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Eur J Plant Pathol
https://doi.org/10.1007/s10658-023-02745-5
Unveiling thebiocontrol potential ofTrichoderma
AditiSharma · BhupeshGupta· ShaliniVerma·
JoginderPal· Mukesh· Akanksha·
PraneetChauhan
Accepted: 3 August 2023
© Koninklijke Nederlandse Planteziektenkundige Vereniging 2023
Abstract Trichoderma, a well-known fungal genus
and opportunistic plant symbiont, is a quintessential
alternative to chemicals with great potential to mini-
mize disease incidence. The mycoparasitic ability
along with antibiosis and induction of host immunity
are the main mechanisms of biocontrol by this fun-
gus. Fungi belonging to genus Trichoderma have been
identified as potential biocontrol agents due to major-
ity of isolated antifungal bioactive compounds. This
review summarizes the biological control activity
exerted byTrichodermaspp. against plant pathogenic
fungi, bacteria, viruses, nematodes and insect pests.
In addition, the research on formulations advocates
that encapsulation could be a promising tool for
increasing efficacy and durability of these fungi
under field conditions. Further, advances in different
areas of science and technology would strengthen the
future research on Trichoderma-based products for its
efficient use in agriculture.
Keywords Trichoderma· Biological control·
Bioactive compounds· Parasitism· Formulation
Introduction
Plant pathogens pose a major threat to food security,
and their management has become a big challenge in
modern times. In the name of intensive agriculture,
the indiscriminate use of chemicals has resulted in
negative outcomes in the past few years. Many exam-
ples from previous research into the heavy reliance of
agriculture on synthetic pesticides and fertilizers have
shown negative impacts of these molecules on human
and plant health, the environment, and on the ecosys-
tem (Tilman, 1998 and 1999; Nicolopoulos-Stamati
etal., 2016). Moreover, plant pathogens have become
resistant to several chemicals, and these molecules
also affect non-targeted organisms (Padovani et al.,
2004; Sharma etal., 2019; Topping etal., 2020). The
biological control of pathogens by antagonistic liv-
ing microorganisms is a promising approach for the
management of plant diseases and pests (Ab Rahman
etal., 2018; Ons etal., 2020). There are many bacteria
A.Sharma(*)
College ofHorticulture andForestry, Thunag- Mandi,
Dr. Y. S. Parmar University ofHorticulture andForestry,
Nauni, Solan173230, HimachalPradesh, India
e-mail: aditi.bhardwaj650@gmail.com
B.Gupta· S.Verma· Mukesh· Akanksha
Department ofPlant Pathology, Dr. Y.S. Parmar University
ofHorticulture andForestry, Nauni, Solan173230,
HimachalPradesh, India
J.Pal
Department ofPlant Pathology, CSK Himachal
Pradesh Krishi Vishwavidyalaya, Palampur,
HimachalPradesh176062, India
P.Chauhan(*)
Department ofPlant Pathology, Dr Khem Singh Gill Akal
College ofAgriculture, Eternal University, Barusahib,
SirmourHimachalPradesh173101, India
e-mail: chauhanpraneet78@gmail.com
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(such as Pseudomonas, Bacillus, Paenibacillus, and
Streptomyces), fungi (such as Trichoderma, Glomus,
Beauveria, endophytic fungi) and viruses that are
being deployed for the control of various pests and
pathogens (Latz etal., 2018; Raymaekers etal., 2020;
Sala etal., 2019). Among fungal biocontrol agents the
Trichoderma genus is the most extensively studied and
exploited.
Weindling in 1932 identified the genus Tricho-
derma as having biocontrol potential against plant
pathogens (Weindling, 1932 and 1934). These fungi
are ubiquitous, colonize above and belowground
plant organs, grow as endophytes, and are among
the predominant components of soil mycoflora. The
ability of Trichoderma to sense, invade and attack
pathogenic fungi has been the impelling cause for its
commercial success as biopesticides (Hermosa etal.,
2012; Verma etal., 2007). The use of Trichoderma
harzianum against Sclerotium rolfsii in 1972 was the
first successful example of biocontrol efficacy under
field conditions (Wells et al., 1972). Trichoderma,
a genus of familyHypocreaceae, are asexual fungi
that generally reproduce via chlamydospores, can
survive at different pH ranges, and have an optimum
temperature range of 25–35°C (Shah & Afiya, 2019).
These antagonistic fungi can be most frequently iso-
lated from soils, and temperate and tropical zones
contain approximately 101 –103 culturable spores of
Trichoderma per gram of soil (Vinale etal., 2008).
Generally, the morphological taxonomy of Tricho-
derma is based on fungal hyphae, spore size, shape,
colony color and appearance of mycelium on specific
culture media. However, molecular techniques are
more precise and reliable methods to discover diverse
Trichoderma species (Atanasova et al., 2013; Bis-
settet al., 2003; Hewedy etal., 2020; Kamala etal.,
2015). Due to the diverse use of these fungi, quick
and accurate identification is necessary. Researchers
and taxonomists around the globe have developed a
series of identification tools that make Trichoderma-
based studies more accessible (Dou etal., 2020; Dru-
zhinina etal., 2005; Hebert etal., 2003; Raja etal.,
2017). The genus Trichodermacomprises 495 iden-
tified species based on molecular phylogeny, and
they show a variety of biological activities (Har-
manet al., 2004; Druzhinina etal., 2006; Bissettet al.,
2015; Qin & Zhuang, 2016; Index Fungorum, 2022).
There are several well known species of Trichoderma
such as T. harzianum, T. hamatum, T. asperellum,
T. viride, T. koningii, T. pseudokoningii, T. afro-
harzianum and T. cyanodichotomus that have been
identified as promising biocontrol agents (del Car-
men etal., 2021; Mukherjee etal., 2013). Genomic
studies have facilitated a more advanced understand-
ing of the phylogenetic relationships of these fungi,
together with furthering investigations on sexual
crossings, and their role in ecosystems (Zhou etal.,
2020). The capacity of Trichoderma spp. to produce
different enzymes, antibiotics, to induce resistance in
plants, and to act as parasites of different pathogens,
make these fungi the most studied biopesticide and
biofertilizer (Solanki etal., 2011; Waghunde etal.,
2016). Furthermore, the development of formula-
tions of Trichoderma spp. ensures the protection of
the active ingredient under extreme pH, humidity,
chemicals and UV radiation conditions, giving the
biocontrol fungi a competitive advantage over major
pathogenic microbes. Formulations of Trichoderma
spp have mostly adopted solid or liquid fermentation
technologies together with various organic and inor-
ganic carriers (Sanjeev etal., 2014). Recent advances
in research have shown the use of novel methods for
the development of formulations, which can retain
conidial viability and work well under field con-
ditions (Locatelli et al., 2018; Swain et al., 2021;
Yobo etal., 2019).
