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.
Key word;-Biocontrol, biofilm, competation, Methionin, spore, Sidrophore
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1.Introduction
It is a persistent issue worldwide that an enormous number of plant pathogens varying from the smallest
viroid to more complex pathogens such as 700 viruses, 2000bacteria, 10000 fungi spp., oomycetes and
nematodes species cause many important plant diseases and are responsible for major crop losses at least
20–40% yield(Savary etal.,2012). Recently new fungal and fungal-like plant pathogen occurance have
increased by more than 7 fold since 2000 (Fisher et al.,2012). Every year plant diseases cause an
estimated 40 billion dollars losses worldwide either directly or indirectly (Roberts et al.,2006). To address
food security agricultural yields must increase to match the growing human population in the near future.
There is now a strong push to develop low-input and more sustainable agricultural practices that optional
alternatives to chemicals for controlling pests and diseases, a major factor of heavy losses in agricultural
production. Based on the adverse effects of some chemicals on human health, the environment and living
organisms researchers are focusing on potential biological control microbes as viable optional for the
management of pests and plant pathogens (Sharifah Farhana te al.,2018). The terms “biological control”
and its abbreviated synonym “biocontrol” have been used in different fields of biology most notably
entomology and plant pathology. In entomology, it has been used to describe the use of live predatory
insects, entomopathogenic nematodes, or microbial pathogens to suppress populations of different pest
insects. In plant pathology, the term applies to the use of microbial antagonists to suppress diseases as
well as the use of host specific pathogens to control weed populations . In both fields, the organism that
suppresses the pest or pathogen is referred to as the biological control agent(BCA). DeBach (1964)
defined biological control as "the action of parasites, predators, or pathogens in maintaining another
organism's population density at a longer average than would occur in their absence." Smith (1919) first
used term "biological control" to signify the use of natural enemies whether introduced or otherwise
manipulated to control insect pests. DeBach (1964) further refined the term and distinguished "natural
control" from "biological control" National Research Council took into account modern biotechnological
developments and referred to biological control as “the use of natural or modified organisms, genes, or
gene products, to reduce the effects of undesirable organisms and to favor desirable organisms such as
crops, beneficial insects, and microorganisms”, but this definition spurred much subsequent debate and it
was frequently considered too broad by many scientists who worked in the field (US Congress, 1995).
The history of Biological Control may be divided into 3 periods: 1. The preliminary efforts when living
agents were released rather haphazardly with no scientific approach. Little precise information exists on
successes during this time. Roughly 200 A.D. to 1887 A.D., 2. The intermediate period of more
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discrimminating biocontrol which started with the introduction of the Vedalia beetle, Rodolia cardinalis
Mulsant, for control of the cottony cushion scale in 1888. Period extended from 1888to ca. 1955; and 3.
The modern period characterized by more careful planning and more precise evaluation of natural
enemies. Period from 1956 to the present. Biological control was discovered by trial and error and then
practiced in agriculture long before the term itself came into use (Baker and Cook, 1974). The era of
modern biological control, involving the deliberate transfer and introduction of natural enemies of insect
pests, was launched 100 years ago with the highly successful introduction of the vadalia beetle from
Australia to California in 1888 to control the cottony cushion scale of citrus. the German plant pathologist
C. F. von Tubuef wrote a somewhat speculative article entitled "Biologische Bekampfung von
Pilzkrankheiten der Pflanzen." This is apparently the first reference in the scientific literature to the term
"Biologische Bekampfung" or "biological control" (Baker, 1987). More broadly, the term biological
control also has been applied to the use of the natural products extracted or fermented from various
sources. These formulations may be very simple mixtures of natural ingredients with specific activities or
complex mixtures with multiple effects on the host as well as the target pest or pathogen. biocontrol differ
depending on the target of suppression; number, type and source of biological agents; and the degree and
timing of human intervention. Most broadly, biological control is the suppression of damaging activities
of one organism by one or more other organisms, often referred to as natural enemies. There is increasing
evidence that biological control occurs naturally on plant surfaces (e.g. in the rhizosphere, phylloplane
and fruit surfaces) by the activity of epiphytic microflora. The most convincing indirect evidence for this
control comes from examples where the use of an agricultural chemical to control a particular leaf disease
results in the occurrence of another disease problem previously regarded as unimportant. The increasing
use of chemicals as pesticides to eliminate Plant pathogen has provided effective solutions in agriculture.
However, due to the fact that the excessive use of these chemicals such as thiabendazole and o-
phenylphenol causes environmental pollution, and as plant pathogenic agents are quickly become resistant
to chemical pesticides The one of the major disadvantage of chemical pesticides is that many of them are
not able to breakdown into simple and safer constituents and remained intact over a long timeperiod
polluting soil environmental(Gilden 2010). Synthetic pesticides are also non-targeted in nature as they
affect the broad spectrum of microbe including plant beneicial microbe and the whole biodiversity
loss.Considering the high price of pesticides and their accumulation in plants or soil which has harmful
effects on humans, extensive researches are being conducted in the world to replace this method with
more recent methods to confront fungicidal resistant pathogens. Since the late 1900s, scientists have made
great efforts to use natural antagonisms of terricolous microorganisms to protect plants. Biological control
depends on knowledge of biological interactions at the ecosystem, organism, cellular, and molecular
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levels and often is more complicated to manage compared with physical and chemical methods. (Baker
and Cook, 1974). Recently, the use of biological control agents, especially bacteria has attracted a lot of
attention due to the ability of some species to suppress different plant diseases and the possibility of
combining with other control methods (Arrebola et al.,2010 ). Therefore, various sources of antibiotic
production are screened, among which bacillus especially is an important alternative to extract antibiotics
and their industrial production. One reason for its growing popularity is its record of safety during the past
100 years considered as the era of modem biological control (Waage and Greathead, 1988). For the
management of plant diseases, including plant parasitic nematodes (Cook et al.,1983). All biological
control interactions between plants and microbes occur naturally at a macroscopic and microscopic level
in the form of mutualism (Bronstien, 1994) protocooperation (James etal.,1995), commensalism(Yoon et
al.,1977]), neutralism (Halimann 2001), competition (TrenbathB,1976), amensalism (Arthur 1989),
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.
