Review The mechachanism and mode of action in microbial biocontrol agents against plant disease. Birhanu Gizaw* Microbial Biodiversity Directorate, Ethiopian Biodiversity Institute, P. O. Box 30726 Addis Ababa, Ethiopia. Abstract Pathogenic microorganisms are the main constraints affecting the production and productivity of crops both in terms of quality and quantity up to 20–40% yield loss. Existing plant disease management relies predominantly on toxic pesticides. Continuous use of chemicals for plant disease control will have adverse effect on the environmental, human and animal health, biodiversity loss. Researchers are focusing on potential biological control microbes as viable optional for the management of pests and plant pathogens.The purposeful utilization of living organisms whether introduced or indigenous, other than the disease resistant host plants, to suppress the activities or populations of one or more plant pathogens is referred to as bio control. Biological control involves the use of beneficial organisms, their genes, and/or products, such as metabolites, that reduce the negative effects of plant pathogens and promote positive responses by the plant. In this direction, a number of commercial products have been registered both at national and inter-national levels based on different fungal and bacterial antagonists.Understanding mode of action in microbial antagonistic activities are very impotant to screen and formulate new potential biocontrol agent. The modes of mechanism included direct inhibition of spore germination and mycelial growth, competition with pathogen for space and nutrients, bio lm fi formation, sidrophore production, induction of host resistance and iron depletion, where the iron, methionine competition was considered as the key action. 0
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Review
The mechachanism and mode of action in microbial biocontrol agents against plant disease.
Birhanu Gizaw*
Microbial Biodiversity Directorate, Ethiopian Biodiversity Institute, P. O. Box 30726 Addis Ababa, Ethiopia.
Abstract
Pathogenic microorganisms are the main constraints affecting the production and productivity of crops both in terms of quality and quantity up to 20–40% yield loss. Existing plant disease management relies predominantly on toxic pesticides. Continuous use of chemicals for plant disease control will have adverse effect on the environmental, human and animal health, biodiversity loss. Researchers are focusing on potential biological control microbes as viable optional for the management of pests and plant pathogens.The purposeful utilization of living organisms whether introduced or indigenous, other than the disease resistant host plants, to suppress the activities or populations of one or more plant pathogens is referred to as bio control. Biological control involves the use of beneficial organisms, their genes, and/or products, such as metabolites, that reduce the negative effects of plant pathogens and promote positive responses by the plant. In this direction, a number of commercial products have been registered both at national and inter-national levels based on different fungal and bacterial antagonists.Understanding mode of action in microbial antagonistic activities are very impotant to screen and formulate new potential biocontrol agent. The modes of mechanism included direct inhibition of spore germination and mycelial growth, competition with pathogen for space and nutrients, biofilm formation, sidrophore production, induction of host resistance and iron depletion, where the iron, methionine competition was considered as the key action.
parasitism (Price, 1977), and predation (Price et al., 1980, Pal, 2006). Pathogen populations thus can be
limited by antagonistic microorganisms in very different ways. The nature of the mode(s) of action does
not only determine how a pathogen population is affected by the antagonist. Also the characteristics of the
microbial biocontrol agent depend on the exploited mode of action. Possible risks for humans or the
environment, risks for resistance development against the biocontrol agent, its pathogen specificity and its
dependency on environmental conditions and crop physiology may differ between different modes of
action. Preferences for certain modes of action for an envisaged application of a biocontrol agent will also
have impact on the screening methods used to select new antagonists (Köhl et al.,2011). The objective of
this paper is to review the modes of action and antagonisms in biocontrol microorganisms for disease
management.
