6 Trichoderma Species Our Best Fungal Allies

plants
Review
Trichoderma Species: Our Best Fungal Allies in the Biocontrol
of Plant Diseases—A Review
Paulina Guzmán-Guzmán 1 , Ajay Kumar 2 , Sergio de los Santos-Villalobos 3 , Fannie I. Parra-Cota 4 ,
Ma. del Carmen Orozco-Mosqueda 5 , Ayomide Emmanuel Fadiji 6 , Sajjad Hyder 7 ,
Olubukola Oluranti Babalola 6 and Gustavo Santoyo 1, *
1 Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo,

Morelia 58030, Mexico
2 Department of Postharvest Science, ARO, Volcani Center, Bet Dagan 50250, Israel
3 Instituto Tecnológico de Sonora (ITSON), Ciudad Obregón 85000, Mexico
4 Campo Experimental Norman E. Borlaug, Instituto Nacional de Investigaciones Forestales,
Agrícolas y Pecuarias (INIFAP), Ciudad Obregón 85000, Mexico
5 Departamento de Ingeniería Bioquímica, Tecnológico Nacional de México en Celaya, Celaya 38010, Mexico
6 Food Security and Safety Focus Area, Faculty of Natural and Agricultural Sciences, North-West University,
Private Bag X2046, Mmabatho 2735, South Africa
7 Department of Botany, Government College Women University Sialkot, Sialkot 51310, Pakistan
* Correspondence: gustavo.santoyo@umich.mx
Abstract: Biocontrol agents (BCA) have been an important tool in agriculture to prevent crop losses
due to plant pathogens infections and to increase plant food production globally, diminishing the
necessity for chemical pesticides and fertilizers and offering a more sustainable and environmentally
friendly option. Fungi from the genus Trichoderma are among the most used and studied microor-
ganisms as BCA due to the variety of biocontrol traits, such as parasitism, antibiosis, secondary
metabolites (SM) production, and plant defense system induction. Several Trichoderma species are
Citation: Guzmán-Guzmán, P.;
well-known mycoparasites. However, some of those species can antagonize other organisms such as
Kumar, A.; de los Santos-Villalobos,
nematodes and plant pests, making this fungus a very versatile BCA. Trichoderma has been used in
S.; Parra-Cota, F.I.; Orozco-Mosqueda,
agriculture as part of innovative bioformulations, either just Trichoderma species or in combination
M.d.C.; Fadiji, A.E.; Hyder, S.;
Babalola, O.O.; Santoyo, G.
with other plant-beneficial microbes, such as plant growth-promoting bacteria (PGPB). Here, we re-
Trichoderma Species: Our Best Fungal view the most recent literature regarding the biocontrol studies about six of the most used Trichoderma
Allies in the Biocontrol of Plant species, T. atroviride, T. harzianum, T. asperellum, T. virens, T. longibrachiatum, and T. viride, highlighting
Diseases—A Review. Plants 2023, 12, their biocontrol traits and the use of these fungal genera in Trichoderma-based formulations to control
432. https://doi.org/10.3390/ or prevent plant diseases, and their importance as a substitute for chemical pesticides and fertilizers.
plants12030432
Keywords: Trichoderma; biocontrol agent; bioformulations; mycoparasitism; antibiosis; secondary
Academic Editors: Jesus Munoz
Rojas and Paulina Estrada-de los
metabolites
Santos
Received: 19 December 2022

Revised: 8 January 2023 1. Introduction
Accepted: 13 January 2023
The continuing and growing world human population is demanding more food,
Published: 17 January 2023
putting enormous pressure on various agricultural production systems. In this sense,
producing more requires more significant extensions of open-field cultivation areas, which
are generally dedicated to the cultivation of grains and forages; likewise, greater efficiency
Copyright: © 2023 by the authors.
and investment in producing fruits and vegetables under greenhouse conditions are needed.
Licensee MDPI, Basel, Switzerland. To increase plant growth, chemical fertilizers have been used to enhance plant production
This article is an open access article to the limit of its innate capacities [1].
distributed under the terms and On the other hand, any agricultural system is exposed to the infection of potential
conditions of the Creative Commons pathogens, be they viruses, bacteria, fungi, or other types of macro-organisms [2], causing
Attribution (CC BY) license (https:// serious economic losses each year, which is why, again, the use of chemical pesticides is
creativecommons.org/licenses/by/ the first option of many agricultural producers. The main advantage of these pesticides is
4.0/). their immediate use and “solution” to the problem. However, the collateral damage caused
Plants 2023, 12, 432. https://doi.org/10.3390/plants12030432 https://www.mdpi.com/journal/plants

Plants 2023, 12, 432 2 of 35
by the use of fertilizers and pesticides in the environment and human and animal health
has been widely documented [3–6]. In addition, chemical pesticides induce resistance in
pathogens, making them challenging to control after years of continuous application [7].
Fortunately, many countries, mainly in North America and Europe, and some Asian
countries, are trying to regulate and decrease its use [8–10]. Likewise, the mentality of
consumers is changing to organic forms of production, leaving aside large fruits and
vegetables and excellent aesthetics. Other developing countries are still struggling with
these issues [11].
An important part of sustainable agriculture practices is the control or effective man-
agement of plant diseases. Fungi belonging to several genera have been widely used as
effective biocontrol agents against fungal phytopathogens, such as Alternaria, Penicillium,
Pichia, Aspergillus, and Trichoderma, with Trichoderma being the most used in the field [12,13].
The fungi Aspergillus terreus and Penicillium citrinum were able to diminish disease symp-
toms caused by the pathogen Sclerotium rolfsii, inducing salicylic and jasmonic acid accumu-
lation in sunflower plants [13], proving to be effective biocontrol agents. Ten endophytic
fungi, which include Penicillium sp., Guignardia mangiferae, Hypocrea sp., Neurospora sp.,
Eupenicillium javanicum, Lasiodiplodia theobromae, and Trichoderma sp., showed inhibition
under greenhouse conditions against Fusarium oxysporum f.sp. cucumerinum, the main
causal agent of cucumber stem rot disease [14]. Among 32 fungal isolates from the plant
Brugmansia aurea, A. aculeatus inhibited the growth of F. solani and A. fumigatus, showing
potential as BCA [15].
Fungal BCAs are also effective against other kinds of pests, such as insects and nema-
todes [16–18]. Several Trichoderma species have been proven to be effective at controlling
pests such as Tetranychus urticae and different insects that affect important crops [17]. Arbus-
cular mycorrhizal fungi (AMF) have been widely studied because of their positive effects
on plant growth promotion; nonetheless, they are also effective against phytopathogens,
such as Meloidogyne incognita and other nematodes [18]. The fungus Arthrobotrys oligospora,
which forms adhesive structures to capture nematodes, is another potential BCA of phy-
topathogens [19,20]. This information suggests the versatility of fungal BCA to counteract
several types of phytopathogens.
Fungal biocontrol agents can also protect plants against abiotic stresses, such as
high temperatures [21,22]. They are also used as plant defense enhancers due to their
ability to induce systemic resistance, protecting them against several pathogens, all of
which lead to an increase in plant yield. In this regard, fungi also have played important
roles in enhancing plant growth and crop production [23]. Fungi that can induce plant
growth include species from the genera Trichoderma, Aspergillus, Fusarium, Penicillium,
Piriformospora, Rhizoctonia, Colletotrichum, Gliocladium, Phoma, and others [24,25]. The
fungus Acremonium sp. showed plant growth-promoting traits on Allium tuberosum plants,
increasing root and shoot length, as well as antifungal activity against Botryiosphaeria
dothidea and Botrytis cinerea [26]. The fungi Alternaria sp., Phomopsis sp., and Cladosporium sp.
increased the biomass of tobacco plants, showing potential as plant growth-promoting
fungi [27]. T. virens and T. atroviride can promote secondary root system development and
biomass production of Arabidopsis and tomato plants [28,29], being one of the most used
genera as plant growth—promoters.
The damage caused by the use of chemical fertilizers and pesticides and the growing
use of biocontrol agents presents the need to steer agricultural production systems toward
sustainability and stop using synthetic fertilizers and pesticides as much as possible.
An efficient, low-cost, and eco-friendly alternative is the application of microorganisms
that promote plant growth and offer protection against pests and pathogens, such as the
fungi of the genus Trichoderma [30,31]. The use and application of bioinoculants with
Trichoderma as an antagonistic agent is one of the most active biological control strategies
in various countries. In fact, between 50 and 60% of the global market for biological
control agents (BCAs) around the world is based on the content of several Trichoderma
species [32,33]. The controlling action of these Trichoderma-based biopesticides mainly
Plants 2023, 12, 432 3 of 35
includes fungal and oomycete pathogens, such as Acremonium cucurbitacearum, Alternaria

spp., Aphanomyces cochlioides, Aspergillus spp., Lasiodiplodia theobromae, Botrytis cinerea,
Botrytis spp., Collisletotnicios spp., Collisletnicios spp., Diplodia natalensis, Fusarium spp.,
Gaeumannomyces graminis var. tritici, Lasiodiplodia theobroma, Phoma betae, Rhizoctonia solani,
Rhizopus oryzae, Pythium spp., Serpula spp., Sclerotium spp., Verticillium dahliae, among
others [32].
Trichoderma comprises several species of filamentous fungi that are common inhab-
itants of the soil, rhizosphere, and endosphere of plants. These fungi have attracted our
attention because they can control the growth and infection of potential pathogens such
as fungi or nematodes [17]. In this work, these beneficial aspects of different Trichoderma
species are reviewed, exhibiting different modes of action that benefit many sustainable
agricultural production systems.
2. An Overview of the Genus Trichoderma