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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-
Induced Systemic Acquired Resistance Signaling, Herbivore-Induced Resistance Signaling, hormonal
regulation of induced systemic resistance by beneficial microbes. Using Microbial Biocontrol agents
(MBCAs) for disease control through induction of resistance or priming relies on a complex sequence of
events where the MBCA initially has to establish on the host, followed by the release of specific inducers
which are recognized by specific receptors by the plant and there after triggering pathways within the host
plant resulting in the onset of defense reactions or priming to make the plant ready for later challenges by 11
pathogens. The first part of this sequence of events depends on the MBCA, the second part on the genetics
and physiological status of the plant. (Romanazzi et al.,2016). In the current concept of the plant immune
system, pattern-recognition receptors (PRRs) have evolved to recognize common microbial compounds,
such as bacterial flagellin or fungal chitin, called pathogen- or microbe-associated molecular patterns
(PAMPs or MAMPs) (Boller et al ,2009, Zipfel, 2009). Plants also respond to endogenous plant-derived
signals that arise from damage caused by enemy invasion, called damage-associated molecular patterns
(DAMPs) (Boller et al ,2009,). Pattern recognition is translated into a first line of defense called PAMP-
triggered immunity (PTI), which keeps most potential invaders in check (Fig 5). Successful pathogens
have evolved to minimize host immune stimulation and utilize virulence effector molecules to bypass this
first line of defense, by either suppressing PTI signaling or preventing detection by the host (Bardoel et
al.,2011, De Jongeet al., 2010, Dodds 2010, Pel MJC et al., 2013). In turn, plants acquired a second line
of defense in which resistance (R) NB-LRR (nucleotide-binding–leucinerich repeat) receptor proteins
mediate recognition of attacker-specific effector molecules, resulting in effector-triggered immunity (ETI)
(Dodds et al.,2010). ETI is a manifestation of gene-for-gene resistance (Flors HH. 1971), which is often
accompanied by a programmed cell death at the site of infection that prevents further ingress of biotrophic
pathogens that thrive on living host tissue. The onset of PTI and ETI often triggers an induced resistance
in tissues distal from the site of infection and involves one or more long-distance signals that propagate an
enhanced defensive capacity in still undamaged plant parts (Dempsey et al., 2012 , Shah et al.,
2013).Systemic acquired resistance (SAR), is mediated by salicylic acid (SA), a compound which is
frequently produced following pathogen infection and typically leads to the expression of pathogenesis-
related (PR) proteins. These PR proteins include a variety of enzymes some of which may act directly to
lyse invading cells, reinforce cell wall boundaries to resist infections, or induce localized cell death. A
second phenotype, first referred to as induced systemic resistance (ISR), is mediated by jasmonic acid
(JA) and/or ethylene, which are produced following applications of some nonpathogenic rhizobacteria.
Interestingly, the SA- and JA- dependent defense pathways can be mutually antagonistic, and some
bacterial pathogens take advantage of this to overcome the SAR. For example, pathogenic strains of
Pseudomonassyringae produce coronatine, which is similar to JA, to overcome the SA-mediated pathway
(He et al. 2004).Recently, epigenetic regulation of pathogen- and β-aminobutyric acid (BABA)-induced
priming for SA-dependent defenses and herbivore-induced priming for JA-dependent defenses was shown
to be inherited by the next generation via chromatin remodeling or DNA methylation (Luna et al.,2012,
Rasmann et al.,2012). Hence, plants seem to have the capacity to memorize a stressful situation and
subsequently immunize not only themselves but also their offspring against future attacks (Pastor et
al.,2013). Generally This induced resistance is of two types representing two distinct pathway responses:
12
systemic acquired resistance (SAR) and induced systemic resistance (ISR). Typically, SAR is induced by
pathogens while ISR is salicylic acid in dependent and is induced by non-pathogenic bacteria (Van Loon
et al., 1998). For example, S.cerevisiae, Rhodosporidiumlpaludigenum, Candidalsaitoana, C.loleophila
and Metschnikowia species induce an innate immune response and eventually cause resistance against
phyllosphere pathogens in fruits (De Miccolis Angelini etal. 2019; Droby etfal. 2002; Hadwiger etfal.
2015; Hershkovitz etfal. 2012; Sun et al. 2018).
4.Mixed-path antagonism
4.1. Antibiotics
The term antibiotic was coined from the word „antibiosis‟ which literally means “against life”. In the
past, antibiotics were considered to be organic compounds produced by one microorganism which are
toxic to other microorganisms (Russell, 2004). It is secondry antimicrobial metabolites belonging to
heterogeneous groups of organic, low-molecular weight compounds produced by microorganisms that are
deleterious to the growth or metabolic activities of other microorganisms (Thomashow et al.,1997).
Antibiotics produced by bacteria include volatile antibiotics (hydrogen cyanide,aldehydes, alcohols,
ketones) and nonvolatile antibiotics: polyketides(diacetylphloroglucinol; DAPG and mupirocin),
heterocyclic nitrogenous compounds (phenazinederivatives: pyocyanin, phenazine-1-carboxylic acid;
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)
Bacillomycin, fengycin Bacillus amyloliquefaciens FZB42
Fusariumoxysporum
Wilt Koumoutsi et al. (2004)
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
indirectly promotes plant growth. Antagonistic bacteria Serratia marcescens reduce mycelial network of
Sclerotium rolfsii by expressing chitinase (Ordentlich et al.,1988). Lysobacter is capable of producing
glucanase that is involved in the control of diseases caused by Bipolaris and Pythium sp. (Palumbo et al.,
2005). Hydrolytic enzymes directly contribute in the parasitization of phytopathogens and rescue plant
from biotic stresses [Haran et al., 1996]. The proteases reduced the activities of the pathogen enzymes
exo- and endopoly galacturonase , pectin methyl esterase, pectate lyase, chitinase, b- 1,3- glucanase and
cutinase, that are essential for the pathogen during host infection. The secretion of chitinolytic
enzymes is considered a desirable characteristic for biocontrol agents as it allows degrading
fungal cell walls, Chitin degrading activity has been measured in biocontrol yeasts of
16
the genera Aureobasidium,Candida,Debaryomyces,Metschnikowia, Meyerozyma,
Pichia,Saccharomyces,Tilletiopsis, and Wickerhamomyces and in Saccharo mycopsis (Zajc et al. 2019).
4.5. Bacteriocin
Bacteriocins are proteinaceous toxins that are secreted by bacteria that lives in competitive microbial
environment. They destroy the neighboring bacterial species by damaging the bacterio-cinogenic cells
(Riley et al., 2002). Bacteriocins are very effective in reducing or inhibiting the growth of
phytopathogens (Beneduzi et al., 2012). Bacteriocins have narrow killing spectrum as compared to
conventional antibiotics and these have damaging effect on the bacteria that are closely relative of
bacteriocin producing bacteria (Riley et al., 2002). Colicins are most prominent bacteriocins synthesized
by Escherichia coli. Similarly, megacins is produced by B. megaterium; marcescins from Serratia
marcescens; cloacins from Enterobacter cloacae; and pyocins comes from P. pyogenes (Cascales et
al.,2007). Bacteriocins that are produced by Bacillus spp. remarkably gain importance due broad range of
inhibition of fungal, yeast, gram positive and gram negative species that may have some pathogenic effect
on animals and human beings (Abriouel et al.,2011).
