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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Agron.</journal-id>
<journal-title>Frontiers in Agronomy</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Agron.</abbrev-journal-title>
<issn pub-type="epub">2673-3218</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fagro.2022.932839</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Agronomy</subject>
<subj-group>
<subject>Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Trichoderma- from lab bench to field application: Looking back over 50 years</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Dutta</surname>
<given-names>Pranab</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1507694"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Deb</surname>
<given-names>Lipa</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1959610"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Pandey</surname>
<given-names>Abhay K.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/375116"/>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>School of Crop Protection, College of Post-Graduate Studies in Agricultural Sciences, Central Agricultural University (Imphal), Umiam</institution>, <addr-line>Meghalaya</addr-line>, <country>India</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Department of Mycology and Microbiology, Tea Research Association, North Bengal Regional R &amp; D Center, Nagrakata</institution>, <addr-line>West Bengal</addr-line>, <country>India</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Jonathan Spencer West, Rothamsted Research, United Kingdom</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Pedro Laborda, Nantong University, China; Yasir Iftikhar, University of Sargodha, Pakistan</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Abhay K. Pandey, <email xlink:href="mailto:abhaykumarpandey.ku@gmail.com">abhaykumarpandey.ku@gmail.com</email>; Pranab Dutta, <email xlink:href="mailto:pranabdutta74@gmail.com">pranabdutta74@gmail.com</email>
</p>
</fn>
<fn fn-type="other" id="fn002">
<p>This article was submitted to Disease Management, a section of the journal Frontiers in Agronomy</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>03</day>
<month>10</month>
<year>2022</year>
</pub-date>
<pub-date pub-type="collection">
<year>2022</year>
</pub-date>
<volume>4</volume>
<elocation-id>932839</elocation-id>
<history>
<date date-type="received">
<day>30</day>
<month>04</month>
<year>2022</year>
</date>
<date date-type="accepted">
<day>08</day>
<month>09</month>
<year>2022</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2022 Dutta, Deb and Pandey</copyright-statement>
<copyright-year>2022</copyright-year>
<copyright-holder>Dutta, Deb and Pandey</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<abstract>
<p>Biological control of plant pathogens has become increasingly possible with the use of fungi, which have a high reproductive rate (both sexually and asexually) and a short generation time and are very specific to their target. <italic>Trichoderma</italic> species are found in diverse habitats and experience various interactions with other organisms. They are used as bio-fungicides owing to their plant-protecting abilities, and they produce a large number of secondary metabolites (SMs) accompanied by enrichment in secondary metabolism-associated genes. This article aims to review and discuss the SMs produced by <italic>Trichoderma</italic> species, including their physiology, mode of action, mass production, and industrial and field applications for the control of plant diseases. We also discuss the evolutionary history, taxonomical gradient, classification, and ecology of <italic>Trichoderma</italic> species, as well as indirect and direct mechanisms used as plant protectors with gene improvement strategies. Aside from the bioactivity of SMs derived from <italic>Trichoderma</italic> species, compatibility with fungicides, mass formulation techniques, and industrial applications of <italic>Trichoderma</italic> species, the review focuses on its advent and progress as a global research pioneer.</p>
