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Biological Control of Plant Pathogens, Pests and Weeds

 
     
 

Antagonism - The Mechanism of Biocontrol

Biological control is principly achieved through antagonism (the inhibitory relationships between microorganisms including plants) which involves : (i) amensalism i.e. antibiosis and lysis, (ii) competition, and (iii) parasitism and predation.

 

Amensalism (Antibiosis and Lysis)

Amensalism is a phenomenon where one population adversely affects the growth of another population whilst itself being unaffected by the other population. Generally amensalism is accomplished by secretion of inhibitory substances. Antibiosis is a situation where the metabolites secreted by organism A inhibit organism B, but organism A is not affected. It may be lethal also. Metabolites penetrate the cell wall and inhibit its activity by chemical toxicity. Generally antimicrobial metabolites are produced by underground parts of plants, soil microorganisms, plant residues, etc. Fig. 13.1 shows in vitro interaction of colony of Celletotrichum gloeosporioides (a fungal pathogen associated with fruit rot of guava) and Fusarium oxysporum (a saprophyte) and formation of inhibition zone between the colonies.

 

Substances noxious to certain soil-borne plant pathogens are secreted by roots of maize, clover, lentil (glycine, phenylalanin) and other legumes, flax (hydrocyanic acid), pine (volatile mono-and sesquiterpenes) and by other plant roots. Other plant residues are the source of phenolic and non-volatile compounds. Similarly, antimicrobial substances (antibiotics) produced by microorganisms (soil bacteria, actinomycetes, fungi) are aldehydes, alcohols, acetone, organic acid, nonvolatile and volalite compounds which are toxic to microbes. Changes in microbial structures (cell wall, hyphae, conidia, etc.), may occur when microorganisms lack resistance against the attack by deleterious agents or unfavorable nutritional conditions. A chemical substance (i.e. melanin) is present in their cell walls to resist the lysis. Moreover, cell wall constituents, for example, xylan or xylose containing hetero polysaccharides, may also protect fungal cells from lysis. 

 

Content

Biological control of plant pathogens 

 

Inoculum

 

Historical background

 

Phyllosphere-phylloplane and rhizosphere-rhizoplane regions

 

Antagonism

 

 

Amensalism (antibiosis and lysis)

 

 

Competition

 

 

Predation and parasit­ism : Mycoparasitism, nematophagy and mycophagy

 

Application of biological control

 

 

Crop rotation

 

 

Irrigation

 

 

Alteration of soil pH

 

 

Organic amendments

 

 

Soil treatment with selected chemicals

 

 

Introduction of antagonists : Seed inoculation, vegetative part inoculation and soil inoculation

 

 

Use of mycorrhizal fungi

 

Genetic engineering of biocontrol agents

Biological control of insect pests

 

Microbial pesticidies

 

 

Bacterial, viral and fungal pesticides

 

 

Viral pesticides

 

 

Mycopesticides

Biological control of weeds

 

Mycoherbicides

 

Insects as biocontrol agents


The potent antagonists e.g. Trichoderma harzianum and T. viride are known to secrete cell wall lysing enzymes, 6-1, 3-glucanase (Chet and Henis, 1975), chitinase, and glucanase (Chester and Bull, 1963). However, production of chitinase and 6-1, 3-glucanase by T. harzianum inside the attacked sclerotia of Sclerotium rolfsii has also been reported by Elad et al. (1984).

Siderophores. Siderophores are the other extracellular metabolites which are secreted by bacteria {e.g. Aerobacter aerogenes, Arthrobacter pascens, Bacillus polymyxa, Pseudomonas cepacia, P. aeruginosa, P. fluorescens, Serratia, etc.), actinomycetes (e.g. Streptomyces spp.) yeasts (e.g. Rhodotorula spp.), fungi (Penicillum spp.). and dinoflagellates (Prorocentrum minimum). Siderophores are commonly known as microbial iron chelating compounds because they have a very high chelating affinity for Fe3+ ions and very low affinity with Fe2+ ions. Siderophores are low molecular weight compounds. After chelating Fe3+ they transport it into the cells. Kloepper et al. (1980) were the first to demonstrate the importance of siderophore production by PGPR in enhancement of plant growth. Siderophores after chelating Fe3+ make the soil Fe3+ deficient for other microorganisms. Consequently growth of other microorganisms is inhibited. When the siderophore producing PGPR is present in rhizosphere, it supplies iron to plants. Therefore, plant growth is stimulated.