5.Antagonisms in Rhizospher, phylospher and endophyt microbes
The rhizosphere concept was first introduced in 1904 by Dr Lorenz Hiltner as the soil compartment
influenced by the root (Smalla et al., 2006; Hartmann, 2008). The implication of root exudates as a
nutrient source for bacteria was then initiated, explaining why bacterial density was more impor tant than
in bulk soil. This phenomenon was called the ‘rhizosphere effect’ by Rovira (1956), another major
contributor in rhizosphere research (Burns, 2010). Rhizosphere has been broadly subdivided into the
following three zones (Pratibha et al., 2013). (1).Endorhizosphere (interior of the root): that consists of the
root tissue including the endodermis and cortical layers; (2). Rhizoplane (interior of the root): is the root
surface where soil particles and microbes adhere. It consists of epidermis, cortex and mucilaginous
polysaccharide layer; (3). Ectorhizosphere: that consists of soil immediately adjacent to the root. The
ability to secrete a vast array of compounds into the rhizosphere is one of the most remarkable metabolic
features of plant roots, with nearly 49% of all photosynthetically fixed carbon being transferred to the
rhizosphere through root exudates (Prakash and Karthikeyan, 2013). The phyllosphere is broadly defined
as the surfaces and internal parts of the aerialstructures of plants, including flowers, fruits,stems and
leaves. Specialized microbialcolonists, phytopathogens, spoilage organisms and periodic immigrants have
17
all been describedas residents of this physically diverse habitat. Microorganisms that can grow in the
rhizosphere are ideal for use as biocontrol agents, since the rhizosphere provides the front-line defense
for roots against attack by pathogens. Pathogens encounter antagonism from rhizosphere microorganisms
before and during primary infection and also during secondary spread on the root. In some soils described
as microbiologically suppressive to pathogens. microbial antagonism of the pathogen is especially great,
leading to substantial disease control(Schneider, R. W. 1982). The bacteria known as plant growth-
promoting rhizobacteria (PGPR) live in close vicinity to the plants (endosphereor rhizosphere) and play a
key role in the transformation of many organic and inorganic compounds making them available for plant
growth such as nitrogen, phosphorus, potassium, iron, and zinc( Olanrewaju et al., 2017). PGPR exert
beneficiale effects on plant growth and yield by the production of plant growthregulating substances, such
as indole-3-acetic acid (IAA), gibberellic acid, cytokinin and 1-aminocyclopropane-1-carboxylate (ACC)
deaminase(Glick, 2014). The ACC-deaminase producing PGPR facilitate plantgrowth by decreasing plant
ethylene levels and reducing stress caused by biotic (such as phytopathogenic bacteria/fungi) and abiotic
factors (such as heavy metals, salt, and drought) (Glick et al., 2007). Antifungal metabolites produced by
these rhizobacteria were identified as antibiotics (iturin, surfactins, fengycin, DAPG, Phenazine, etc.), cell
wall degradingenzymes (protease, chitinase, and cellulase), plant growth promotion enzymes and
hormones (indole-3-aceticacid, ACC-deaminase, phosphates, nitrogen fixation), N-acyl-homoserine
lactones and siderophores. (Saira Ali et al.,2020) Bacillus spp. have been tested on a wide variety of plant
species for abilityto control diseases. They are appealing candidates for biocontrol because they produce
endospores that are tolerant to heat and desiccation. The antagonistic effects by PGPR over various phyto
pathogens bolster the possibilities for their useas biocontrol agents (Sang et al., 2011; Lamsal et al.,2013).
Recent findings suggest that competition fornutrient, niche exclusion, induced systemic resistanceand
production of metabolites such as antibiotics,siderophores and hydrogen cyanide are the chief modes of
biocontrol activity in PGPR (Ambrosini andBeneduzi, 2012). The rhizosphere, influenced by root
secretions,can contain up to 1011microbial cells per gram root (Egamberdieva et al.,2008) and more than
30,000 prokaryotic species(Mende et al.,2011). Soil microorganisms (free-living,associative, and
symbiotic rhizobacteria) belonging to the genera like Acinetobacter,Burkholderia, Enterobacter,
Alcaligenes,Arthrobacter, Azospirillum, Azotobacter, Bacillus, Erwinia, Flavobacterium,
Rhizobium,Serratia, Xanthomonas, Proteus, andPseudomonas are the integral parts of rhizosphere biota
(Glick.,1995) and exhibit successful rhizosphere colonization. Diveres microbial genera are identified
from rhizospher of different plants, and horticulture, for example, The fungal genera Alternaria,
Clonostachys, Fusarium, Penicillium and Rhizoctonia are cited to be commonly encountered in both the
rhizosphere and the geocaulosphere of potato (Pieta & Patkowska, 2003; Fiers et al., 2010). Three genera,
18
known to mainly contain rhizobacteria species,were consistently identified in each microenvironment:
Agrobacterium, Bacillus and Pseudomonas. To a lesser extent, genera such as Arthrobacter, Comamonas,
Curtobacterium,Enterobacter, Paenibacillus, Pantoea, Serratia, Sphingobacterium,Stenotrophomonas,
Variovorax and Xanthomonas are frequently found in the vicinity of the potato rhizospher for instance.
6. Biontrol recent progress & future perspectives
Biological control has been used for centuries, but the first big wave of activity in the modern era
followed the spectacular success of the introduction in the late 1880s of the parasitic fly, Cryptochaetum
iceryae (Williston) (Diptera: Cryptochaetidae), and the vedalia beetle, Rodolia cardinalis (Mulsant)
(Coleoptera: Coccinellidae) to control cottony-cushion scale (Icerya purchasiMaskell) (Hemiptera:
Monophlebidae) in California citrus orchards (Caltagirone 1981). However, in the mid-1940s’ the growth
and success of the synthetic pesticide industry caused biocontrol use to almost disappear until the
publication of Rachael Carson’s ‘Silent Spring’ (Carson 1962), While biological control is still seen by
many as a preferable and sustainable alternative for chemical pest control, it should play a much more
important role in managing insects, weeds and diseases. In augmentative biological control, the situation
has changed in the last five years from a dip in uptake of biocontrol around the year 2000 (van Lenteren
2012) to much improved adoption (van Lenteren et al. 2017). This has come about by political
developments in Europe and Asia, and also in Latin America. Demands of retailers and consumers, and
actions by NGOs have helped to instigate this change. In emerging countries such as Brazil, biological
control research and implementation is gaining momentum for both augmentative and classical
biocontrol. (Parra 2014). China and India are also countries that have invested widely in biological control
research, training and adoption. China, for example, has recognised that pesticides and fertilizers have
created serious damage to ecosystems and created food security issues and, as a result, the use of agri-
chemicals will be capped from 2020. In the European Union, the Sustainable Use of pesticides Directive
2009 came into force starting in 2011 to encourage development and introduction of Integrated
PestManagement (IPM) and alternative techniques to reduce dependency on the use of pesticides.
initiatives and developments would seem to herald every prospect for increased funding for biological
control and IPM research in the future and the IOBC is set to play an important implementation and
facilitating role in the renaissance and development of biocontrol worldwide.
19
7. Conclusion
Microbial biological control agents protect plants from damage by diseases via different modes of
action.They may induce resistance or prime enhanced resistance against infections by a pathogen in plant
tissues without direct antagonistic interaction with the pathogen. Another indirect interaction with
pathogens is competition for nutrients and space. MBCAs may also interact directly with the pathogen by
hyperparasitism or antibiosis. Hyperparasites invade and kill mycelium, spores, and resting structures of
fungal pathogens and cells of bacterial pathogens. Production of antimicrobial secondary metabolites with
inhibiting effects against pathogens is another direct mode of action. Low amounts of in situ secreted
secondary metabolites support antagonists to gain a competitive advantage. In some cases, biocontrol
agents have been selected which secrete already efficient secondary metabolites into the growth media
during mass production that are applied together with or without living cells of antagonists in the
biological control product. The rhizosphere is the site of complex dynamic plant–microorganism
interactions and is of interest from multiple environmental perspectives for biocontrol study.
