Prospect of Trichoderma As A Potential Fungicide

International Journal of Human Genetics Medical Biotechnology and Microbiological Studies
ISSN (Online) 2319-1732 : Volume 1 , Issue 3 , December 2012

1
http://www.ijhgmbms.info/article/IJHGMBMSV1I301.pdf
PROSPECT OF TRICHODERMA AS A POTENTIAL FUNGICIDE

Th. Kamala
1
and S. Indira
1*

1
Microbial Resources Division, Institute of Bioresources & Sustainable Development,
Department of Biotechnology, Govt. of India, Takyelpat, Imphal, Manipur 795001, India.
E mail : sidevi1@yahoo.co.in

Abstract

Trichoderma is one of the best known and well
described biocontrol fungi They are included under the
class Deuteromycetes and order Moniliales (Asexual
classification system) and present in nearly all temperate
and tropical soils. They are strong opportunistics invaders,
fast growing, prolific producers of spores and powerful
antibiotic producers. The antagonistic properties of these
fungus are based on the hyperparasitism, antibiosis,
reduction of the saprophytic ability, induced resistance in
the host plant, competition for nutrients, space and
reducing spore dissemination and restraining of
pathogenecity factors of the pathogens which may act co-
ordinately. The activation of each mechanisms implies the
production of specific compounds and metabolites, such as
plant growth factors, hydrolytic enzymes, siderophores,
antibiotics, carbon and nitrogen permeases etc. With the
increasing awareness and public perception regarding the
toxicity levels of concentration or accumulation of
chemical insecticides and pesticides in soil environment,
the use of microbial biocontrol agents to lower inoculum
density of the pathogen in order to reduce the disease
intensities, is a potential nonhazardous alternative. And
the emergence of Trichoderma spp. as effective biological
control agents of the pathogens and as a plant growth
enhancers, has come parts of the world.

Key words: Antibiosis, biocontrol, induced
resistance, Trichoderma, pathogens.

Postal address, fax and phone number of the corresponding
Author:

*Dr. S. Indira Devi
Scientist, Microbial Resources Division, Institute of Bioresources
and Sustainable Development, An autonomous DBT Institute,
Takyelpat, Imphal-795001, India, Fax: +91-3852446120
Phone : 09436892491, E mail : sidevi1@yahoo.co.in

1. INTRODUCTION
At present around 30 of all plant species have
been destroyed by plant pathogens. The intensified use
of chemical pesticides has resulted in accumulation of
toxic compounds in food chain leading to harzardous
to humans and environment [59] and also in the build
up of resistance of the pathogens [36]. In view of this,
effective alternatives to chemical control are being
investigated and the use of biological control agents
seems to be one of the promising approaches [60].
Biopesticides can decompose more quickly than
conventional chemical pesticides and can supplement
the conventional pesticides when used in integrated
pest management (IPM) programs, which offer
potentially higher crop yield and can dramatically
reduced the use of conventional pesticides [73].
Currently in the market, a number of biologically
based products are being sold for the control of fungal
plant diseases [64]. The use of Trichoderma product
has both short term effects: immediate control of
diseases and growth enhancement of crops as well as
long-term effects which are demonstrated by the
decrease in fungal pathogen inoculum in the field [56].
Trichoderma spp. are free living fungi that are
highly interactive in root, soil and foliar
environments. The most commonly use strains of
Trichoderma biocontrol agents are Trichoderma
virens, Trichoderma viride and Trichoderma
harzianum [32]. It has been known for many years
that they produce a wide range of antibiotic
substances and that they parasitize other fungi. The
success of Trichoderma strains as BCAs is due to
their high reproductive capacity, ability to survive
under very unfavourable conditions, efficiency in the
utilization of nutrients, capacity to modify the
rhizosphere, strong aggressiveness against
phytopathogenic fungi, and efficiency in promoting
plant growth and defence mechanisms. These
properties have made Trichoderma a ubiquitous
genus present in any habitat and at high population
densities [31]. Results from different studies showed
that several strains of Trichoderma had a significant
reducing effect on plant diseases caused by pathogens
such as Rhizoctonia solani, Sclerotium rolfsii,
Pythium aphanidermatum, Fusarium oxysporum, F.
culmorum and Gaemannomyces graminis var. tritici
under greenhouse and field conditions [27].
Development of Trichoderma mutants towards
suppression of fungal plant pathogens is an important
method in strain improvement, which yields effective
strains as biological control agents [66]. The UV
mutant of Trichoderma koningii UVTK2 showed
maximum percentage inhibition of mycelial growth

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than other four mutants of Trichoderma koningii [5].
The purpose of this paper is to reviewed and
consolidate the rapidly developing knowledge of the
mechanisms by which Trichoderma spp. provide
beneficial effects in plant growth promotion and
diseases control (Fig.1).