Overview ofthegenus Trichoderma
andmechanism ofbiocontrol
The genus Trichoderma, belonging to the fam-
ily Hypocreaceae, is present in all kinds of soils
and can be cultured on artificial media. Persoon, in
1794, first proposed Trichoderma as a genus on the
basis of material collected in Germany. Later, in
1865, the Tulasne brothers in France illustrated the
link between T. viride and Hypocrea rufa (Persoon,
1794; Tulasne & Tulasne, 1865). Similarly, Wein-
dling was a pioneer in proposing Trichoderma as a
fungus that parasitizes other fungi, and demonstrated
its biocontrol potential in 1932 (Mukhopadhyay &
Kumar, 2020). These fungi form filamentous hyphae
with abundant conidiophores. The asexual conidia
are hyaline, elliptical in shape, and form white to yel-
low mycelium and green conidia on culture media
when completely mature (Atanasova et al., 2013;
Jaklitsch, 2009). In agriculture different Trichoderma
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spp, such as T. atrobrunneum, T. afroharzianum, T.
guizhouense, T. harzianum, T. simmonsii, T. asperel-
lum, T. asperelloides, T. atroviride, T. hamatum, T.
gamsii, T. koningii, T. koningiopsis, T. viridescens, T.
citrinoviride, T. longibrachiatum, T. pseudokoningii,
T. saturnisporum, T. cyanodichotomus, T. spirale and
T. polysporum, have been deployed to control various
diseases and insect pests (Mastouri etal., 2012; Rush
etal., 2021; Sood etal., 2020; Woo etal., 2014). The
biocontrol and symbiotic properties of Trichoderma
are the most important factors that determine its
widespread application in agriculture. According to
Rush etal. (2021), of all the fungal biocontrol agents,
50–60% belong to the genus Trichoderma. A recent
review by Tyśkiewicz etal. (2022), states that approx-
imately 77 commercial Trichoderma-based biofun-
gicides are available and approved by the European
Union (Thambugala etal., 2020). The vast majority
of Trichoderma species are not associated with their
sexual state and therefore differentiation of species
within the genus becomes very difficult. However,
enormous advances have been made in the taxonomy
of Trichoderma based on DNA Barcoding and Multi-
locus Identification System (MIST) (Cai etal., 2022;
Tang etal., 2022).
The powerful biocontrol machinery of Tricho-
dermaspp. is the driving unit for its use as prophy-
lactic and curative treatments against plant pathogens,
particularly when chemical methods become inef-
fective or economically unfeasible. Trichoderma is
known to exhibit several direct and indirect biocontrol
mechanisms against different pathogens. The myco-
parasitic effect of Trichoderma involves the sensing
of prey, chemotaxis, adhesion to host surfaces, and
physical attack through coiling and intense branching
of mycelium around the pathogen hyphae (Mukherjee
etal., 2012; López- Bucio etal., 2015; Guler etal.,
2016; Redda et al., 2018). They are also known to
produce low-molecular-weight volatile or nonvola-
tile antibiotics or secondary metabolites that restrict
the growth of pathogens. The fungus releases several
glucanases, chitobioses, chitinase enzymes, antibiot-
ics like viridin, gliotoxin and peptaibols (Dou etal.,
2020). These biocontrol fungi are also considered one
of the richest sources of peptaibols, and over 80% of
peptaibiotics entered in the database is synthesized by
this genus (Neumann etal., 2015). In addition, T. har-
zianum is known to produce harzianic acid that shows
antifungal activity, stimulation of plant growth and
chelating properties (Vinale etal., 2009). It has been
well established that Trichoderma species compete
very well against pathogens for nutrients and space in
the soil and rhizosphere (Solanki etal., 2011). Fungi
belonging to this genus are also well known to indi-
rectly affect pathogenic microbes by inducing local or
systemic defense mechanisms in plants. Trichoderma
activates two types of induced resistance in plants,
i.e. systemic acquired resistance (SAR) and induced
systemic resistance (ISR) (Baiyee etal., 2019; Etim
& Onah, 2022; Shoresh etal., 2010). Besides its bio-
efficacy against pathogens, it has been suggested by
many researchers that the presence of Trichoderma
in rhizosphere leads to increased tolerance towards
abiotic stresses (Ghorbanpour et al., 2018; Tripathi
et al., 2021). Additionally, Trichoderma spp. also
possess plant growth promoting properties (Halifu
etal., 2019). Figure1 depicts the multifaceted role of
Trichoderma.
Antifungal properties ofTrichoderma
Pathogenic fungi cause serious problems to the pro-
duction of agricultural commodities both at pre and
post harvest stages. These fungi exhibit huge vari-
ability in terms of their mode of infection, reproduc-
tion, spore formation and nutritional strategy (Agrios,
2005). They are regarded as one of the dominant
causes of plant diseases. A plethora of strategies to
colonize and invade plants have been developed by
these microbes. They are generally classified into
four different phyla namely, Chitridiomycota, Oomy-
cota, Ascomycota and Basidiomycota. Among these
phyla Synchytrium, Phytophthora, Pythium, Magna-
porthe, Erysiphe, Cladosporium, Botrytis, Fusarium,
Colletotrichum, Rhizoctonia, Puccinia and Ustilago
are some important genera, causing huge economic
losses to crops every year (Doehlemann etal., 2017).
Trichoderma is one of the most widely applied bio-
control agents used in plant disease management. Dif-
ferent species of Trichoderma multiply rapidly, and
advantageously inhibit the growth of fungi by hyper-
parasitic effect (Sreenivasaprasad & Manibhushan-
rao, 1990). There are numerous examples of hyper-
parasitism of Rhizoctonia solani by different species
of Trichoderma by coiling the mycelium of the path-
ogenic fungi (Elad etal., 1983; Inayati etal., 2020;
Naeimi etal., 2010). Recently, hyperparasitism by this
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fungi has also been reported against Epichloespecies
that causes “choke disease” of grasses (Górzyńska
et al. 2018; Węgrzyn & Górzyńska, 2019). It has
been reported that when Trichoderma is cocultured
with Rhizoctonia, hyperparasitic functional genes and
antibiosis genes are upregulated (Halifu etal., 2020).