8. ReferenceArthurW,MitchellP(1989) Arivesed scheme for the classification of population interctions,Oikos.141-
143.
Ambrosini A, Beneduzi A (2012). Screening ofplant growth promoting Rhizobacteria isolated from
sunflower (Helianthus annuus L.). Plant and Soil356, 245–264.
Aggarwal S, Stewart P, Hozalski R (2016). "Biofilm Cohesive Strength as a Basis for Biofilm
Recalcitrance: Are Bacterial Biofilms Overdesigned?". Microbiology Insights. 8 (Suppl 2), 29
32.
Altomare C, Norvell W A, Bjorkman T, Harman G E. (1999). Solubilization of phosphate and micro
nutrients by the plant growth promoting fungus Trichoderma harzianum Riafi. Applied
Environmental Microbiology. 65: 2926-2933.
An D, Parsek MR (June 2007). "The promise and peril of transcriptional profiling in biofilm
communities". Current Opinion in Microbiology. 10 (3): 292–296.
Ahmed E, Holmstrom SJM (2014). Siderophores in environmental research: roles and applications.
Microb Biotechnol 7:196–208.
20
Ali SS, Vidhale NN (2013). Bacterial siderophore and their application: a review. Int J Curr Microbiol
Appl Sci 2:303–312.
Abriouel H, Franz CM, Omar NB, Galvez A(2011). Diversity and applications of Bacillus bacteriocins. FEMS Microbiol Rev. 2011; 35: 201-232.Ahmad F, Ahmad I, Khan M.S(2008).Screening of free-living rhizospheric bacteria fortheir multiple
plant growth promoting activities.Microbiol Res 163:173–181.
Al-Ajlani, M.M., Sheikh, M.A, Ahmad Z, Hasnain S(2007). Production of surfactin from Bacillus
subtilis MZ-7 grown on pharmamedia commercial medium. Microb. Cell Fact.6, 17–24.
Arrebola E, Jacobs R, Korsten L(2010). Iturin A is theprincipal inhibitor in the biocontrol activity of
Bacillus amyloliquefaciens PPCB004 against postharvest fungal pathogens. J Appl Microbiol
108:386-395.
AtanasovaL, Crom S L, GruberS, F. CoulpierF, Seidl-SeibothV, KubicekCP,. Druzhinina I.S (2013).Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism, BMC Genomics 14.1186/1471-2164-14-121.
Alstrom S(1991) Induction of disease resistance in common bean susceptible to halo blight bacterial
pathogen after seed bacterization with rhizosphere pseudomonads. J. Gen. Appl. Microbiol.
37:495–501.
Bronstien JL(1994).Our current understanding of mutualism,Q.Rev.Biol.69.31-51.
Baker K F and R. J. CookRJ(1974). Biological Control of Plant Pathogens, W. H. Freeman and Co,
San Francisco, California. 433 pp. (Book, reprinted in 1982, Amer. Phytopathol. Soc., St. Paul,
Minnesota).
Beneduzi, A., Ambrosini, Passaglia, L.M.P.(2012). Plant growth-promoting rhizobacteria (PGPR): their
potential as antagonists and biocontrol agents. Genet. Mol. Biol. 35, 1044–1051.
Burns RG (2010) Albert Rovira and a half-century of rhizosphere research. The Rovira Rhizosphere
Symposium (Gupta VVSR, Ryder M & Radcliffe J, eds), pp. 1–10. SARDI PRCWC, Adelaı¨de,
Australia.
Beneduzi A, Ambrosini A, Passaglia LM(2012). Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol. 35: 1044-1051.
Beneduzi A, Ambrosini A, Passaglia LM(2012). Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol.35: 1044-1051.
Boller T, Felix G (2009). A renaissance of elicitors: perception of microbe-associated molecular
patternsand danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379–406.21
Bardoel BW, Van der Ent S, Pel MJC, Tommassen J, Pieterse CMJ(2011) Pseudomonas evades
immune recognition of flagellin in both mammals and plants. PLoS Pathog. 7:102-106.
Boukhalfa H, Lack JG, Reilly SD, Hersman L, Neu MP (2003) Siderophore production and facilitated
uptake of iron and plutonium in P. p u t i d a . No. LA-UR-03-0913. Los Alamos National
Laboratoy.
Briandet R, Herry J, Bellon-Fontaine M (August 2001). "Determination of the van der Waals, electron
donor and electron acceptor surface tension components of static Gram-positive microbial
biofilms". Colloids Surf B Biointerfaces. 21 (4): 299–310.Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM(2006). The role of root exudates in rhizosphere
interations with plants and other organisms. Annu. Rev. Plant Biol. 57:233–66.
Chet I(1987). Trichoderma application, mode of action, and potential as biocontrolagent of soil-borne
pathogenic fungi.Pages 137-160.in: Innovative Approaches to PlantDisease Control. I. Chet,
ed., John Wiley, New York.
Carsolio CN, Benhamou S, Haran C, Cortes A, Gutierrez I, Chet and Herrera-EstrellaA(1999). Role of the Trichoderma harzianum endochitinase gene, ech42, in mycoparasitism. Appl. Environ. Microbioly. 65. 929-935.Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R(2007)Colicin biology. Microbiol Mol
Biol. 71:158-229.
Cortés C, Gutiérrez A, Chet I, Herrera-Estrella A(1999) Role of Trichoderma harzianum
endochitinase gene, ech42, in mycoparasitism. Applied and Environmental Microbiology 65: 929-
935.
CookRJ, BakerKF (1983). The Nature and practice of biological control of plantpathogens,American
Phytopathology society. Bronstien JL(1994).Our current understanding of
mutualism,Q.Rev.Biol.69.31-51.
Cai Y, Wang R, An MM, Bei-Bei L (2010) Iron-depletion prevents biofilm formation in Pseudomonas aeruginosa through twitching motility and quorum sensing. Braz J Microbiol 41(1):37–41.
Chi M et al (2015) Increase in antioxidant enzyme activity, stress tolerance and biocontrol efcacy of
Pichia kudriavzevii with the transition from a yeast-like to bioflm morphology. Biol Cont 90:113–
119.
Costa-Orlandi CB (2017) Fungal bioflms and polymicrobial diseases. J Fungi (Basel) 3:22.
Cziferszky A, Mach RL, Kubicek C P( 2002): Phosphorylation positively regulates DNA binding
22
of the carbon catabolite repressor Cre1 of Hypocrea jecorina. The Journal of Biological
Chemistry 277: 14688-14694.
Caltagirone LE (1981) Landmark examples in classical biological control. Annu Rev Entomol 26:213–
232
Compant S, Clément C, Sessitsch A (2010) Plant growthpromoting bacteria in the rhizo- and
endosphere of plants:Their role, colonization, mechanisms involved and prospects for utilization.