2.Direct antagonism
2.1. Mycoparasitism / Hyperparasitism
Hyper-parasitism is the most considered and the most direct form of antagonism (Pal et al., 2006). This
kind of interaction is often observed between fungi. For bacteria, hyperparasitism rarely has been
reported. Bdellovibrio bacteriovorus is a predatory bacterium which has the unusual property to use
cytoplasm of other Gram-negative bacteria as nutrients (McNeely et al.,2017). Hyperparasites invade and
kill mycelium, spores, and resting structures of fungal pathogens and cells of bacterial pathogens
(Ghorbanpour et al.,2018). There are four major classes of hyperparasites: obligate bacterial pathogens,
hypoviruses, facultative parasites, and predators. (Tjamos et al., 2010). Hyper-parasitism involves tropic
growth of bio control agent towards the target organism, coiling, final attack and dissolution of target
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pathogens cell wall or membrane by the activity of enzymes (Tewari, 1996). The ability of any fungi to
attack the other fungal species and utilizing their nutrients is called Mycoparasitism (Atanasova et
al.,2013). It is a complex mechanism that generally involves the production of a cell wall lytic enzyme
that degrades the pathogen fungus cells wall such as cellulases, chitinases, β-1,3-glucanases, proteinases,
lipases and in case of hyperparasites of oomycota, cellulase. (Rabea et al., 2003, Horbach et al., 2011). It
is one of the main mechanisms involved in Trichoderma (Sharma, 1996). Trichoderma harzianum
exhibits excellent mycoparasitic activity against Rhizoctonia solsni hyphae (Altomare et al., 1999). The
ATP (adenosine triphosphate)-binding cassette (ABC) transporter proteins of Trichoderma work both in
the process of nutrient uptake and myco- parasitism also (Locher, 2004). Other mechanisms of parasitism
are associated with fungi such as Verticillium chlamydosporium and Paecilomyces lilacinus, which can
infect the egg masses and cysts of the cereal cyst and root knot nematodes. For example, oospores of
Phytophthora and Pythium spp. are frequently found to be infected by Olpidiopsis gracilis, whilst
sclerotia of R. solani are infected by the obligate sclerotial mycoparasite Verticillium biguttatum.(
Pankhurst et al.,2005). Generally mycoparasitism can be described in four sequential steps (Chet, 1987):
The first stage is chemotropic growth. The biocontrol fungi grow tropistically toward the target fungi that
produce chemical stimuli, a volatile or water- soluble substance produced by the host fungus serves as a
chemo attractant for parasites. The next step is recognition. Lectins of hosts(pathogens) and carbohydrate
receptors on the surface of the biocontrol fungus may be involved in this specific interaction. The third
step is attachment and cell wall degradation. Mycoparasites can usually either coil around host hyphae or
grow alongside it and produce cell wall degrading enzymes such as chitinases and b-1,3-glucanase to
attack the target fungus, The final step is penetration. The biocontrol agent produces appressoria-like
structures to penetrate the target fungus cell wall, and kill their hosts by cell wall degrading enzymes,
often in combination with antimicrobial secondary metabolites (Chet, 1987, Chet et al., 1998, Inbar and
Chet 1994, Di Pietro, et al, 1992, Harman et al.,2004). There are several fungal parasites of plant
pathogens, including those that attack sclerotia (i.e. Coniothyrium minitans) while others attack living
hyphae (i.e. Pythium oligandrum) and, a single fungal pathogen can be attacked by multiple
hyperparasites. For example, Acremonium alternatum, Acrodontium crateriforme, Ampelomyces
quisqualis, Cladosporium oxysporum, and Gliocladium virens are just a few of the fungi that have the
capacity to parasitize powdery mildew pathogens (Heydari and Pessarakli, 2010). There are 30
hyperparasitic species against Rhizoctonia solani belonging to 16 genera have been reported
byJeffries(1995). Approximately 30 fungal species which show hyperparasitism against rust pathogens,
including Cladosporium uredinicola against Puccinia violae (Traquair et al.,1984) and Alternaria
alternata against Puccinia striiformis f. sp. tritici (Zheng et al.,2017). The most studied mycoparasites are
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belonging to the genera Trichoderma and Clonostachys Other hyperparasites attack plant-pathogenic
nematodes during different stages of their life cycles (i.e. Paecilomyces lilacinus and Dactylella
oviparasitica). The molecular level induction of mycoparasitism was first reported in 1994 (Carsolio et
al., 1999), based on the study of regulation of an endochitinase-encoding gene (ech42). Ech42 was
expressed during the mycoparasitic interaction between T. harzianum and Rhizoctonia solani. Another
study showed that in the P1 mutant strain of T. atroviride, the expression of exochitinase nagI or
endochitinase ech42 gene was needed to induce mycoparasitism in treatments containing purified
colloidal chitin from the fungal cell walls (Vinale et al., 2008). Production and regulation of lytic enzymes
such as chitinases, glucanases, and proteases by Trichoderma spp also play key roles in the
mycoparasitism/biocontrol process (Mukherjee et al., 2008). In high glucose conditions, glucose is
metabolised preferentially through the repression of genes required for utilization of other carbon sources.