Rice sheath blight, caused by Rhizoctonia solani,
is one of the major constraints in the production of
Oryza sativa L. (rice) and can be effectively managed
by different species of Trichoderma (Safari Motlagh
etal., 2022). According to Xu etal. (2022), intercrop-
ping of maize and soybean significantly increased
the density and composition of Trichoderma and
antagonized pathogenic Fusarium species in the
rhizosphere. It has also been documented that pro-
tective treatment with T. asperelloidesenhances the
expression of defense genes (viz., PR-1, PR-2, PR-3,
and CHS) resulting in a lower incidence of root rot
in Solanum lycopersicumL. (Heflish etal., 2021). In
addition to this, Trichoderma produces several vola-
tile or nonvolatile compounds that inhibit pathogen
growth. The antibiosis and mycoparasitic activity
of these biocontrol fungi has been shown to reduce
the growth of Rhizoctonia solani, which causes seed
rot in Gossypium L. (Gajera et al., 2020). Cultural
extracts of T. asperellum andMetarhizium anisopliae
inhibit conidial germination, and exhibit chitinolytic
activity against Leveillula taurica (Guigón López
etal., 2019). Trichoderma longibrachiatum produces
several secondary metabolites that inhibit fungal
pathogens such as Colletotrichumlagrnarium, Bot-
rytis cinerea, and Fusarium oxysporum (Du et al.,
2020). Hydrolytic activity of enzymes produced by
T. harzianum, T. guizhouense, T. atroviride and T.
Fig. 1 Multifaceted role of Trichoderma
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koningiopsis also reduced the incidence of Penicil-
lium digitatum Sacc.,Alternaria alternata(Fr.) Keissl
andColletotrichum gloeosporioides (Penz.) Penz. &
Sacc. (Ferreira et al., 2020). Volatile organic com-
pounds of T. asperellum,T. harzianum, andT. atrovir-
ide reduced the growth of Plasmopara viticola (P. vit-
icola,Berk. & M. A. Curtis; Berl. & De Toni), which
causes grapevine downy mildew (Lazazzara et al.,
2021). A recent study reports the mycoparasitic action
of T. asperellum, T. harzianum, T. hamatum, T. vir-
ideand T. longibrachiatum against Biopolaris oryzae,
Rhizoctonia solani, Fusarium semitectumandCurvu-
laria oryzae (Klaram etal., 2022). Further, xylanase
secreted byT. asperellum stimulates systemic resist-
ance in poplar (Populus L.) againstAlternaria alter-
nata, Rhizoctonia solani, and Fusarium oxysporum
(Guo etal., 2021a). Biopriming with Trichoderma is
also an adaptive strategy to enhance the plant defense
against pathogenic microbes. A recent report docu-
mented that plants primed with T. harzianumshowed
higher activity of resistance enzymes (such as super-
oxide dismutase, catalase, peroxide, phenylalanine
ammonia lyase and polyphenol oxide) compared
to plants inoculated with Fusarium oxysporum f.
sp. lycopersici (Zehra etal., 2023). Biocontrol with
T. asperellum induced resistance against Puccinia
striiformis f. sp. tritici, causal agent of stripe rust of
wheat (genus Triticum; L.), as reported by Esmail
et al. (2023). Table 1 depicts some research on the
antifungal effects of different Trichoderma species
against pathogenic fungi in agriculture.
Antibacterial properties ofTrichoderma
Plant pathogenic bacteria cause serious disease out-
breaks in many economically important crops with
severe consequences on food production and secu-
rity. Infected plants exhibit different types of damag-
ing symptoms such as blight, canker, galls and over-
growth, wilts, leaf spots, specks, scab and soft rots
(Agrios, 2005). Phytopathogenic bacteria contain
various virulence factors that enable them to infect
and colonize host tissues successfully. Due to wide
host ranges and the development of antibiotic resist-
ance, their management has become a challenging
task. Thus, many methods are now being adopted
for developing effective strategy to control these
pathogenic prokaryotes. One of the best strategies is
biocontrol of bacterial pathogens with different antago-
nistic microbes (Sharma etal., 2017). The potential of
Trichoderma in controlling the growth of pathogenic
bacteria has been demonstrated by different research-
ers. Different species of Trichoderma have shown
induced resistance against Xanthomonas euvesicato-
riain tomato plants (Fontenelle etal., 2011). Tricho-
derma asperellum produces siderophores, indole-
3-acetic acid, hydrogen cyanide, and salicylic acid.
These secondary metabolites are known to inhibit the
growth of Ralstonia solanacearum that causes wilt
in potato (Solanum tuberosum L.) (Mohamed et al.,
2020). Bacterial pathogens utilize different patho-
genicity factors such as secretion systems (type I, II,
III, IV), quorum sensing (QS), enzymes, toxins, hor-
mones, polysaccharides, proteinases and siderophores
that contribute to disease development in host plants
(Siphathele et al., 2018). Thus, bioactive compounds
secreted by the biocontrol microbes must target these
virulence factors for effective disease control. Bio-
active compounds produced by T. harzianum have
shown high efficacy in inhibiting bacterial patho-
gens such as Xanthomonas campestris, Clavibacter
michiganensis, Escherichia coli, and Pseudomonas
aeruginosa (Anwar & Iqbal, 2017). Biofilm protects
bacteria against adverse environmental conditions and
the quorum sensing mechanism has been targeted by
researchers for management of bacterial pathogens. A
secondary metabolite produced by T. atroviride was
reported to interfere with the gene pathways involved
in biofilm formation of Xanthomonas campes-
trispv.campestris that causes black-rot disease in cru-
cifers (Papaianni etal., 2020). Secondary metabolites
of Trichoderma koningiopsisalso inhibited the growth
of Erwinia mallotivora, the causal agent of papaya
(Carica papaya L.) dieback disease (Tamizi et al.,
2022). Antibacterial enzymes produced by T. harzi-
anumhave shown inhibitory activity against a highly
virulent bacterium, Erwinia amylovora (Smirnova
et al., 2017). Similar activity of Trichoderma spp.
against Erwinia carotovora has been reported by
Sulaiman et al. (2020). Secondary metabolites of T.
koningiopsis have also been shown to have biocontrol
activity against Erwinia mallotivora that causes die-
back in papaya (Tamizi etal., 2022). The potential of
Trichoderma to control other important bacteria such
as Ralstonia solanacearum causing wilt was demon-
strated by different workers. Crude extract contain-
ing secondary metabolites of this fungus when tested
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Table 1 Antifungal action of different Trichoderma species
Trichoderma species Fungal Pathogens Disease Mechanism Reference
T. asperelloidesandT. afroharzianum Erysiphe necator Grapevine powdery mildew Enzymatic distortion of conidial
structure
Sawant etal., 2017
T. longibrachiatum, T. afroharzi-
anum, T. koningiop, T. citrinovi,
T. rossicum, T. gamsii
Fusarium oxysporum, Rhizoctonia
solani and Botrytis cinerea Wilt, blight and rot Mycoparasitism Redda etal., 2018
Trichoderma viride Phytophthora infestans Late blight Induction of resistance Purwantisari etal., 2018
Trichoderma harzianum,
Trichoderma longibranchia-
tum, Trichoderma yunnanense,
Trichoderma asperellum
Colletotrichum gloeospori-
oidesandPhytophthora capsici Tomato anthracnose, Blight and
fruit rot of chilli
Production of cellulases and
chitinases
De la Cruz-Quiroz etal., 2018
Trichoderma harzianum Phytophthora cactorumandPhy-
tophthoraspp.