</abstract>
<kwd-group>
<kwd>microbial biocontrol agents</kwd>
<kwd>ecology</kwd>
<kwd>mode of action</kwd>
<kwd>disease control</kwd>
<kwd>industrial application</kwd>
</kwd-group>
<counts>
<fig-count count="4"/>
<table-count count="7"/>
<equation-count count="0"/>
<ref-count count="242"/>
<page-count count="25"/>
<word-count count="12105"/>
</counts>
</article-meta>
</front>
<body>
<sec id="s1">
<title>Background</title>
<p>The use of novel agricultural technologies has improved production, but some modern practices damage the environment. Increasing yields in an environment-friendly manner has become one of the recent challenges of advanced farming (<xref ref-type="bibr" rid="B227">Weller et&#xa0;al., 2014</xref>). There are a number of diseases that can be caused by bacteria, fungi, viruses, nematodes, and mycoplasmas in crops. Fungal pathogens are one of these plant pathogenic organisms that cause significant damage to agricultural crops around the world that reduce crop yields with an estimated loss of 15&#x2013;17% during cropping and harvesting (<xref ref-type="bibr" rid="B227">Weller et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B153">Pandey et&#xa0;al., 2018</xref>). Mycotoxin production also results from fungal contamination of food commodities. Many approaches have been used to manage these pathogens, including cultural, mechanical, microbial biocontrol agents, and the use of resistant cultivars and chemical fungicides. The use of fungicides for the treatment of plant diseases may cause serious health and environmental effects (<xref ref-type="bibr" rid="B201">Suryanarayanan et&#xa0;al., 2016</xref>). Some of the negative effects of plant diseases on our everyday lives may go unnoticed. It is sometimes hard to get food if our crops do not succeed. Therefore, it is crucial for us to diversify our foods and develop eco-friendly agricultural technologies, so that we can grow healthier crops.</p>
</sec>
<sec id="s2">
<title>Existing disease management options in crops</title>
<p>Synthetic fungicides are currently used to control plant diseases, but they play a major role in limiting the availability of nutritionally adequate and safe food (<xref ref-type="bibr" rid="B177">Russell, 2005</xref>). In order to ensure a sustainable production in the future, plant disease management strategies are needed (<xref ref-type="bibr" rid="B177">Russell, 2005</xref>; <xref ref-type="bibr" rid="B227">Weller et&#xa0;al., 2014</xref>). In contemporary agriculture systems, agrochemicals are important to reduce crop losses (<xref ref-type="bibr" rid="B31">Carvalho, 2006</xref>). In general, agrochemicals can be divided into fertilizers and pesticides. Nitrogen, phosphorus, and potassium are all elements found as chemical compounds in growth regulators and pesticides (<xref ref-type="bibr" rid="B31">Carvalho, 2006</xref>). The four main types of pesticides are insecticides, fungicides, nematicides, and herbicides. The majority of plant diseases are caused by fungi and oomycetes, and fungi can also cause chronic and acute health problems in human beings (<xref ref-type="bibr" rid="B227">Weller et&#xa0;al., 2014</xref>). For instance, in addition to causing Fusarium head blight, <italic>Fusarium graminearum</italic> also produces a mycotoxin, deoxynivalenol, that has a harmful effect to both animals and humans (<xref ref-type="bibr" rid="B227">Weller et&#xa0;al., 2014</xref>). Increasingly, widespread availability and greater efficacy of these fungicides have been attributed to increased crop productivity and combating fungal pathogens. Therefore, fungicides are essential for plant disease control (<xref ref-type="bibr" rid="B173">Reuveni and Reuveni, 1998</xref>).</p>