Soil Biol. Biochem. 42, 669678.
Dodds PN, Rathjen JP(2010). Plant immunity: towards an integrated view of plant-pathogen
interactions.Nat. Rev. Genet. 11:539–48
De Jonge R, Van Esse HP, Kombrink A, Shinya T, Desaki Y(2010) Conserved fungal LysM
effectorEcp6 prevents chitin-triggered immunity in plants. Science 329:953–55.
De Bruijn, I., de Kock, M.J.D., Yang, M., de Waard, P., van Beek, T.A., Raaijmakers, J.M.,(2007).
Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide
antibiotics
in Pseudomonas species. Mol. Microbiol. 63, 417–428.
De las Mercedes Dana, M, Limón MC, MejíasR, Mach RL, BenítezT, Pintor-ToroJA,
KubicekCP(2001)Regulation of chitinase 33 (chit33) gene expression in Trichoderma
harzianum. Current Genetics 38: 335-342.
DonzelliB G G, Lorito M.ScalaF, Harman G E(2001). Cloning, sequence and structure of a
gene encoding an antifungal glucan 1,3-β-glucosidase from Trichoderma atroviride (T.
Donlan RM (2002). "Biofilms: Microbial Life on Surfaces". Emerging Infectious Diseases. 8 (9):
881–890. harzianum). Gene 277: 199-208.
De Souza JT, Arnould C, Deulvot C, Lemanceau P, Gianinazzi-Pearson V(2003). Effect of 2, 4-
diacetylphloroglucinol on Pythium: cellular responses and variation in sensitivity among
propagules and species. Phytopathology. 93: 966-975.
De Souza JTA, Arnould C, Deulvot C, Lemanceau P, Gianinazzi-Pearson V, Raaijmakers J.M (2003).
Effect of 2,4-diacetylphloroglucinol on Pythium: cellularresponses and variation in sensitivity
among propagules and species.Phytopatholol.93:966–975.
Dempsey DA, Klessig DF(2012). SOS: too many signals for systemic acquired resistance? Trends
Plant Sci. 17:538–45.23
Di Pietro A(1993). Chitinolytic enzymes produced by Trichodermaharzianum : antifungalactivity of
purified endochitinase and chitobiosidase.Phytopathol. 83:302-307.
DeBach P (1964). The scope of biological control. p. 3-20. In Biological Control of Insect Pests and
Weeds(P. DeBach, editor). Chapman and Hall Ltd., London. 844 pp
De Miccolis Angelini RM, Rotolo C, Gerin D, Abate D, Pollastro S, Faretra F(2019) Global
transcriptome analysis and dilerentially expressed genes in grapevine after application of the
yeastderived defense inducer cerevisane. Pest Manag Sci 75:2020– 2033.
Egamberdieva, D. et al. (2008). High incidenceof plant growthstimulating bacteria associated with the rhizosphere of wheat grown onsalinated soil in Uzbekistan. Environ.Microbiol..10: 1–9.Flors HH(1971). Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275–96.
Fardeau S, Mullie C, Dassonville-Klimpt A, Audic N, Sonnet P (2011) Bacterial iron uptake: a
promising solution against multidrug resistant bacteria. In Science against microbial pathogens:
communicating current research and technological advances, pp. 695–705.
FickeA, Aubertot JN, HollierC (2012). Crop Losses Due to Diseases and Their Implications for
Global Food Production Losses and Food Security, Springer.
FisherMC, HenkDA, BriggsCJ, BrownstienJS, Maldoff LC, McCrawSL, GurrSJ(2012).Emerging
fungal threats to animal plant and ecosystem health, nature 484.
Frankowski Jens, Matteo Lorito, Felice Scala, Roland Schmid, Gabriele Berg, Hubert Bahl.(2001).
Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Arch
Microbiol 176 :421–426.
Ghorbanpour M, Omidvari M, Abbaszadeh-Dahaji P, Omidvar R, and Kariman K. (2018). Mechanisms underlying the protective effects of beneficial fungi against plant diseases. Biol. Control 117, 147–157.doi: 10.1016/j. biocontrol.2017.11.006
Glick, B.R., 2014. Bacteria with ACC deaminase can promote plant growth and help to feed the world.
Microbiol. Res. (Pavia) 169, 30–39.
Gilden RC, Hu ing K, Sattler B (2010) Pesticides and Health Risks. J Obstet Gynecol Neonatal Nurs.
39: 103-110.
Glick, B.R., Cheng, Z., Czarny, J., Duan, J., 2007. Promotion of plant growth by ACC
deaminase-producing soil bacteria. Eur. J. Plant Pathol. 119, 329–339.
Glick BR (1995). The enhancement of plantgrowthby free-living bacteria. Can J Microbiol.
1995. 41. 109–117.
Glick R, Gilmour C, Tremblay J, Satanower S, Avidan O, Deziel E, Greenberg EP, Poole K, Banin E
24
(2010) Increase in rhamnolipid synthesis under iron-limiting conditions influences surface
motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol192(12):2973–2980
GoreckiRJ, Harman GE, and Mattick LR(1985).The volatile exudates fromgerminating pea seeds of
different viability and vigor.Can. J. Botany.63:1035- 1 0 3 9 .
Glick BR (2012). Plant Growth-Promoting Bacteria : Mechanisms and Applications. Scientifica 2012,
https://doi.org/10.6064/2012/963401.
Glandorf DC, Verheggen P, Jansen T, JorritsmaJW, Smit E, Leefang P, Wernars K, Thomashow L S,
Hall-Stoodley L, Costerton JW, Stoodley P (February 2004). "Bacterial biofilms: from the natural
environment to infectious diseases". Nature Reviews Microbiology. 2 (2): 95–108.
Hissen, A.H.T, Chow JMT, PintoLJ. and Moore MM (2004) Survival of Aspergillus fumigatus in
serum involves removal of iron from transferrin: the role of siderophores. Infect Immun 72, 1402–
12.
Haas D, Defago G(2005). Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3, 307–319. Halfeld-Vieira, B.A., Vieira, J.R., Romeiro Jr., R.S., Silva, H.S.A., Mc,B.P., 2006.1408.Hartmann A (2008) Multitrophic interactions in the rhizosphere. Rhizosphere microbiology: at the
interface of many disciplines and expertises. FEMS Microbiol Ecol 65: 179.
Howell CR, BeierRC and Stipanovic RD (1988). Production of ammonia by Enterobacter cloacae and
its possible role in te biological control of pythiumm pre-emergence damping –off by the
bacterium.Phatopathology, 78:1075-1078.
Heydari A. and Pessarakli M. 2010. A Review on Biological Control of Fungal Plant Pathogens Using Microbial Antagonists. Journal of Biological Sciences 10: 273-290.
Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI (2005). "Aminoglycoside
antibiotics induce bacterial biofilmformation". Nature. 436 (7054):Bibcode:2005Natur.436.1171H
Haran S, Schickler H, Chet I(1996). Molecular mechanisms of lytic enzymes involved in the
biocontrol activity of Trichoderma harzianum. Microbiol.142: 2321-2331.