The first description of the fungus Trichoderma as a genus was in 1794 by Persoon, while
Tulasne and Tulasne suggested the sexual state of a Hypocrea species in 1865 [34]. Likewise,
in 1932 Weindling was a pioneer in proposing Trichoderma as a fungus that “parasites”
other fungi with the potential to control them [35]. Trichoderma species belong to the
Hypocreaceae family. They present filamentous hyphae, with optimal growth temperatures
between 25 and 30 ◦ C, and they are widely present in various environments, preferring
those where there is a decomposing organic matter [36]. Trichoderma conidiophores are
abundant and end in phialides, pyramidal in shape, and their branches grow in pairs [37].
Asexual conidia are formed abundantly, elliptical in shape, and hyaline, which then develop
from white to yellow, and then green conidia when completely mature [36].
Enormous advances have been made in the taxonomy of Trichoderma; however, there
are still some issues to be resolved when differentiating species within the genus since
the vast majority of Trichoderma species are not associated with their sexual state and are
therefore handled as monoclonal and mitotic. Recent attempts to improve their classifi-
cation based on barcode oligonucleotide include online tools such as TrichoKEY [38] and
DNA Barcoding markers (TrichoMARK), such as internal transcribed sequences (ITS), tef1,
and rpb2 genes, to perform specific BLAST type searches (TrichoBLAST) [39]. Recently,
Dou and colleagues [40] proposed a Multilocus Identification System (MIST) online for the
identification of Trichoderma and Hypocrea (anamorphs) species for automated detection of
349 Trichoderma possible species, also based on a set of three DNA barcodes. Online websites
are https://trichokey.com (accessed on 18 December 2022) and http://mmit.china-cctc.org
(accessed on 18 December 2022), respectively.
Genome sequencing techniques allowed for a more in-depth study of the genus
Trichoderma, with T. virens, T. atroviride, and T. reesei being the first species among the genus
to have their genome sequenced. This allows a better understanding of their lifestyle as
mycoparasites and the difference between species [41].
Some examples of species include T. harzianum, T. aggressivum, T. citrinoviride, T. asperellum,
T. ghanense, T. hamatum, T. koningii, T. pseudokoningii, T. virens, T. longibrachiatum, T. polysporum,
T. tomentosum, T. atroviride, T. gamsii, T. koningii, Hypocrea jecorina/Trichoderma reesei, T. spirale,
T. viridescens, T. viride, and T. koningiopsis, which have been found in different ecosystems,
such as soils of forests, gardens, decaying wood, cultivated mushroom compost, cereal
grains, from various regions of the world, and in marine environments [42–44].
Trichoderma spp. has been (mostly) considered as non—pathogenic and opportunistic
plant symbionts, which can colonize plant roots, establishing a beneficial interaction with
their hosts mediated by Trichoderma effector proteins and hormonal crosstalk in exchange
for plant-derived sugars [45–48].
During the Trichoderma– plant interaction, the benefits received by the plant are not
just an increase in biomass and overall nutrition but also protection against several phy-
topathogens, either by acting directly over the pathogen as a mycoparasite and competing
for nutrients or indirectly by inducing the plant defense system [49–52]. Several species
their hosts mediated by Trichoderma effector proteins and hormonal crosstalk in exchange
for plant-derived sugars [45–48].
During the Trichoderma–plant interaction, the benefits received by the plant are not
just an increase in biomass and overall nutrition but also protection against several phy-
Plants 2023, 12, 432 topathogens, either by acting directly over the pathogen as a mycoparasite and competing 4 of 35
for nutrients or indirectly by inducing the plant defense system [49–52]. Several species
from this genus have been studied and used in field assays as effective biocontrol agents,
such as this
from T. harzianum,
genus haveT. been
virens,studied
T. atroviride,
and usedT. asperellum, T. hamatum,
in field assays T. gamsii,
as effective T. viride,
biocontrol agents,
among others [30,51,53–56]. Some of these species will be reviewed further.
such as T. harzianum, T. virens, T. atroviride, T. asperellum, T. hamatum, T. gamsii, T. viride,
among others [30,51,53–56]. Some of these species will be reviewed further.
3. Mechanisms for Protecting Plants Exerted by Trichoderma
3. The
Mechanisms
biocontrolfor Protecting exerted
mechanisms Plants Exerted by Trichoderma
by Trichoderma, which lead to efficient plant pro-
tection, The
can biocontrol mechanisms
be direct when the fungusexerted by Trichoderma,
interacts which by
with the pathogen lead to efficient plant
mycoparasitism,
protection,or
competition, can be direct when
antibiosis; the fungus
and indirect if theinteracts
fungus with the pathogen
enhances by mycoparasitism,
plant defense systems so
thecompetition, or antibiosis;
plant can defend and its
itself against indirect if the[57,58].
pathogen fungusAdditionally,
enhances plant defense systems
Trichoderma spp. can so
thediverse
exert plant can defend
direct plantitself against its pathogen
growth-promoting [57,58].
activities Additionally,
by producing someTrichoderma
molecules,spp.
suchcan
exert diverse direct
as phytohormones. plant1 growth-promoting
Figure depicts the biocontrolactivities by producing
properties some molecules,
of Trichoderma, such
exerting pro-
as phytohormones.
tection on crop plants. Figure 1 depicts the biocontrol properties of Trichoderma, exerting
protection on crop plants.
Figure 1. Direct biostimulation and biocontrol properties of Trichoderma species. Beneficial Trichoderma spp.
Figure
exert1.fungal-root
Direct biostimulation
communicationand biocontrol properties
via diffusible of Trichoderma
and volatile compounds, species. Beneficial
regulation of Tricho-
the stress
derma spp. exert fungal-root communication via diffusible and volatile compounds, regulation of
hormone ethylene, and production of phytohormones, such as auxins (indole-3-acetic acid). Some
the stress hormone ethylene, and production of phytohormones, such as auxins (indole-3-acetic
of the plant-protecting mechanisms of Trichoderma include parasitism, antibiotic and secondary
acid). Some of the plant-protecting mechanisms of Trichoderma include parasitism, antibiotic and
metabolites
secondary production,
metabolites or activation
production, of the induced
or activation systemic
of the induced resistance
systemic(ISR). Trichoderma
resistance (ISR).can trigger
Tricho-
both growth-stimulating effects and plant defense action by the elicitation of salicylic
derma can trigger both growth-stimulating effects and plant defense action by the elicitation of sali- acid (SA),
ethylene (ET), and jasmonic acid (JA) dependent pathways against several types of
cylic acid (SA), ethylene (ET), and jasmonic acid (JA) dependent pathways against several types ofpotential plant
pathogens
potential plantsuch as nematodes
pathogens such asand fungi. and fungi.
nematodes
3.1.3.1. Mycoparasitism
Mycoparasitism
Mycoparasitism
Mycoparasitism is is
oneone
ofof the
the mainmechanisms
main mechanismsofofinhibition
inhibitionofofthe
themycelial
mycelial growth
growth of
fungal pathogens, providing nutrients to the mycoparasite when they kill their prey. In
of fungal pathogens, providing nutrients to the mycoparasite when they kill their prey. In
some cases, Trichoderma obtains the nutrients but does not kill the pathogen (biotrophic
some cases, Trichoderma obtains the nutrients but does not kill the pathogen (biotrophic
mycoparasites). In work by Kubicek and collaborators [41], they compared the genome
mycoparasites). In work by Kubicek and collaborators [41], they compared the genome of
of three Trichoderma species (T. reesei, T. virens and T. atroviride), as well as their respective
teleomorph or sexual forms (Hypocrea jecorina, H. virens and H. atroviridis, respectively).
The authors found high conservation of the genetic origin (up to 96%), in addition to the
fact that several genes that code for antagonistic or mycoparasitic activities are conserved
in these species, suggesting that mycotrophy is an ancestral lifestyle in this genus [41,59].
There are three main steps during the act of mycoparasitism. This function can be
carried out in the rhizosphere of plants, an ecosystem efficiently colonized by Trichoderma
and where the biological control of potential pathogens is important to avoid plant dis-
Plants 2023, 12, 432 5 of 35
eases. First, Trichoderma requires recognition of the host (or possible plant pathogenic
fungus), where the production of oligochitins has been proposed as sensor molecules [60].
Likewise, it is known that during this previous step, various genes that encode proteases
and oligopeptide transporters are expressed before contact with the fungal host. Second,
hydrophobin-like proteins may have a relevant function once Trichoderma encounters the
plant-pathogenic fungus, which leads to the formation of papillae or appressoria-like
structures. The third step occurs when Trichoderma coils around the pathogen hyphae and
starts degrading it via the production of cell-wall degrading enzymes, such as cellulases
and hemicellulases, chitinases, proteases, and -1,3-glucanases, among other secondary
metabolites, that are essential for mycoparasitism [60]. It should be noted that the host
that is being parasitized also produces metabolites and reactive oxygen species (ROS) as
defense mechanisms in response to the attack, which in turn, Trichoderma turns on genes
involved in detoxification and response to stress. Interestingly, these lytic proteins are also
produced and purified using Trichoderma as a host for biotechnological purposes [61].
3.2. Antibiosis
The biological control mechanism known as antibiosis involves the production and
excretion of secondary metabolites, which include compounds of a different chemical
nature with cytotoxic activity, that can limit or inhibit pathogen growth. Antibiosis is one of
the main modes of action of Trichoderma and other biological control agents, such as plant
growth-promoting bacteria (PGPB) [34,51,62]. In fact, the expression of coding genes to
produce antibiotic metabolites is increased in the presence of pathogens and compounds
produced by plants, exerting a stimulating effect of protection and fine signaling between
the plant, the pathogen, and the biocontrol agent [34,51].
The various species of Trichoderma are a factory of secondary metabolites, as more
than 180 different types of compounds have been proposed and can be classified accord-
ing to their function in competition and iron-quelating metabolites, inducers of plant
resistance, plant growth-promoting metabolites, antibiotics, and if the metabolites are
volatile or non-volatile [63–65]. For example, T. virens species produce trichodermamides,
while T. koningii synthesizes Koninginins, both with antimicrobial and antifungal activ-
ity [66,67]. Furthermore, in T. harzianum and T. virens, compounds such as azaphilones,
viridins, nitrogen heterocyclic compounds (e.g., harzianopyridone and harzianic acid), and
volatile terpenes have been characterized, and are involved in the biocontrol of pathogenic
fungi [30]. The production of hydrolytic enzymes and proteases, such as exo- and endochiti-
nases, chitinases, xylanases, glucanases, lipases, endo-and exopeptidases, among others
with antifungal action, have also been characterized in different Trichoderma spp. [68]. The
volatile organic compound (VOC) 6-pentyl-2H-pyran-2-one (6-pentyl-α-pyrone, 6-PP) is
the most abundant VOC from T. atroviride, and it enhances plant growth and regulates
sugar transport in Arabidopsis roots, along with other VOCs produced by the fungus [69].
Figure 2 shows a glimpse of the metabolite’s arsenal involved in fungal antagonism and
some compounds involved in plant growth promotion (e.g., indol-3-acetic acid).
3.3. Competition
Bulk and rhizospheric soil are complex ecosystems with a continuous battle to access
resources and maintain survival. In the rhizosphere, a much richer environment than bulk
soil due to the excretion of nutrients by the plant roots, such as amino acids, vitamins,
organic acids, saccharides, etc., competition is an essential strategy for survival [70,71].
For this reason, those organisms residing in the rhizosphere with efficient metabolic and
competitive capacities will access the best “sites” where the resources exist. In this sense,
Trichoderma species, as mentioned before, are capable of producing a series of antagonistic
compounds (e.g., antibiotics or lytic enzymes), which, in conjunction with further rapid
growth and colonization strategies (e.g., metabolic versatility), they can occupy spaces in
the rhizosphere and, directly, benefit the growth of plants and restricting the development
of other potentially pathogenic microorganisms [72,73]. However, this strategy is also em-
Plants 2023, 12, 432 6 of 35
ployed by PGPB, which exhibits efficient colonization mechanisms to occupy rhizospheric