Analysis of the promoter sequence of mycoparasitism-related genes showed that control by carbon
catabolite repression occurred through binding of the CRE1 protein (Cortés et al. 1998; Kubicek &
Penttilä 1998; Mach et al. 1999; de las Mercedes et al. 2001; Donzelli et al. 2001). A Trichoderma
catabolite repressor gene (cre1) was cloned from Trichoderma spp. and molecular studies confirmed its
role in catabolite repression of the mycoparasitism-related gene ech42 (Ilmén et al. 1996; Lorito et al.
1996; Cziferszky et al. 2002). Nitrogen catabolite repression is another regulatory mechanism by which
genes required for utilisation of poor nitrogen sources are repressed in the presence of primary nitrogen
sources such as glutamine or ammonia. In T. atroviride, the response of the protein aseprb1 is also
controlled by nitrogen catabolite repression (Olmedo-Monfil et al. 2002). Repression is thought to be
mediated through interaction of regulatory proteins with GATA motifs within the promoter region has
been identified in other mycoparasitic genes from T. atroviride, T. harzianum, and T. hamatum (Cortés et
al. 1998; Donzelli et al. 2001; Steyaert 2002), Promoter analysis of a chitinase gene (ech42) and
proteinase gene (prb1) implicated in mycoparasitism has led to the prediction of a global induction
pathway for mycoparasitism-related genes (Cortés et al. 1998). The molecular level induction of
mycoparasitism was first reported in 1994 (Carsolio et al., 1999), based on the study of regulation of an
endochitinase-encoding gene (ech42). Generally In hyperparasitism, the pathogen is directly attacked by a
specific BCA that kills it or it spropagules. Where as in mycoparasitism, two mechanisms operate among
involved species of fungi. This may be hyphal of interfungus interaction i.e., fungus-fungus interaction,
several events take place which lead to predation viz., coiling, penetration, branching and sporulation,
resting body production, barrier formation and lyses. The bio-nematicide Bacillus firmusalso colonizes the
rhizosphere of the plant where it parasitizes the eggs and larvae of nematodes especially of the
rootknotnematodes.
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Mycoprasitic coiling of Trichoderma atrovide around Botrytus cinerea hyphae.Arrow indicate site of penetration
3.Indirect Antagonism
3.1. Competition for nutrion and space
Competition is diffcult to study mechanistically: it is likely more important in natural environments,
where resources are limited and competitors plentiful. In community ecology, niche and nutrient
competition have been intensely studied as determinants of species diversity. Germination and growth of
plant pathogens depend on nutrient uptake. From the microbial perspective, soils and living plant surfaces
are frequently nutrient limited environment. So to colonize the phytosphere, a microbe must effectively
compete for the available nutrients (Pal et al., 2006). Both the biocontrol agents and the pathogens
compete with one another for the nutrients and space to get established in the environment. This process
of competition is considered to be an indirect interaction between the pathogen and the biocontrol agent
whereby the pathogens are excluded by the depletion of food base and by physical occupation of site
(Lorito et al., 1994). Competition for carbohydrates in the carbohydrate rich wound environment in yeast
seen and competition for the limited amounts of nitrogen sources such as amino acids play the key roles
in the antagonistic interactions . Yeast can consume a broad range of carbohydrates such as disaccharides
and monosaccharides but also various nitrogen sources (Spadaro et al.,2010). Spadaro and Droby (2016)
reviewed competition processes between antagonistic Pichia guilliermondii and pathogenic Penicillium
digitatum, P. expansum, B. cinerea, or Colletotrichum spp. in wounds of different fruits and
Aureobasidium pullulans and P. expansum in apple wounds.The competition for nutrients is concerned
biocontrol agents compete for the rare but essential micronutrients, such as iron and manganese especially
in highly oxidized and aerated soils. In these soils iron is present in ferric form, which is insoluble in
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water and where the concentration may be as low as 10 -8 M, too low to sport the microbial growth
(Lindsay, 1979). Iron is required in several metabolic processes including tricarboxylic acid cycle,
electron transport chain, oxidative phosphorylation, and photosynthesis (Messenger and Barclay 1983;
Fardeau et al. 2011). It also regulates the biosynthesis of porphyrins, vitamins, antibiotics, toxins,
cytochromes,siderophores, pigments, and aromatic compounds, and nucleicacid synthesis (Messenger and
Barclay 1983). Recently it has also been observed that iron plays an important role in the microbial
biofilm formation as it regulates the surface motility of microorganism (Glick et al. 2010; Cai et al. 2010).