Collar rot of pear Mycoparasitism Sanchez etal., 2019
Trichoderma asperellum Corynespora cassiicolaandCur-
vulariaaeria Leaf spot of lettuce Induced defense response Baiyee etal., 2019
Trichoderma longibrachiatum Colletotrichum spp. Botrytis
cinerea, and Fusarium oxyspo-
rum
Anthracnose, grey mold rot and
wilt
Secondary metabolite production Du etal., 2020
Trichoderma harzianum,T.
guizhouense,T. atrovirideandT.
koningiopsis
Penicillium digitatum,Alternaria
alternataandColletotrichum
gloeosporioides
Green mould, leaf spot, anthrac-
nose of citrus
Hydrolytic activity of enzymes Ferreira etal., 2020
Trichodermalongibrachiatum, T.
harzianum, T. pleuroti Sclerotinia sclerotiorum,Scle-
rotium rolfsii andFusarium
oxysporum, Macrophomina
phaseolina
Rot, Blight, Wilt and Charcoal
Rot
Mycoparasitism and volatile
organic compounds
Rajani etal., 2021
T. gamsii,T. viridarium,T. hama-
tum,T. olivascens,T. virens,T.
paraviridescens,T. linzhiense,T.
hirsutum,T. samuelsii, andT.
harzianum
Phytophthora cinnamomi Oak Decline Mycoparasitism Ruiz-Gómez & Miguel-Rojas,
2021
Trichoderma asperellum,T. harzi-
anum, andT. atroviride Plasmopara viticola Grapevine downy mildew Volatile organic compounds Lazazzara etal., 2021
Trichoderma erinaceum Pythium ultimum Damping off and root rot Secondary metabolites Siebatcheu etal., 2023
T. asperellum, T. harzianum, T.
hamatum, T. virideand T. longi-
brachiatum
Biopolaris oryzae, Rhizoctonia
solani, Fusarium semitec-
tumandCurvularia oryzae
Brown spot, sheath blight, leaf
blight
Mycoparasitism Klaram etal., 2022
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in vitro and in planta for the management ofbacte-
rial wilt resulted in effective control (Yan & Khan,
2021). Zhang etal. (2022) reported that trichokonins
A, peptaibols produced byTrichoderma longibrachia-
tum SMF2 inhibit the growth of Xanthomonas ory-
zae pv. oryzae with a minimum inhibitory concentra-
tion of 54μg/mL. Trichokonin A resulted in damage
to bacterial cell membranes and loss of permeability.
Similarly, another peptaibol analog (named Trichogin
GA IV) produced by Trichoderma longibrachiatum
has shown antibacterial action against Xanthomonas
campestris pv. campestris that causes black rot of cru-
cifers (Caracciolo etal., 2023). There are reports that
suggest a vital role in defense induction by this fungus
against bacterial blight causing pathogens. Activa-
tion of reactive oxygen species and induction of PR
proteins by T. asperellum was documented against
Xanthomonas oryzae pv. oryzae (Singh etal., 2019).
Recently, Islam etal. (2023) advocated that four strains
of Trichoderma (viz., T. paraviridescens, T. para-
viridescens, T. erinaceumand T. asperellum)induced
resistance against X. oryzaepv.oryzae by upregulating
core defense-related genes such as OsPR1,OsPR10,O
sWR KY4 5, OsWRKY62, OsWRKY71, OsHI-LOX,
and OsACS2 after 24 h of inoculation. The attain-
ment of sustainable bacterial disease management is
extremely difficult and continuously increasing the
amount of dataon the biocontrol potential of Tricho-
derma can play a vital role in generating effective strat-
egies for bacterial disease management. In a recent
study on transgenic plants it was advocated that a gene
encoding a sphingomyelinase, identified in T. harzi-
anum, generated disease resistance to Pseudomonas
syringae pv. tabaci and tolerance to Xylella fastidi-
osa. This gene was expressed in all transgenic tobacco
lines that were tested and can be utilized in molecular
breeding to achieve resistance against pathogens (Ber-
bert etal., 2022). Thus, these findings further strength-
ened the fact of using these potential antagonistic fungi
against bacterial plant pathogens (Table2).
Antiviral properties ofTrichoderma
Plant viruses comprise one of the most important
groups of plant pathogens, sometimes causing up to
100% yield loss due to systemic infection. In the present
scenario, nearly 47% of the emerging and re-emerg-
ing plant pathogens are viruses (Saikia et al., 2022).
Viruses are notorious mesobiotic pathogens that are
responsible for huge economic losses in many crops
due to their ability to sequester and reprogram the host
cellular machinery for their replication. The manage-
ment of viruses is very difficult and indirect due to their
transmission by biotic agents like many insects, fungi
and nematodes. The exploitation of antagonistic poten-
tial, resistance induction and plant-growth-promoting
activities of Trichoderma spp. is a well-investigated
area in plant protection. Therefore, many researchers
have exploited Trichoderma spp. for the management of
viral pathogens through induction of host resistance.
Tobacco mosaic virus (TMV) is a single-stranded
RNA virus that infects many important plant species,
essentially tobacco and tomato plants (Ge etal., 2012;
Scholthof etal., 2011). An endophytic fungal strain,
T. koningii produced 6-pentyl-α-pyrone that induced
systemic resistance in Nicotiana tabacumcv. White
Burley against TMV (Taha et al., 2021). In addi-
tion to this, nigirpexin (azaphilone derivatives), a
compound obtained from one strain of T. afroharzi-
anumhas also shown antiviral activity against TMV
(Xie etal., 2022). Abdelkhalek etal. (2022) reported
the protective activity of T. hamatumagainst tobacco
mosaic virus. Trichoderma inoculated plants showed
significant increases in reactive oxygen species scav-
enging enzymes thereby inducing defence in plants.
Cucumber mosaic virus (CMV) is one of the most
widespread and harmful plant viruses, infecting more
than 1200 plant species worldwide and it is efficiently
transmitted by more than 80 aphid species (Dubey
& Singh, 2010). A strain of T. asperellum induced
resistance against yellow strain ofCucumber mosaic
virus in Arabidopsis plants through salicylic acid
(SA) signaling cascade (Elsharkawy etal., 2013).The
molecular mechanisms underlying T. asperel-
lummediated resistance were revealed as the upregu-
lation of resistance-related genes such as pr1, pal1,
etr1, sod, rip and lox1. This biocontrol fungus also
increased the hydrogen peroxide (H2O2) content in
plants, thereby inducing systemic resistance against
CMV (Tamandegani et al., 2021). T. harzianum in
combination with other biocontrol fungi has proven
to activate resistance against Maize chlorotic mottle
virus(MCMV) andSugarcane mosaic virus(SCMV)
that are generally transmitted by thrips and aphids.