spaces and endophytic regions [74]. Therefore, when selecting Trichoderma biocontrol
Plants 2023, 12, x FOR PEER REVIEW species (or other biocontrol microorganisms), it is important to perform antagonism 6tests to-
of 36
wards beneficial organisms for plants, such as PGPB [75] to determine their synergistically
or detrimental potential among each other.
Figure
Figure2.2. Examples of
ofTrichoderma
Trichoderma secondary
secondary metabolites
metabolites involved
involved in plant
in plant interactions
interactions with
with growth-
growth-promoting effects
promoting effects (A) (A) and secondary
and secondary metabolites
metabolites involved
involved in in mycoparasitism
mycoparasitism witheffect
with antibiotic antibi-
(B).
otic effect (B).
3.4. Induction of Plant Defense System
3.3. Competition
When attacked by various pathogens or mechanical damage, plants turn on de-
fense systems
Bulk that allow them
and rhizospheric to protect
soil are complex themselves,
ecosystems such
withasasystemic
continuousacquired
battle resistance
to access
(SAR) [76]. In some other cases, plant-associated microbes can
resources and maintain survival. In the rhizosphere, a much richer environment induce the plant
thandefense
bulk
systems, such as the rhizobacteria-induced systemic resistance (RISR)
soil due to the excretion of nutrients by the plant roots, such as amino acids, vitamins,pathway, which phe-
notypically resembles SAR [1], in response to the presence of the microorganism.
organic acids, saccharides, etc., competition is an essential strategy for survival [70,71]. It could
be this
For that Trichoderma-induced
saidreason, those organisms residingsystemic in resistance (TISR)with
the rhizosphere is very similar
efficient to RISR since
metabolic and
both are regulated by the jasmonic acid and ethylene (JA/ET) signaling pathway
competitive capacities will access the best “sites” where the resources exist. In this sense, [52,77,78].
However, the
Trichoderma plant defense
species, system
as mentioned and the
before, are signaling
capable ofthat coordinates
producing theofresponse
a series antagonis- are
highly variable, even within the same plant kingdom. In fact, Bakker et
tic compounds (e.g., antibiotics or lytic enzymes), which, in conjunction with further rapid al. [78] mention
that in and
growth RISR, there is no induction
colonization of themetabolic
strategies (e.g., expression of pathogenesis-related
versatility), they can occupy proteins
spaces(PR),
in
as in SAR, which is stimulated by the attack of fungal or herbivore pathogens.
the rhizosphere and, directly, benefit the growth of plants and restricting the development Nonethe-
ofless, T. potentially
other hamatum strain Th23 can
pathogenic induce PR-1 and
microorganisms PR-7However,
[72,73]. expression in strategy
this tomato plants
is also upon
em-
infection
ployed with Tobacco
by PGPB, Mosaic Virus
which exhibits (TMV)[79].
efficient Themechanisms
colonization overall planttoresponse to pathogens
occupy rhizospheric
includes the production of antifungal glucanases and chitinases, thaumatins, as well as the
spaces and endophytic regions [74]. Therefore, when selecting Trichoderma biocontrol
synthesis of oxidative enzymes, including peroxidases (POD), polyphenol oxidases (PPO),
species (or other biocontrol microorganisms), it is important to perform antagonism tests
and lipoxygenases [80] and the activation of several transcription factors involved in the
towards beneficial organisms for plants, such as PGPB [75] to determine their synergisti-
plant immune response to biotic stressors [81]. T. hamatum strain Th23 induces CAT, SOD,
cally or detrimental potential among each other.
and PPO enzymatic activity in tomato plants during infection with TMV and reduces H2O2
and malondialdehyde (MDA) concentrations [79]. One of them is NPR1, a transcription
3.4. Induction of Plant Defense System
factor that is widely known for its action in modulating both SAR and RISR pathways [82].
When attacked
T. harzianum TR 274by variousthe
induces pathogens
expression or of
mechanical damage, plantsgenes
several defense-related turn on defense
in Phaseolus
systems that allow them to protect themselves, such as systemic acquired
vulgaris plants, such as glu, chit, and pal [83], which are genes related to TISR; and resistance (SAR)the
[76]. In some other cases, plant-associated microbes can induce the
commercial formulation BIOSPARK™, made from Trichoderma spp. induces resistance plant defense systems,
such as the rhizobacteria-induced systemic resistance (RISR) pathway, which phenotypi-
cally resembles SAR [1], in response to the presence of the microorganism. It could be said
that Trichoderma-induced systemic resistance (TISR) is very similar to RISR since both are
regulated by the jasmonic acid and ethylene (JA/ET) signaling pathway [52,77,78]. How-
ever, the plant defense system and the signaling that coordinates the response are highly
Plants 2023, 12, 432 7 of 35
in Lansium domesticum plants against the insect Unaspis mabilis [84]. Some TISR elicitor
compounds are homologous to those produced by rhizobacteria, such as siderophores,
acyl-homoserine lactones, and antimicrobial compounds, among others [85,86]. It should
be taken into account that the TISR response has been little studied compared to RISR.
Trichoderma elicitors may be regulated in different ways according to the species; for ex-
ample, SM1/EPL1 from T. virens and T. atroviride induce a defense response in plants, but
SM1 from T. harzianum seems to be downregulating plant defense responses, allowing root
colonization [83]. This suggests that species and type of elicitor are important factors to
consider when inducing TISR in plants, so it is necessary to delve further into the elicitors
and induction pathways of plant defense systems.
4. Biocontrol Potential of Registered Trichoderma Species

With over 200 Trichoderma species registered [40,87] and their potential to be used as
biocontrol agents and plant growth promoters, it has led to many studies to gain more
knowledge about their mechanisms of action, focusing studies on mycoparasitism and
competition [60,88], production of secondary metabolites with antagonistic activity [63,68]
and induction of plant systemic resistance [52,89].
Among the registered Trichoderma species, T. harzianum, T. asperellum, T. atroviride,
T. longibrachiatum, T. viride, and T. virens are the most sampled ones [55]. The first three
species are among the most used biocontrol agents, using mycoparasitism and competition
as their primary mechanism of action against fungal phytopathogens. Meanwhile, species
such as T. virens, T. longibrachiatum, and T. viride use antibiosis as a strong mechanism
of action against several plant pathogens [50,88,90,91]. Here, we review the Trichoderma
species mentioned above, focusing on their biocontrol traits and the most recent literature
on this subject, summarized in Table 1.
Table 1. Main Trichoderma species used in agriculture and their biocontrol traits.
Trichoderma
Biocontrol Traits Biocontrol Effect Reference
Species
Competition and mycoparasitism inhibit the growth of several
[92]
plant pathogens
Parasitism and Competition against Ph. cinnamomi inhibits the pathogen growth [93]
competition
Competition inhibits the growth of N. parvum [94]
Competition and antagonistic activity against F. avenaceum and
[95]
F. culmorum
Ethyl acetate extract inhibits growth and has antifungal activity
[92]
against 25 plant pathogens
Swollenin TaSwo1 confers protection in Capsicum annum plants
[96]
against A. solani and R. solani
T. atroviride
Vel1-derived secondary metabolites and parasitism-related enzymatic
[97]
activity influences mycoparasitic activity against F. graminearum
Secondary metabolites
production and Fungal culture inhibits the growth of pathogen F. avenaceum [95]
antibiosis
Fermented culture inhibits the growth of B. cinerea [98]
Tal6, a LysM effector, antagonizes several plant pathogens [99]
VOC=Volatile organic acid VOCs inhibit the growth of pathogen F. avenaceum [95]
6-PP production under dark conditions enhances antagonistic
[100]
activity against R. solani and F. oxysporum
VOCs inhibit the growth of R. solani, B. cinerea, and F. oxysporum,
[101]
conferring resistance in Arabidopsis plants
Plants 2023, 12, 432 8 of 35
Table 1. Cont.
Trichoderma
Species
SA induced defense response in grapevine Tempranillo cultivar,
[94]
protecting the plant against N. parvum
Increasing the defense-related enzymatic activity in tomato plants
confers resistance against B. cinerea and diminishes the [98]
Plant defense
disease’s symptoms
induction/Priming
Modification of gene transcripts related to plant defense, and
induction of plant-defense VOCs, confer resistance to the moth [102]
S. littotalis and the aphid M. euphorbiae in tomato plants
Priming JA and SA defense pathways increased gene expression
[103]
confers resistance against B. cinerea in Arabidopsis plants
Parasitism and
Growth inhibition of F. oxysporum in in vitro confrontations [104]
competition
Competition for nutrient and space and mycoparasitism inhibits the
[105]
growth of F. sudanense
Growth inhibition of A. cerealis in in vitro confrontations [106]
Mycoparasitism inhibits the growth of F. oxysporum [107]
Growth inhibition of several postharvest pathogens of sweet potato
[108]
in in vitro assays
Mycoparasitism inhibits the growth of F. oxysporum, A. alternata,
[109]
A. flavus, and A. carbonarius
Competition for space with the pathogen F. pseudograminearum in the
[110]
rhizosphere soil of wheat plants
Mycoparasitism of F. graminearum inhibits the pathogen growth [111]
Growth inhibition of C. truncatum in in vitro confrontations [112]
6-PP application on maize roots diminishes root damage by the
[113]
scarab P. vetula
T. harzianum Secondary metabolite production regulated by the transcriptional
coactivator ThMBF-1 is important to inhibit the growth of B. cinerea [114]
and F. oxysporum and to confer resistance in tomato plants
Reduction of cucumber mosaic virus infection on cowpea plants by
[115]
three peptaibols: trichorzins HA II, HA V, and HA VI.
Aspartic protease P6281 inhibits the growth and spore formation of
B. cinerea, M. circinelloides, A. flavus, A. fumigatus and inhibits the [116]
growth of R. solani
Secondary metabolites
production and Chitinase activity and hydrophobicity are essential for the
[117]
antibiosis mycoparasitism of R. solani
SMs from the fungal extract inhibit the growth of F. graminearum [73]
Culture filtrate from T. harzianum has antifungal activity against
[107]
F. oxysporum
The enzyme ThLAAO induces the expression of defense-related
genes in tobacco plants, conferring resistance against B. cinerea and [118]
S. sclerotiorum
Epl-1 down-regulates virulence genes in B. cinerea during
[119]
in vitro confrontations
Culture filtrate from T. harzianum inhibits P. ultimum growth [120]
SM from culture filtrates reduce the growth of several
[121]
plant pathogens
Plants 2023, 12, 432 9 of 35
Table 1. Cont.
Trichoderma
Species
Metabolites extracts alleviate the symptoms caused in wheat
[122]
seedlings by the pathogen F. culmorum
In planta expression of ThKEL1 induces the expression of genes
involved in SA and JA pathways in Arabidopsis and rapeseed plants, [123]
conferring resistance against B. cinerea
JA signaling induction in tomato against the feeding insect N. viridula [124]
SA and JA/Et signaling induction in tomato plants upon infection
[125]
with the nematode M. incognita
Strong VOC priming in tomato plants to attract the parasitoid A. ervi
[126]
to exert biocontrol over the aphid M. euphorbiae
Induction of antioxidant enzymes in tomato plants upon
[104]
F. oxysporum infection
Induction of Et, JA, ISR pathways, and isoprenoid biosynthesis in
[127]
tomato plants upon M. euphorbiae infestation
Induction of defense-related enzymes, SA accumulation, and
[128]
phenolic compounds in wheat, conferring resistance to B. sorokiniana
Plant defense
induction/Priming Induction of several plant defense-related compounds in tomato
[106]
plants upon infection with A. cerealis
Increased protection and reduction of cell death in soybean plants
[107]
upon F. oxysporum infection
SA signaling pathway and priming are induced by Epl-1 in tomato
[119]
plants against B. cinerea
Induction of antioxidant activity and redox homeostasis in cucumber
[129]
plants promotes resistance against F. oxysporum
Induction of priming, defense-related enzymatic activity, antioxidant
enzymatic activity, and reduction of ROS accumulation in chili
[112]
pepper plants, protecting and reducing symptoms from
C. truncatum disease
Competition and mycoparasitism inhibit the growth of
[130]
eight phytopathogens
Parasitism of the maize moth pathogen O. furnicalis, inducing
[131]
enzymatic activity related to plant defense in maize
Growth inhibition of C. truncatum in in vitro confrontations [112]
Competition and mycoparasitism inhibit the growth of several
[92]
plant pathogens
Parasitism and Growth inhibition of R. solani and A. alternata under salt
T. asperellum [132]
competition stress conditions
Competition and mycoparasitism inhibit the growth of F. proliferatum
[133]
f.sp. malus domestica MR5, and other plant pathogens
Growth inhibition of the lettuce pathogens C. cassiicola and C. aeria [134]
Competition and mycoparasitism inhibit the growth of F. oxysporum
[135]
f.sp. cucumerinum Owen and F. graminearum
Mycoparasitism inhibits the growth of P. noxius and confers
[136]
resistance in E. japonica plants
Plants 2023, 12, 432 10 of 35
Table 1. Cont.
Trichoderma
Species
Elicitor protein Epl1-Tas induces enzymatic activity related to plant
defense response in P. davidiana × P. alba var. pyramidalis, conferring [137]
resistance against A. alternata
Hydrophobin HFBII-4 induces enzymatic activity and gene
expression related to plant defense response in P. davidiana × P. alba [138]
var. pyramidalis, conferring resistance against A. alternata
The fermented broth has antifungal activity against F. oxysporum,
F. graminearum, and B. cinerea and increases the resistance of wheat [139]
against F. graminearum
The crude extract containing peptaibols inhibits spore germination of
A. solani, R. solani, and F. moniliforme, and it has antibacterial activity [140]
against M. luteus
Secondary metabolites Crude extract and 6-PP inhibit the growth of M. maydis [141]
production and
antibiosis Ethyl acetate extract inhibits growth and has antifungal activity
[92]
against 25 plant pathogens
Liquid fermentation extract inhibits F. proliferatum f.sp.
[133]
malus domestica MR5 growth and spore germination
Filtered fermentation liquor inhibits F. graminearum growth [135]
Crude citric extract inhibits F. oxysporum f.sp. lycopersici growth and
induces enzymatic activity related to plant defense response in [142]
tomato plants
Vel1-derived SM induces the expression of defense-related genes in
maize plants, conferring resistance against C. herostrophus and [143]
F. verticilloides
VOCs prevent postharvest rot caused by F. incarnatum in
[144]
Cucumis melo fruits, and they inhibit pathogen growth
VOCs inhibit F. proliferatum f.sp. malus domestica MR5 growth [133]
Induction of defense-related genes in tomato plants, granting
[130]
resistance against A. alternata
Induction of hypersensitive response in Pisum sativum plants in
[145]
response to the pathogen E. pisi
Induction of systemic resistance and reduction of ROS accumulation
[146]
Plant defense in tomato leaves upon infection with F. oxysporum and B. cinerea
induction/Priming Induction of priming, defense-related enzymatic activity, antioxidant
enzymatic activity, and reduction of ROS accumulation in chili
[112]
pepper plants, protecting and reducing symptoms from
C. truncatum disease
Induction of defense-related enzymatic activity in lettuce plants upon
[134]
infection with C. cassiicola and C. aeria
Antagonistic and mycoparasitic activity against F. oxysporum f.sp.
Parasitism and [147]
physalia, diminishing disease severity in Physalis peruviana plants
competition
Mycoparasitic activity against R. solani. [148]
Excess production of secondary metabolites enhances antibiosis and
T. virens mycoparasitic capacity against P. aphanidermatum and S. rolfsii and [149]
Secondary metabolites confers protection on Cicer arietinum plants against S. rolfsii
production and
Chitinase and cellulase activity inhibit R. solani growth [150]
antibiosis
Secondary metabolites inhibit the growth of R. solani AG2 and induce
[151]
JA and SA accumulation in A. thaliana plants
Plants 2023, 12, 432 11 of 35
Table 1. Cont.
Trichoderma
Species
Non-volatile secondary metabolites inhibit the growth of R. solani
and downregulate genes coding for defense enzymatic activity in [148]
the pathogen
Ferricrocin, a siderophore, is involved in ISR induction in maize
[152]
against C. heterostrophus
Endopolygalacturonase TvPG2 induces resistance in tomato plants
[153]
against B. cinerea via ISR induction
Cell-free supernatant inhibits the growth of F. oxysporum f.sp. physalia,
[147]
and confers resistance in P. peruviana plants
Culture filtrate induces ISR in tomato plants, conferring resistance to
F. oxysporum f.sp. lycopersici. Priming and induction of JA defense [154]
pathway in tomato plants against F. oxysporum f.sp. lycopersici
Volatile secondary metabolites inhibit R. solani growth [148]
Induction of defense-related genes confers resistance against R. solani
[155]
Plant defense in Vigna radiata susceptible and resistant varieties.
induction/Priming
Induced systemic resistance in maize plant against C. graminicola, via
[156,157]
the induction of oxylipins and ketol, as ISR signals
Competition and mycoparasitism inhibit the growth of six
[140]
phytopathogens, being more effective against R. solani and A. solani
Competition and antibiosis inhibit the growth of Sclerotium rolfsii and
[158]
M. phaseolina
Parasitism and Mycoparasitism inhibits the growth of F. pseudograminearum [159]
competition
Parasitism of eggs and second-stage juveniles of H. avenae [160]
Mycoparasitism inhibits the growth of M. phaseolina [161]
Competition diminishes the presence of Magnaporthiopsis maydis in
maize plants and its negative effect on plant growth and disease [162]
symptoms in field conditions
The crude extract containing peptaibols has antibacterial activity
[140]
against M. luteus
Dendrobine has antibacterial properties against
[163]
plant-pathogenic bacteria
T. longibrachiatum Synthetic analogs to the peptaibol Trichogin inhibit the growth of
Pyricularia oryzae, reduce disease symptoms in rice and barley plants, [164]
and alter the spore and mycelial structure of the pathogen
The hydrophobin HYTLO1 induces the expression of defense-related
[165]
Secondary metabolites genes in Lotus japonicus plants
production and Metabolites inhibit the growth of M. phaseolina [161]
antibiosis
Sesquiterpenes and cyclodepsipeptides inhibit the growth of several
[166]
plant fungal pathogens and the nematode pathogen M. incognita
Culture filtrate and sorbicillinoids inhibit the growth of several plant
[167]
pathogens and confer resistance in tomato plants against Ph. infestans
Ethyl acetate extract has effective toxicity against the cotton aphid
[168]
A. gossypii
Fermentation crude extract and fungicide compounds inhibit the
[169]
growth of the pathogen V. mali
VOCs inhibit the growth of S. rolfsii and M. phaseolina [158]
Plants 2023, 12, 432 12 of 35
Table 1. Cont.
Trichoderma
Species
Induction of JA/Et and SA pathways, conferring resistance in
[77]
Plant defense cucumber plants against B. cinerea
induction/Priming Induction of defense-related enzymatic activity and flavonoids and
[160]
lignin content in wheat roots upon infection with H. avenae
Competition inhibits S. sclerotiorum growth in dual confrontations [170]
Parasitism and
competition Competition inhibits F. solani, R. solani, and S. rolfsii growth in
[171]
dual confrontations
VOCs show antibacterial and antifungal activity [171]
T. viride Secondary metabolites VOCs inhibit the growth of S. rolfsii in soil and in dual confrontations,
production and affecting the mycelial structure. VOCs induce defense-related [172]
antibiosis enzymatic activity in okra plants upon infection with S. rolfsii
Crude and ethanol extract show antibacterial and antifungal activity [171]
Induction of antioxidant enzymatic activity and reduction of ROS
Plant defense
accumulation in Phaseolus vulgaris plants upon infection with [170]
induction/Priming
S. sclerotiorum
4.1. Trichoderma Atroviride

