activates, in addition to the already mentioned defense reactions, a localized programmed cell death that can efficiently halt the spreading of biotrophic pathogens (Table 2). Numerous endophytes have been reported to confer upon their hosts the resistance against phytopathogens, particularly fungi and nematodes. The best-known and most intensively studied endophytes are the Neotyphodium spp. and their Epichloë teleomorphs. The mechanism underlying this property of endophytes is an area of active research and includes secondary metabolites such as alkaloids, antibiotic substances (Schulz and Boyle 2005; Strobel et al. 2002), altering plant biochemistry, enhancing the host plant’s nutrient uptake and competition for host photosynthates (Wang et al. 2007). So far, about 5000 plant diseases have been reported in India, of which, around 1000 affect crops of economic importance. About 800 of them are caused by fungal pathogens, 50 are caused by bacterial, viral, and nematode pathogens each and a few due to mycoplasma. Fungal diseases have been rated as the most prevalent Table 2  The compounds secreted by different pathogens Pathogen

Effector compound

Chemical nature

Enzymes Fusarium spp and Botrytis Cutinases Pectinases cinerea Ralstonia solanacearum, Cellulases Didymella bryoniae Saprophytes fungi Toxins Pseudomonas syringae pv Tabtoxin Phaseolotoxin tabaci Pseudomonas syringae pv Tentoxin Cercosporin phaseolicola Victorin or HV toxin Alternaria alternate T-toxin Cercospora HC-toxin Cochliobolus victoriae Cochliobolus heterostrophus C. carbonum Exobasidium azalea Gibberella fujikuroi Rhodococus fasciens Ralstonia solanacearum

Indole -3- acetic acid Growth regulators Gibberellic acid Cytokinins Ethylene

Arch Microbiol

biotic stress contributing to yield loss of important crops in India is 18–31 % (Table 3). Endophytes are effective in protecting the plants from potent pathogens and pests. Foliar and systemic fungal endophytes reduce the herbivory by secreting the alkaloids toxic to vertebrates and insects (Schardl 2001). It helps in resistance to diseases, by mechanisms associated with nutritional status of host plant, and also increases plant growth by their tolerance to abiotic stress condition (Redman et al. 2002; Bae et al. 2008). First mechanism is the competition between fungal endophyte and the pathogen for same resources. The second mechanism is based on the ability of fungal endophytes to induce the plant host to produce the phytoalexins, and biocidal compounds, or the capacity of endophyte itself for the production of fumigants

Table 3  Contribution of fungal diseases toward yield loss in some major crops of India Crop

Pathogen

Disease

Total yield loss (%)