Both of these viruses pose serious threats to cereal
production and result in a severe viral syndrome
known as maize lethal necrosis (MLN)(Kiarie etal.,
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Table 2 Antimicrobial and insecticidal properties of different Trichoderma species
Antibacterial action of Trichoderma
Trichoderma species Pathogens/Pest Disease /Order Mechanism Reference
Trichoderma asperellum Ralstonia solanacearum Wilt Induction of plant resistance Konappa etal., 2018
Trichoderma viride Xanthomonas citri Canker Enzymatic activity Jatav etal., 2018
Trichoderma asperellum Xanthomonas
oryzaepv.oryzae Bacterial blight
of rice
Oxidative burst-mediated
defense
Singh etal., 2019
Trichoderma atroviride Xanthomonas campes-
trispv.campestris Black rot Antibiofilm activity of
metabolite
Papaianni etal., 2020
Trichoderma harzi-
anum,Trichoderma
virideandTrichoderma
virens
Pectobacterium carotovo-
rumsubsp.carotovorum Soft rot Growth inhibition Abd-El-Khair etal., 2021
Trichodermaharzianum,T.
virensandT. koningii Ralstonia solanacearum Wilt Secondary metabolites Guo etal., 2021b
Trichoderma harzianum Clavibacter michiganen-
sissubsp.michiganensis Tomato wilt Antagonistic activity Abo-Elyousr etal., 2022
Trichoderma koningiopsis Erwinia mallotivora Papaya Dieback Secondary metabolites Tamizi etal., 2022
Antiviral action of Trichoderma
Trichoderma sp. Zucchini yellow mosaic
virus (ZYMV)
Squash Induction of systemic
resistance
Abdel-Shafi etal., 2013
Trichoderma harzianum Cucumber mosaic
virus(CMV) Solanum lycoper-
sicum
var.cerasiforme
Induced systemic resistance Vitti etal., 2016
Trichoderma albolutescens Pepper mottle virus (PMV) Tobacco and hot
pepper
Antiviral Trichothecenes Ryu etal., 2017
Trichoderma koningii Tobacco mosaic
virus(TMV)
Tobacco Increased the activities
of pathogenesis-related
enzymes
Taha etal., 2021
Trichoderma asperellum,
Trichoderma longibra-
chiatum, and Trichoderma
asperlloides
Tomato yellow leaf curl
virus (TYLCV)
Tomato Resistance Al Abedy etal., 2021
Trichoderma harzianum Papaya ringspot virus
(PRSV) Cucumeropsis
mannii Resistance induction Etim & Onah, 2022
Nematicidal action of Trichoderma
Trichoderma longibrachiatum Heterodera avenae Molya disease of
wheat
Direct parasitic and lethal
effect on eggs and
resistance induction
Zhang etal., 2017
Trichoderma atroviridae Globodera rostochiensis Golden potato
cyst
Chitinolytic activity Abbasi etal., 2017
Trichoderma atroviride Meloidogyne javanica Root-knot Induction of plant resistance Medeiros etal., 2017
Trichoderma harzianum Meloidogyne incognita Root-knot Induction of plant resistance Singh etal., 2017
Trichoderma asperellum,T.
atroviride,Trichodermasp. Meloidogyne javanica Gall Reduction of gal egg
mass and eggs
Kiriga etal., 2018
Trichoderma viride Meloidogyne javanica Root-knot Direct antagonism, lytic
enzymes production and
induction of defense
responses
Hajji-Hedfi etal.,2021
T. harzianum Meloidogyne incognita Root-knot Secondary metabolites
and defense-related
enzyme activity
Yan etal., 2021
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2020). Whitefly transmitted pepper leaf curl virus
(PeLCV) is also a cosmopolitan plant virus that ham-
pers a wide range of crops. The suppressive effects
of T. polysporum, T. atroviridae, T. harzianum and
their consortia were analyzed against PeLCV by
Rochal etal. (2021). In this study, authors reported
Trichoderma-induced innate host immunity prim-
ing and stress tolerance in plants against Pepper leaf
curl virus. The role ofTrichoderma in triggering the
plant immunity has been studied in isolation both at
the local and systemic level. In this context, various
signature molecules fromTrichoderma,together with
their roles in activating the plant immune responses,
have been identified (Salwan et al., 2022). Table 2
depicts the research findings of different research-
ers advocating for the biocontrol potential of Tricho-
dermaagainst viruses.
Nematicidal properties ofTrichoderma
Nematodes are ubiquitous, free-living microscopic
entities that result in 12—25% annual losses in sev-
eral economically important crops (Agrios, 2005;
Bernard etal., 2017; Jones etal., 2013; Nicol etal.,
2011; Seinhorst, 1970). There are more than 4100
plant parasitic nematodes, of which the root-knot
nematodes and cyst nematodes have the most detri-
mental effects on crops (Decraemer & Hunt, 2006;
Jones et al., 2013; Mai & Abawi, 1987). Efficient
eco-friendly methods are necessary for the manage-
ment of nematodes, as nematicides lead to environ-
mental hazards and resistance development (Chen
etal., 2020). Therefore, researchers are focusing on
the use of biocontrol methods against nematodes to
reduce the losses to agricultural comodities (Moosavi
& Zare, 2020).
Along with other antagonistic fungi, significant
research has been carried out on the use of various
Trichoderma spp. for controlling plant-parasitic nem-
atodes (Sharon etal., 2011). The direct antagonistic
mechanism of these fungi against nematodes involves
parasitism of nematode eggs and juveniles, conidial
attachment on the nematode surfaces, hyphae coiling
around second generation juveniles, and enzymatic
lysis of eggs (Sahebani & Hadavi, 2008). Tricho-
derma harzianum possesses strong egg-parasitic
ability, and the chitinolytic enzymes produced by the
Table 2 (continued)
Trichoderma asperellumand
Trichoderma harzianum Pratylenchus brachyurus Root lesion Non-volatile metabolites de Oliveira etal., 2021