2. DIFFERENT BIOCONTROL MECHANISMS
EXHIBITED BY TRICHODERMA

2.1. INDUCED SYSTEMIC RESISTANCE
Induced systemic resistance (ISR) of plants against
pathogens is a widespread phenomenon that has been
intensively investigated with respect to the underlying
signaling pathways as well as to its potential use in
plant protection. Plants are capable of producing an
immune response after primary pathogen infection
which is known as systemic acquired resistance (SAR).
The activation of SAR correlates with the expression of
pathogenesis related (PR) genes, including acidic and
basic -1,3-glucanase and chitinase, which acts against
the cell walls of the pathogens [33]. Three classes of
compounds produced by Trichoderma and induce
resistance in plants are now known eg. peptides,
proteins and low molecular weight compounds [24].
These compounds induced ethylene production,
hypersensitive responses and other defence related
reactions in plants [55]. The ability of Trichoderma sp.
to induce local and systematic resistance has been
shown with T. harzianum in agricultural crops such as
bean, cotton, tobacco, lettuce, tomato and maize [62].
T. asperellum in cucumber [11] and T. virens in cotton
[11] (table 1). The molecular basis of Trichoderma
strains produce a set of ATP-binding cassette (ABC)
transporters [65]. These include resistance to
environmental toxicants that are produced by soil
microflora or introduced by human activity and
secretion of antibiotics and cell-wall degrading
enzymes that are necessary for establishing of a
compatible interaction with a host fungus.

2.2. COMPETITION
For a Trichoderma species to be rhizosphere
competent, it must colonize the rhizosphere beyond 2
cm. depth from the seed [44] or proliferate to a
concentration that exceeds the initial population coated
on the seed [21]. Rhizosphere competence of a
particular isolate of Trichoderma makes it a successful
biological agent. Trichoderma spp, either added to the
soil or applied as seed treatments, grow readily along
with the developing root system of the treated plant
[39]. In addition, root colonization by these beneficial
fungi also induces significant changes in the plant
metabolic machinery.

2.3. FUNGISTASIS
Good antagonists are usually able to overcome the
fungistatic effect of soil that results from the presence
of metabolites produced by other species, including
plants, and to survive under very extreme competitive
conditions. Trichoderma strains grow rapidly when
inoculated in the soil, because they are naturally
resistant to many toxic compounds, including
herbicides, fungicides and pesticides such as DDT, and
phenolic compounds [31]. Resistance to toxic
compounds may be associated with the presence in
Trichoderma strains of ABC transport systems [24]. In
the relevant study, a number of indigenous
Trichoderma isolates were isolated from different
agro-climatic conditions of NE India with reference to
Manipur and the biocontrol properties of these isolates
were evaluated against Rhizoctonia solani, Fusarium
oxysporum, Pythium ultimum and P. aphanidermatum
using Dual plates assay technique. Among the total
isolates, T. harzianum (T86) showed maximum
inhibition activity against the R. solani, F. oxysporum,
P. ultimum, and P. aphanidermatum (Fig.2) [74].

Fig. 1. Potential Biocontrol activities exhibited by Trichoderma

Fig.2. Antagonistic activity of indigenous Trichoderma against
different Pathogens. A. R. solani, B. F. oxysporum, C. P. ultimum and
D. P. aphanidermatum.


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Table 1. Table showing the effectiveness of Trichoderma species against various pathogens in plants [22].