  Colony interaction between Fusarium oxysporum (FO) and Colletotrichum gloesporioides (CG), and formation of inhibition zone (Courtesy: Dr R.R. Pandey, Manipur University, Imphal).
 
Fig. 13.1. Colony interaction between Fusarium oxysporum (FO) and Colletotrichum gloesporioides (CG), and formation of inhibition zone (Courtesy: Dr R.R. Pandey, Manipur University, Imphal).
In recent years, role of siderophores in biocontrol of soil-borne plant pathogens is of much interest. Microbiologists have developed the methods for introduction of siderophore producing bacteria in soil through seed, soil or roots.

Gupta, Sharma, Dubey and Maheshwari (1999) have isolated a strain of P. aeruginosa (GRC) from potato rhizosphere which was found to secrete hydroxamate type of siderophore after 48 h of incubation. It also secreted hydrocyanic acid and indole acetic acid. Moreover, this strain also displayed antagonistic properties against two plant pathogens, Macrophomina phaseolina and Fusarium oxysporum. Fig. 13.2. shows the inhibition in colony of M. phaseolina (MP) by a fluorescent pseudomonas (FP).

 

Competition

Among micro-organisms competition exists for nutrients, including oxygen and space but not for water potential, temperature, or pH. Amensalism involves the combined action of certain chemicals such as toxins, antibiotics and lytic enzymes. Success in competition for substrate by any particular fungal species is determined by competitive saprophytic ability (Garrett, 1950) and inoculum potential (Garrett, 1956) of that species. Competitive saprophytic ability is "the summation of physiological characteristics that make for success in competitive colonization of dead organic substrates" (Garrett, 1956).

  Growth inhibition in colony of Macrohpomina phaseolina (MP) due to siderophore of a fluorescent, Pseudomonas GRC2 (FP) (Courtesy : Mr. Chandra P. Gupta, Deptt of Microbiology, Gurukul Kangri Univ., Haridwar).
 
Fig. 13.2. Growth inhibition in colony of Macrohpomina phaseolina (MP) due to siderophore of a fluorescent, Pseudomonas GRC2 (FP) (Courtesy : Mr. Chandra P. Gupta, Deptt of Microbiology, Gurukul Kangri Univ., Haridwar).

Garrett (1950) has suggested four characteristics which are likely to contribute to the competitive saprophytic ability (i) rapid germination of fungal propagules and fast growth of young hyphae towards a source of soluble nutrients, (ii) appropriate enzyme equipment for degradation of carbon constituents of plant tissues (iii) excretion of fungistatic and bacterio-static growth products including antibiotics, and (iv) tolerance of fungistatic substances produced by competitive microorganisms.

 

Inoculum potential is defined under section Inoculum. Possession of any of the four characteristics and inoculum potential' is sufficient for a microbe to get success in microbial competition.

 

Biological control of Forties annosus by inoculating the freshly cut stumps of pine with Peniophora gigantea is a result of competition, as is the control of Pseudomonas tolaasii on mushroom by other bacteria (Baker and Cook, 1974). The fate of plant pathogens in competition for food and space depends on other factors also such as, cellulolysis rate that mediates the speed of saprophytic tissue penetration (Garrett, 1975). Species of Trichoderma and Gliocladium are the two potent antagonists which produce antibiotics to destroy mycelia of other fungi. Some examples of successful competitors competing for nutrients with other microorganism are : bacteria vs S. scabies (for oxygen), soil amoebae vs Gaeumannomyces graminis var. tritici (wheat roots), T. viride vs Fusarium roseum (wheat straw), Chaetomium sp. vs Cochliobolus sativus (wheat straw,), Arthrobacter globiformis vs Fusarium oxysporum f. lini (glucose and nitrate).