T. citrinoviride, T. ghanense,
T. harzianum, T. koningi-
opsis, T. simmonsii, and
T. virens
Meloidogyne javanica and
M. incognita Root-knot Sesquiterpene and pol-
yketide-like metabolites
Moo-Koh etal., 2022
Insecticidal action of Trichoderma
T. longibrachiatum Leucinodes orbonalis Lepidoptera Parasitism Ghosh & Pal, 2016
T. longibrachiatum Bemisia tabaci Hemiptera Parasitism Anwar etal., 2016
T. viride Corcyra cephalonica Lepidoptera Production of antifeedant
compounds
Vijayakumar and Alagar,
2017
T. harzianumT. atroviride T.
citrinoviride Xylotrechus arvicola Coleoptera Parasitism Rodríguez-González
etal., 2017
T. viride T. harzianum Odontotermes formosanus Blattodea Repellent activity Xiong etal., 2018
Trichoderma sp Aphis gossypii Hemiptera Secondary metabolites
toxicity
Nawaz etal., 2020
Trichoderma sp. Locusta migratoria Orthoptera Secondary metabolites
toxicity
Laib etal., 2020
Trichoderma koningiopsis Diatraea saccharalis Lepidoptera Enhanced insecticidal
activity of Beauveria
bassiana
Mejía etal., 2021
Trichoderma chlorosporum Philaenus spumarius Hemiptera Secondary metabolites
toxicity
Ganassi etal., 2022
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fungi results in lysis of nematode eggs (Szabó etal.,
2012). The reduction in nematode infestation by chi-
tinase and protease production is the most important
attribute in Trichoderma biocontrol (Sharon et al.,
2011). Chitinolytic activity of T. asperelloides has
been recorded against M. incognita (Sayed et al.,
2019). In addition to enzyme activity, a significant
antibiosis effect of different secondary metabolites of
T. harzianumisolates has been reported that result in
strong mortality of nematode juveniles (Babu etal.,
2019). Nematicidal metabolites of this fungi have
been isolated and characterized by different workers,
and are categorized as acetic acid, gliotoxin, trichor-
zianine, viridin trichodermin and cyclonerodiol
(Li etal., 2007; Zhou et al., 2018; Shi etal., 2020).
Several compounds classified in the koninginins
group, isolated from solid fermentation products
ofT. neokongii, also showed nematicidal properties
(Lang etal., 2015; Zhou etal., 2014). Similarly, dif-
ferent nematicidal compounds from diverse species
of Trichoderma are being harnessed to develop for-
mulations against parasitic nematodes such asMeloi-
dogyne incognita,M. javanica,M. hapla, Globodera
pallida,Heterodera avenae,andPratylenchus brach-
yurus (Braithwaite et al., 2016; Tariq-Javeed etal.,
2021). Sesquiterpene and polyketide-like metabo-
lites, produced by strains of T. harzianum, T. kon-
ingiopsis, T. ghanense, and T. virens, have shown
51–100% mortality of second-stage juveniles of M.
javanica and M. incognita (Moo-Koh etal., 2022).
Volatile organic compounds (VOCs) of Trichoderma
inhibit populations of Panagrellus redivivus, Cae-
norhabditis elegans, and Bursaphelenchus xylophi-
lus (Yang et al., 2012). Besides these mechanisms,
the role of induced systemic resistance (ISR) has
been well documented in recent years (Goverse &
Smant, 2014). Current research is focusing on uti-
lizing jasmonic acid regulated defences by Tricho-
derma against nematodes (Martínez-Medina et al.,
2017). There are reports that support the mecha-
nism of induced systemic resistance by Trichoderma
against M. incognita (Pocurull et al., 2020). Nowa-
days, different species of Trichoderma are being
deployed that show lethal effects against nematodes
(Elgorban etal., 2014; Braithwaite etal., 2016; Fan
etal., 2020).Trichoderma harzianumandT. asperel-
lum have shown biocontrol potential against juve-
niles of M. javanica in banana (Genus Musa L.)
(Almeida etal., 2022). There are various examples of
the nematicidal effect of different Trichoderma spp.
and their mode of action (Table2).
Insecticidal properties ofTrichoderma
Insects are considered important pests in agricultural
and horticultural production systems, causing huge
losses to crops during both production and storage.
According to recent estimates, insect pests result in
18- 25% average losses in agricultural productivity
worldwide. These losses are generally more common
in food-deficit regions with fast-growing populations,
and may also be due to emerging or re-emerging pests
(Srivastava & Subramanian, 2016). However, indis-
criminate use of pesticides for controlling insect pests
has led to pollution of soil, water, food sources, as
well as poisoning of nontarget insects and the devel-
opment of resistance. To obviate these harmful effects
and obtain higher yields, biocontrol of insect pests
using specific antagonistic microbes is an effective
alternate strategy (Sindhu etal., 2017). The manage-
ment of these insect pests is very difficult, and several
workers are concentrating on using ecofriendly meth-
ods to manage them (Litwin etal., 2020; Manivel &
Rajkumar, 2018). There are many reports that have
determined the insecticidal potential of Trichoderma
in various crops (Battaglia et al., 2013; Contreras-
Cornejo et al., 2018; Coppola et al., 2019; Muvea
etal., 2014).
Many Trichoderma spp. are capable of actively
parasitizing the bodies of insects. The vast major-
ity of research studies carried out in this area have
reported different percentages of insect mortality. It
was reported that T. longibrachiatum and T. harzi-
anum are able to parasitize adult hemipterans such
as Bemisia tabaci Gennadius and Cimex hemipterus
L., causing mortality rates of 40% and 90% within
5 -14days, respectively (Anwar etal., 2016; Zahran
etal., 2017). Secondary metabolites (peptaibols) of
T. atroviride and T. harzianum resulted in mortality
rates of 100% in 15days in red flour beetle (Tribo-
lium castaneum Herbst), wheat aphids (Schizaphis
graminum Rondani and Diuraphis noxia Kurdj) and
the cotton aphid (Aphis gossypii Glover, Amrasca
bigutulla bigutulla Ishida) (Nawaz et al., 2020;
Rahim & Iqbal, 2019). Fungal chitinases have been
exploited to combat losses caused by insect pests.
Chitinolytic enzymes derived from T. viride were
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examined in vitro and in vivo to target the peri-
trophic matrix of Lepidopteran insects (Berini
et al., 2016). These chitinases are known to attack
the insect cuticle. Field inoculation with T. harzi-
anumin the rhizosphere of maize plants resulted in
alterations in the arthropod community by activating
defense responses against herbivory. Furthermore,
research showed a reduced abundance of specific
insects under field conditions (Contreras-Cornejo
et al., 2021). Antifeedant activity of some com-
pounds, such as methyl linoleate and linoleic acid,
produced by these biocontrol fungi has been reported
against hemiptera (Kaushik et al., 2020). Recently,
a Trichoderma sp. was exploited to control a leaf-
cutting ant (Cotazo-Calambas et al., 2022). There
are some examples that advocated the activation of
resistance to insect pests by Trichoderma. This bio-
control fungus has been shown to induce jasmonic
acid (JA) mediated resistance against the scale insect
Unaspis mabilis Lit & Barbecho (Silva etal., 2019).