<p>It is believed that the first generation of fungicides was derived from the Bordeaux mixture, which was discovered in 1885, and powdery and downy mildew on grapes can be controlled with this chemical (<xref ref-type="bibr" rid="B227">Weller et&#xa0;al., 2014</xref>). Second-generation fungicides include organic chemicals, such as dithiocarbamates, and were first synthesized in 1934 (<xref ref-type="bibr" rid="B49">De Waard et&#xa0;al., 1993</xref>). These synthetic fungicides only affect plants on the surface and make no contact with the plant&#x2019;s inner tissue. Organic fungicides of the third generation (1970&#x2013;80) penetrated host tissues and controlled infections caused by fungal pathogens (<xref ref-type="bibr" rid="B49">De Waard et&#xa0;al., 1993</xref>). Fungicides of the fourth generation (from 1980 to the present) inhibit fungi from penetrating plant tissue, thus causing plant resistance (<xref ref-type="bibr" rid="B177">Russell, 2005</xref>). As a result of pesticide use, humans and ecosystems suffer adverse effects. Agrochemicals adversely affect the environment, food chain, and soil and disrupt the ecological balance in the environment (<xref ref-type="bibr" rid="B10">Anderson et&#xa0;al., 2004</xref>). In the long run, nitrogen fertilizers can contaminate ground water, and fertilizers based on ammonium can decrease pH levels and make soils more susceptible to Fusarium wilt (<xref ref-type="bibr" rid="B31">Carvalho, 2006</xref>). In particular, fungicides negatively affect saprobic fungi such as <italic>Penicillium</italic> species and <italic>Trichoderma</italic> species in soils (<xref ref-type="bibr" rid="B201">Suryanarayanan et&#xa0;al., 2016</xref>).</p>
<p>Due to frequent use of the fungicides, fungicide resistance develops, resulting in failures in controlling disease (<xref ref-type="bibr" rid="B218">Vinale et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B28">Burketova et&#xa0;al., 2015</xref>). Gray mold is caused by <italic>Botrytis cinerea</italic> on vegetables, fruits, and ornamental flowers. <italic>Botrytis cinerea</italic> developed resistance to benzimidazoles due to a mutation in &#x3b2;-tubulin, a protein-coding gene. Currently, QoI (quinol oxidation inhibitor) fungicides such as strobilurins are important fungicides and azoxystrobin is the world&#x2019;s most popular fungicide, with extensive mitigation activity against many pathogens of food crops (<xref ref-type="bibr" rid="B99">Ishii, 2006</xref>). Nevertheless, QoI fungicides induce pathogen resistance. Melon and cucumber powdery mildew, as well as cucumber crops&#x2019; downy mildew, developed a fungicide resistance to QoI groups of fungicides in Japan (<xref ref-type="bibr" rid="B99">Ishii, 2006</xref>). In addition, <xref ref-type="bibr" rid="B77">Fraaije et&#xa0;al. (2005)</xref> found that <italic>Mycosphaerella graminicola</italic>, a wheat pathogen, has developed resistance to strobilurin, a Qol groups of fungicide. A range of fungicides called DMI (demethylation inhibitors; also known as sterol biosynthesis inhibitors) are deployed to combat diseases in vegetables, cereals, fruit crops, and other plantation crops (<xref ref-type="bibr" rid="B99">Ishii, 2006</xref>). Apple scab fungi such as <italic>Venturia inaequalis</italic> and <italic>V. nashicola</italic> have developed resistance to DMI fungicides (<xref ref-type="bibr" rid="B99">Ishii, 2006</xref>). The use of pesticides at higher concentrations is required to curb pesticide resistance (<xref ref-type="bibr" rid="B206">Tranier et&#xa0;al., 2014</xref>) along with other strategies such as alternation or mixing with other modes of action (<xref ref-type="bibr" rid="B145">Mikaberidze et&#xa0;al., 2014</xref>). Consequently, pesticide effectiveness decreased (<xref ref-type="bibr" rid="B230">Widawsky et&#xa0;al., 1998</xref>). Since the use of synthetic fungicides causes environmental contamination and pathogen resistance, therefore, alternative methods for battling pathogens have increasingly become important in recent years (<xref ref-type="bibr" rid="B92">Hasan et&#xa0;al., 2013</xref>). In achieving high-quality crops, non-chemical products are a critical component.</p>