Trichoderma atroviride is a filamentous fungus that can be isolated from soil, mainly in
temperate climates, with optimal growth at 25 ◦ C, presenting thin and hyaline colonies
and inconspicuous aerial hyphae and gray to dark green conidia after 2 to 7 days [173].
It has a characteristic coconut smell due to the production of the volatile compound
6-pentyl-2H-pyran-2-one, or 6-PP, which also is involved in biocontrol against several plant
pathogens, including Cylindrocarpon destructans, Mcrophomina phaseolina, Phytophthora sp.,
and others, and it is also involved in plant growth-promotion and induction of systemic
resistance [174–176].
T. atroviride has biocontrol capacity on different plant pathogens, including fungi,
oomycetes, and pests, such as nematodes or insects, by exerting different mechanisms of
biocontrol [17,31], which are presented below with recent examples from the literature.
4.1.1. Parasitism and Competition

In a competition for space and nutrients, T. atroviride inhibits Phytophthora cinnamomic
growth and zoospore formation. In a tripartite interaction with tomato plants, T. atroviride
enhances protection against the disease induced by this oomycete [93]. Also, T. atroviride
competes with and is capable of antagonizing Fusarium avenaceum and Fusarium culmorum,
important maize pathogens [95], and the grapevine pathogen Neofusicoccum parvum [94].
In dual culture assays, T. atroviride can parasitize several fungal pathogens, including
Neofusicoccum batangarum, N. parvum, Phytophthora nicotianae, Penicillium digitatum,
P. commune, P. roqueforti, P. verrucosum, Aspergillus steynii, Fusarium proliferatum,
F. verticilloides, F. sporotrichoides and F. poae [92].
As stated before, the main mechanism used by T. atroviride as a biocontrol agent
against fungal pathogens is mycoparasitism [50]. Nonetheless, this fungus also uses other
strategies to limit the growth of different plant pathogens.
4.1.2. Secondary Metabolites

The effect of secondary metabolites as a biocontrol trait can be tested as whole fungal
cultures or extracts, as individual components, or as a mix of components that had been
identified from the whole extract. Whole fungal culture (soluble metabolites) from a local
T. atroviride strain BC0584 and its volatile organic compounds (VOCs) are capable of in-
hibiting the growth of F. avenaceum. In contrast, both soluble metabolites and VOCs did
Plants 2023, 12, 432 13 of 35
not have any statistical significance in inhibiting the growth of F. culmorum. Nonethe-
less, in confrontation assays, both pathogens are controlled by T. atroviride BC0584 [95].
The production of VOCs is a characteristic of Trichoderma species, and 6-PP is probably
the most characterized VOC from the species that synthesize this compound, such as
T. atroviride [175]. The synthesis of 6-PP is regulated by dark conditions when it is pro-
duced in more quantities. It enhances the antagonistic activity of T. atroviride P1 and IMI
206,040 strains against R. solani and F. oxysporum [100]. Fermented cultures are used to
obtain certain metabolites, such as antibiotics, and are obtained at the end of several days
of the fungus growing in a liquid medium [177]. The fermented culture from T. atroviride
CCTCCSBW0199 could inhibit the growth of B. cinerea in an in vitro assay to 73% [98],
indicating an antibiosis mechanism to control the pathogen.
In a broad-range pathogen study, Stracquadanio and collaborators [92] found that
the ethyl acetate extract and the fungal filtrate from T. atroviride (TS) inhibit growth and
have strong cytotoxic activity against 25 pathogens, which includes 7 species of Penicillium,
6 species of Aspergillus, 6 species of Fusarium, 2 species of Neofusicoccum, 2 species of
Colletotrichum, and 2 species of Phytophthora. The velvet complex proteins in Trichoderma
are involved in several physiological processes, including secondary metabolite synthe-
sis [91]. In a study to unravel the role of vel1, a member of the velvet complex in T. atroviride
T23, Karuppiah and collaborators [97,143] found that the fungal extract of the wild-type
strain and the vel1 overexpressing strain, both alone and in the co-culture with Bacillus
amyloliquefaciens 1841, inhibit the growth of the wheat pathogen F. graminearum, and de-
crease the disease severity in plants treated with those strains; the authors also note that
the co-cultures have better inhibition rate over the pathogen, and induce a stronger plant
resistance that the single cultures [97].
Swollenins are proteins with similarity to plant expansins and are involved in the
remodeling of plant cell walls and colonization [178]. TaSWO1, a swollenin secreted by
T. atroviride, can induce resistance in Capsicum annum plants against A. solani and R. solani,
reducing the symptoms caused by these pathogens [96]. The LysM effector identified as Tal6
from T. atroviride IMI 206,040 binds fungal chitin, preventing the plant from sensing the BCA,
allowing it to establish a beneficial interaction, and enhancing T. atroviride mycoparasitic
activity against B. cinerea, Sclerotium cepivorum, Colletotrichum lindemutianum and R. solani
AG2 [99].
The capacity of T. atroviride to produce a wide range of volatile and non-volatile sec-
ondary metabolites is indicative of its capacity to control different types of phytopathogens,
which makes this fungus a capable BCA in many agricultural situations.
4.1.3. Plant Defense Induction and Priming

Trichoderma, colonization of roots, can induce different plant defense responses; for
example, T. atroviride SC1 induces SA-mediated defense response in grapevine Tempranillo
cultivar, enhancing the plant protection against N. parvum, which is also inhibited in dual
cultures with T. atroviride [94]. Leal and collaborators (2021) also performed co-cultures of
T. atroviride with B. subtilis PTA-271. They found that co-culture is better at enhancing plant
protection than the inoculation of single organisms.
Some of the secondary metabolites produced by T. atroviride can induce plant resistance;
for instance, fermented culture from T. atroviride CCTCCSBW0199 alone or in combination
with brassinolide increases peroxidase (POD) and superoxide dismutase (SOD) activity
in tomato plants, which then increases the plant resistance and reduces the symptoms
induced by B. cinerea [98].
Trichoderma species, when colonizing the plant, alter plant transcriptome, modifying
gene transcription involved in plant defense responses, such as T. atroviride P1, which
modifies gene transcripts related to plant defense, and induces plant-defense related
VOCs to attract aphid-predatory wasps Aphidius ervi. They provide a better defense
mechanism against the aphid Macrosiphum euphorbiae and the moth Spodoptera littotalis in
tomato plants [102], proving that T. atroviride may be able to control pathogens indirectly,
Plants 2023, 12, 432 14 of 35
modulating plant physiology. Besides modification of the transcription of genes involved

in plant defense responses, colonization by T. atroviride also induces Arabidopsis’s sRNA-
mediated gene silencing, leading to an increase in gene expression of JA and SA-mediated
pathways, which in turn induces priming and increases resistance in the plant against
B. cinerea [103].
Plant defense induction by T. atroviride is an important mechanism of action for
this BCA due to the span of plant pathogens that can be controlled with it since direct
mechanisms such as mycoparasitism may be limited. Still, it can be complemented with
indirect mechanisms. Therefore, T. atroviride is an effective antagonist of several fungal,
oomycete, insect, and other plant pathogens.
4.2. Trichoderma Harzianum

T. harzianum is frequently found in temperate climates, with optimal growth at
30 ◦ C, but can grow fine at 35 ◦ C; conidiation is presented at day 2 in concentric zones
when growing in Petri dishes, changing from green to dark green/brownish in color; unlike
T. atroviride, T. harzianum has no particular odor [37,179].
This fungus is found in several substrates such as soil, other fungi, decaying plant
material, and as an endophyte of several plants, acting as a biocontrol agent for different soil-
borne diseases. It has been used widely in agriculture, being one of the active ingredients
of commercial products used to control crop diseases and to promote plant growth and
yield [179].
As a biocontrol agent, T. harzianum is efficient at inhibiting plant pathogens such as
Fusarium solani or mycotoxin—producing fungi by competition, antibiosis, and inducing
plant defense responses [109,180]. It is also a biocontrol agent of pests such as aphids by
inducing the plant defense system against them [126]. Examples of direct and indirect
mechanisms of biocontrol from T. harzianum are presented below.

