NeBIO

Vol. 3, No. 2, June 2012, 69-77

Role of endophytic microorganisms in sustainable agriculture

Momota, P1, B.K. Singh2 and S.Indira Devi1 1Microbial Resources Division, 2Natural Product Chemistry Institute of Bioresources and Sustainable Development, DBT, Govt. of India Takyelpat Institutional Area, Imphal-795001 ABSTRACT The plant kingdom is colonized by diverse range of endophytic microorganisms. Some microbes form non-pathogenic relationships with their host, where they colonize the internal tissues of the host plant and form a range of associations including symbiotic, mutalistic, commensalistic and trophobiotic relationships. Most endophytes appear to originate from the rhizosphere or phyllosphere. Endophytic microorganisms can promote plant growth and yield and can act as strong biocontrol agents against various diseases including insect-pest. Endophytes can stimulate plant growth hormones, increase disease resistance, improve the plants ability withstand environmental stress conditions (e.g. drought, pH, temperature etc.) or enhance N2 fixation and increase in nutrient supply. Therefore, the endophytic micro floral community is of dynamic structure and its potential contribution on sustainable agricultural development needs to be exploited for high yield in order to overcome food crisis. Hence, the importance of endophytes in association with agriculture is a boon to mankind and research exploitation to get a potentially novel endophyte should be encouraged. Keywords: Endophytes, plant growth, biocontrol agents, stress tolerance

Agriculture and its product is the ultimate source of livelihood worldwide. Due to consequent hurdles, the present production is not able to meet the demanding and growing population. As an aid or looking to the alternative prospect, use of endophytic microbes comprising mainly of fungus and bacteria as plant growth promotion and as biocontrol agent is upcoming area of research. Also, the continuing exploitation on environment and health factors due to used of harmful chemicals like fertilizers and pesticides has caused increasing alarm all over. Therefore, there is a need to promote a more advantageous agent that which solves the maximum problems and also protects the environment. Microbes are dominant living structure on the universe and its impact on agriculture in association with the fruitful harmless microbes is a boon to agrobusiness. The context revolving endophytism and the varied contribution in the field of agriculture. Endophytes are defined as organisms that
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asymptomatically infect the internal tissues of plants during at least part of their life cycle (Petrini, 1991). In general, endophytic bacteria originate from the epiphytic bacterial communities of the rhizosphere and phylloplane, as well as from endophyte-infested seeds or planting materials. (Hallmann et al. 1997). The plant associated microbes lives in varying relation with the host, the host provide nutrients to the microbes and in turn the plant get benefited from the associates by promoting plant growth, increase yield, vigour tolerance to a list of biotic and abiotic stress such as increased resistance against plant pathogens and parasites, tolerance against pH, temperature, drought, salinity etc. Production of active metabolites by the associates contributes much to the host plant. Exploitation of beneficial properties of endophytes is of great relevance at an applied level, either to increase production yields of agricultural crops, control of plants diseases or pests, adapt plant to suitable growth conditions, or in reforestation activities. (Jose G et al. 2009). (Pablo et

S. Indira Devi

Email: sidevi1@yahoo.co.in NECEER, Imphal

Role of endophytic microorganisms in sustainable agriculture Momota et al __________________________________________________________________________________________________

al. 2008) classified bacterial endophytes as obligate or facultative. Obligate endophytes strictly dependent on the host plant for their growth and survival and transmission to other plants occurs vertically or via vectors. Endophytic colonization: Colonization traits usually relates to the bacterial traits involved in the entire plant-colonization process. In the interactive colonization processes, communication between the plant and microbe has a key role (Rosenblueth et al. 2006) (Figure 1). Bacterial root colonization often starts with the recognition of specific compounds in the root exudates by the bacteria (DeWeert et al. 2002) .These compounds probably also have major roles in belowground community interactions (Bais et al.2004) Theoretically, plants simultaneously communicate with commensalistic, mutualistic, symbiotic and pathogenic microorganisms via compounds exuded by their roots (Bais et al. 2006) .However, it has been suggested that plants can communicate to specifically attract microorganisms for their own ecological and evolutionary benefit (Compant et al. 2005) Owing to the complexity of the plantmicrobe interactions in soil, it is extremely difficult to understand the detailed mechanisms involved in these putative selection processes.

Competent endophytes (yellow cells) are proposed to have all properties of opportunistic endophytes, and, in addition, be well adapted to the plant environment. (Pablo et al.2008).