<p>In order to achieve sustainable agriculture, fertilizers and pesticides must be reduced or eliminated (<xref ref-type="bibr" rid="B154">Pandey et&#xa0;al., 2021</xref>). Most countries have implemented regulatory measures that minimize disease control based on chemical fungicides and encourage alternative mitigation strategies (<xref ref-type="bibr" rid="B230">Widawsky et&#xa0;al., 1998</xref>). The Integrated Plant Disease Management system is an effective alternative crop management method. Sustainable agriculture is achieved through combining synthetic fungicides, organic fertilizers, biological control, better soil management, and water management (<xref ref-type="bibr" rid="B31">Carvalho, 2006</xref>; <xref ref-type="bibr" rid="B201">Suryanarayanan et&#xa0;al., 2016</xref>). One way to control pests and pathogens without using chemicals is to develop disease-resistant varieties of food crops (<xref ref-type="bibr" rid="B230">Widawsky et&#xa0;al., 1998</xref>). In addition to introducing disease-resistant cultivars, scientists are striving to increase yields by developing high-yielding varieties (<xref ref-type="bibr" rid="B31">Carvalho, 2006</xref>). Sustainable agriculture can also be achieved through organic farming. Natural bio-agrochemicals can be derived from organic debris such as phenolic compounds, flavonoids, terpenoids, alkaloids, and fatty acids (<xref ref-type="bibr" rid="B39">Chou, 2010</xref>). Using <italic>Trichoderma</italic> to manage crop diseases is not an exception. However, the findings of the research are scattered throughout the papers. Although, few researchers reviewed the use of <italic>Trichoderma</italic> for crop disease management. These reviews, however, were either crop specific (<xref ref-type="bibr" rid="B151">Olowe et&#xa0;al., 2022</xref>) or did not provide detailed information about the mode of action of <italic>Trichoderma</italic> in disease management (<xref ref-type="bibr" rid="B8">Al-Ani and Li, 2018</xref>; <xref ref-type="bibr" rid="B140">Meher et&#xa0;al., 2020</xref>) or its taxonomical and chemical characteristics (<xref ref-type="bibr" rid="B12">Asad, 2022</xref>). Thus, in this paper, we compiled a comprehensive review of <italic>Trichoderma</italic> species, their taxonomy, classification, and ecology, as well as indirect and direct mechanisms utilized as plant protective mechanisms. In addition, the review is focused on the compatibility, mass formulation techniques, and industrial applications of <italic>Trichoderma</italic> species more specifically on the advent and progress of <italic>Trichoderma</italic> research at a global level. The compiled reports will provide the scientific community with detailed information on the biology and multifaceted uses of the genus <italic>Trichoderma</italic>.</p>
</sec>
<sec id="s3">
<title>
<italic>Trichoderma</italic>: A multifunctional microbial biocontrol agent</title>
<p>The genus <italic>Trichoderma</italic> is one of the most prevalent culturable fungi in the family Hypocreaceae and can be found in all types of ecological diversity. The genus is soil-dwelling, free-living, cosmopolitan, facultatively anaerobic, filamentous, and asexually reproducing and is widely distributed in root and soil ecosystems and plant debris. This fungus has long been recognized as a microbial biocontrol agent that can replace chemical fungicides against the large range of fungi that cause root rot, soilborne, and foliar disease (<xref ref-type="bibr" rid="B90">Harman et&#xa0;al., 2006</xref>) and for increasing root and shoot development, crop productivity, resistance to abiotic stresses, and nutrient uptake (<xref ref-type="bibr" rid="B178">Saba et&#xa0;al., 2012</xref>). By enhancing crop productivity, it also contributes to food security in a sustainable way without causing ecological imbalance. Since the first recognized application of <italic>Trichoderma</italic> species in early 1930, they have been widely applied for the management of many plant pathogens and associated diseases (<xref ref-type="bibr" rid="B95">Howell, 2003</xref>; Harman et&#xa0;al., 2006). Some of them are wilt disease, dry root rot, damping off, and collar rot caused by <italic>Fusarium</italic> spp., <italic>Rhizoctonia</italic> spp., <italic>Pythium</italic> spp., <italic>Phytophthora</italic> spp., and <italic>Sclerotium rolfsii</italic>, respectively (<xref ref-type="bibr" rid="B233">Yang et&#xa0;al., 2011</xref>). <italic>Trichoderma</italic> shows diverse versatility, high competence, and profuse root-colonizing nature and also exists as a virulent plant symbiont (<xref ref-type="bibr" rid="B156">Papavizas, 1985</xref>). Characteristically, the fungus is identified through rapid growth, bright green to yellow-colored conidia and branched conidiophores (<xref ref-type="bibr" rid="B122">Kumar et&#xa0;al., 2019</xref>). Due to its eco-friendly nature, the fungus has been recognized as a substitute to commercial synthetic fungicides against a broad range of fungal pathogens. It is also extensively utilized as a model organism to understand biological interaction among antagonistic fungi, mechanisms, host-defense response, and plethora of heterologous proteins affecting plant metabolism and physiology.</p>
<sec id="s3_1">
<title>Historical perspectives</title>
<p>
<italic>Trichoderma</italic> was first described 200 years ago by <xref ref-type="bibr" rid="B163">Persoon (1794)</xref> in Germany. In India, it was first isolated by <xref ref-type="bibr" rid="B204">Thakur and Norris (1928)</xref> from Madras. In the early 20<sup>th</sup> century during World War II, this fungus was identified as cellulolytic and identified as <italic>T. viride</italic> QM6a but later renamed <italic>T. reesei</italic> by Elwyn T. Reese due to its ability to decay wood (<xref ref-type="bibr" rid="B190">Simmons, 1977</xref>). In 1932, the first ever evidence of <italic>T. lingorum</italic> (Tode) Harz. (<italic>H. virens</italic>) as a mycoparasite having biocontrol potential against <italic>Rhizoctonia solani</italic> was established, followed by discovery of gliotoxin as the first antimicrobial compound from <italic>Trichoderma</italic> species in 1934 (<xref ref-type="bibr" rid="B225">Weindling, 1932</xref>; <xref ref-type="bibr" rid="B226">Weindling, 1934</xref>). Earlier studies by <xref ref-type="bibr" rid="B86">Gutter (1957)</xref> also highlighted the discovery of an effect of light on conidiation of <italic>T. reesei</italic> in 1957. However, the genus <italic>Trichoderma</italic> was classified for the first time in 1969 by <xref ref-type="bibr" rid="B174">Rifai (1969)</xref>, leading to a concept for the identification of species belonging to the genus <italic>Trichoderma</italic>, and by 2006, more than 100 distinct species had been described (<xref ref-type="bibr" rid="B53">Druzhinina et&#xa0;al., 2006</xref>).</p>
<p>The first evidence of <italic>T. harzianum</italic> suppressing <italic>Sclerotium rolfsii</italic> in the field was reported in 1972 (<xref ref-type="bibr" rid="B228">Wells et&#xa0;al., 1972</xref>). Research on cloning studies on <italic>Trichoderma</italic> species dates back to 1983 reported cloning of first cellulase of <italic>T. reesei</italic> (<xref ref-type="bibr" rid="B187">Shoemaker et&#xa0;al., 1983</xref>) followed by cloning of the first mycoparasitism-related genes <italic>(prb1)</italic> and its induction by cell walls in 1993 (<xref ref-type="bibr" rid="B83">Geremia et&#xa0;al., 1993</xref>). In 1986, the ability of <italic>Trichoderma</italic> to support plant growth was discovered for the first time (<xref ref-type="bibr" rid="B32">Chang et&#xa0;al., 1986</xref>). Specifically, the genus boosts plant immunity by induced resistance in 1997 (<xref ref-type="bibr" rid="B18">Bigirimana et&#xa0;al., 1997</xref>) and internal colonization of root system by <italic>Trichoderma</italic> in 1999 (<xref ref-type="bibr" rid="B236">Yedidia et&#xa0;al., 1999</xref>). The first commercial formulation of <italic>Trichoderma</italic>, Binab T, for biological control of plant diseases was registered in 1989.</p>
</sec>
<sec id="s3_2">
<title>Taxonomy, phylogeny, and classification of <italic>Trichoderma</italic>
</title>
<p>