In an in vitro assay of F. oxysporum f.sp. lycopersici in confrontation with five
Trichoderma species, all the species were able to inhibit the pathogen’s growth, being
both T. harzianum strains tested, BHU-BOT-RYRL4 and MTCC936, the ones that inhib-
ited the pathogen’s growth the most (83.17% and 72.13%, respectively) [104]. In a rhi-
zosphere colonization assay with wheat plants, T. harzianum Tr904, as well as T. gamsii
and T. afroharzianum, colonized the rhizosphere and competed for space and nutrients
with the pathogen Fusarium pseudograminearum, preventing plant disease caused by this
pathogen [110].
In the dual confrontation of T. harzianum against Fusarium sudanense, the BCA parasites
the pathogen degrading its hyphae and inhibiting its growth by also competing for space
and nutrients, preventing seed rot in wheat plants [105]. T. harzianum has also shown
antagonistic ability in vitro during the confrontation with the pathogen Alternaria cerealis,
limiting its growth [106], and the strain T. harzianum T-soybean showed mycoparasitic
activity against F. oxysporum, reducing its growth by 45.45% [107].
In dual confrontation assays, two strains of T. harzianum, CMML20-26 and CMML20-27,
showed strong antagonistic activity against several sweet potato postharvest pathogens, in-
cluding Fusarium ipomeae, F. oxysporum, F. solani, Penicillium citrinum, P. rotoruae,
Aspergillus wentii, Mucor variicolumellatus and M. phaseolina [108]. T. harzianum MRI001
can mycoparasite F. oxysporum, A. alternata, Aspergillus carbonarius, and A. flavus, overgrow-
ing the pathogens and reducing the production of the mycotoxins ochratoxin and aflatoxin
B1 , produced by A. carbonarius and A. flavus respectively [109]. In a confrontation assay,
T. harzianum inhibits the growth of the chili pepper pathogen Colletotrichum truncatum,
competing for space [112]. Several Egyptian T. harzianum strains showed mycoparasitic
activity against F. graminearum, M. phaseolina, and F. solani, the strain T. harzianum Th6, the
most effective one against all three pathogens [111,181].
Plants 2023, 12, 432 15 of 35
T. harzianum has proved to be an effective mycoparasite, not only by degrading its

host hyphae but by competing for space and nutrients against a wide range of fungal plant
pathogens. These characteristics make this fungus a competent BCA against soil-borne
fungal pathogens, with prominent applications in agriculture.

T. harzianum is also a good producer of secondary metabolites with important bio-
control traits. Inoculation of T. harzianum induces VOCs production in maize roots, and
the exogenous application of 6-PP diminishes the damage caused by the root herbivore
Phyllophaga vetula [113], indicating that the volatiles produced by the fungus induces
resistance in the plant, even though, no direct biocontrol of P. vetula was observed by
T. harzianum. ThMBF1 is a transcriptional coactivator from T. harzianum T34 involved in the
synthesis of several secondary metabolites. Its regulation is vital to maintaining biocontrol
capability over B. cinerea and F. oxysporum since its overexpression significantly reduced
the BCA capacity to inhibit the pathogens’ growth and its capacity to confer resistance in
tomato plants [114].
Some important secondary metabolites from Trichoderma species are peptaibols, which
are involved in antibiosis activity against several plant pathogens [63]. Three peptaibols
from T. harzianum HK-61, named trichorzins HA II, HA V, and HA VI, reduced lesions
caused by Cucumber mosaic virus (CMV) up to a 90% (trichorzin HA V) in Vigna sesquipedalis
plants [115].
Other important secondary metabolites are proteases. The aspartic protease P6281 from
T. harzianum GIM 3.442 significantly reduces the growth of B. cinerea, Mucor circinelloides,
A. flavus, A. fumigatus, and R. solani, disrupting the cell wall integrity of B. cinerea, preventing
it from causing lesions in fruits such as orange and apples, and inhibiting spore formation
in B. cinerea, M. circinelloides, A. flavus, and A. fumigatus [116].
Secondary metabolites can have antibiosis or antimicrobial activity. SM present in the
fungal extract of T. harzianum CCTCC-RW0024 strain showed antifungal activity against
F. gramineraum, inhibiting the pathogen growth up to 96.3% and conferring resistance in
maize plants [73]. The culture filtrate from T. harzianum T-soybean has antifungal activity
against F. oxysporum, inhibiting the pathogen growth up to 60.4%, granting resistance in
soybean against F. oxysporum [107]. Culture filtrate from T. harzianum can inhibit the growth
of the bean pathogen Pythium ultimum and, combined with chamomile extract, reduces
disease symptoms in Phaseolus vulgaris seeds caused by this pathogen [120]. Cell-free
culture filtrates improved in chitinase activity, showed fungal growth inhibition against the
pathogens Dematophora necatrix, F. solani, F. oxysporum, and Pythium aphanidermatum, and
the effect is concentration-dependent, were at a concentration of 25% of the filtrate showed
the maximum growth inhibition rate for all the pathogens tested [121]. The G-protein signal
regulatory mechanism is involved in fungal processes such as pathogenesis and secondary
metabolism synthesis [182], and the Thga3 subunit from T. harzianum Th33 is involved in
its mycoparasitic ability against R. solani, regulating chitinase activity, hydrophobicity, and
growth of the fungus [117].
Some secondary metabolites produced by T. harzianum can induce plant defense
mechanisms, such as the flavoenzyme ThLAAO (L-amino acid oxidase) from T. harzianum
ETS323, which has antibiotic activity, and when it is expressed in tobacco plants, induces
the expression of genes related to SA-, JA- and Et- mediated defense pathways, as well
as ROS accumulation, conferring resistance to Sclerotinia sclerotiorum and B. cinerea, and
resistance to B. cinerea in cabbage plants [118]. The expression of the gene thkel1 from
T. harzianum CECT 2431 in Arabidopsis and Brassica napus plants caused resistance to
B. cinerea in Arabidopsis and P. lingam in rapeseed, increasing the expression of genes
related to SA- and JA- mediated defense pathways [123]. Other SM can regulate virulence
genes from the pathogen, such as Epl-1 from T. harzianum, which represses virulence genes
in B. cinerea, and induces SA- mediated defense pathway and priming in tomato plants,
conferring resistance to the pathogen [119]. SM from culture filtrates of T. harzianum and
Plants 2023, 12, 432 16 of 35
the fungus diminished the adverse effects that Fusarium culmorum causes in wheat plants,
such as reduced germination or lower plant growth, and modified antioxidant enzymatic
activity, overall conferring protection against the pathogen [122].
T. harzianum is a proficient secondary metabolites producer. This ability works in
its favor as a BCA, regulating and inhibiting the growth of several phytopathogens and
using its SM to induce plant resistance, protecting plants not just in a direct manner but
indirectly as well. This makes the study of secondary metabolites produced by Trichoderma
an important subject to take advantage of in agriculture.

T. harzianum is effective at inducing plant defense systems against insects, such as
with the feeding insect Nezara viridula, whose growth is impaired in tomato plants that
had been inoculated with T. harzianum T22, also inducing the expression of loxD and PIN2
genes, related to the JA-mediated defense pathway in the plants [124]. T. harzianum T22
also induces a strong plant VOCs priming in tomatoes, attracting the parasitoid A. ervi, so
the plants can defend themselves against the aphid M. euphorbiae [126], reprogramming
the plant transcriptome and metabolome to favor induction of JA, Et and ISR defense path-
ways, and increasing isoprenoid biosynthesis, leading to a strong defense response against
M. euphorbiae [127].
Besides, T. harzianum can also induce resistance against other pathogens, such as ne-
matodes. T. harzianum diminishes infection symptoms caused by the nematode Meloidogyne
incognita in tomato plants, inducing the gene expression of PR1, PR5, JERF3, and ACO,
which are related to SA- and JA/Et- mediated defense responses in plants [125].
The production of ROS is one of the defense responses in a plant that can be induced
by beneficial microbes, such as T. harzianum induction of accumulation of H2 O2 and other
important defense-related enzymatic activity, such as SOD, in tomato plants, upon infec-
tion with F. oxysporum f.sp. lycopersici [104]. To confer protection against F. oxysporum,
T. harzianum colonizes cucumber roots reducing ROS and reactive nitrogen species (RNS)
accumulation caused by the pathogen, promoting redox homeostasis, and increasing
antioxidant enzymatic activity to enhance plant protection [129]. T. harzianum induced
priming, defense-related enzymatic activity (PAL, POX, PPO), as well as antioxidant enzy-
matic activity (SOD, catalase (CAT), and others) in chili pepper plants upon infection with
C. truncatum, also diminishing the symptoms caused by the pathogen and ROS induced
accumulation, protecting the plant against its pathogen [112].
A defense-related enzymatic activity such as PAL, POX, CAT, and ascorbate peroxidase
is induced by inoculation with T. harzianum UBSTH-501 in wheat plants, conferring resis-
tance against Bipolaris sorokiniana infection, and promoting SA and phenolic compounds
accumulation, as well as lignin and suberization in leaves, to reinforce plant defense [128].
Upon infection of tomato plants with A. cerealis, T. harzianum induces the accumulation
of different phenolic compounds, such as flavonoids and terpenoids, and increases the
plant antioxidant enzymatic activity, diminishing the infection caused by A. cerealis [106].
Soybean plants treated with T. harzianum T-soybean showed less cellular death caused by
F. oxysporum and increased protection against the pathogen [107].
It is worth noting that the induction of plant defense systems mediated by T. harzianum
causes the plant to reprogram its metabolite synthesis to favor the production of compounds
that can help the plant to defend itself against pathogens that cannot be directly attacked
by T. harzianum, such as aphids or viruses, conferring this way a whole protection against
different kinds of phytopathogens.
4.3. Trichoderma Asperellum

T. asperellum grows well in temperatures ranging from 25 ◦ C to 30 ◦ C, and it is a
cosmopolitan species, found frequently in agricultural and undisturbed soils and plant
material, with lifestyles ranging from saprotrophy to biotrophy [183]. Conidia appear after
5 days and are dark green in color, forming at the center of the colony in Petri dishes [135].
Plants 2023, 12, 432 17 of 35
Along with T. atroviride, T. asperellum is considered a strong mycoparasite of different

plant pathogenic fungi by competition, hyperparasitism of host or antibiosis, and it can
induce plant resistance [112,135,184]. Below, we present examples of the direct and indirect
biocontrol mechanisms used by T. asperellum.