Rice

Pyricularia oryzae

Blast

21

Wheat

Puccinai recondiata

Leaf rust

30

Maize

H. maydis H. turcicum

Leaf blight

30

Sorghum

Sphacelotheca reiliaria

Grain mold

18

Pigeon pea

Fusarium udum

Wilt

24

Chickpea

Fusarium oxysporum

Wilt

23

Brassica

Alternaria brassiceae

Blight

30

Soybean

Phakospora packyrhizi

Rust

23

Potato

Phytophthora infestans

Late blight

31

and antimicrobial compounds, e.g., Spilanthes calva inoculated with the spores of Piriformospora indica, and then it produces antifungal compounds that inhibit the growth of soil-borne pathogens Trichophyton mentagrophytes and F. oxysporum (Rai et al. 2002; Mishra et al. 2014). The effect of P. indica only/or in combination with BioZinc (zinc gluconate) on diseases causing isolate F. solani in Pennisetum glaucum (pearl millet) was done in green house condition. Seeds of pearl millet were treated with pathogenic F. solani and P. indica only/or in combination with Bio-Zinc at the time of sowing under green house condition (Fig. 1). Combination of Bio-Zinc and P. indica not only enhanced the seed germination and plant growth but also decreases the symptoms caused by F. solani. Seed germination and different plant growth parameters were found to be increase in the combinational treatment compared to alone treatments (Mishra et al. 2014). Researchers have reported fungal endophytic strains from various plant species (Table 4) wherein several of them produce antibiotic substances (Strobel et al. 2002; Schulz and Boyle 2005; Wang et al. 2007) that inhibit the growth of several fungal pathogens (Liu et al. 2001; Park et al. 2005). Inoculation of Chaetomium and Phoma endophytes in wheat induces plant defense mechanisms and severity reduced foliar disease caused by Puccinia and Pyrenophora sp. (Dingle and McGee 2003; Istifadah and McGee 2006). Out of three hundred twenty-two endophytic fungi isolated from Chinese cabbage (Brassica campestris), only sixteen isolates completely suppressed disease caused by Plasmodiophora brassicae in sterile soil (Usuki et al. 2002). The sedentary endoparasitic cyst nematodes, belonging to the group Heterodera, are an economically important

Fusarium solani

Control

P. indica

Bio- Zinc

P. indica +Bio- Zinc

Fig. 1  Combination of P. indica with Bio-Zinc decreases the pathogenicity of F. solani from Pennisetum glaucum

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pest that causes yield losses on a number of different crop species. Root exudates of host plants stimulate the hatching of mobile second-stage juveniles (J2s) that are dormant in nematode cysts. It was suggested that P. indica may induce systemic resistance in plants (Molitor and Kogel 2009). Daneshkhah et al. (2013) reported that the cell wall extract and culture filtrate of this endophytic fungus antagonized the growth and development of cyst nematode Heterodera schachtii in A. thaliana. The antagonists were shown to affect nematode penetration and life cycle in the host plant. Besides well-established agricultural methods such as crop rotation, biological pest control based on the application of antagonists is a promising alternative to expensive and toxic nematicides. The production of secondary fungal metabolites and enzymes such as chitinases may attribute to toxicity against plant parasitic nematodes (Shinya et al. 2008). Similar results were obtained earlier with root exudates from tomato plants colonized by the AMF fungus Table 4  Fungi those are commonly isolated as endophytes from different plants Endophytes

Plant species

References

Phomopsis spp.

Neolitsea sericea Ginkgo biloba L. Taxus chinensis

Hata and Sone (2008) Thongsandee et al. (2012) Liu et al. (2009) Larran et al. (2002) He et al. (2012) Thongsandee et al. (2012) Wang et al. (2011) Bezerra et al. (2012) He et al. (2012)

Colletotrichum spp. Triticum aestivum Cinnamomum camphora Ginkgo biloba L. Huperzia serrata Cladosporium spp. Opuntia ficus indica Cinnamomum camphora Penicillium spp. Lycopersicum esculen- Larran et al. (2001) Wang et al. (2011) tum Mill. Huperzia serrata Acremonium spp.

Taxus chinensis Huperzia serrata

Table 5  Functions of root endophytic fungi on growth of the plant

Liu et al. (2009) Glienke-Blanco et al. (2002)