Competition for micro nutrients exists because biocontrol agents have more efficient utilizing uptake
system for the substances than the pathogens (Nelson, 1990). This property can be attributed to the
production of iron binding ligands called siderophores as in Erwinia caratovora (Kloepper et al. 1980).
Siderophores are low molecular-weight chelating agents with a high affinity for ferric iron. Siderophores
are produced by microorganisms under restricted iron conditions (Haas, 2014). (Fig2). Till to date more
than 500 different siderophores were reported, of which 270 were well characterized (Boukhalfa et al.
2003), while the rest remain uncharacterized and their functions are yet to be determined (Ali and Vidhale
2013). Siderophores exhibiting novel structures with two types of ligands and modified aminoacids, not
found elsewhere in nature with variation from one species to another. They exhibit requisite (I)
hydrophilic properties for chelating iron in extracellular aqueous environment (II) lipophilic properties for
entering through the lipoprotenaceous membrane receptors of the cell and (III) hydro-lipo-phile properties
depending upon the aqueous or fatty environment under which they are destined to function. Depending
on the oxygen ligands for Fe (III) coordination, siderophores can be classified into three main categories,
namely (1) hydroxamate(C=O, N-(OH &aminoacids) and (2) catecholates(derivates if 2-3 dihydroxy
benzoic acid) groups and carboxylates, (Ali & Vidhale 2013, Winkelmann and Drechsel (1997) have
classified bacterial siderophores in to 5 types namely (i)catecholate (ii) hydroxamates (iii) peptide
siderophores (iv)mycobactin and related siderophores (v) citrate hydroxamate siderophores. Table 1.
Fungal siderophores have been classified into five families (i) ferrichromes (ii) coprogens (iii)
rhodotoluric acid (iv) fusarinines (v) rhizoferrins.The majority of fungal siderophores belong to the
hydroxamate class. Exceptions are the carboxylate-type siderophore rhizzoferrin produced by various
Mucorales and the catecholate pistillarin produced by the marine species Penicillium bilaii .(Thieken et
al., 1992, Capon et al., 2007), whiles prokaryotic organisms produce both hydroxamates and
catecholates. Many siderophores produced by bacteria and fungi are strong enough to remove iron from
host-binding proteins. In case of gram-negative bacterial membranes, an outer membrane receptor, a
periplasmic binding protein, and a cytoplasmic membrane protein belonging to ATP-binding cassette
transporter (ABC-transporter) are involved in the transport of siderophore iron (Fe (Ahmed and 7
Holmstrom 2014). Once siderophores bound to ferric iron moves to cytosol, the ferric iron gets reduced to
ferrous form and the ferrous form of iron becomes free from the siderophores. After release of iron,
siderophores either get degraded or recycled by excretion through efflux pump system. For example, A.
fumigatus secretes two main hydroxamate siderophores, triacetylfusarinine C and fusarinine C, which
have higher affinity for iron than transferrin and are capable of obtaining iron directly from the protein
(Hissen etal., 2004).Siderophores chealate the Fe (II) ions and the membrane bind protein receptors
specifically recognize and take up the Siderophore-Fe-complex (Mukhopadhyay and Mukherjee, 1998).
This results in making iron unavailable to the pathogen, which produce less siderophores with lower
binding power. The result is less pathogen infection and biological control. Iron competition is the mode
of action of several fungal antagonists. For example, Trichoderma asperellum producing iron-binding
siderophores controls Fusarium wilt (Segarra et al.,2010). P. putida produce the pseudofactin siderophore
that have ability to abolish the Fusarium oxysporum and Rhizoctonia solani from rhizosphere by lowering
iron availability in soil (Beneduzi et al., 2012). The yeast Metschnikowia pulcherrima transforms
pulcherriminic acid and iron ions to the red pigment pulcherrimin. This process leads to iron depletion in
media inhibiting development of B. cinerea, A. alternata, and P. expansum (Saravanakumar et al.,2008).