Species &
strain
Plant Pathogens Evidence or effects Time after
application
Efficacy Reference
T. virens 5-6
G-6-5 and G-
11
Cotton Rhizoctonia
solani
Protection of plants;
induction of fungitoxic
terpenoid phytoalexins
4 days 78% reduction in diseae; ability to
induce phytoalexins required for
maximum biocontrol activity.
[11]
T. harzianum-
T39
Bean Colletotrichum
lindemuthianu;
Botrytis cinera
Protection of leaves when
T39 was present only on
roots.
10days 42% reduction infection area;
number of spreading lesions
reduced.
[33]
T. harzianum
T39
Tamato,
Pepper,
Tobacco,
lettuce, bean
B. cinerea Protection of leaves when
roots.
7days 25-100% reduction in grey-mould
symptoms
[19]
T. asperellum
T-203
Cucumber Pseudomonas
Syringae Pv,
Lachrymans
roots; production of
antifungal compounds in
leave.
5 days Upto 80% reduction in disease on
leaves; 100 fold reduction in level
of pathogenic bacterial cells in
leaves.
[32]

T. harzianum
T22 , T.
Atroviride P1
Bean B.cinerea &
Xanthomonas
Pv. Phasseoli
T22 or P1 was present only
on roots; production of
antifungal compounds in
leaves.
7-10days 69% reduction in grey-mould (B-
cinerea) symptoms with T22; lower
level of control with P1. 54%
reduction in bacterial disease
symptoms.
M.L.,unpubl
ished
observation
T. harzianum
T-1 & T22;
T.virensT3
Cucumber Green-mottle
Mosaic virus
Trichoderma strains were
present only on roots
7 days Disease-induced reduction in
growth eliminated
[21]

T. harzianum
T22
Tomato Alternaria
solani
t22 was present only on
roots.
3 months Upto 80% reduction in early blight
symptoms from natural field
infection
[2]
T. harzianum
T22
Maize Colletotrichum
graminicola
present only on roots
14 days 44% reduction of lesion size on
wounded leaves; no disease on
non-wounded leaves.
[22]
Trichoderma
GT3-2
Cucumber C.orbiculare,
P. syringae,
Pv.
Lachrymans
present only on roots;
induction of lignification
and superoxide generation
1 day 59% & 52% protection from
disease caused by C. orbiculare or
P. syringae, respectively.
[50]
T. harzianum Pepper Phytopthora
capsici
Protection of stems when
present only on roots;
enhanced produced of the
phytoalexin capsidiol
9 days Nearly 40 % reduction in lesion
length
[58]
T. harzianum
NF9
Rice Magnaporthe
grisea;
Xanthomonas
oryzae
pv.oryzae
NF-9 was present only on
roots
14 days 34-50% reduction in disease Tong Xu,
unpublished
observation.

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2.4. COMPETITION FOR NUTRIENTS
Starvation is the most common cause of death for
microorganisms, so that competition for limiting nutrients
results in biological control of fungal phytopathogens [31].
For instance, in most filamentous fungi, iron uptake is
essential for viability [48] and under iron starvation, most
fungi excrete low-molecular weight ferric-iron-specific
chelators, termed siderophores, to mobilize environmental
iron [48]. Some Trichoderma BCAs produce highly
efficient siderophores that chelate iron and stop the growth
of other fungi [30]. For this reason, soil composition
influences the biocontrol effectiveness of Pythium by
Trichoderma according to availability. The efficient use of
available nutrients by Trichoderma is based on the ability
of Trichoderma to obtain ATP from the metabolism of
different sugars, such as those derived from polymers and
all of them rendering glucose [31].

2.5. PLANT ROOT COLONIZATION

Trichoderma strains must colonize plant roots prior to
stimulation of plant growth and protection against
infections. Colonization implies the ability to adhere and
recognize plant roots, penetrate the plant, and withstand
toxic metabolites produced by the plants in response to
invasion by a foreign organism, whether plant pathogen or
not. There are no data in the literature concerning
Trichoderma genes specifically expressed during the
interaction between fungus and plant roots, but there are
several reports on altered gene expression during
mycorrhizal development [57]. Some Trichoderma strains
establish long-lasting colonization and penetrate into the
epidermis. There they produce or release compounds that
induce localized or systemic plant resistance responses,
plant reacts against fungal invasion by synthesizing and
accumulating phytoalexins, flavonoids, terpenoids,
phenolic derivatives and other antimicrobial compounds.
Trichoderma strains are generally more resistant to these
compounds than most fungi [24].