<italic>Trichoderma</italic> was historically described as a genus of anamorphic fungi found primarily in rotting plant material and soil (<xref ref-type="bibr" rid="B163">Persoon, 1794</xref>) with <italic>T. reesei</italic> as the first evidence for the existence of the genus. As early as 1865, <xref ref-type="bibr" rid="B209">Tulasne and Tulasne (1865)</xref> postulated a sexual relationship between <italic>Hypocrea</italic> (<italic>H. jecorina</italic>) and <italic>Trichoderma</italic> (<italic>T. reesei</italic>). Their hypothesis was confirmed 100 years later (<xref ref-type="bibr" rid="B119">Kuhls et&#xa0;al., 1996</xref>). As a consequence, Rossman et&#xa0;al. (1999) described the genera <italic>Hypocrea</italic>, <italic>Podostroma</italic>, and <italic>Sarawakus</italic> belonging to the Hypocreaceae family and class Ascomycetes as teleomorphs of <italic>Trichoderma.</italic> According to <xref ref-type="bibr" rid="B19">Bisby (1939)</xref>, for many years, due to morphological similarity in the majority of <italic>Trichoderma</italic> species as rapid growth, bright green conidia with repetitive branched conidiophore, it was considered as a single species, <italic>T. viride.</italic> Earlier classification of the genus <italic>Trichoderma</italic> included consolidated taxonomical scheme proposed by <xref ref-type="bibr" rid="B174">Rifai (1969)</xref> that introduced the concept of &#x201c;species aggregate&#x201d; and identified nine species under the genus based on morphological characterization in a monograph. In later studies, <xref ref-type="bibr" rid="B20">Bissett (1991)</xref> attempted to classify <italic>Trichoderma</italic> by integrating similar forms within species concept based on morphology, that is, conidiophore branching system into five sections such as <italic>Pachybasium</italic>, <italic>Saturnisporum</italic>, <italic>Trichoderma</italic>, <italic>Longibrahiatum</italic>, and <italic>Hypocreanum.</italic> <xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref> presents morphological characteristics used for identification of important <italic>Trichoderma</italic> species. In the 20<sup>th</sup> century, several new DNA-based approaches, such as rDNA sequence analysis, random amplified polymorphic DNA (RAPDs) analysis and PCR fingerprinting methods were used in fungal systematics and taxonomical studies including identification and phylogenetic classification of various <italic>Trichoderma</italic> species. Several studies demonstrated great genetic diversity among <italic>Trichoderma</italic> species by identifying four distinct species within the <italic>T. harzianum</italic> aggregate as <italic>T. harzianum s. str., T. atroviride, T. longibrachiatum</italic> and <italic>T. asperellum</italic>(<xref ref-type="bibr" rid="B93">Hermosa et&#xa0;al., 2000</xref>
<italic>)</italic>. The biotypes within <italic>T. harzianum s. str.</italic> as <italic>T. harzianum</italic> Rifai and <italic>T. hamatum</italic> (Bon.) Bain were linked to biocontrol and mycoparasitic activity, whereas, <italic>T. aggressivum</italic> was associated with green mold of mushroom (<xref ref-type="bibr" rid="B180">Samuels et&#xa0;al., 2002</xref>). Phylogenetic studies based on 18S rDNA sequence analysis (<xref ref-type="bibr" rid="B120">Kulling-Gradiner et&#xa0;al., 2002</xref>), where, small mitochondrial rDNA subunit, ITS1, 5.8S rDNA, ITS2, 28S rDNA, translation elongation factor (TEF-1), and endochitinase 42 were used to construct a phylogenetic tree, suggested <italic>Trichoderma</italic> as a monophyletic branch under <italic>Hypocreaceae</italic> and identified 46 species under three sections, namely, <italic>Trichoderma</italic>, <italic>Pachybasium</italic>, and <italic>Longibrachiatum.</italic> In a recent study, <xref ref-type="bibr" rid="B87">Gu et&#xa0;al. (2020)</xref> identified four new species of <italic>Trichoderma</italic> in the <italic>Harzianum</italic> clade (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>) based on ITS, RPB2, and TEF1-alpha sequence data set.</p>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>Identification features of <italic>Trichoderma</italic> species based on morphological characteristics.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Species name</th>