Glomus mosseae which reduced nematode penetration (Vos et al. 2011). Varma and Wieczorek (unpublished data) exhibited that P. indica colonizes roots of many plant species, including A. thaliana and promote their growth, development and seed production as well as confers resistance to various biotic and abiotic stresses. They emphasized that exudates of P. indica significantly affects the development of cyst nematode H. schachtii. The result obtained in the study carried out showed that P. indica improve crop productivity and protection in A. thaliana against plant parasitic nematodes. In continuation, Bajaj et al. (unpublished data) described biocontrol potential of P. indica against soybean cyst nematode (SCN), H. glycines by inoculating Glycine max with fungus. Fungal endophytes may contribute to their host plant defenses against various phytopathogens through plant physiology control (Gimenez et al. 2007). An increase in plant growth will prevent a variety of biotic stresses, reflecting plant vigor or persistence and considered as a potential protection to pathogen challenge (Kuldau and Bacon 2008). The fungal root endophytes have been reported in increasing the yield and biomass of host plant and belong to diverse genera, including Chaetomium, P. indica, Fusarium, Phialocephala. It has been documented by researchers that plants infected with endophytes have high yield (Barka et al. 2000), resistance to drought stress and are tolerant to unsuitable soil conditions (Malinowski et al. 2004). Root endophytic fungi, P. ndica forms asexual chlamydospores and can easily be grown on various medium (Pham et al. 2004; Prasad et al. 2005). The chlamydospores occur as typical pyriform. P. indica readily colonizes the A. thaliana and increases the yield and salt tolerance in barley plant (Oelmuller et al. 2009; Varma et al. 2013). The fungus uses unidentified signaling pathway to protect its host from pathogen and induces systemic resistance (Waller et al. 2005; Serfling et al. 2007). Plants infected with P. indica results in higher yield, early flowering and seed production and increase fresh weight (Varma et al. 2013; Prasad et al.

Fungi

Host

Effect on plant

Cryptosporiopsis spp.

Larix decidua

Increased root length

Periconia macropinosa Brassica compestris

13

Increased root growth Increased root biomass phosphorus intake

Phialocephala fortinii

Rhododendron spp.

Piriformospora indica

Zea mays, Nicotiana tobaccum, Baco- Increased growth and early rooting in tobacco calli pamonniera, Artemisia annua Spilanthes calva, Withania somnifera Increased overall growth and yield, number of flowers and fruits

Arch Microbiol P. indica/Chinese Cabbage

P. indica/Arabidopsis

Ethylene

Jasmonic acid

Cytokinin

Auxin

Signal transduction

Ethylene regulatedgenes ETR1 EIN2 EIN3/EIL1 Jasmonicacid regulatedgenes VSP PDF1.2 LOX2

Auxin regulatedgenes BcAUX1 (Arabidopsis)

Transcription

Cytokinin regulated genes

TIR1 AUX1 PINs (Chinese Cabbage)

Cytokinin regulated genes CRE1, AHK2, AHK3 Cytokinin regulated genes ARR5 Cytokinin biosynthesis genes

Growth promotion

ISR andplant defense

Fig. 2  Induced systemic resistance and plant defense response of P.indica/Araidopsis and P.indica/Chinese cabbage model

2013). Tolerance to abiotic stress was induced in Arabidopsis thaliana; overall growth and biomass production was achieved in herbaceous mono- and dicots, medicinal plants, and other important crops (Chadha et al. 2014) (Table 5). P. indica inoculated plants have shown resistance against various pathogens like Fusarium culmorum (W.G. Sm.) Sacc., and protection against the leaf pathogen by a mechanism of induced resistance (Fig. 2). In addition to resistance, it also increases the yield and salt stress tolerance (Waller et al. 2005). F. solani isolated from root tissues of tomato elicited induced systemic resistance against the tomato foliar pathogen Septoria lycopersici and triggered PR genes, PR5, and PR7 expression in roots (Kavroulakis et al. 2007; Mendoza and Sikora 2009). Fungal endophyte-mediated plant resistances to pathogens have been well studied in agricultural crops, grass systems (Terry and Joyce 2004), and forest trees (Ganley et al. 2008).

Conclusions Plant growth and development cannot be adequately described without acknowledging microbial interactions. We need to determine the extent of microbial associations in the plant kingdom. This question will only be answered as

technology is developed to detect their presence in plant tissues. What we have learned is that there is a need to understand how plant–microbes communicate in these endosymbiotic relationships, and how they regulate basic genetic and physiological functions. In the present review, authors advocate the deployment of fungal diversity and its role to overcome the biotic stress in plants. Endophytic fungal association with plants helps it to protect from various pathogen and pests and adapts to survive in stress condition. Acknowledgments  In the present chapter some of the research has been partially supported by DBT, DRDO and ICAR project under guidance of Prof. (Dr.) Ajit Varma.

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