In dual culture between several strains of Trichoderma, with the phytopathogens Fusar-
ium camptocerus, F. oxysporum, A. alternata, F. solani, Colletotrichum gleosporoides, Ganoderma
applanatum, B. cinerea and Cytospora chrysosperma, the Trichoderma strain TaspHu1, identified
as T. asperellum, showed better biocontrol traits, inhibiting the growth of the pathogens
by showing mycoparasitic activity and competition for space and nutrients [130]. In a
dual confrontation assay, T. asperellum inhibits the growth of the chili pepper pathogen
Colletotrichum truncatum, competing for space [112].
In dual confrontation assays, T. asperellum IMI393899 showed a mycoparasitic capacity
of several fungal pathogens, including Neofusicoccum batangarum, N. parvum, C. gloeosporoides,
Phytophthora nicotianae, Phytophthora parvispora, Penicillium digitatum, P. roqueforti, P. verrucosum,
Fusarium proliferatum, F. sporotrichoides, F. langsethiae, F. graminearum and F. poae [92].
T. asperellum T1 showed antifungal activity in dual confrontation assays against the pathogens
Corynespora cassiicola and Curvularia aeria, the causal agents of leaf spot in lettuce, in-
hibiting the growth of the pathogens, and overgrowing them in the Petri dish [134].
Confrontation of T. asperellum 6S-2 against the apple pathogen Fusarium proliferatum
f.sp. malus domestica MR5 leads to the degradation of the pathogen mycelia during the
mycoparasitic interaction [133]. In dual culture antagonism assays, T. asperellum TA showed
mycoparasitic activity against the white-rot fungus Phellinus noxius, conferring resistance
in Eryobotria japonica plants in an in planta assay, showing fewer symptoms caused by
the pathogen [136]. Additionally, T. asperellum GDSF1009 showed biocontrol traits by
competing and mycoparasite the pathogens F. oxysporum f.sp. cucumerinum Owen and
F. graminearum, reducing their growth [135].
Trichoderma species are also used in agriculture because some of them are resistant to
several abiotic stresses. T. asperellum ACCC30536 salt-tolerant mutants T3 and T5 showed
antifungal capacity against R. solani and A. alternata under salt stress conditions, conferring
resistance in PdPap plants by activating SOD, CAT, and POD enzymatic activities [132].
This shows the potential of isolating strains from extreme environments or conditions to
favor plant growth under stressful situations.
Besides parasitizing other fungi, T. asperellum GDFS1009 is capable of parasitizing the
moth Ostrinia furnacalis, a maize pest, when it ingests the BCA conidia, and when inoculated
in maize plants, T. asperellum GDFS1009 induces POD, SOD, proline, protease, and PPO
activities, increasing defense against the moth, and the co-inoculation with the well-known
entomopathogen Beauveria bassiana has a better protection effect in the plants [131].
It is noteworthy the potential of T. asperellum as a mycoparasite, showing that it cannot
only parasitize in a strong manner fungal pathogens but other plant pests such as moths.
Moreover, the resistance of this fungus to abiotic stresses makes it a good candidate for
agricultural uses in extreme conditions, protecting and promoting the growth of important
crops under these circumstances.

As mentioned before, vel1 is involved in secondary metabolite biosynthesis. Its overex-
pression in T. asperellum induces the expression of defense-related genes in maize plants, con-
ferring resistance against the pathogens Cohilohorus herostrophus and Fusarium verticilloides
and the co-culture of T. asperellum with B. amyloliquefaciens provides better protection against
the pathogens [143].
Secondary metabolites from T. asperellum that can induce defense responses in plants
include Epl1-Tas, which induces the expression of genes related to the SA-mediated defense
pathway (NPR1, TGA, and PR1), JA-mediated defense pathway (COI1, JAZ, MYC2, and
Plants 2023, 12, 432 18 of 35
ORCA3) and auxin signaling (TIR1 and ARF1) in Populus davidiana × P. alba var. pyramidalis
(PdPap), and increases defense-related enzymatic activity, conferring over 90% more resis-
tance to the pathogen A. alternata [137]. The expression in planta of the class II hydrophobin
HFBII-4 from T. asperellum ACCC30536 in PdPap plants alters the expression of genes
related to auxin signaling, SA and JA defense pathways, and defense-related enzymatic
activity (PAL, POD, PPO enzymes), reducing ROS accumulation and diminishing lesion
area caused by A. alternata [138].
Secondary metabolites from T. asperellum GDFS1009 contained in fungal fermented
broth, alone or in combination with B. amyloliquefaciens, showed antagonistic activity against
F. graminearum, F. oxysporum, and B. cinerea, and conferred resistance to F. graminearum
in wheat plants [139]. Ethyl acetate extract and the fungal filtrate from T. asperellum IMI
393,899 showed growth inhibition activity and strong cytotoxic activity against 25 pathogens,
including Penicillium spp., Aspergillus spp., Fusarium spp., Neofusicoccum spp., Colletotrichum spp.
and Phytophthora spp. [92].
Some of the secondary metabolites from Trichoderma species that have antibiotic activity
are peptaibols [63], such as crude fungal extract containing peptaibols from T. asperellum
IRAN 3062C, showing the growth inhibition of Micrococcus luteus, R. solani and A. solani, and
inhibition of spore germination in A. solani, R. solani and Fusarium monilifome [140]. Another
SM, such as the VOC 6-PP and the filtrate from T. asperellum P1, inhibits the growth of the
maize pathogen Magnaporthiopsis maydis [141]. In field conditions, T. asperellum P1 confers
resistance in maize plants to M. maydis [162]. Filtered fermentation extract from T. asperellum
GDFS1009 inhibited the growth of the pathogens F. oxysporum f.sp. cucumerinum Owen and
F. graminearum in 67.59% and 100%, respectively, and induced resistance in tobacco and
cucumber plants, observed as increased defense-related enzymatic activity [135]. The crude
citric acid extract from T. asperellum showed antagonistic capacity against F. oxysporum f.sp.
lycopersici, inhibiting its growth and diminishing the severity of the symptoms caused by
this pathogen in tomato plants, increasing PPO and POD enzymatic activity [142].
Secondary metabolites such as VOCs can have growth inhibitory effects over pathogens,
such as VOCs released by T. asperellum T76-14, which in vitro assays show growth inhi-
bition of the melon pathogen Fusarium incarnatum, also preventing the postharvest rot in
melon fruits caused by this pathogen [144]. Both VOCs and liquid fermentation extract
from T. asperellum 6S-2 can inhibit the growth of the pathogen Fusarium proliferatum f.sp.
malus domestica MR5 and the liquid extract also showed the capacity to inhibit pathogen
spore formation [133].
The secondary metabolites, both volatile and non-volatile, produced by T. asperellum
show the capacity to inhibit fungal pathogen growth and to induce plant defense systems.
This suggests the versatility of the SM from this fungus to act as an important biocontrol
mechanism and its potential to be used in agriculture.

T. asperellum TaspHu1 increases resistance in tomato plants against A. alternata inducing
the plant defense pathways, which was observed by an increase in JAR1, MYC2, NPR1, PR1,
and GH3.2 gene expression, genes involved in JA- and SA-mediated defense signaling [130].
T. asperellum T42 induces a hypersensitive response (HR) in Pisum sativum plants upon
infection with Erysiphe pisi, observed as an increased antioxidant enzymatic activity and
lignin accumulation in the plants, and the co-culture with Pseudomonas fluorescens has
a stronger HR induction in the plants [145]. T. asperellum induced priming, increased
defense-related enzymatic activity, and antioxidant enzymatic activity in chili pepper
plants upon infection with C. truncatum, diminishing the symptoms caused by the pathogen
and conferring resistance in the plant [112]. Root dipping with T. asperellum T1 increases
β-1,3-glucanase, chitinase, POX, and phenol oxidase activity in lettuce, inducing resistance
against the pathogens C. cassiicola and C. aeria [134].
Plants 2023, 12, 432 19 of 35
The inoculation of T. asperellum in tomato plants reduces the ROS accumulation caused
by the pathogens B. cinerea and F. oxysporum. It induces ISR in the plants upon B. cinerea
infection, reducing the symptoms caused by the pathogen [146].
Along with the strong mycoparasitic capacity of T. asperellum, its ability to induce
plant resistance and confer protection against different pathogens makes this fungus an
extraordinary example of an efficient BCA that is already one of the most ubiquitous
Trichoderma species. Thus, its application in agricultural fields may be facilitated.
4.4. Trichoderma Virens

T. virens is a ubiquitous fungus isolated from soil and plant matter. In nature, two
strains can be identified and distinguished by their secondary metabolite production:
strains “Q” and strains “P”. Q strains are characterized by the production of gliotoxin,
dimethylgliotoxin, viridiol, and viridin. Meanwhile, P strains produce gliovirin, heptelidic
acid, viridiol, and viridin, but no gliotoxin nor dimethylgliotoxin [185].
Gliotoxin and gliovirin are two important metabolites produced by this fungus with
strong toxic activity and roles in the establishment of beneficial interactions with plants
and in pathogenic interactions with plant pathogens [186,187]. Hence, the strong use of
secondary metabolites as a primary mechanism of biocontrol by this fungus. Nonetheless,
mycoparasitism is also important for the biocontrol capacity of T. virens, along with the
induction of plant defense responses to protect plants against different pathogens.

T. virens is an effective mycoparasite and antagonist of several plant fungal pathogens,
such as F. oxysporum f.sp. physalia, whose growth is inhibited in dual confrontation with
T. virens Gl006, alone or in combination with Bacillus velezensis Bs006 supernatant. Nonethe-
less, the major reduction in the pathogen’s growth is when confronted with the BCA alone
(above 70%) [147]. In dual confrontation assays, T. virens ZT05 showed mycoparasitic
activity over R. solani, penetrating the pathogen hyphae [148], thus inhibiting its growth.
Its mycoparasitic abilities have been known for several decades, when it was first observed
as coiling hyphae around R. solani back in 1932 by Weindling, R. [50].

Secondary metabolites produced by microorganisms can be tested using cell-free
supernatants, such as the cell-free supernatant from T. virens Gl006, which alone or in com-
bination with cells or cell-free supernatant from B. velezensis Bs006, has antagonistic activity
over F. oxysporum f.sp. physalia, diminishing disease severity caused by this pathogen in
Physalia peruviana plants [147]. Culture filtrates from T. virens TriV_JSB100, or the fungus,
induces priming in tomato plants upon infection with F. oxysporum f.sp. lycopersici, dimin-
ishing the symptoms caused by the pathogen [154]. Jogaiah and collaborators [154] also
noted that the inoculation of T. virens induced the JA-mediated defense pathway in the
plant. In contrast, the fungal culture filtrate primarily induces the SA-mediated defense
pathway, resulting in an overall resistance to the pathogen.
Some secondary metabolites are antibiotics, such as viridin from T. virens IMI 304061,
one of the main SMs found in the culture filtrate from an SM-overexpressing strain from
T. virens IMI 304061, named G2, which has better antibiosis effect over the pathogen Pythium
aphanidermatum and confers greater protection in Cicer arietinum plants against Sclerotium
rolfsii [149]. Gliotoxin from T. virens T23 is important to control S. rolfsii, causing structural
damage to the pathogen hyphae [188]. The volatile and non-volatile SMs from T. virens
ZT05 showed growth inhibition of R. solani at 80.1% and 63.32% respectively. The non-
volatile SMs repressed defense-related enzymatic activity in R. solani, indicating that the
BCA could regulate the defense mechanism of the pathogen against the mycoparasite [148].
Chitinase and cellulase protein activity are important traits in BCA. Several T. virens
mutant strains with enhanced chitinase and cellulase activities showed to be more effective
Plants 2023, 12, 432 20 of 35
at inhibiting R. solani growth in dual confrontation assays than the T. virens wild-type
strain [150].
Secondary metabolites biosynthesis is regulated by different enzymes, such as p450
monooxygenases [189]. Tvcyt2 is a member of the p450 monooxygenases in T. virens and
is involved in SM biosynthesis [151]. Ramírez-Valdespino and collaborators [151] found
that the overexpression of tvcyt2 results in a higher concentration of SMs, leading to an
increased antagonistic activity against R. solani AG2 and a stronger JA- and SA-mediated
defense response in Arabidopsis plants.
Some other SMs can induce plant resistance, such as the intracellular siderophore
ferricrocin from T. virens, which is involved in inducing ISR in maize upon infection with
the pathogen Cochliobolus heterostrophus, since null mutants in the gene tex10, the one coding
for ferricrocin, failed to induce ISR in the maze, and were more aggressive at colonizing the
plants [152]. TvPG2, a constitutive endopolygalacturonase from T. virens I10, is involved in
inducing ISR in tomato plants against B. cinerea, regulating the expression of the inducible
tvpg1 gene coding for TvPG1 endopolygalacturonase, which leads to the resistance against
the pathogen [153].