  Post-interaction events during mycoparasitism. A, coiling (a, antagonist; h, host hypha); B, penetration; C, barrier formation (b) by host; D, branch formation and sporulation (s) by antagonist; E, chlamydospore (c) formation; F, lysis of host hypha (diagrammatic, after Dubey and Dwived, 1986).  
 
Fig. 13.3. Post-interaction events during mycoparasitism. A, coiling (a, antagonist; h, host hypha); B, penetration; C, barrier formation (b) by host; D, branch formation and sporulation (s) by antagonist; E, chlamydospore (c) formation; F, lysis of host hypha (diagrammatic, after Dubey and Dwived, 1986).
 

Predation and Parasitism

Predation is an apparent mode of antagonism where a living microorganism is mechanically attacked by the other with the consequences of death of the farmer. It is often violent and destructive relationship. Parasitism is a phenomenon where one organism consumes another organism, often in a subtle, non-debilitating relationship. These aspects are dealt with the example of fungi, nematodes and amoebae (Table 13.3).

 

Mycoparasitism

When one fungus is parasitized by another one the phenomenon is called as mycoparasitism. The parasitising fungus is called hyperparasite and the parasitized fungus as hypoparasite (Fig. 13.3). Mycoparasitism commonly occurs in nature. As a result of inter-fungus interaction i.e. fungus-fungus interaction, several events take place which lead to predation viz., coiling, penetration, branching, sporulation, resting body production, barrier formation and lysis (Fig. 13.3).

In coiling (A) an antagonist, the hyperparasite (a) recognizes its host hyphae i.e. the hypoparasite (h) among the microbes and comes in contact and coils around the host hyphae. The phenomenon of recognition of a suitable host by the antagonists has been discovered in recent years. Manocha (1985) has given a molecular basis of host specificity and host-recognition by mycoparasites. Cell wall surface of host and non-host contains D-galactose and N-acetyl D-galactosamine residues as lectin binding sites. With the help of lectins present on the cell wall, an antagonist recognizes the suitable sites (residues of lectins) and binds the host hypha. As a result of coiling, the host hypha loses the strength. If the antagonist has capability to secret cell wall, degrading enzymes, it can penetrate the cell wall of host hyphae and enter in lumen of the cells. The event of entering in lumen of host cell is known as penetration (Fig. 13.3. B). Several cell wall degrading enzymes such as cellulase b-1, 3-glucanase, chitinase,etc. have been reported (Elad et al, 1982).

 

Sometimes host develops a resistant barrier ( Fig. 13.3B) to prevent the penetration inside the cell. Cytoplasm accumulates to form a spherical, irregular or elongated structure, so that the hypha of antagonist could not pass towards the adjacent cells of the hypha (Fig. 13.2C). Depending upon nutrition, the antagonist forms branches and sporulates (s) inside the host hypha (Fig. 13.2D). Until the host's nutrients deplete, the antagonist produces resting bodies, the survival structures, for example, chlamydospores (c) inside the host hypha (Fig. 13.2E). Finally post-infection events lead to lysis of the host hypha (Fig. 13.2F) due to loss of nutrients and vigor for survial. Example of parasitism and post-infection events are given in Table 13.2 and Fig. 13.3 (Dubey and Dwivedi, 1986).

Table 13.2. Examples of predation and parasitism

Mode of

antagonism

Plant pathogens

Antagonists

(hosts)

Post-infection events

Mycoparasitism:

Rotrytis alii

Gliocladium roseum

Penetration of hypae

Cocchliobolus

sativus

Myrothecium

verrucaria and

Epicoccum purpurascens

Antibiosis and penetration

Rhizoctonia solani

and Fomes annosus

Trichoderma viride

Coiling, cytoplasm coagulation

Sclerotium rolfsii

T. harzianum

Coiling, penetration and

lysis

Nematophagy:

Heterodera

rostochiensis

Phialospora

heteroderae

Penetration of cysts

and egg killing

Mycophagy:

Cocchliobolus

sativus

Soil amoebae

Perforation in conidia

Gaeumannomyces

graminis var.

tritici

Soil amoebae

Penetration and lysis

of hyphae

Source : Various mycological/microbiological research and review papers.