Recently, it was shown that Saccharomycopsis schoenii lacks several components of the sulfur
assimilation pathway and thus likely acquires methionine from its prey (Junker et al. 2019). Among
yeasts, the inability to take up sulfur is specifc to Saccharomycopsis, but some plant pathogenic fungi and
Trichoderma species show a similar phenomenon, which may indicate that methionine is an important
target for such organisms and highly competed over (Junker et al.2019).
Type of siderophore Class
1 Caecholate Enterobacterine
2 Hydroxamate Aferrioxamines
Ferrichrom
Aerobacline
3 Carboxylate Rhizoferrin
4 Mixed Lysine derivatives Myobactine
Ornithine derivatives pyoverdine
Histamine derivatives Anguibctine
Table .1. Sidrophore class
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Fig.2. Sidrophor Iron chelation
Biofilm formation may also be considered a specific and highly successful strategy to compete for space.
Bioflms are microbial communities that live and grow on surfaces and can be comprised of a single
species or represent multi-species consortia (Costa-Orlandi et al. 2017). A biofilm comprises any
syntrophic consortium of microorganisms in which cells stick to each other and often also to a
surface.These adherent cells become embedded within a slimy extracellular matrix that is composed of
extracellular polymeric substances (EPS).The cells within the biofilm produce the EPS components,
which are typically a polymeric conglomeration of extracellular polysaccharides, proteins, lipids and
DNA. Because they have three-dimensional structure and represent a community lifestyle for
microorganisms, they have been metaphorically described as "cities for microbes".(Hall-Stoodley et
al.,2004, .Aggarwal et al.,2016, Watnick et al.,2005, López et al.,2010). Microbes form a biofilm in
response to various different factors, which may include cellular recognition of specific or non-specific
attachment sites on a surface, nutritional cues, or in some cases, by exposure of planktonic cells to sub-
inhibitory concentrations of antibiotics. A cell that switches to the biofilm mode of growth undergoes
a phenotypic shift in behavior in which large suites of genes are differentially regulated. A biofilm may
also be considered a hydrogel, which is a complex polymer that contains many times its dry weight in
water. Biofilms are not just bacterial slime layers but biological systems; the bacteria organize themselves
into a coordinated functional community. (O'Toole et al.,1998, Karatan et al., 2009, Hoffman et al.,2005,
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An D, Parsek ,2007). The formation of a biofilm begins with the attachment of free-floating
microorganisms to a surface. The first colonist bacteria or yeast of a biofilm may adhere to the surface
initially by the weak van der Waals forces and hydrophobic effects they can anchor themselves more
permanently using cell adhesion structures such as pili. During surface colonization bacteria cells are able
to communicate using quorum sensing (QS) products such as N-acyl homoserine lactone (AHL). Once
colonization has begun, the biofilm grows by a combination of cell division and recruitment.
Polysaccharide matrices typically enclose bacterial biofilms. In addition to the polysaccharides, these
matrices may also contain material from the surrounding environment, including but not limited to
minerals, soil particles, and blood components, such as erythrocytes and fibrinThe final stage of biofilm
formation is known as dispersion, and is the stage in which the biofilm is established and may only
change in shape and size.The development of a biofilm may allow for an aggregate cell colony (or
colonies) to be increasingly resistant to antibiotics. Cell-cell communication or quorum sensing has been
shown to be involved in the formation of biofilm in several bacterial species. The process of biofilm
development is summarized by five major stages of biofilm development , Initial attachment, Irreversible
attachment, Maturation I, Maturation II, Dispersion (O'Toole et al., 1998, Briandet et al.,2001, Takahashi
et al.,2010, Donlan 2002, Watnick, etal., 2000)
In biocontrol yeasts, bioflm formation, mainly in the phyllo- and carposphere (i.e., in wounds), is now
considered an important mode of action and has been widely studied. Besides P. fermentans,bioflm
formation has also been implicated in the protective and biocontrol activities of A. pullulans, Kloeckera
apiculata, S. cerevisiae, Pichia kudriavzevii, W. anomalus, and M. pulcherrima (Chi et al. 2015; Klein
and Kupper 2018; Ortu et al. 2005; Pu et al. 2014; Wachowska et al. 2016). In a S. cerevisiae for strain,
bioflm cells were far more effcient than planktonic cells in colonising the inner surface of apple wounds,
thereby controlling the development of blue mould caused by P. expansum (Ortu et al. 2005; Scherm et al.