T. virens can induce plant defense systems, conferring resistance to different pathogens;
for example, T. virens IARI-P3 induces PR10 gene expression in susceptible and resistant
Vigna radiata plants when infected with R. solani, reducing significatively disease symptoms
caused by the pathogen [155]. T. virens induces ISR in maize plants by increasing gene
expression of two oxylipins coding genes, 12-OPDA (12-Oxo-10(Z),15(Z)-phytodienoic
acid) and an Υ -ketol, 9,10-KODA (10-oxo-9-hydroxy- 12(Z), 15(Z)-octadecadienoic acid),
granting resistance to the pathogen Colletotrichum graminicola [156,157].
T. virens has been one of the most used BCA among the Trichoderma genus. It is
an important secondary metabolite producer with biocontrol activity against many phy-
topathogens. Its secondary metabolites show great potential to be used in agriculture
to control phytopathogens and to induce plant protection against them. Besides, along
with other secondary metabolites from Trichoderma spp., compounds such as gliotoxin are
showing medical applications as possible treatments against cancer [190–192], suggesting
the span of applications that this fungus has, not being limited to agricultural uses.
4.5. Trichoderma Longibrachiatum

T. longibrachiatum is frequently isolated from agricultural soils, mushrooms, and
marine environments, and it grows better at tropical temperatures rather than in temperate
climates [193]. This fungus has been reported to cause cardiac and pulmonary mycoses in
immunocompromised humans [194–196]. Nonetheless, it has also been reported to be used
as an important biocontrol agent [159,169], exerting parasitism and inducing plant defense
systems, along with the production of several important secondary metabolites, as shown
by the examples described below.

In dual confrontation assays, T. longibrachiatum EF5 showed mycoparasitic activity
against M. phaseolina, showing hyphal entanglement between both fungi [161], and antago-
nistic activity with mycelia modifications on M. phaseolina and S. rolfsii [158].
T. longibrachiatum (TG1) coils around Fusarium pseudograminearum in a mycoparasitic in-
teraction. In a tripartite interaction with wheat plants under salt stress conditions, the
BCA reduces the disease symptoms caused by the pathogen [159]. Tested under field
conditions, T. longibrachiatum T7407 had a negative effect in the presence of the pathogen
Magnaporthiopsis maydis in soil by competing with it, thus protecting maize plants from
this pathogen and diminishing disease incidence [162]. Besides being a mycoparasite,
T. longibrachiatum T6 can parasitize eggs and second-stage juveniles from the plant pathogen
nematode Heterodera avenae, reducing its viability [160].
Plants 2023, 12, 432 21 of 35
The parasitic ability of T. longibrachiatum is a trait that should be exploited more,

especially since it is a parasite of important fungal and nematode phytopathogens, but
should be taken carefully under field applications, considering that it is the only fungus
from the genus Trichoderma to be reported as an opportunistic human pathogen so far.

Peptaibols are SMs with antibiotic activity, as mentioned before [63]. The crude fungal
extract from T. longibrachiatum containing peptaibols showed antibacterial activity against
the pathogen M. luteus [140]. Synthetic analogs to the peptaibol Trichogin GA IV from
T. longibrachiatum are effective antagonistic compounds to inhibit Pyricularia oryzae, a rice
pathogen. They can reduce disease symptoms in barley and rice plants [164], which indi-
cates that those synthetic analogs could be used as biocidal compounds instead of chemical
compounds. The crude fungal extract containing peptaibols from T. longibrachiatum IRAN
3067C showed growth inhibition of several plant pathogens, mainly effective against
R. solani and A. solani [140].
Other SMs with antibiotic activity includes dendrobine from T. longibrachiatum MD33,
which is an endophyte of the plant Dendrobium nobile, known to be the only plant producing
dendrobine [163,197]. Sarsaiya and collaborators [163] showed that the T. longibrachiatum
MD33 has strong antibacterial activity against Bacillus subtilis, B. mycoides, and Staphylococcus sp.,
showing the potential of this BCA to inhibit pathogenic bacteria. Three cyclodepsipeptides
and six sesquiterpenes compounds identified among the SM produced by T. longibrachiatum
showed antibiotic activity against several plant pathogens [166]. Only the three cyclodep-
sipeptides and two sesquiterpenes identified by Du and collaborators [166] inhibited the
growth of the nematode Meloidogyne incognita, and just the remaining four sesquiterpenes
were able to inhibit the fungal pathogens Colletotrichum lagrnarium, C. fragariae, B. cinerea
PTQ1, and CMQ1, F. oxysporum f.sp. cucumerinum and F. oxysporum f.sp. lycopersici, show-
ing pathogen specificity of the SM tested. Culture filtrate containing 13 SMs, known as
sorbicillinoids, from T. longibrachiatum SFC100166 showed in vitro growth inhibition of the
pathogens Alternaria brassicola, B. cinerea, Colletotrichum coccodes, Cladosporium cucumerinum,
Cylindrocarpon destructans, Magnaporthe oryzae and Phytophthora in festans [167]. When
tested separately, eleven of the sorbicillinois identified inhibited the pathogens tested, with
P. infestants being the most affected by the compounds, and four sorbicillinois were able to
induce resistance in tomato plants against this pathogen [167]. VOCs from T. longibrachiatum
EF5 inhibited the growth of the pathogens S. rolfsii (57%) and M. phaseolina (35%) by al-
tering mycelia structure [158], suggesting that these compounds may be important to the
biocontrol traits of T. longibrachiatum.
Some secondary metabolites induce plant defense responses, such as the hydrophobin
HYTLO1 from T. longibrachiatum MK1, which is perceived by Lotus japonicus, activating the
expression of Ca2+ -mediated signaling, leading to the induction of defense-related genes in
the plant [165].
Some SMs from T. longibrachiatum have biocontrol activity over other organisms,
such as the ethyl acetate extract from T. longibrachiatum AUMC 5125 that has effective
antibiotic activity over the cotton aphid Aphis gossypii [168]. Fermentation crude extract
from T. longibrachiatum T6 showed antagonistic activity against eleven phytopathogens
tested, being especially effective against Valsa mali¸ inhibiting up to 95% [169].
As shown by the examples above, secondary metabolites from T. longibrachiatum play
important roles in its biocontrol capacity, and considering that this fungus may cause
human diseases, SMs could be studied to be used alone, without the need for the microor-
ganism, diminishing health concerns about the use and introduction of microorganisms in
the environment.

T. longibrachiatum H9, a novel strain, colonized cucumber roots promoting plant
growth and inducing JA/Et and SA defense signaling pathways, conferring resistance in
Plants 2023, 12, 432 22 of 35
cucumber to the pathogen B. cinerea [77]. In a greenhouse experiment, T. longibrachiatum

T6 induced flavonoid and lignin content, as well as defense-related enzymatic activity in
wheat roots, conferring resistance against the nematode H. avenae [160].
T. longibrachiatum has shown to be a versatile biocontrol agent, parasitizing not only
fungi but nematodes as well, and it is a good secondary metabolite producer, being used to
obtain important compounds such as peptaibols. This fungus has good potential to be an
efficient BCA, and its traits could be exploited in field conditions, considering the potential
to use SMs in substitution of synthetic compounds.
4.6. Trichoderma Viride

T. viride has optimal growth at 25 ◦ C and does not grow at 35 ◦ C; it can be isolated
from soil and organic matter, some of its strains have a faint coconut smell, and coni-
dia can be observed after 2 days. T. viride is considered the type species of the genus
Trichoderma [173,198], and it is one of the most common species found in soil.
T. viride has been used as a biocontrol agent, especially due to its mycoparasitic ability.
It has been reported that T. viride can mycoparasite fungal pathogens such as F. moniliforme,
Cryphonectria parasitica, and Schizophyllum commune [199–202]. The use of commercial chiti-
nases derived from T. viride causes damage to the silkworm Bombix mori [203], suggesting
the ability of this fungus to degrade chitin from insects that could cause plant diseases.
Below, we present recent examples regarding the biocontrol mechanisms of T. viride.

By competing for space and nutrients in dual culture assays, T. viride showed an-
tagonistic activity against the pathogen Sclerotinia sclerotiorum, presenting a clear zone
of inhibition in the culture plates on day 4 of interaction, indicating antibiosis mecha-
nisms exerted by T. viride over the pathogen, and a 67.284% growth inhibition by day 6 of
confrontation [170].
In dual confrontation assays, T. viride showed antagonistic activity against the pathogens
Fusarium solani, R. solani, and S. rolfsii, limiting their growth by 29.76%, 15.27%, and 19.73%,
respectively [171].

T. viride produces SM with antifungal activity. The crude mycelial extract and the
ethanolic extract from this fungus showed antifungal activity against Candida albicans,
Fusarium solani, F. oxysporum, R. solani, and Pythium ultimum, and antibacterial activity
against Bacillus subtilis, Escherichia coli, and Pseudomonas fluorescens showing inhibition
zones in the culture plates. In contrast, the VOCs produced by T. viride showed antibacterial
activity against B. subtilis and E. coli and antifungal activity against C. albicans, F. solani, and
R. solani [171].
VOCs from T. viride BHU-V2 showed antagonistic activity against S. rolfsii, inhibiting
the pathogen growth both in vitro and in soil experiments. It was determined that VOCs
are capable of altering the structure of the pathogen hypha, thus limiting its growth [172].
Singh and collaborators [172] also showed that VOCs from T. viride increase PAL, PPO,
chitinases, and β-1,3-glucanase activity in okra plants, inducing resistance and diminishing
cell death caused by S. rolfsii.

In glasshouse experiments, inoculation of T. viride alone or in combination with
Trichoderma erinaceum suppressed the disease caused by Sclerotinia sclerotiorum in
Phaseolus vulgaris cv. Anupama plants. Nonetheless, the combination of the BCAs had
better results [170]. Kumar and collaborators [170] also found that plants pretreated with
either Trichoderma species or their combination reduced ROS accumulation induced by the
pathogen, enhancing antioxidant activity in the plants.
Plants 2023, 12, 432 23 of 35
Despite being the species reviewed here with less recent literature regarding its bio-
control traits, T. viride has been studied as a plant growth promoter or enhancer of desirable
traits in plants [204,205] or as an important organism in bioremediation or preparation of
surfaces for bioremediation of toxic organic compounds such as toluene [206] or TNT [207]
or heavy metals such as lead [208]. These make an interesting Trichoderma species to study
further in various possible applications, not limited to agricultural uses.
4.7. Other Trichoderma Species

Besides being the most used Trichoderma species as biocontrol agents and/or plant
growth promoters [55], other species are surfacing. T. lignorum, in combination with
B. bassiana, was effective at controlling leafcutter ants (Atta cephalotes) populations [209].
T. koningii reduced disease severity in grapevines caused by the pathogens Phaeomoniella
chlamydospora and P. minimum [210]. T. erinaceum can suppress an infection caused by
S. sclerotiorum in bean plants [170]. It is also capable of overgrowing R. solani and inducing
ROS and defense-related enzymatic activity in rice plants [211]. T. citrinoviride resulted in
an effective mycoparasite of six pathogens of ginseng plants: R. solani, B. cinerea, Alternaria
panax, Cylindrocarpon destructans, Phytophthora cactorum, and Pythium spp. [212].
These studies about other Trichoderma species, and the constant reports of new iso-
lates and their applications in industry and medicine, for example, show the diversity of
species belonging to this genus and their potential to be used outside of the traditional
plant growth promotion and biocontrol abilities attributed to Trichoderma since it was first
described. Hence, not only new isolates or species should be of interest, but additional
information about the “classic” Trichoderma species and its applicability in other fields could
be addressed.
5. Other Biocontrol Strategies Involving Trichoderma spp.