Similarly, activation of salicylic acid (SA) mediated
resistance in tomato plants against Bemisia tabaci
was also reported by Jafarbeigi etal. (2020). Use of
Trichoderma against various insects and its mode of
action are well documented in Table2. However, it is
necessary to note that the majority of studies exam-
ining Trichoderma as a mycopesticide were carried
out under controlled conditions. Thus, a greater num-
ber of investigations under field conditions should be
performed. Furthermore, an emphasis on the possi-
ble effects of Trichoderma on natural enemies should
be conducted simultaneously. Nevertheless, the
direct and indirect effectiveness of these fungi make
it a sustainable alternative for use in the management
of insect pests.
Bioactive compounds secreted byTrichoderma
Current research on phytoprotection has shown that
bioactive compounds play a vital role in ecofriendly
disease management systems. These compounds
consist of alkaloids, flavonoids, terpenes, phenolic
acids, salicylic acids and benzoic acid, and play a
pivotal role in host resistance induction against dif-
ferent pathogenic microbes and pests (Manganyi &
Ateba, 2020; Sharma etal., 2023). Trichoderma spp.
are known to produce a plethora of bioactive com-
pounds that includes alkenes, ketones, alcohols,
esters, monoterpenes and sesquiterpenes that induce
plant growth and reduce biotic and abiotic stress
(Bisen etal., 2016). These secondary metabolites are
involved in multifarious roles in different fields of sci-
ence and technology. Bioactive compounds auch as
Trichocaranes, Koninginins, Trichosetin, Cyclonero-
diol, Harzianolide, Trichokonin, Viridiol and 6-pen-
tyl-2H-pyran-2-one are secreted by different species of
Trichoderma and are known to regulate plant growth
(Bononi et al., 2020; Keswani et al., 2014). Several
metabolites such as Viridepyrone, Massoilactone,
Koninginins, Viridin, Viridiofungins, Harzianopyri-
done, T22 azaphilone, Harzianolide, Trichostroma-
ticins and Harzianic acid have shown antimicrobial
action and are used in biocontrol (Khan etal., 2020).
Trichoderma citrinoviride is known to produce sec-
ondary metabolites known as bisorbicillinoids that
are known to affect the feeding preference of the
aphidSchizaphis graminum Rondani (Evidente etal.,
2009). Gliotoxins, produced by Trichoderma spp.,
exhibit bioactivity against some human and plant
pathogenic fungi. Trichoderma virens produces glio-
toxin that shows an inhibitory effect against Rhizoc-
tonia bataticola, Macrophomina phaseolina, Pythium
debaryanum, Sclerotium rolfsii and Rhizoctonia solani
(Scharf etal., 2016; Shyamli etal., 2005). There are
reports that advocate the antifungal effect of Tricho-
derma metabolites against Fusarium oxysporum, Bot-
rytis fabae and other soil borne fungi under field con-
ditions (Barakat etal., 2014; Zhang etal., 2014).
A newly identified species of T. phaya-
oense increased plant height, shoot and root dry
weight values and was able to tolerate metalaxyl at
recommended dosages. In addition to its plant growth
promoting ability, this fungus effectively controlled
gummy stem blight and wilt of Cucumis melo L.
(muskmelon) (Nuangmek etal., 2021). Nevertheless,
antimicrobial compounds such as 1- pentanol, 1-hex-
anol, myristonyl pantothenate, bisabolol,
d
-Alanine,
and diethyl trisulphide, secreted by T. longibrachia-
tum, showed potential plant growth promotion and is
reported to trigger amino sugar metabolism in plants
against Macrophomina phaseolina (Sridharanet al.,
2021). It has been reported that volatile compounds
identified as alkenes, alkanes, and esters produced
by T. koningiopsis exerted biocontrol action against
fungi by suppressing plant disease and promoting
plant growth (You etal., 2022). A recent report advo-
cates that T. asperellum promotes pea growth, and
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secondary metabolites play a vital role in suppression
of Globiosporangium ultimum (Moussa etal., 2023).
T. asperellumhas also been reported to promote the
growth of Allium cepa L. (onion) plants by increasing
photosynthetic activity, peroxidase activity and con-
tent of phenolic compounds (Rodríguez-Hernández
etal., 2023). In addition, Trichodenones, Trichoder-
mamide B, Harzianum A, Aurocitrin, Harziphilone,
Viridin, Virone, Viridiofungin etc. are used as anti-
cancer agents (Ebrahimi etal., 2021). Table3 depicts
the application of various bioactive compounds
produced by Trichoderma. Thus, it is evident that
the study of bioactive volatile compounds of Tricho-
derma has emerged as a frontier area of research in
recent years. Although this area of research is devel-
oping, the emergence of recent techniques has played
a vital role in the identification and characterization
of these volatile compounds. Recently, the coupling
of modern omics technology has opened up new areas
of research on these bioactive compounds.
Trichoderma bioformulations forefficient
application
The recent shift from application of synthetic fertiliz-
ers and pesticides to organic methods has brought into
focus the use of microbes that carry analogous functions
in agriculture. The bioformulations that are available in
global markets comprise of talc, liquid and secondary
metabolite based formulations. For the development of
efficient formulations, different factors such as selection
of potent antimicrobial strains, their shelf life, storage,
quality control, application, biosafety and registration are
taken into account. It has been well documented in the
above sections that several species of Trichoderma pos-
sess such biocontrol ability. For commercialization, the
mass multiplication of Trichoderma is of utmost impor-
tance. Researchers around the globe have adopted dif-
ferent formulation strategies such as the use of carboxyl
cellulose vermiculite, powders (such as talc, kaolin,
chitosan, vermiculite, ethyl cellulose, biochar, peat, and
arabic gum), alginate capsules, microencapsulation, dis-
persible granules, and seed coatings for effective delivery
of this bioagent (Lewis & Lumsden, 2001; Sriram etal.,
2011; Swaminathan etal., 2016). To address the draw-
backs of low viability and short shelf life of the biocon-
trol agent during storage, microencapsulation had been
developed. This process involves coating of the active
substances by extremely small capsules, providing the
living cells with a physical barrier against the external
environment. It has been documented that microencap-
sulation of T. harzianum in maltodextringum arabic
resulted in the highest conidial survival after spray-dry-
ing compared to nonencapsulated conidia (Muñoz-Cel-
aya et al., 2012). In another study, the development
of Trichoderma sp. formulations in encapsulated gran-
ules (CG) ensured better stability of formulations due to
good interaction between the alginate matrix and the pol-
ymers used in the formulation. It was also advocated that
this method enhanced the viable cell concentrations of
Trichoderma above 106CFU/g after 14months of stor-
age at 28°C (Locatelli etal., 2018). Further, granular and
liquid formulations of T. asperellum improved its antago-
nism against Rhizoctonia solani on corn seedlings (Her-
rera et al., 2020). Encapsulation of T. harzianum with
nanocellulose and carboxymethyl cellulose is docu-
mented to favor the fungal growth due to the extra carbon
source. These compounds are actively used as promising
materials for protecting and delivering microbial inocu-
lants (Brondi etal., 2022). Recently, Santos-Díaz et al.