Harman GE, Howell CR.,VitarboA, Chet I, and Lorito M(2004) Trichoderma species - opportunistic,
avirulent plant symbionts. Nature Rev. Microbiol. 2:43-56.
HeP, Chintamanani S, Chen Z, Zhu L, Kunkel B N, Alfano JR, Tang X, and Zhou J M(2004).
Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III
effectors and coronatine. Plant J. 37:589-602.
HarmanGE and Nelson EB(1994). Mechanisms of protection of seed and seedlingsby biological
25
control treatments: Implications for practical disease control. Pages 283-292.in: Seed Treatment:
Progress and Prospects. T. Martin, ed., BCPC, Farnham,UK.
Hadwiger LA, McDonel H, Glawe D (2015) Wild yeast strains as prospective candidates to induce
resistance against potato late blight (Phytophthoralinfestans). Am J Potato Res 92:379–386.
Hershkovitz V (2012) Global changes in gene expression of grapefruit peel tissue in response to
the yeast biocontrol agent Metschnikowialfructicola. Mol Plant Pathol 13:338–349.
HorbachR, Navarro-QuesadaAR,KnoggeW, H.B. DeisingHB (2011), When and how to kill a plant
cell: infection strategies of plant pathogenic fungi, J. Plant Physiol. 168 .51–62.
HalimannJ(2001). Plant interaction with endophytes bacteria,CABI Publishing , New york.
Hubertus Haas (2014) Fungal siderophore metabolism with a focus on Aspergillus fumigatus Nat.
Prod. Rep. 31, 1266–1276.
Inbar J, and Chet I(1994) A newly isolated lectin from the plant pathogenic fungusSclerotiumrolfsii:
purification, characterization and role in mycoparasitism. J. Microbiol.140:651-657.
Ilmén M, Thrane C, Penttilä M(1996) The glucose repressor gene cre1 of Trichoderma: isolation and
expression of a full-length and a truncated mutant form. Molecular and General Genetics
251:451-460.
Junker K, Chailyan A, Hesselbart A, Forster J, Wendland J (2019) Multi-omics characterization of the
necrotrophic mycoparasite Saccharomycopsis schoenii. PLoS Pathog 15:e1007692
JamesG, BeaudtteL, CostertonJ(1995).Inter species bacteria interaction in biofilms.J.Ind.Micrbial.Biotechnol.15(257-262).
Klein MN, Kupper KC (2018) Bioflm production by Aureobasidium pullulans improves biocontrol
against sour rot in citrus. Food Microbiol 69:1–10.
Köhl J, Postma J, Nicot P, Ruocco M, and Blum B (2011). Stepwise screening of microorganisms for
commercial use in biological control of plant pathogenic fungi and bacteria. Biol. Control 57, 1–12.
Kubicek CP, Penttilä ME(1998) Regulation of production of plant polysaccharide degrading enzymes
by Trichoderma. In: Harman, G. E.; Kubicek, C. P. ed. Trichoderma and Gliocladium. Vol. 2:
enzymes, biological control and commercial application. London, Taylor and Francis. Pp. 49-72.
Kim H, Jeun Y (2006). Resistance Induction and Enhanced Tuber Production by Pre-inoculation with
Bacterial Strains in Potato Plants against Phytophthora infestans. Mycobiology 34(2), 67–72.
Karatan E, Watnick P (June 2009). "Signals, regulatory networks, and materials that build and break
bacterial biofilms". Microbiology and Molecular Biology Reviews. 73 (2): 310–47.26
Kuc J. (1982). Induced immunity to plant disease. ´ Bioscience 32:854–60
Kloepper J W, Leong J, Teintze M, Schroth M N. (1980). Pseudomonas siderophores: A mechanism explaining disease suppression in soils. Current Microbiology. 4: 317-320.
Laureijs E, Thomas-Oates JE, Bakker PA and Van Loon LC (2001) Effect of genetically modified
Pseudomonas putida WCS358r on the fungal rhizosphere microflora
of field-grown wheat. Appl. Environ. Microbiol. 67:3371-3378.
Lorito, M. 1998: Chitinolytic enzymes and their genes. In: Harman, G. E.; Kubicek, C. P. ed.
Trichoderma and Gliocladium. Vol. 2: enzymes, biological control and commercial application.
London, Taylor and Francis. Pp. 73-100.
Locher KP(2004). Structure and mechanism of ABC transporters, Curr. Opin. Struct. Biol. 14 .426–
431.
Lugtenberg B, KamilovaF(2009).Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol.
63:541–56.
López Daniel, VlamakisHera, KolterRoberto (2010). "Biofilms". Cold Spring Harbor Perspectives
in Biology. 2 (7).
Lamsal K, Kim SW, Kim YS, Lee YS. 2013.Biocontrol of late blight and plant growth promotion
in tomato using rhizobacterial isolates. Journal ofMicrobiology and Biotechnology 23(7), 897–904.
Luna E, Bruce TJA, Roberts MR, Flors V, Ton J. 2012. Next-generation systemic acquired
resistance.Plant Physiol. 158:844–53.
Lorito M, Hayes C K, Zonia A Scala, F, Del S G, Woo SL, Harman G E. (1994). Potential of genesand gene productsfrom Trichoderma sp.and Gliocladium sp. for the development of biologicalpesticides. Molecular Biotechnology. 2: 209- 217.
McNeely, D., Chanyi, R. M., Dooley, J. S., Moore, J. E., and Koval, S. F.(2017). Biocontrol Of
Burkholderia cepacia complex bacteria and bacterial phytopathogens by Bdellovibrio bacteriovorus.
Can. J. Microbiol. 63, 350–358.
Mukherjee, K.P, C.S. Nautiyal and A.N. Mukhopadhyay. 2008. Molecular mechanisms of plant and microbe coexistence. Springer, Heidelberg
Mukhopadhyay, A S N, Mukherjee P K. (1998). Biological control of plant diseases: status in India in Biological suppression of Plant Diseases: Phytopathogens, Nematodes and weeds. Eds. Singh, S. P. and Husain, S. S. 7: 1-20. Mukherjee M, Mukherjee PK, Kale SP(2007). cAMP signalling is involved in growth, germination, mycoparasitism and secondary metabolism in Trichoderma virens. Microbiology.153: 173442.
27
Mach RL, PeterbauerC K, Payer K, Jaksits S, WooS L, Zeilinger S, Kullnig CM, Lorito M,
KubicekC P(1999). Expression of two major chitinase genes of Trichoderma atroviride (T.
harzianum P1) is triggered by different regulatory signals. Applied and Environmental
Microbiology 65: 1858-1863.
MilnerRJ, PearsonJ, NesbitJW, CloseP(1996). Immunophenotypic Classification of Canine Malignant
Lymphoma on Formalin-Mixed Paraffin Wax-Embedded Tissue by Means of CD3 and CD79a
Cell Markers. J Vet Res, 63 (4), 309-13.
Maksimov IV, Abizgil RR, Pusenkova LI (2011). Plant Growth Promoting Rhizobacteria as
Alternative to Chemical Crop Protectors from Pathogens (Review). Applied Biochemistry and
Microbiology 47(4), 373–385.