Lessons can be learned from the well-studied Rhizobiumplant interaction, which indicates the existence of highly evolved species-specific communication systems (Bais et al. 2006) or from plantPseudomonas associations, in which two distinct plants (flax and tomato) have attracted specific minority strains of the Pseudomonas sp. involved, rather than the whole Pseudomonas community (Lemanceau et al. 1995). Much like the bacteria selected in the rhizosphere, particular endosphere bacteria might also be selected to establish residence inside plants (Van Overbeek, et al. 2008). Bacterial traits required for effective root colonization are subject to phase variation, a regulatory process for DNA rearrangements orchestrated by site-specific recombinase. (Van der Broek et al. 2003). Endophytic population sizes are dependent on, and positively correlated with, plant developmental stage, progressively increasing from the seedling stage onwards and reaching a maximum (e.g. 107 CFU g/1 fresh weight at the senescence stage of potato plants) (Van Overbeek et al. 2008). The propose role of endophytic microbes As growth promoter: There are numbers of mechanisms by which bacteria may promote plant growth and health which includes the production of plant growth phytohormones like auxins, cytokinins, gibberellins and ethylene, solubilised insoluble phosphate, produced HCN and siderophore and can fixed atmospheric N2. A number of mutually beneficial relationships between plants and microorganisms affect agricultural productivity and health of the plants in general, and these systems have also been the canter of intensive studies (Smith and Read, 1996). In symbiotic relationships, the microorganism helps the plant with nutrient assimilation or contributes biochemical activities that the plant lacks; microbes also confer a degree of protection against plant diseases. The plants, in turn, supply competitive advantage to the corresponding microbes. Volatile substances such as 2-3 butanediol and aceotin produced by bacteria seem to be a newly discovered mechanism responsible for plant-growth promotion (Ryu et al. 2003). Endophytes produce adenine ribosides that stimulate growth and mitigate browning of pine tissues (Pirttil et al. 2004).
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Figure 1. Types of endophytes and their root colonization process. Soil-inhabiting bacteria might become endophytic by chance (e.g. via colonization of natural wounds or following root invasion by nematodes). Such bacteria are considered passenger endophytes (red cells) and are often restricted to the root cortex tissue. Opportunistic endophytes (blue cells) show particular root colonization characteristics (e.g. a chemotactic response, which enables them to colonize the rhizoplane and then invade the internal plant tissues through cracks formed at the sites of lateral root emergence and root tips).Opportunistic endophytes are confined to particular plant tissues (e.g. the root cortex).

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Role of endophytic microorganisms in sustainable agriculture Momota et al __________________________________________________________________________________________________

Endophyte and insect control: Webber (1981) was probably the first researcher to report plant protection by an endophytic fungus, in which the endophyte Phomopsis oblonga protected elm trees against the beetle Physocnemum brevilineum the capacity of endophytic fungus to repel insects, induce weight loss, growth and development reduction and even to increase pest death rate, was correlated with toxin production. In several cases, it was shown that the mode of action of certain fungi was based on the capability to render the plant unpalatable to several types of pests like aphids, grasshoppers, beetles, etc (Carroll et al. 1988). Alkaloids from N. lolii and L. perenne are capable of altering insect behaviour. Several of these alkaloids were added to the diet of adult individuals of the Coleoptera Heteronychus aratur. Peramine, lolitrem B, lysergol-type alkaloids, festuclavine and lisergic acid showed no effects on the insect. Ergovine showed moderate effects whereas ergotamine, ergovaline from the ergot-type alkaloid family seem to be responsible for the plant resistance (Ball et al. 1997). Miles et al. (1998) showed that endophytic isolates of Neotyphodium sp. produce N-formilonine and a paxiline nalogous in the host Echinopogum ovatus. These compounds show insecticidal activity against L.bonariensis and other insects. Other indirect effect of endophytic fungi with applied interests is the control of ectoparasites in domestic animals. Haematobia irritans larvae of horn fly, which is a cattle ectoparasite, were killed when cattle manure was amended with seed extracts containing lolines from plants infected with N. coenophialum (Dougherty et al.1998). Biopesticidal role of endophyte: Biopesticides, term as an agent of biological origin may be viruses, bacteria, pheromones, plant or animal compounds. The outstanding feature of biopesticides is environment friendly, easy biodegradability, faster rate of product development, low research expenditure, do not disturb natural biocenosises also application of biopreparation lowers the chemical loading to the environment, does not worsen the soil fertility ,natural ways of decomposition in nature, non toxicity for warm-blooded organisms and overcoming the anti-environment chemical pesticide (V.P. Patyka and G.Omelyanets) 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 (Kumar et al. 2008). Burkholderia brasilensis is an endophyte of roots, stems and leaves of sugarcane plant while Burkholderia tropicalis is confined to its roots and stems, with effective biopesticide properties. (Reis et al. 2000). Tolerance to different environmental stress: Endophytic microorganisms actively response to various biotic and abiotic stress factors that which hampers the overall agricultural scenario. Biotic stress tolerance mechanisms such as biocontrol of phytopathogens in the root zone (through production of antifungal or antibacterial agents, pathogen antagonism, siderophore production aiding plant nutrition by iron chelation, P solubilisation and induction of systematic acquired host resistance. Endophytes from potato plants showed antagonistic activity against fungi (Berg et al. 2005; and also inhibited bacterial pathogens belonging to the genera Erwinia and Xanthomonas. Some of the endophytic isolates produced in particular, various bacteria and fungi- especially of the genera peudomonas, Bacillus and Trichoderma- produce a range of metabolites against other phytopathogenic fungi (Raijaamkers et al. 2002). Production of antibiotics sensitive to plant pathogens such as alkaloids, terpenoids, aromatic compounds, polypeptides and secretion of enzymes that has the capacity to hydrolyse compounds like cellulose, hemicellulose, chitin, proteins etc.. Fusarium spp. E4 and E5 promote the growth of Euphorbia pekinensis, and increased its terpenoids content (Yong et al. 2009). Sturz et al. (1997), found that 61 of 192 endophytic bacterial isolates from potato stem tissues were effective biocontrol agents against Clavibacter michiganensis subsp. sepedonicus.