(2022) described a step-by-step protocol for the stor-
age stability and partical size determination of Tricho-
dermaspp. in hydrogel beads. Encapsulation in hydrogel
beads provides an effective carrier and long-lasting bio-
product. Pradhan etal. (2022) evaluated the performance
of two types of formulations (tablet and powder based)
of Trichoderma viride against Fusarium wilt disease in
chickpea (Cicer arietinumL.). Under field conditions the
biocontrol potential of the powder based formulation was
superior for reducing wilt incidence. Table3 depicts the
recent research that advocates the use of different for-
mulations of Trichoderma and its bioefficacy. For large
scale promotion of Trichoderma formulations, it is neces-
sary to strengthen research-industry partnerships to scale
up production and delivery systems of these biocontrol
agents.
Conclusion andfuture perspectives
Trichoderma is lucratively used as potent biocontrol
agents worldwide due to its prominent antimicrobial
activity against a broad range of phytopathogens and
insects. Undoubtedly, the chemically diverse second-
ary metabolites produced by these fungi are the main
source of their efficient biocontrol potential. Mul-
tiple strategies have been adapted for development
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Table 3 Application of bioactive compounds and formulations produced by Trichoderma species
Bioactive compound Trichoderma spp Effect Reference
6-pentyl-α-pyrone Trichoderma harzianum Plant metabolism and fruit quality Carillo etal., 2020
Sesquiterpenes and cyclodepsipeptides Trichoderma longibrachiatum Active against Colletotrichum lagrnarium, Bot-
rytis cinerea, Fusarium oxysporumf. sp.cuc-
umerinum and Meloidogyne incognita
Du etal., 2020
Acetonic extracts—palmitic acid and acetic acid Trichoderma virideandTrichoderma harzianum Active against Fusarium proliferatumandFusar-
ium verticillioides Yassin etal., 2021
Citric acid Trichoderma asperellum Active against Fusariumoxysporumf. sp.lyco-
persici and tomato growth promotion
Al-Askar etal., 2021
Sesquiterpenes-cedrene Trichoderma guizhouense Modulates root development Li etal., 2022
6-pentyl-α-pyrone and cyclooctanol TrichodermavirideandTrichoderma harzianum Active against Alternaria alternata Yassin etal., 2022
6-pentyl-α-pyrone Trichoderma asperellum Active against Magnaporthiopsis maydis Degani & Gordani, 2022
6-pentyl-α-pyrone, viridiofungin A, the chemical
structures of harzianic acid, iso-harzianic acid
and harzianolide
Trichodermaspp. Active against Phakopsora pachyrhizi El-Hasan etal., 2022
Phosphatases, siderophores, hydrogen cyanide,
ammonia, gibberellic acid and indole-3-acetic
acid
Trichoderma harzianum Plant growth-promoting properties Abdenaceur etal., 2022
Current studies on application of different Trichoderma formulations
Trichoderma spp Formulation technique Application Reference
Trichodermaspp. Trichogenic lipid nanoemulsion Signalling of resistance against Sclerospora
graminicola Nandini etal., 2019
Trichoderma reesei Lignin based encapsulation Efficient enzyme-responsive drug delivery sys-
tem for fungal spores
Peil etal., 2020
Trichoderma harzianum Calcium Alginate Microparticles Improved chitinolytic and cellulosic activity,
greater control against Sclerotinia sclerotiorum Maruyama etal., 2020
Trichoderma harzianum Nanocellulose/carboxymethyl cellulose nano-
composite
Better protecting and delivery of microbial
inoculants
Brondi etal., 2022
Trichoderma sp. Hydrogel based formulation Enhanced growth and yield parameters of rice Singh etal., 2022
Trichoderma asperellum Submerged liquid fermentation Yielded high microsclerotia Locatelli etal., 2022
Trichoderma asperellum Biopriming of chilli seeds with sodium alginate Enhanced efficacy in seed biopriming and toler-
ance Fusarium solani Chin etal., 2022
Trichoderma atrobrunneum Biopolymer-based emulsions Maintenance of 70–100% conidial viability after
3–6months
Martínez etal., 2023
Trichoderma asperellum Microcapsules Improved the survivability ofT. asperel-
lumconidia, biocontrol of cucumber powdery
mildew caused bySphaerotheca fuliginea
Qi etal., 2023
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of biopesticide formulations of Trichoderma, such
as whole organism, spore suspension and talc-based
formulations, which have proved successful in con-
trolling various plant pathogens. However, there are
many challenges in the efficient use of Trichoderma
as a biopesticide. Its potential to be used in curative
treatments and postharvest management systems still
remains unclear. The curative property of Trichoderma
and its mechanism of biocontrol should be studied in
detail because only partial curative effects have been
so far been observed. Current research should focus
on improving the efficacy of Trichoderma-based for-
mulations under field conditions. The interaction of
Trichoderma with soil microbiome and plant micro-
biome should also be studied in depth. More studies
optimizing the time of application of formulations are
necessary to improve its biocontrol performance. In
addition, one serious challenge for future research is
understanding the pathogen recognition mechanism
involded in indirect biocontrol. Researchers should
focus on how Trichoderma assists plants in recogniz-
ing specific pathogens and effectors involved in the
activation of resistance in plants during Trichoderma-
pathogen interactions. The research on immunization
treatments of Trichoderma biomolecules should also
be strenghthened. The biosynthesis and secretion of
secondary metabolites involves the expression of dif-
ferent genes in Trichoderma, and the potential for
overexpression of these genes needs to be investigated
for further application of these compounds in vivo.
The variables that affect biocontrol performanace and
establishment of Trichoderma under field conditions,
greenhouse and in postharvest disease management
should be identified. In addition, the research on smart
methods of delivery systems should be strengthened.
Furthermore, to produce a consistent biocontrol effect
the application of these fungi should be amalgamated
with sustainable crop management practices. Conse-
quently, the development of the -omic era has opened
up new areas of research that can provide a conveni-
ent source of candidate genes for further utilization in
transgenics and crop improvement.
Acknowledgements The authors are grateful to the Depart-
ment of Plant Pathology, Dr Y S Parmar University of Horti-
culture and Forestry Solan, for continuous support.
Author’s contributions All authors have contributed equally
in manuscript preparation. All authors have read, revised, and
approved the manuscript.
Data availability Data sharing not applicable to this article
as no datasets were generated or analysed during the current
study.
Declarations
Conflict of interests The authors declare that they have no
competing interests.
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