2.6. PLANT GROWTH PROMOTING
ACTIVITY

Root colonization by Trichoderma strains frequently
enhances root growth and development, crop
productivity, resistance to abiotic stresses and the uptake
of nutrients [14]. Crop productivity in fields can increase
up to 30% after the addition of Trichoderma hamatum or
Trichoderma koningii [24] (fig.3). Trichoderma strains
that produce cytokinin - like molecules, eg. Zeatyn and
gibberellin GA3 or GA3- related have been recently
detected. The controlled production of these compounds
could improve biofertilization [29]. Together with the
synthesis or stimulation of phytohormone production,
most Trichoderma strains acidify their surrounding
environment by secreting organic acids, such as gluconic,
citric or fumaric acid [20]. These organic acids are able to
solubilize phosphates, micronutrients and mineral cations
including iron, manganese and magnesium [24]. Pill et
al. [76] have attributed many factors to the growth
promoting properties of some Trichoderma isolates,
including increased plant growth hormone synthesis,
enhanced nutrient uptake, enhanced dissolution of soil
nutrients, enhanced root development, increased root hair
production and deeper rooting. Using T. harzianum
through soil mixing plus root dipping method of
treatment gave the best values of mineral contents in
broccoli leaves in two crop seasons [67].

2.7. MYCOPARASITISM
Mycoparasitism, the direct attack of one fungus on
another, is a very complex process that involves
sequential events, including recognition, attack,
subsequent penetration and killing of the host. It is
believed that fungi secrete exochitinases constitutively at
low levels. When chitinase degrade fungal cell walls, they
Fig. 3. Plant growth promotion effects of Trichoderma spp. strains
on : pepper (top), lettuce (lower left) and tomato (lower right)
plants grown in the greenhouse [27].


5
release oligomers that induce exochitinases and attack
begins [50]. During this process Trichoderma secrets cell
wall degrading enzymes (CWDEs) that hydrolyze the cell
wall of the host fungus, subsequently releasing oligomers
from the pathogen cell wall [8]. It is believed that
Trichoderma secretes hydrolytic enzymes at a constitutive
level and detects the presence of another fungus by
sensing the molecules released from the host by
enzymatic degradation [24]. Once the fungi come into
contact, Trichoderma spp. attach to the host and can coil
around it and form appressoria on the host surface.
Attachment is mediated by the binding of carbohydrates
in the Trichoderma cell wall to lectins on the target fungi
[46]. (fig.4). Its mycoparasitism involves a
complementary action of antibiosis, nutrient competition
and cell wall degrading enzymes such as chitinase, -1,3-
glucanases and proteases.

2.8.PRODUCTION OF CELL WALL
DEGRADING ENZYMES (CWDES)

Many CWDEs from different Trichoderma strains have
been purified and characterized [49]. It has been shown
that -1,3- glucanases inhibit spore germination or the
growth of pathogens in synergistic cooperation with
chitinases [71] and antibiotics [24]. Many -1,3-
glucanases have been isolated, but only a few genes have
been cloned, eg, bgn 13.1 [71] and lam 1.3 [58] from T.
harzianum, glu 78 [58] from T. atroviride, and Tv-bgn 1
and Tv- bgn 2 [15] from T. virens. Since chitin is the major
component of most fungal cell walls, a primary role has
been attributed to chitinases in the biocontrol activity of
Trichoderma [23]. Chitinase enzyme can be secreted
from different Trichoderma spp. and degrade the cell wall
of many phytopathogens. During our study, we have
assayed the chitinase activity of the indigenous
Trichoderma isolates (fig.5). Proteases are another group
of enzymes that break down (hydrolyze) peptide bonds of
proteins. Proteases involved in the degradation of
heterologously produced proteins have been characterized
[29]. For example, alkaline protease Prb 1 from T.
harzianum IMI 206040 has been demonstrated to play an
important role in biological control [71] and prb1
transformants showed an increase of upto fivefold in the
biocontrol efficiency of Trichoderma strains against R.
solani. The role of proteases in mycoparasitism has been
reinforced with the isolation of new protease -
overproducing strains of T. harzianum [3]. De Marco and
Felix [40]observed that the biocontrol potential of an
Indian Trichoderma isolate against C. perniciosa was due
to protease activity. Once Trichoderma is attached, it coils
around the pathogen and forms the appresoria. The
following step consists of the production of CWDEs and
peptaibols [10], which facilitate both the entry of
Trichoderma hypha into the lumen of the parasitized
fungus and the assimilation of the cell-wall content (fig. 4).