Madigan MT & Martinko JM (2006). Brock biology of microorganisms. 11thedition. Pearson Prentice
Hall Inc
Messenger AJ, Barclay R (1983) Bacteria, iron and pathogenicity. Biochem Educ 11(2):54–63
Mendes R. et al. (2011) Deciphering therhizosphere microbiome for diseasesuppressive
bacteria.Science332,1097–1100.
Nelson, E B. (1990). Exudate molecules initiating fungal responses to seed seeds and roots. Plant and Soil. 129: 61-73.Ortu G, Demontis MA, Budroni M, Goyard S, d’Enfert C, Migheli Q (2005) Study of bioflm formation
in Candida albicans may help understanding the biocontrol capability of a for strain of
Saccharomyces cerevisiae against the phytopathogenic fungus Penicillium expansum. J Plant
Pathol 87:300.
Ordentlich A, Elad Y, Chet I(1988).The role of chitinase of Serratia marcescens in biocontrol of
Sclerotium rolfsii. Phytopathology. 78: 84-88.
Olanrewaju OS, Glick BR., Babalola OO (2017). Mechanisms of action of plant growth
promoting bacteria. World J. Microbiol. Biotechnol. 33 (11), 197.
Pel MJC, Pieterse CMJ (2013). Microbial recognition and evasion of host immunity. J. Exp. Bot.
64:1237–48.
Parra JRP (2014) Biological control in Brazil: an overview. Scientia Agricola 71(5):420–429.
Pal kk, Gardner BM(2006).Biological control of plant pathogen plant health instr. 2(1117-1142).
28
Prakash, P, Karthikeyan, B., 2013. Isolation and purificationof plant growth promoting rhizobacteria
(PGPR) from therhizosphere of Acorus calamus grown soil. Ind. StreamsRes. J. 3, 1-13.
Pratibha, Lal, S. and Goswami, A.K. (2013). Effect of pruning and planting systems on growth,
flowering, fruiting and yield of guava cv. Sardar. Indian Journal of Horticulture, 70(4): 496-500.
Palumbo JD, Yuen GY, Jochum CC, Tatum K, Kobayashi DY(2005). Mutagenesis of Beta-1,3-
Glucanase Genes in Lysobacter Enzymogenes Strain C3 Results in Reduced Biological Control
Activity Toward Bipolaris Leaf Spot of Tall Fescue and Pythium Damping-Off of Sugar Beet.
Phytopathol. 95: 701-707.
Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V. 2013. Primed plants do not forget. Environ. Exp.
Bot. 94:46–56.
Pu L, Jingfan F, Kai C, Chao-an L, Yunjiang C (2014) Phenylethanol promotes adhesion and biofilm
formation of theantagonistic yeast Kloeckera apiculata for the control of blue mold on citrus.
FEMS Yeast Res 14:536–546.
Price PW, Bouton CE, Gross P, McPheronBA, Thompson JN, WeisAE(1980).Interaction among three
trophic level influence of plants on inetactions beween insect herbivores and natural
enemies.Annu.Rev.Ecol.Syst.11(41-65).
PankhurstCE, LynchJM (2005) Encyclopedia of Soils in the Environment, Biocontrol of soil-borne plant diseases.Price PW (1977). General conceptsnon the evolutionary biology of parasits,Evolution 31.405-420.
Rovira AD (1956). Plant root excretions in relation to the rhizosphere effect. Plant Soil 7: 178–217.
Raaijmakers, J.M., de Bruijn, I., Nybroe, O., Ongena, M., (2010). Natural functions of popeptides from
Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol. Rev. 34, 1037–
1062.
Riley MA, Wertz JE(2002). Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol. 56: 117-137. Ramette AY,Moenne-Loccoz and DefagoG (2003).Prevalance of fluorecnce pseudomonads producing
antifungal phloroglucinols and /or hydrogen cyanide in soil naturally suppressive or conducive
to tobacco root rot.FEMS Micro.ECOL.,44:35-43.
Rocha-Ramirez V, Omero C, Chet I, Horwitz BA, Herrera-Estrella(2002) A. Trichoderma atroviride G-
protein alpha-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryot Cell 1:
594-605.
Raaijmakers J M and MazzolaM. (2012). Diversity and natural functions of antibiotics produced by
beneficial and plant pathogenic bacteria. Annu. Rev. Phytopathol. 50, 403–424.
29
Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R(2012). Herbivory in the previous generation
primes plants for enhanced insect resistance. Plant Physiol. 158:854–63.
Russell A. D. (2004). Types of antibiotics and synthetic antimicrobial agents. In: Denyer S. P., Hodges N.
A. & German S. P. (eds.) Hugo and Russell‟s pharmaceutical microbiology. 7th Ed. Blackwell
Science, UK. Pp. 152-186.
Ross AF.( 1961). Systemic acquired resistance induced by localized virus infections in plants.
Virology 14:340–58.
Roberts MJ, Schimmelpfennig DE, Ashley E, Livingston MJ, Ash MS, Vasavada U( 2006).The Value
of Plant Disease Early-warning Systems: a Case Study of USDA’s Soybean Rust Coordinated
Framework, United States Department of Agriculture, Economic Research Service,.S. Savary,
RabeaEI, BadawyMET, StevensCV, SmaggheG, SteurbautW(2003), Chitosan as antimicrobial agent:
applications and mode of action, Biomacromolecules 4.1457–1465.
RomanazziG, SanzaniSM, Bi Y, TianS, Martínez P G and Alkan, N. (2016). Induced
resistance to control postharvest decay of fruit and vegetablePostharvest Biol. Technol. 122, 82–94.
Silo-Suh LA, LethbridgeBJ, RaffelS J, HeH, ClardyJ, HandelsmanJ(1994). Biological Activities of Two
Fungistatic Antibiotics Produced by Bacillus Cereus UW85. Appl Environ Microbiol , 60 (6),
2023-30.
Spadaro D, Ciavorella A, Dianpeng Z, Garibaldi A and Gullino ML(2010). Effect of culture media and
pH on the biomass production and biocontrol efficacy of a Metschnikowia pulcherrima strain to
be used as a biofungicide for postharvest disease control. Can. J. Microbiol. 56, 128–137.
Spadaro D, and Droby S (2016). Development of biocontrol products for postharvest diseases of fruit:
the importance of elucidating the mechanisms of action of yeast antagonists. Trends Food Sci.
Technol. 47, 39–49.
Sang MK, Kim Do J, Kim BS, Kim KD. 2011.Root Treatment with Rhizobacteria Antagonistic to
Phytophthora Blight Affects Anthracnose Occurrence, Ripening and Yield of Pepper Fruit in the
PlasticHouse and Field. Biological Control 101(6), 666–678.
Saira Ali, Sohail Hameed, Muhammad Shahid, Mazhar Iqbal, George Lazarovits ,Asma Imran(2020).
Functional characterization of potential PGPR exhibiting broad-spectrumn antifungal activity.
Microbiological Research 232 (2020) 126389.
Schneider, R. W. 1982. Suppressive Soils and plant Disease. St. Paul: Am. Phytopathol. Soc. 88 pp.