<th valign="top" align="center">Mycelial characteristics</th>
<th valign="top" align="center">Conidiophores</th>
<th valign="top" align="center">Conidia</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Watery white to light green, colorless ring-like zones on reverse side, 7&#x2013;8 cm diam. in 5 days</td>
<td valign="top" align="left">Highly branched, loose tufts, short-skittle shaped phialides of size 7.2&#x2013;11.2 &#xd7; 2.5&#x2013;3.1 &#xb5;m</td>
<td valign="top" align="left">Sub globose or short ovoid conidia with truncate base, size 2.8&#x2013;3.2 &#xd7; 2.5&#x2013;2.9 &#xb5;m, 12h spore germination time</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. asperellum</italic>
</td>
<td valign="top" align="left">Smooth, hairy, yellowish green, cotton pattern, 1&#x2013;2 ringed Concentrics, emit coconut odor</td>
<td valign="top" align="left">Compact form, nine-pin shaped phialides attenuated into long neck arise singly/opposite pairs along branches, usually 6.8&#x2013;7.2 &#xd7; 3.0&#x2013;3.4 &#xb5;m</td>
<td valign="top" align="left">Globose or short ovoid, green colored, size 3.6&#x2013;4.0 &#xd7; 3.4&#x2013;4.0 &#xb5;m, 12&#x2013;13h spore germination time</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Green to dark yellowish green after 2&#x2013;3 days, no odor, smooth surface, cottony white mycelial mat, aerial hyphae</td>
<td valign="top" align="left">Long, slender phialides, swollen in middle, horn-shaped, size 6.2&#x2013;10.5 &#xd7; 3.1&#x2013;3.9 &#xb5;m</td>
<td valign="top" align="left">Globose to obovoid, smooth walled, usually 2.6&#x2013;3.0 &#xd7; 2.0&#x2013;2.4 &#xb5;m, 13h spore germination time</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. atroviride</italic>
</td>
<td valign="top" align="left">Watery white, submerged, translucent smooth, floccose, changed yellowish green to artemisia green after 2 days, dull yellowish at reverse, odorless</td>
<td valign="top" align="left">Highly branched, oblong shaped, curved phialides, constricted at base, appear in ampulliform, swollen at middle, narrow at tips, 5.2&#x2013;10.5 &#xd7; 2.4&#x2013;2.8 &#xb5;m</td>
<td valign="top" align="left">Globose, green colored, 2.4&#x2013;3.6 &#xb5;m, 12&#x2013;13 spore germination time</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. longibrachiatum</italic>
</td>
<td valign="top" align="left">Submerged transluscent/watery white, yellowish green to lily green after 2 days, no smell</td>
<td valign="top" align="left">Smooth, irregular tufts, singly/2&#x2013;3 verticels, lageniform, constricted at base, 3.4&#x2013;5.2 &#xd7; 2.3&#x2013;3.0 &#xb5;m</td>
<td valign="top" align="left">Obovoid to ellipsoidal, dilute green, apex rounded, 2.4&#x2013;3.6 &#xb5;m, 12&#x2013;13 spore germination time</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. koningii</italic>
</td>
<td valign="top" align="left">Creamy white, white to terreverte, crusty, compact, glaucous -like</td>
<td valign="top" align="left">Intercalary/terminal, phialides narrow at base, alternate to conical apices, singly and laterally, nine-pin bowling shaped, 3.8&#x2013;7.6 &#xd7; 2.5-3.2 &#xb5;m</td>
<td valign="top" align="left">Ellipsoidal/oblonged, rounded apex, acute base, 2.5&#x2013;4.2 &#xd7; 1.8&#x2013;2.6 &#xb5;m, 14h spore germination time</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. virens</italic>
</td>
<td valign="top" align="left">Watery white to green color with dull blackish green granules, no odor, 7&#x2013;8 cm in 5 days</td>
<td valign="top" align="left">Branched irregularly near apex, terminated by cluster of 3&#x2013;6 bunched phialides, lageniform to ampuliform phialides, swollen at middle, attenuated at apex, 4.4&#x2013;12.8 &#xd7; 2.6&#x2013;4.2 &#xb5;m</td>
<td valign="top" align="left">Broadly ellipsoidal to obovoid, rounded ends, green color, usually 3.2&#x2013;5.6 &#xd7; 2.5&#x2013;3.9 &#xb5;m, 13 h spore germination time</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
  <p>Source: <xref ref-type="bibr" rid="B122">Kumar et&#xa0;al. (2019)</xref>.