2.9. SECONDARY METABOLITES

Secondary metabolites are heterogenous group of
natural compounds that are produced by
microorganisms. Trichoderma produces a plethora of
secondary metabolites with biological activity [41].
These compounds possess diverse structures which
belong to different classes of molecule and accordingly
Fig. 4. Scanning electron micrographs of Trichoderma spp. hyphae
interacting with those of Rhizoctonia solani or Sclerotium rolfsii. I.
Condensed coiling of Trichoderma hamatum around a hypha of R.
solani (XI, 700). 2, Hooks of T. hamatum attached to a hyphae of R.
solani (XI, 800). 3, Appressorium like structure, formed by T.
hamatum, attached to a hyphae of R. solani. Note partial degradation of
host cell wall (X8,300). 4, Hypha of T. hamatum coiling around and
penetrating one [73].

Fig.5.Graphs showing the enzymatic activity of some selected
Trichoderma isolates from NE India. (Each bar represents the average
of three independent measurements).


6
possess a range of bioactives properties [31] (table.2).
The earlier studies revealed that antimicrobial
metabolites produced by Trichoderma is effective
against a wide range of fungal phytopathogens eg.,
Fusarium oxysporum, Rhizoctonia solani, Curvularia
lunata, Colletotrichum acutatum, Colletotrichum
lagenarium and Colletotrichum gloeosporioides etc.
[68]. Also it is found that there is large variety of
volatile secondary metabolites produced by
Trichoderma such as Ethylene, Hydrogen cyanide,
Aldehydes and Ketones which play an important role in
controlling the plant pathogens [4]. The production of
secondary metabolites by Trichoderma spp. is strain
Trichoderma spp. are known to produce a number of
antibiotics such as Trichodernin, Trichodermol,
Harzianun and Harzianolide [7]. The combination of
hydrolytic enzymes and antibiotics results in a higher
level of antagonism than that obtained by either
mechanism alone [9]. From different Trichoderma
dependent and includes antifungal substances
belonging to a variety of classes of chemical
compounds. They were classified by Ghisalberti and
Sivasithamparam [17] into three categories (i) Volatile
antibiotics, (ii) water-soluble compounds, (iii)
peptaibols [72]. It is important to mention that
biocontrol strains, seven known compounds were
extracted, isolated and characterized from fungal
culture filtrates; (1)T22 azaphilone; (2)T39 butenolide;
(3) harzianopyridone;(4) harzianolide; (5) 1-hydroxy-3-
methyl-anthraquinone; (6)1,8-dihydroxy-3-methyl-
anthraquinone and (7) 6PP [20] (fig. 6).

Fig. 6. Secondary metabolites produced by Trichodermaspp.
Level of production = not produced; + produced (05 mg
L
1
); ++ produced (525 mg L
1
); +++ produced (2550 mg
L
1
) [18].
3. INFLUENCE OF ENVIRONMENTAL
PARAMETERS ON TRICHODERMA STRAINS
WITH BIOCONTROL POTENTIAL

Temperature is a key parameter to manipulate for
growth, sporulation and saprophytic ability as well as
production of volatile and non-volatile metabolites,
involved in nutrition, competition, mycoparasitism, and
extra cellular enzymes that disintegrate cell wall of
fungi. It has been demonstrated that Trichoderma
strains are active under a wider range of temperature
[47]. The optimum temperature for growth differs
among the Trichoderma isolates; although most
Trichoderma strains are mesophilic [47]. Daneilson and
Davey [61] also reported the difference of optimum
temperature for growth among the Trichoderma
species.
Water conditions have been shown to strongly
affect Trichoderma activities, most particularly spore
germination and germ tube growth and mycelial growth
[54]. They have a critical effect on sporophytic ability
[16] on the interaction with other fungi [18] and on
enzyme production [77]. Information about the
influence of water conditions on metabolic activities of
Trichoderma strains is essential for planning their
pH can also play a role in the regulation of extracellular
enzyme production for -1-6-glucanase of Trichoderma
harzianum [38] The effect of pH in the in vitro
activities of Trichoderma extracellular enzymes was
examined. Optimal pH values were pH=5.0 for -
glucosidase, cellobiohydrolase and NAGase, pH=3.0
for -xylosidase, pH=6.0 for trypsin-like protease and
pH=6.0-7.0 for chymotrypsin-like protease activities
[47]. Extracellular enzymes of the examined
mycoparasitic Trichoderma strains were found to be
able to display activities under wider range of pH
values than those allowing mycelia growth [47]. High
salinity may increase the severity of diseases caused by
a variety of plant pathogens [69], and the search for
new Trichoderma strains capable of overcoming
extreme environmental conditions is timely. Although
Trichoderma is widely used for biological control in
many climatic zones [70], its ability to tolerate salinity
has not been extensively investigated. Saline-tolerant
Trichoderma strains may be implemented in plant
disease management in extreme conditions together
with resistant plants created by traditional breeding or
genetic manipulation efforts.