2003)(Fig.3).
Fig3.Colonisation a of the inner surface of an apple wound by the Saccharomyceslcerevisiael or strain M25.
10
b Penicillliumlexpansum germ tubes grow onto the yeast cells, but contact with the apple tissue is prevented by a thick yeast cell layer. The presence of an extracellular matrix is likely to assure an elective protection of the apple tissue (Ortu et al. unpublished)
3.2. Induction of host resistance
Plants actively respond to a variety of environmental stimuli, including gravity, light, temperature,
physical stress, water and nutrient availability. Plants also respond to a variety of chemical stimuli
produced by soil- and plant-associated microbes. Such stimuli can either induce or condition plant host
defenses through biochemical changes that enhance resistance against subsequent infection by a variety of
pathogens. Induction of host defenses can be local and/or systemic in nature, depending on the type,
source, and amount of stimuli. Plants are central players in a complex food web in which numerous
members profusely take advantage of the plant’s resources. Besides microbial pathogens and insect
herbivores, plants also nurture a vast community of commensal and mutualistic microbes that provide the
plant with essential services, such as enhanced mineral uptake, nitrogen fixation, growth promotion, and
protection from pathogens(Shoresh et al.,2010). These plant microbiota are predominantly hosted by the
root system, which deposits up to 40% of the plant’s photosynthetically fixed carbon into the rhizosphere,
rendering this small zone around the roots one of the most energy-rich habitats on Earth (Bais 2006).
Several genera of the rhizosphere microbiota, which are referred to as plant growth–promoting
rhizobacteria (PGPR) and fungi (PGPF), can enhance plant growth and improve health (Lugtenberg
2009, Shoresh et al.,2010). Evidence showed PGPR strains can promote plant health through stimulation
of the plant immune system (Alstrom, 1991 Van Peer 1991). The term induced resistance is a generic
term for the induced state of resistance in plants triggered by biological or chemical inducers, which
protects nonexposed plant parts against future attack by pathogenic microbes and herbivorous insects
(Kuc, 1982) Generally, induced resistance confers an enhanced level of protection against a broad
spectrum of attackers (Walters 2013). In the 1960s, Ross coined the term SAR for the phenomenon in
which uninfected systemic plant parts become more resistant in response to a localized infection
elsewhere in the plant (Ross, 1961). There are different Systemic Acquired Resistance like Pathogen-
PCA, PCN, and hydroxyphenazines) andphenylpyrrole antibiotic (pyrrolnitrin) (de Souza et al. 2003,
Ahmad et al. 2008). Hydrogen cynid (HCN) effectively blocks the cytochrome oxidase pathways and is
highely toxic to all aerobic microorganism at picomolar concentration(Ramett et al., 2003).Supression of
black rot tobacco caused by Thielaviopsis basicola caused to be due to hydrogen cynid production(Howell
et al., 1988). In response to stressful conditions, bacteria secrete several types of antibiotics with varying
specificity and modes of action (Glick, 2012). Antibiotics produced by PGPR include kanosamine, 2,4-
diacetylphloroglucinol (2, 4-DAPG), Martínez-Viveros oligomycin A, butyrolactones,xanthobaccin
phenazine-1-carboxylic acid, pyrrolnitrin, zwittermycin A, viscosinamide (Viveros et al.,2010). The
bacterial strain of P. fluorescens BL915 involve in the production of antibiotic known as pyrrolnitrin have
ability to inhibit deterioration of Rhizoctonia solani. 2,4-DAPG is an extensively studied antibiotic
involved in the membrane destructionof Pythium spp.(De Souza et al.,2003). Pseudomonas spp. also
synthesizes phenazine that contains the antagonistic activity against Fusarium oxysporum (Beneduzi et
al.,2012). In Pseudomonas many antibiotic metabolites such as pyrrolnitrin have been studied
(Raaijmakers and Mazzola,2012). Many Bacillus ssp. Produced antibiotics like circulin, polymyxin and
colistin that are actively involved in the growth inhibition of pathogenic fungi as well as Gram-negative
13
and Gram-positive bacteria. In Bacillus, especially lipopeptides such as iturin, surfactin, and fengycin