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Role of endophytic microorganisms in sustainable agriculture Momota et al __________________________________________________________________________________________________ Table 1. Example of reported bacterial endophytes and plants harbouring them.
ENDOPHYTES Protobacteria Azorhizobium caulinodans Azospirillum brasilense Bradyrhizobium japonicum Gluconacetobacter diazotrophicus Methylobacterium mesophilicum Rhizobium leguminosarum Rhizobium radiobacter Proteobacteria Azoarcus sp. Burkholderia pickettii Burkholderia cepacia Burkholderia sp. Chromobacterium violaceum Herbaspirillum seropedicae Herbaspirillum rubrisulbalbicans Proteobacteria Citrobacter sp. Enterobacter sp. Enterobacter sakazakii Enterobacter cloacae Erwinia sp. Pantoea sp. Pantoea agglomerans Pseudomonas chlororaphis Pseudomonas putida, P.fluorescens Serratia marcescens Firmicutes Bacillus sp. Bacillus megaterium Clostridium Paenibacillus odorifer Staphylococcus saprophyticus Bacteroidetes Sphingobacterium sp. Actinobacteria Arthrobacter globiformis Curtobacterium flaccumfaciens Kocuria varians Microbacterium testaceum Nocardia sp. PLANT SPECIES Rice Banana Rice Sugarcane, coffee Citrus plants Rice Carrot, rice Kallar grass, rice Maize Yellow lupine, citrus plants Banana, pineapple, rice Rice Sugarcane, rice, maize, sorghum, Sugarcane Banana Maize Soybean Citrus plants, maize Soybean Rice, soybean Citrus plants, sweet potato Marigold (Tagetes spp.) Carrot Rice Citrus plants Maize, carrot, citrus plants Grass Miscanthus sinensis Sweet potato Carrot Rice Maize Citrus plants Marigold Maize Citrus plants REFERENCE Engelhard et al. 2000 Weber et al. 1999 Chantreuil et al. 2000 Jimenez Salgado et al. 1997 Araujo et al. 2002 Yanni et al. 1997 Surette et al. 2003 Engelhard et al. 2000 McInroy and Kloepper 1995 Araujo et al. 2001; Barac et al. 2004 Engelhard et al. 2000 Phillips et al. 2000 Olivares et al. 1996; Weber et al. 1999 Olivares et al. 1996 Martinez et al. 2003 McInroy and Kloepper 1995 Kuklinsky-Sobral et al. 2004 Araujo et al. 2002; Hinton et al. 1995 Kuklinsky-Sobral et al. 2004 Kuklinsky-Sobral et al. 2004 Araujo et al. 2002 Sturz and Kimpinski 2004 Surette et al. 2003 Gyaneshwar et al. 2001 Araujo et al. 2001, 2002 Araujo et al. 200, Surette et al. 2003 Miyamoto et al. 2004 Reiter et al. 2003 Surette et al. 2003 Phillips et al. 2000 Chelius and Triplett 2000 Araujo et al. 2002 Sturz and Kimpinski 2004 Zinniel et al. 2002 Araujo et al. 2002