Besides the direct or indirect use of Trichoderma spp. in the biocontrol of plant
pathogens, that is, applied in field or greenhouse conditions as conidia, hyphae, a mix of
its metabolites, other new and forthcoming biocontrol strategies have been arising over
the past years. These include the combined use or co-inoculation of Trichoderma species
with plant growth-promoting bacteria or mycorrhizae, where the co-inoculation of the
BCA T. viride and several arbuscular mycorrhizal fungi (AMF) such as Rhizoglomus clarum,
Funneliformis monosporum, Acaulospora laevis, and Dentiscutata nigra, had a positive and
synergistic effect on the overall health of Allium cepa plants [205], and the co-inoculation
of T. harzianum with Bacillus sp. proved effective in controlling the disease caused by
F. oxysporum f.sp. capae on shallot plants [213].
Trichoderma species are not only capable of cooperating with other beneficial mi-
crobes, but they can even change the plant rhizosphere microbiome and microbial com-
munities, favoring plant resistance against several pathogens. T. harzianum CCTCC-
RW0024 modifies the rhizosphere microbiome in maize plants, conferring resistance against
F. graminearum [73]. Moreover, T. harzianum changes microbial communities in the rhizo-
sphere of Piper nigrum plants, favoring the presence of other beneficial microbes [214]
and diminishing the incidence of Plasmodiophora brassicae, Alternaria sp. and Fusarium sp.
pathogens in the rhizosphere of cabbage plants [215]. The presence of T. asperellum M45a
in the watermelon rhizosphere modifies microbial composition, increasing the presence
of plant-growth-promoting rhizobacteria and reducing the presence of plant pathogenic
fungi, and disease incidence caused by Fusarium oxysporum f.sp. niveum in watermelon
plants [216]. T. asperellum also modifies endophytic microorganisms’ population in maize
stalk, increasing resistance against F. graminearum and F. verticilloides [217]. This information
suggests that changes in the microbiome could have a biocontrol effect on important plant
pathogens, thanks to the presence of Trichoderma species.
Trichoderma has also been used for the green biosynthesis of nanoparticles and their
subsequent use in agriculture. Ag, ZnO, and CuO nanoparticles have been biosynthesized
using T. harzianum, and those nanoparticles showed an inhibitory effect over A. alternata,
Plants 2023, 12, 432 24 of 35
Pyricularia oryzae, and S. sclerotiorum [218], and ZnO nanoparticles showed biocontrol
capability against Fusarium sp., R. solani and M. phaseolina, three important pathogens of
cotton plants [219]. T. viride has also been used to synthesize TiO2 , showing larvicidal and
pupicidal effects on Helicoverpa armigera, a pest of important crops such as maize, wheat,
and beans [220]. This shows that Trichoderma can be used as a bio-tool to obtain chemical
products that are beneficial in agriculture, in substitution of chemical fungicides [221].
These new approaches aim to minimize the harmful effects on health and the envi-
ronment that chemical fungicides present. Trichoderma seems to have an important role in
replacing chemical agricultural products.
6. Trichoderma Bioformulations in Agriculture for Use in Biocontrol

The use of Trichoderma as a biocontrol and plant growth promoter in agriculture is
not new. There is significant research about the bioformulations that are most effective in
the field, as well as the issues regarding the use and distribution of such products, such
as acceptance from the farmers’ community, the introduction of different species in the
environment, and their efficacy compared to chemical fertilizers and pesticides [12,222–224].
Hence, the importance of producing or manufacturing Trichoderma-based products, alone
or in combination with other BCA, is their efficacy when tested so that the consumers
will receive them well and would be willing to switch to bioformulations and use fewer
chemical products on their crops.
Several Trichoderma-based formulations have been tested under greenhouse or field
conditions, showing positive results such as increased plant growth, production, and
resistance against diseases.
Wong and collaborators [62] combined T. harzianum CBF2- with Pseudomonas aeruginosa
DRB1 using four different formulations: Pesta granules, Talc powder, alginate beds, and
liquid formulation, and these bioformulations were tested to biocontrol F. oxysporum f.sp.
cubense, the causing agent of banana wilt. Pesta granules and Talc powder were more
efficient at diminishing disease symptoms in the plant (66.67% and 58.33%, respectively),
followed by alginate beds (46.75%) and liquid formulations (43.06%). The four formulations
were better than the application of Benomyl, a known chemical antifungal agent, with only
a 37.50% reduction in disease symptoms [62]. As Pesta granules formulation, both BCA
were viable for at least 180 days when stored at 4 ◦ C, and the formulation showed better
performance in BCA viability and storage [62].
Using five different agro-based wastes (vermicompost, vegetable wastes, used tea
leaves, sugarcane bagasse, and cow dung) to grow T. lixii TvR1 and use as bio-products,
sugarcane bagasse was the most efficient substrate to grow Trichoderma, and in pot experi-
ments using spinach, promoted the plant growth [225]. Using a formulation of T. asperellum
in coconut fiber promoted the growth of tomato plants and conferred resistance against
F. oxusporum f.sp. lycopersici in field trials [226]. T. harzianum grown on a spent mush-
room substrate (SMS) of Pleurotus ostreatus showed growth promotion in tomato plants
and increased disease resistance against F. oxysporum f.sp. lycopersici. The bioformulation
used was the best among several substrates, including combinations of SMS with paddy
straw [227]. Two formulations from T. citrinoviride, dustable powder and granules, were
effective against B. cinerea and C. destructans in vitro. Both were effective at preventing
disease caused by A. panax in ginseng plants [213].
Seeds of chickpea and lentils treated with a formulation made with the mutant strain
T. virens G2 on tamarind seeds and talcum powder, named TrichoBARC, improved yield
and reduced seed mortality in chickpea and lentils in field trials, and induced resistance
against S. rolfsii in chickpea plants [149]. Seed-coating with a bioformulation made with
T. harzianum and chitosan-PEG as the delivery system showed antagonistic activity against
F. oxysporum, M. phaseolina, and Aspergillus niger, the bioformulation also promoted the
growth of safflower and groundnut plants, and resistance against M. phaseolina and
A. niger [228].
Plants 2023, 12, 432 25 of 35
Commercial formulations T34 Biocontrol (Biocontrol Technologies S.L) from T. asperellum

T34 and Trianum P (Koppert) from T. harzianum T22 induced systemic resistance in tomato
plants, repressed reproduction of the plant nematode Meloidogyne incognita and, T34 Bio-
control also reduced the nematode infectivity [229]. The commercial product Xedavir made
with T. asperellum (Xeda International® ) was tested in vitro against F. graminearum and
F. verticilloides [230]. As spore suspension, Xedavir inhibits germination of F. graminearum up
to 53%, F. verticilloides up to 22%, and as the cell-free extract, Xedavir inhibits F. graminearum
and F. verticilloides germination up to 82% and 76%, respectively. Xedavir also showed
the capacity to inhibit the production of the mycotoxin deoxynivalenol (DON) from
F. graminearum [230].
One concern about the use of BCA in the field is precisely the introduction of species in
the environment, which is why some studies are focusing on using local BCA strains [231].
Nonetheless, another option to avoid the use of whole microorganisms is the use of elicitor
agents. Nandini and collaborators [232] formulated nanoemulsions using total lipids
extracted from six Trichoderma species. The nanoemulsion from T. brevicompactum showed
a remarkable capacity to induce resistance and hypersensitive response in pearl millet
plants against the downy mildew pathogen Sclerospora graminicola, both in vitro and in
field conditions [232], showing the feasibility of using elicitors from the microorganisms,
without the necessity for the living organism.
The results of field or greenhouse testing of the Trichoderma-based formulations are
promising, and studies regarding this issue should complement in vitro assays of its bio-
control capacity, to facilitate the application and distribution of bioformulations.
7. Conclusions
The use of chemical pesticides and fertilizers has been detrimental to human and envi-
ronmental health. That is why the search for more sustainable and environmentally friendly
solutions has led to the research of organisms as biocontrol agents. Such as Trichoderma,
which possesses different biocontrol traits, which makes it one of the most effective organ-
isms studied against various types of plant pathogens, not being limited to controlling
fungi and oomycetes, but insects, pests, and nematodes as well, either by limiting their
growth by competition, antibiosis, or parasitism, or by enhancing plant protection against
them, making this fungus a versatile option to control several phytopathogens.
Trichoderma has been used in different types of formulations in agriculture, mainly to
promote plant growth and increase crop yield. Nonetheless, the use of Trichoderma-based
formulations for the control of pathogens also needs to be considered in studying such
products, especially under field conditions, since most of the studies that consider this
aspect are done in vitro in dual confrontations.
Another interesting point to remark on is the use of secondary metabolites from
Trichoderma or green biosynthesis of nanoparticles using this fungus, which can be used
in agriculture to promote plant growth or to inhibit pathogen growth without the fungus
per se, or using Trichoderma strains isolated from local environments, eliminating the
introduction of foreign strains into the environment.
It is clear that the different Trichoderma species are used as mycoparasites, and specific
species such as T. atroviride or T. harzianum are among the strongest and classic mycopar-
asites. Nonetheless, there are emerging Trichoderma species that have been isolated and
applied from local areas and are promising candidates as biocontrol agents. Trichoderma
as biocontrol agents started being studied as mycoparasites. Nonetheless, its use against
other plant pathogens such as nematodes and insects is gaining notice due to the different
mechanisms it has to exert control of such a variety of plant pathogens, regulating both soil
and aerial-borne diseases.
There is still much to be done regarding applying Trichoderma-based formulations
in field conditions and interaction with other soilborne microorganisms to understand
better its interaction within the plant microbiome and its biocontrol traits. This a field to be
exploited in depth for further research.
Plants 2023, 12, 432 26 of 35
Author Contributions: P.G.-G.: Conceptualization, Writing—Original draft preparation. A.K.:

Writing—Review & Editing. S.d.l.S.-V.: Writing—Review & Editing. F.I.P.-C.: Writing—Review
& Editing. M.d.C.O.-M.: Writing—Review & Editing. A.E.F.: Writing—Review & Editing. S.H.:
Writing—Review & Editing. O.O.B.: Writing—Review & Editing. G.S.: Conceptualization, Writing-
Original draft preparation, Supervision. All authors have read and agreed to the published version
of the manuscript.
Funding: This research was funded by CONACYT-México (Proposal: A1-S-15956) and CIC-UMSNH
(2021–2022).
Data Availability Statement: Not applicable.
Acknowledgments: G.S. thanks CONACYT-México (Proposal: A1-S-15956) and CIC-UMSNH
(2021–2022) for financial support to our research projects.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or
in the decision to publish the results.
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6 Trichoderma Species Our Best Fungal Allies

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plants

1 Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo,

Received: 19 December 2022

Plants 2023, 12, 432. https://doi.org/10.3390/plants12030432 https://www.mdpi.com/journal/plants

includes fungal and oomycete pathogens, such as Acremonium cucurbitacearum, Alternaria

2. An Overview of the Genus Trichoderma

ployed by PGPB, which exhibits efficient colonization mechanisms to occupy rhizospheric

4. Biocontrol Potential of Registered Trichoderma Species

4.1. Trichoderma Atroviride

4.1.1. Parasitism and Competition

4.1.2. Secondary Metabolites

4.1.3. Plant Defense Induction and Priming

modulating plant physiology. Besides modification of the transcription of genes involved

4.2. Trichoderma Harzianum

4.2.1. Parasitism and Competition

T. harzianum has proved to be an effective mycoparasite, not only by degrading its

4.2.2. Secondary Metabolites

4.2.3. Plant Defense Induction and Priming

4.3. Trichoderma Asperellum

Along with T. atroviride, T. asperellum is considered a strong mycoparasite of different

4.3.1. Parasitism and Competition

4.3.2. Secondary Metabolites

4.3.3. Plant Defense Induction and Priming

4.4. Trichoderma Virens

4.4.1. Parasitism and Competition

4.4.2. Secondary Metabolites

4.4.3. Plant Defense Induction and Priming

4.5. Trichoderma Longibrachiatum

4.5.1. Parasitism and Competition

The parasitic ability of T. longibrachiatum is a trait that should be exploited more,

4.5.2. Secondary Metabolites

4.5.3. Plant Defense Induction and Priming

cucumber to the pathogen B. cinerea [77]. In a greenhouse experiment, T. longibrachiatum

4.6. Trichoderma Viride

4.6.1. Parasitism and Competition

4.6.2. Secondary Metabolites

4.6.3. Plant Defense Induction and Priming

4.7. Other Trichoderma Species

5. Other Biocontrol Strategies Involving Trichoderma spp.

6. Trichoderma Bioformulations in Agriculture for Use in Biocontrol

Commercial formulations T34 Biocontrol (Biocontrol Technologies S.L) from T. asperellum

Author Contributions: P.G.-G.: Conceptualization, Writing—Original draft preparation. A.K.:

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