have been investigated (Ongena and Jacques,2008).(Table.2) Six classes of antibiotic compoundsnamely
phenazines, phloroglucinols, pyoluteorin, pyrrolnitrin,cyclic lipopeptides (diffusible compounds) and
hydrogen cyanide(HCN; volatile compound) are better correlated with the biocontrol of root diseases
(Haas and Defago, 2005; Beneduzi and Ambrosini,Passaglia, 2012). Two antibiotics namely
biosurfactants and lipopeptide have gained attention due to their biocontrol potential againstwide-
spectrum phytopathogens including bacteria, fungi, oomycetes,protozoa, nematodes and plants (Al-Ajlani
et al., 2007; de Bruijn et al.,2007; Raaijmakers et al., 2010). Huge numbers of known antibiotics are
produced by actinomycetes (8700 different antibiotics), bacteria (2900) and fungi (4900) (Bérdy,2005).
Production of antimicrobial metabolites, mostly with broad-spectrum activity, has been reported for
biocontrol bacteria belonging to Agrobacterium, Bacillus, Pantoea, Pseudomonas, Serratia,
Stenotrophomonas, Streptomyces, and many other genera. Bacillus produces twelve major antibiotics
including bacillomicin, mycobacillin, fungistatin, iturin, fengycin, plipastatin, surfactin, bacilysin, etc.
(Stien, 2005; Al-Ajlani et al., 2007) whereas Pseudomonas spp. produce only six antibiotics
(Shanmugaiah et al., 2010). More recently, Pseudomonas putida WCS358r strains genetically engineered
to produce phenazine and DAPG displayed improved capacities to suppress plant diseases in field-grown
wheat (Glandorf et al. 2001). Also fungal antagonists can produce antimicrobial compounds. For
Trichoderma and closely related Clonostachys (former Gliocladium), 6-PAP, gliovirin, gliotoxin, viridin
and many more compounds with antimicrobial activity have been investigated (Ghorbanpour et al.,2018).
Antibiotics at low concentrations can be involved in signaling and microbial community interactions,
communication with plants, and regulation of biofilm formation. Raaijmakers and Mazzola(2012). A
wide range of functions of antimicrobial metabolites at low concentrations: there is evidence that
antimicrobials including lipopetides protect bacteria from grazing by bacteriovorus nematodes such as
Caenorhabditis elegans. Also volatile antibiotic compounds may play a role in long-distance interactions
amongst soil organisms including bacterial predators. Lipopeptides of Bacillus and Pseudomonas are
involved in the surface attachment of bacterial cells and biofilm formation by activating signaling
cascades finally resulting in the formation of extracellular matrices which protect microorganisms from
adverse environmental stresses. Several biocontrol strains are known to produce multiple antibiotics
which can suppress one or more pathogens. For example, Bacillus cereus strain UW85 is known to
produce both zwittermycin (Silo-Suh et al. 1994) and kanosamine (Milner et al. 1996). The ability to
produce multiple antibiotics probably helps to suppress diverse microbial competitors, some of which are
likely to be plant pathogens. The ability to produce multiple classes of antibiotics, that differentially
inhibit different pathogens, is likely to enhance biological control. More recently, Microbial genome
14
analysis revealed huge numbers of cryptic antibiotic gene clusters encoding still unknown antibiotics.
Antibiotics mode of action has different mechanism , The antimicrobial potency of most classes of
antibiotic are directed at some unique feature of the bacterial, structure or their metabolic processes. The
most common targets of antibiotics. The mechanism of antibiotic actions are as follows: (Talaro and
Chess, 2008; Madigan and Martinko, 2006; Wright, 2010)
Inhibition of cell wall synthesis Breakdown of cell membrane structure or function Inhibition of the structure and function of nucleic acids Inhibition of protein synthesis Blockage of key metabolic pathwaysAntibiotics play an important role in disease management, used as biocontrol agent and faced
challenge due to limitations because antibiotics are prepared under natural circumstances. Ecological
and other components that effect the antimicrobial action of antibiotics were examined to utilize the
potential of antibiotics that are produced by PGPR in crop protection.