Bacterial endo-phytes are capable of suppressing nematode proliferation and this may benefit other crops in rotation with the host plants (Sturz and Kimpinski, 2004). Munumbicins, antibiotics produced by the endophytic bacterium Streptomyces sp. strain NRRL 30562 isolated from Kennedia nigriscans. Subsequently, it has been reported that certain endophytic bacteria isolated from field-grown potato plants can reduce the in vitro growth of Streptomyces scabies and Xanthomonas campestris through production of siderophore and antibiotic compound. Iron is an essential growth element for all living organisms. The scarcity of iron in soil habitats and on plant surfaces gives rise to an enraged

competition (Loper et al. 1997). Under iron-limiting conditions endophytes produce low-molecular-weight comp-ounds called siderophores to competitively acquire ferric ion. (Whipps et al. 2001). The ability to act as bioprotectants via Induce Systemic Resistance has been demonstrated for both rhizobacteria and bacterial endophytes, and considerable progress has been made in elucidating the mechanisms of plantendophyte -pathogen interaction. Volatiles secreted by B. subtilis GBO3 and B. amyloquefaciens IN937a were able to activate an ISR pathway in Arabidopsis seedlings challenged with the soft-rot pathogen Erwinia carotovora subsp. carotovora (Nielsen et al. 2002). Detoxification of pathogen virulence factors.

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Role of endophytic microorganisms in sustainable agriculture Momota et al __________________________________________________________________________________________________ Table 2. List of some endophytic microbial biopesticides. (Kabaluk et al. 2010)
Microbialpesticide Trichoderma spp Bacillus subtilis Organism Fungus Bacterium Target Downy mildew, Rhizoctonia cerealis, gray mold, Phytopathogenic fungi Bacterial wilt, tobacco black, root rot, Powdery mildew, gray mold, Alternaria blight, large patch, brown patch, Pythium blight, Phytophthora blight Monochamus alternatus, Dendrolimus punctatus, Coffee berry borer, diamondback moth, thrips, grasshoppers, whiteflies, aphids, codling moth Plant soil borne diseases Whitefly, coffee green bug, homopteran pests Whitefly Nematode Powdery mildew, gray mold, brown patch Fusarium wilt, Botrytis grey mold, root rot, stem rot, stemend rot, damping off, seed rot, soil borne damping off, crown rot, Rhizoctonia, Phytophthora, wilt, seed damping off, early root rot Botrytis spp. Root rots and bacterioses Enhancing of resistance to root diseases

Beauveria bassiana

Fungus

Pseudomonas fluorescens Verticillium lecanii Paecilomyces lilacinus Verticillium chlamydosporium Streptomyces colombiensis Streptomyces griseoviridis K61

Bacterium Fungus Fungus Bacterium Bacterium

Bacillus subtilis QST713 Actinomyces levendula Klebsiella oxytoca and Bacillus mucilaginosus

Bacterium Bacterium Bacterium

For example, certain biocontrol agents are able to detoxify albicidin toxin produced by Xanthomonas albilineans (Zhang et al. 1997). The detoxification mechanisms include production of a protein that reversibly binds the toxin in both Klebsiella oxytoca (Walker et al. 1988) and Alcaligenes denitrificans (Basnayake et al. 1995), as an irreversible detoxification of albicidin mediated by an esterase that well occurs in Pantoea dispersa (Zhang et al. 1997). Abiotic stress is a serious threat to agriculture and result in the deterioration of the environment (Bray et al. 2000). Abiotic stress leads to a series of morphological, physiological, biochemical and molecular changes that adversely affect plant growth and productivity (Wang et al. 2001). Drought, salinity, extreme temperatures and oxidative stress are often interconnected, and may induce similar cellular damage. (Wang et al. 2000) For example, drought and/or salinization are manifested primarily as osmotic stress, resulting in the disruption of homeostasis and ion distribution in the cell (Zhu et al. 2001). High temperature stress causes extensive denaturation and aggregation of cellular proteins, which, if unchecked, lead to cell death. Warming effect: Temperature appears to be a major parameter affecting fluctuation of endophyte occurrence in plant tissues (Ju et al. 2006).It is known that soil warming may impact beneficial associations between plants and fungal endophytes (Fig. 2b) Newman et al. 2003), and it has been, however, demonstrated that the endophyte infection