7

Table.2. Bioactive metabolites from Trichoderma species (Singh and Singh, 2009).

Metabolites Isolated from Biological activity References

Trichodermin, Trichodermol, Sequiterpenoids Trichoderma polysporum and T.
sporulosum
Growth inhibitors [24]

Trichoviridin and isocyanides T. hamatum Inhibited growth of micrococcus
tuleus
[13]

1,3,6,8-tetrahydroxyanthraquinone and 1-acetyl-
2,4,5,7-tetrahydroxy-9,10-anthracenedione
Athroquinone

T. viride Pigments [71]
T-2 toxin T. lignorum Toxin 40

Lignoren sesquiterpenoid T. lignorum HKI 0257 Antibacterial and antifungal
activities
[1]

Lipopeptaibol T. longibrachiatum - [6]

2,4-dihydroxy-3-methoxymethyl-5-
methylacetophenone and 2,4-dihydroxy-3,5-
dimethylacetophenone (clavatol)
T. pseudokonongii - [42]

Octaketide-derived acetal diol T. koningii and T. harzianum Antagonistic activity against
fungus
[17]

Trichodermin T. polysporum and T.
sporulossum
Antibiotic [59]

Bisorbicillinoid Trichoderma spp. USF-2690. - [49]

Demethylsorbicillin and oxosorbicillinol Trichoderma spp. USF-2690 Free radical scavenging activity [48]

Crude extracts T. sect. Pachybasium and T.
sect. longibrachiatum
Antimicrobial activity [35]

Harzianopyridone T. harzianum Antifungal [39]

The implications of the changes may extend
beyond halotolerance and may include additional
characteristics advantageous to biocontrol in changing
environments [25]. There is evidence that isolates with
the highest level of in vitro biocontrol activity may not
perform well in vivo condition since environmental
conditions and competition with other microorganisms
are much more restrictive. The value of this biocontrol
agent also depends on the applicability of selected
isolates to different ecozones [32]. It is therefore,
essential to select Trichoderma isolates under a range
of conditions and to evaluate them for biocontrol
ability.

4. CONCLUSION AND FUTURE PROSPECTS

More than ever before sustainable economy and
protection of our environment are dominant topics in
our everyday life. Research on Trichoderma will help
to mitigate the amount of chemicals being released
into the environment. Investigation on the
mechanisms responsible for the biocontrol exerted by
Trichoderma spp. on several plant pathogens have led
to a better understanding of such mechanisms, as well
as to the isolation of several genes encoding either
enzymes and structural or regulatory proteins, or
components of signaling pathways that are involved
in process such as the specific recognition of hosts by
Trichoderma. The discovery of new potential

8
Trichoderma antagonists will led to new challenges in
research, development and registration of biocontrol
agents in a market where chemical pesticides
dominate. Commercial use and application of
biological disease control have been slow mainly due
to their variable performances under different
environmental conditions in the field. To overcome
this problem and in order to take the biocontrol
technology to the field and improve the
commercialization of biocontrol, it is important to
develop new formulations of biocontrol
microorganisms with higher degree of stability and
survival. In order to have more effective biological
control strategies in the future, it is critical to carry
out more research studies on some less developed
aspects of biocontrol agents, mass production of
biocontrol microorganisms and the use of
biotechnology and nano-technology in improvement
of biocontrol mechanisms and strategies.

ACKNOWLEDGEMENTS: We thanks Department
of Biotechnology for giving financial support during
this work.

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