 

Nematophagy

This is the phenomenon of eating upon nematodes by fungi. However, several nematode eating i.e. nematophagous fungi (NF) are known which develop different kinds of trap (T), arrest the pathogenic nematodes (N) and finally kill them (Fig. 13.4). Morphological and biochemical aspects of trap formation is discussed by Cook (1977). Examples of nematode trapping fungi are Arthrofyotrys, Dactylaria, Dactyleela, etc. Phialospora heteroderae penetrates the cysts and kills the eggs of Heterodera rostochiensis.

  Nematophagy : N, a nematode; NTF, a nematode trapping fungus; T, a ring like trap formed by NTF (diagrammatic).
 
Fig. 13.4.  Nematophagy : N, a nematode; NTF, a nematode trapping fungus; T, a ring like trap formed by NTF (diagrammatic).

Besides the fungi eating on nematodes, a spore forming bacterium, Bacillus penetrans kills the nematode and, therefore, is used for the control of Meloidogyne sp. B. penetrans is resistant to nematicides. Being an obligate parasite, this bacterium can not be grown in axenic culture. The bacterium shows host specificity and its spores survive for a long time. These spores adhere to the surface of infectious second-stage female larvae and eat on it. Adherance is followed by infection but it is not apparent until the adult stage comes (Kerr, 1982).

Mycophagy

Mycophagy is the phenomenon of feeding on fungi by amoebae. In recent years, mycophagy has become a new field of research as far as biocontrol of soil-borne plant pathogens is concerned. Many soil amoebae are known to feed on pathogenic fungi. For example, take-all disease of wheat caused by Gaeumannomyces graminis var. tritici was very severe in Australia. Finally it was found that some natural soil exhibited suppressiveness against this disease. Microbiological analysis of soils showed the presence of several amoebae in the soil. These amoebae played a significant role in take-all decline of wheat. The antagonistic soil amoebae e.g. Arachnula, Archelle, Gephyramoeba, Geococcus, Saccamoeba, Vampyrella, etc. (Old, 1977; Chakraborty et al, 1983) make perforation on the hyphal wall of Cochliobolus sativus, G. graminis var. tritici, Fusarium oxysporum and Phytophthora cinnamomi (Chakraborty and Warcup, 1982; Dwivedi, 1986) and on the conidial wall of C. sativus (Chakraborty and Old, 1983) and F. oxysporum (Pussard et. al. 1979), and develop round cysts on the lysed hyphae (Dwivedi, 1986).

  Mycophagy (A-C). Feeding of amoebae (a) upon fungal conidia (Ic) and fungal hypha (II h). A, attachment of amoeba; B, engulfment (I) and hole formation (II); C, digestion of conidium (I) (diagrammatic).
 
Fig. 13.5. Mycophagy (A-C). Feeding of amoebae (a) upon fungal conidia (Ic) and fungal hypha (II h). A, attachment of amoeba; B, engulfment (I) and hole formation (II); C, digestion of conidium (I) (diagrammatic).

 

Chakraborty et al. (1983) have described the following three major steps of feeding on fungal propagules by soil amoebae ( Fig. 13.5A-C ).

(i) Attachment: Attachment of trophozoites of amoebae (a) to fungal propagules i.e. conidia (c) or hyphae (h) appears to be a matter of chance. It takes place by chemotaxis or thigmotaxis (Fig. 13.5A).

(ii) Engulfment: Fungal propagules (e.g. spores, conidia, fragments of hyphae) are fully engulfed by amoebae (b). The small trophozoites attached the hyphal wall or spore and make perforations on it.

(iii) Digestion: The completely or partially engulfed propagules/cyloplasm of the host fungi are digested in a large central vacuole formed inside the cyst (Fig. 13.5C).

 

Based on pot-bioassay study, Dwivedi (1986) has suggested the biological control of take-all of wheat by using soil amoebae as a biocontrol agent.

 
     
 
 
     



     
 
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