frequency (Fujimura et al. 2008) reported that warming increased the density of different fungal endophyte genotypes within individual root sections of arctic willow (Salix arctica) at a tundra site in the Canadian High Arctic. However, it did not affect the composition, richness or evenness of the community. A study with the endophyte Burkholderia phytofirmans strain PsJN demonstrated that a temperature increase from 10 to 300C reduced the colonization of this strain in the tomato rhizosphere, whereas endophytic abundance was not affected (Pillay and Nowak, 1997). After successful colonization, rhizosphere as well as endophytic bacteria may alleviate temperature or drought stress on plants (Aroca & Ruiz-Lozano, 2009) by inducing a systemic response (Yang et al. 2009). This demonstrates the potential role of certain strains for use in agriculture Drought stress: The ability of many symbiotic fungi to confer drought tolerance goes well together with the suggestion that symbiotic fungi were involved in the movement of plants onto land (Redecker et al. 2000). Some endophytes, moreover, can improve plant growth during drought stress exposure (Fig. 2.1b; Elmi and West, 1995; Hesse et al. 2004; Rodriguez et al. 2008). Endophyte infection conferred population stability in tall fescue during drought stress through improved tiller and whole plant survival (West et al. 1993). Such endophytes have been shown to induce mechanisms of drought avoidance (morphological adaptations), drought
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Role of endophytic microorganisms in sustainable agriculture Momota et al __________________________________________________________________________________________________

Figure 2. Potential effects of (a) elevated CO2 concentrations, b) warming and drought on beneficial plantmicrobe interactions.

tolerance (physiological and biochemical adaptations) and drought recovery in infected grasses (reviewed in Malinowski and Belesky, 2000). These features could be beneficial for plant especially on sites where water is the growth-limiting factor (Hesse et al. 2004). Increase carbondioxide level: Most information on the effects of elevated ambient CO2 on plantassociated bacteria has so far been obtained by studies performed within the long-term Free Air CO2 Enrichment (FACE) experiment performed in Switzerland (Hebeisen et al. 1997). In addition to the differential effects reported by Drigo et al. (2009), showed that elevated CO2 increased the dominance of Pseudomonas sp., which are known to include many plant growth-promoting members, associated with plants. (Fig.2a). Conclusion Plants community is associated with diverse microbial associations, ranging from beneficial to opportunistic and even pathogens. The area of interest is confine to the beneficial associates of microbial flora, due to their immense role in plant growth, development and protection. Therefore, the symbiotic associates and its contribution to the host plant can no longer be ignored and need a rooted study, especially in their mechanisms in conferring host plant various biotic and abiotic stress tolerances. Many studies have investigated tolerance of the endophytic microbes to stress response such as antipathogen mechanism against nematodes, insects, pests and microbes, drought, salinity, extreme
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temperature (cold/heat), heavy metal pollution, etc. Interesting, study on plant-microbe interaction and plant growth development cause by the beneficial microbe is the foci recently. Some arises to the point that endophyte exibit host specificity and environment adaptation mechanism, in which the response to various stress factors are based on the host and the environmental factor from which it was obtained. Indeed, the propose role of endophyte being able to survive in unfavourable conditions is one of the major area requiring attention. Several endophytes have been reported to produce growth promoting hormones and confers biochemical properties to plants. Again, the role of endophytes in defence mechanisms against catastrophic plant diseases favours the host plant protection and the ample benefits provided by the endophytes to the host, with increasing importance to agricultural production, combating food crisis worldwide, directly and indirectly is the impact of endophyte on agricultural science. On the other hand, studies on isolation and exploitation of endophytes to get a novel potential strain needs to expertise on culture dependent and independent aspect. As, plant growth and development studies is bridge to host-microbe relation, much advance studies is required to have a clear view on the controlling mechanism of hostmicrobe interaction. Mentioning, that experimental research on this area is at the initial stage either in lab or green house condition, there is an essentiality to effectively transfer the technology to field conditions and further study and observe the changes in order to give the technology a furnish successful application.
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Role of endophytic microorganisms in sustainable agriculture Momota et al __________________________________________________________________________________________________

Acknowledgements The authors express humble gratitude to the Department of Biotechnology (DBT), Government of India, for assisting financial aid to the project.
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