role of endophytic microorganisms in sustainable agriculture

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

Author for correspondence

S. Indira Devi Email: [email protected]

© NECEER, Imphal

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

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

Role of endophytic microorganisms in sustainable agriculture Momota et al __________________________________________________________________________________________________

NeBIO I www.nebio.in I Vol. 3, No. 2, June 2012, 69-77 70

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 below-

ground 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 plant–microbe interactions in

soil, it is extremely difficult to understand the

detailed mechanisms involved in these putative

selection processes.

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).

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

Rhizobium–plant interaction, which indicates the

existence of highly evolved species-specific

communication systems (Bais et al. 2006) or from

plant–Pseudomonas 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 (Pirttilä et al. 2004).



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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Table 1. Example of reported bacterial endophytes and plants harbouring them. ENDOPHYTES PLANT SPECIES REFERENCE

α Protobacteria -

Azorhizobium caulinodans Rice Engelhard et al. 2000

Azospirillum brasilense Banana Weber et al. 1999

Bradyrhizobium japonicum Rice Chantreuil et al. 2000

Gluconacetobacter diazotrophicus Sugarcane, coffee Jimenez Salgado et al. 1997

Methylobacterium mesophilicum Citrus plants Araujo et al. 2002

Rhizobium leguminosarum Rice Yanni et al. 1997

Rhizobium radiobacter Carrot, rice Surette et al. 2003

β Proteobacteria -

Azoarcus sp. Kallar grass, rice Engelhard et al. 2000

Burkholderia pickettii Maize McInroy and Kloepper 1995 Burkholderia cepacia Yellow lupine, citrus plants Araujo et al. 2001; Barac et al. 2004

Burkholderia sp. Banana, pineapple, rice Engelhard et al. 2000

Chromobacterium violaceum Rice Phillips et al. 2000

Herbaspirillum seropedicae Sugarcane, rice, maize, sorghum, Olivares et al. 1996; Weber et al. 1999

Herbaspirillum rubrisulbalbicans Sugarcane Olivares et al. 1996

¥ Proteobacteria Citrobacter sp. Banana Martinez et al. 2003

Enterobacter sp. Maize McInroy and Kloepper 1995

Enterobacter sakazakii Soybean Kuklinsky-Sobral et al. 2004 Enterobacter cloacae Citrus plants, maize Araujo et al. 2002; Hinton et al. 1995

Erwinia sp. Soybean Kuklinsky-Sobral et al. 2004

Pantoea sp. Rice, soybean Kuklinsky-Sobral et al. 2004 Pantoea agglomerans Citrus plants, sweet potato Araujo et al. 2002

Pseudomonas chlororaphis Marigold (Tagetes spp.) Sturz and Kimpinski 2004

Pseudomonas putida, P.fluorescens Carrot Surette et al. 2003 Serratia marcescens Rice Gyaneshwar et al. 2001

Firmicutes - Bacillus sp. Citrus plants Araujo et al. 2001, 2002

Bacillus megaterium Maize, carrot, citrus plants Araujo et al. 200, Surette et al. 2003

Clostridium Grass Miscanthus sinensis Miyamoto et al. 2004 Paenibacillus odorifer Sweet potato Reiter et al. 2003

Staphylococcus saprophyticus Carrot Surette et al. 2003

Bacteroidetes - Sphingobacterium sp. Rice Phillips et al. 2000

Actinobacteria -

Arthrobacter globiformis Maize Chelius and Triplett 2000 Curtobacterium flaccumfaciens Citrus plants Araujo et al. 2002

Kocuria varians Marigold Sturz and Kimpinski 2004

Microbacterium testaceum Maize Zinniel et al. 2002 Nocardia sp. Citrus plants 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 plant-

endophyte -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.



Table 2. List of some endophytic microbial biopesticides. (Kabaluk et al. 2010) Microbialpesticide Organism Target

Trichoderma spp Fungus Downy mildew, Rhizoctonia cerealis, gray mold, Phytopathogenic fungi

Bacillus subtilis Bacterium Bacterial wilt, tobacco black, root rot, Powdery mildew, gray mold,

Alternaria blight, large patch, brown patch, Pythium blight, Phytophthora blight

Beauveria bassiana Fungus Monochamus alternatus, Dendrolimus punctatus, Coffee berry borer,

diamondback moth, thrips, grasshoppers, whiteflies, aphids, codling moth

Pseudomonas fluorescens Bacterium Plant soil borne diseases

Verticillium lecanii Whitefly, coffee green bug, homopteran pests Paecilomyces lilacinus Fungus Whitefly

Verticillium chlamydosporium Fungus Nematode

Streptomyces colombiensis Bacterium Powdery mildew, gray mold, brown patch

Streptomyces griseoviridis K61 Bacterium 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 Bacillus subtilis QST713 Bacterium Botrytis spp.

Actinomyces levendula Bacterium Root rots and bacterioses

Klebsiella oxytoca and Bacillus mucilaginosus

Bacterium Enhancing of resistance to root diseases

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



Figure 2. Potential effects of (a) elevated CO2 concentrations, b) warming and drought on beneficial plant–microbe

interactions.

tolerance (physiological and biochemical adapt-

ations) 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 plant-

associated 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 anti-

pathogen mechanism against nematodes, insects,

pests and microbes, drought, salinity, extreme

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 host-

microbe 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.



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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