Some of antibiotics produced by BCAs
Antibiotic Source Target pathogen Disease Reference2, 4-diacetyl-phloroglucinol Pseudomonas fluorescens F113 Pythium spp. Damping off Shanahan et al. (1992)
Agrocin 84 Agrobacterium radiobacter Agrobacterium tumefaciens Crown gall Kerr (1980)Bacillomycin D Bacillus subtilis AU195 Aspergillus flavus Aflatoxin contamination Moyne et al. (2001)
Xanthobaccin A Lysobacter sp. strain SB-K88 Aphanomycescochlioides
Damping off Islam et al. (2005)
Gliotoxin Trichodermavirens
Rhizoctonia solani Root rots Wilhite et al. (2001)
Herbicolin Pantoea agglomerans C9-1 Erwinia amylovora Fire blight Sandra et al. (2001)Iturin A B. subtilis QST713 Botrytis cinerea and R. solani Damping off Paulitz and Belanger (2001),
Kloepper et al. (2004)
Mycosubtilin B. subtilis BBG100 Pythiumaphanidermatum
Damping off Leclere et al. (2005)
Phenazines P. fluorescens 2-79 and 30-84 Gaeumannomyces graminis var. tritici
Take-all Thomashow et al. (1990)
Pyoluteorin, pyrrolnitrin
P. fluorescens Pf-5 Pythium ultimum and R. solani Damping off Howell and Stipanovic (1980)
Pyrrolnitrin, pseudane
Burkholderia cepacia R. solani and Pyricularia oryzae Damping off and rice blast
Homma et al. (1989)
Zwittermicin A Bacillus cereus UW85 Phytophthora medicaginis and P. aphanidermatum
Damping off Smith et al. (1993)
Table. 2
15
4.2.Hydrogen cyanide (HCN) production
Considerable numbers of free-living rhizospheric bacterial communities, mainly Pseudomonas sp.
(Ahmad et al., 2008; Muleta et al., 2007), are capable of generating HCN by oxidative decarboxylation
from direct precursors such as glycine, glutamate, or methionine. Other rhizobacterial genera reported to
produce HCN include Bacillus (Ahmad et al., 2008) and Chromobacterium (Muleta et al., 2007). HCN
secreted by Pseudomonas fluorescent strain CHAO has been demonstrated to stimulate root
hairvormation and suppress back root rot caused by Thielaviopsis basicola in tobacco plant (Voisard et
al., 1989). Cyanogenesis in bacteria accounts in part for the biocontrol capacity of the strains that suppress
fungal diseases of some economically important plants (Voisard et al., 1989).
4.3.Production of lytic enzymes
Extracellular hydrolytic enzymes such as chitinases, glucanases, proteases and lipases, achieve disease
suppression through lysis of pathogenic fungal cell walls (Maksimov et al., 2011). Except oomycetes, cell
walls of most phytopathogenic fungi are made up of chitin (C8H13O5N), an unbranched, longchain
polymer of glucose derivatives, composed of ß-1,4-linked units of the amino sugar N-acetyl D-
glucosamine (NAG) (Shaikh and Sayyed, 2015). Chitinase activity of PGPR has been well explored for
suppression of fungal phytopathogens (Kim et al., 2008). The role of lytic enzymes such as chitinase and
ß-1,3-glucanase in suppression of anthracnose pathogen Colletotrichum gloeosporioides Penz. have been
established (Vivekananthan et al., 2004) Pseudomonas stutzeri produces extracellular chitinase and ß-1,3-
glucanase, which lyse the pathogen Fusarium sp.. Cladosporium werneckii and B. cepacia can hydrolyze
fusaric acid (produced byFusarium), (Compant et al., 2010).Furthermore, chitinase produced by Serratia
plymuthica C48 was found to inhibit spore germination and germ tube elongation in Botrytis cinerea
(Frankowski et al., 2001). Lysis of fungal cell walls is a direct method of pathogen inhibition which
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