Smalla K, Sessitsch A & Hartmann A (2006) The rhizosphere: ‘soil compartment influenced by the 30
root’. FEMS Microbiol Ecol 56: 165.
Stien T.(2005). Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Biol.
(Mosk.) 56, 845–857.
Shanmugaiah, V., Mathivanan, N., Varghese, B.(2010). Purification, crystal structure andantimicrobial
activity of phenazine-1-carboxamide produced by a growth-promotingbiocontrol bacterium,
Pseudomonas aeruginosa MML2212. J. Appl. Microbiol. 108,703–711
Shaikh SS, Sayyed RZ (2015). Role of Plant Growth-Promoting Rhizobacteria and Their Formulation in Biocontrol of Plant Diseases. In Plant Microbes Symbiosis: Applied Facets
Segarra, G., Casanova, E., Avilés, M., and Trillas, I. (2010). Trichoderma asperellum strain T34
controls Fusarium wilt disease in tomato plants in soilless culture through competition for iron.
Microb. Ecol. 59, 141–149.
Sun C, Fu D, Lu H, Zhang J, Zheng X, Yu T (2018) Autoclaved yeast enhances the resistance against
Pencilium expansum in pesr fruit and its possible mechnisms of action Biol Control 119:51–58.
Sharifah Farhana Syed, Ab RahmanEugenie, SinghCorné M.J, PietersePeer M, Schenk Emerging microbial biocontrol strategies for plant pathogens.J.Plant scince.267(102-111).
ShoreshM,HarmanGE,MastouriF(2010).Induced systemic resistance and responses to fungal
biocontrol agents.Annu.Rev.Phytopathol.48:21-43.
Scherm B, Ortu G, Muzzu A, Budroni M, Arras G, Migheli Q (2003) Biocontrol activity of
antagonistic yeasts against Penicillium expansum on apple. J Plant Pathol 85:205–213.
Silva R, Steindorff AS, Ulhoa CJ, Felix RC (2009). Involvement of G-alpha protein GNA3 in production of cell wall-degrading enzymes by Trichoderma reesei (Hypocrea jecorina) during mycoparasitism against Pythium ultimum. Biotechnol Lett 2009; 31: 531-6.
Shah J, Zeier J (2013). Long-distance communication and signal amplification in systemic acquired
resistance. Front. Plant Sci. 4:30.
Saravanakumar D, Ciavorella A, SpadaroD, Garibaldi,A, and GullinoVM L (2008).
Metschnikowia pulcherrima strain MACH1 outcompetes Botrytis cinerea, Alternaria alternata
and Penicillium expansum in apples through iron depletion. Postharvest Biol. Technol. 49, 121–
128.
TooleO and KolterGAR. (1998). "Flagellar and twitching motility are necessary for Pseudomonas
aeruginosa biofilm development". Molecular Microbiology. 30 (2): 295–304.
Takahashi H, Suda T, Tanaka Y, Kimura B (June 2010) "Cellular hydrophobicity of Listeria 31
monocytogenes involves initial attachment and biofilm formation on the surface of polyvinyl
chloride". Lett. Ap Microbiol. 50 (6): 618–25.
Talaro K. P. & Chess B. (2008). Foundations in microbiology. 8Ed. McGraw Hill, New York.TrenbathB(1976).plant intraction in mixed crop community ,Multiple cropping .129-169.
Traquair, J. A., Meloche, R. B., Jarvis, W. R., and Baker, K. W. (1984). Hyperparasitism of Puccinia
violae by Cladosporium uredinicola. Can. J. Bot.62, 181–184.
Thieken A and Winkelmann G, FEMS Microbiol. Lett(1992) 73, 37–41. Capon RJ, Stewart M,
Ratnayake R, LaceyE and GillJH( 2007) J. Nat. Prod., 2007, 70, 1746–1752.
Tiwari,AK (1996). Biological control of chick pea wilt complex using different formulations of
Gliocladium virens through seed treatment. Ph.D. thesis submitted to G. B. Pant University of
Agriculture and Technology, Pantnagar India, p167.Van Lenteren JC, Bolckmans K, Kohl J, Ravensberg WJ, Urbaneja A (2017) Biological control using
invertebrates and microorganisms: plenty of new opportunities..BioControl. doi:10.1007/s10526-
017-9801-4.
Van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural
enemies, but a frustrating lack of uptake. BioControl 57(1):1–20.
Wright GD (2010) Q & A: Antibiotic resistance: Where does it come from and what can we do about
It. BMC Biol. 8:123.
Walters DR, Ratsep J, Havis ND. 2013. Controlling crop diseases using induced resistance: challenges
for the future. J. Exp. Bot. 64:1263–80.
Watnick P, Kolter R. ( 2000). "Biofilm, city of microbes". Journal of Bacteriology. 182 (10):
2675–2679.
Zeilinger S, Reithner B, Scala V, Peissl I, Lorito M, Mach RL(2006). Signal transduction by Tga3, a novel G protein alpha subunit of Trichoderma atroviride. Appl Environ Microbiol 2005; 71: 1591- 7. Pal K K and B McSpadden Gardener.Biological Control of Plant Pathogens. The Plant Health Instructor. p1-25.
Zeilinger S, Omann M.(2007). Trichoderma biocontrol: signal transduction pathways involved in host sensing and mycoparasitism. Gene Regulation Systems Biol. 1: 227-34.
Waage J and GreatheadDJ (1988). Biological control: challenges and opportunities. In R. K. S. Wood
and M. J. Way (eds.). Biological Control of Pests, Pathogens, a Weeds: Developments and
Prospects. The Royal Soc., London., pp 1-18.
32
Viveros OM, Jorquera MA, Crowley DE, Gajardo G, Mora ML(2010). Mechanisms and practical
considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr. 10:
293- 319.
Van Peer R, Niemann GJ, Schippers B. (1991). Induced resistance and phytoalexin accumulation in
biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r.
Phytopathology 81:728–34.
Vivekananthan R, Ravi M, Ramanathan A, Samiyappan R. (2004). Lytic enzymes induced by
Pseudomonas fluorescens and other biocontrol organisms mediate defence against the
anthracnose pathogen in mango. World Journal of Microbiology and Biotechnology 20(3), 235–
244.
Winkelmann G, Drechsel H. 1997 Microbial siderophores. In: Kleinkauf H, Do¨hren Hvon, eds. Products
of Secondary Metabolism. 7 Weinheim: VCH Verlagsgesellschaft, pp. 199–246.
Yoon H, Klinzing G, Blanch H (1977).Competition for mixed substrates by microbial populaations,
Biotechnol.15(257-262).
Zipfel C (2009). Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 12:414–
20.
Zajc J, Gostincar C, Cernosa A, GundeCimerman N (2019) Stresstolerant yeasts: opportunistic
pathogenicity versus biocontrol potential. Genes (Basel) 10:42.
Zheng L, Zhao J, Liang X, Zhan G, Jiang S, and Kang Z (2017). Identification
of a novel Alternaria alternata strain able to hyperparasitize Puccinia striiformisf. sp. tritici, the
causal agent of wheat stripe rust. Front. Microbiol. 8:71.
.
33