</p>
</fn>
</table-wrap-foot>
</table-wrap>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Phylogenetic tree of four new species of <italic>Trichoderma</italic> identified by <xref ref-type="bibr" rid="B87">Gu et&#xa0;al. (2020)</xref> based on Maximum Likelihood analysis of a combined ITS, RPB2, and TEF1&#x3b1; sequence data set.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fagro-04-932839-g001.tif"/>
</fig>
<p>As per Kirk&#x2019;s classification, taxonomy based on molecular phylogeny in the Ainsworth and Bisby&#x2019;s dictionary of fungi (10<sup>th</sup> edition), teleomorphic stage of the genus <italic>Trichoderma</italic> belongs to the domain Eukarya, kingdom Fungi, phylum Ascomycota, class Sordariomycetes, subclass Hypoceromycetidae, order Hypocreales, family Hypocreaceae, and genus <italic>Hypocrea</italic> species (<xref ref-type="bibr" rid="B220">Voigt and Kirk, 2011</xref>). A total of 75 <italic>Trichoderma</italic> species have been identified; the majority of which are considered as important microbial biological control agents. These include <italic>T. harzianum, T. hamatum</italic>, <italic>T. koningii</italic> Oud., <italic>T. polysporum</italic> (Link ex Pers.) Rifai, and <italic>T. virens</italic> (J. Miller, Giddens, and Foster) von Arx (<xref ref-type="bibr" rid="B89">Harman et&#xa0;al., 2004</xref>). Complete genome-sequencing analysis of the genus <italic>Trichoderma</italic> was assembled, annotated, and analyzed for the first time in the case of <italic>T. reesei</italic> as cellulase producer (<xref ref-type="bibr" rid="B136">Martinez et&#xa0;al., 2008</xref>) followed by <italic>T. virens</italic>, <italic>T. atroviride</italic>, <italic>T. harzianum</italic>, and <italic>T. asperellum</italic> (<xref ref-type="bibr" rid="B117">Kubicek et&#xa0;al., 2011</xref>) as microbial biocontrol species enabled studies on evolution in the context of ecological fitness. In recent years, identification and characterization of newly isolated <italic>Trichoderma</italic> species has been elucidated by development of phenotypic arrays investigating carbon utilization patterns (<xref ref-type="bibr" rid="B116">Kubicek et&#xa0;al., 2003</xref>), oligonucleotide barcode (TrichoOKEY), and similarity search tool (TrichoBLAST) (<xref ref-type="bibr" rid="B114">Kopchinskiy et&#xa0;al., 2005</xref>). At present, Index Fungorum Database listed 471 different names for <italic>Hypocrea</italic> species and 165 records for <italic>Trichoderma</italic>, whereas, International Sub commission on <italic>Trichoderma/Hypocrea</italic> listed 104 species (Internationally) and 13 species (From India) based on characterization at molecular level (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>).</p>
</sec>
<sec id="s3_3">
<title>Environment-induced changes in <italic>Trichoderma</italic> ecology</title>
<p>
<italic>Trichoderma</italic> species are ubiquitous, fast growing, cosmopolitan, and widely distributed as dominant microflora in soil including agricultural, orchard, forest, soil with organic matter (OM), pasture land, and desert soils from cool temperate to tropical climates (<xref ref-type="bibr" rid="B52">Domsch et&#xa0;al., 1980</xref>; <xref ref-type="bibr" rid="B175">Roiger et&#xa0;al., 1991</xref>). Saprophytic <italic>Trichoderma</italic> species were also recovered as mycelia from soil&#x2019;s top horizon (F and H), humid litter of deciduous and coniferous forests as well as from extreme environments such as mangrove swamps, salt marshes, and estuarine sediments (<xref ref-type="bibr" rid="B52">Domsch et&#xa0;al., 1980</xref>; <xref ref-type="bibr" rid="B231">Widen and Abitbol, 1980</xref>). Knowledge on effects of ecological factors on <italic>Trichoderma</italic> species may lead to improve understanding of distribution, population dynamics, survival, and proliferation in soil and rhizosphere. <xref ref-type="bibr" rid="B156">Papavizas (1985)</xref> also found <italic>Trichoderma</italic> populations on plant root surfaces, decaying bark and on resting structure of soilborne fungi such as sclerotia or other fungal propagules.</p>
<p>However, soil colonization, composition, biomass, and biological activity of <italic>Trichoderma</italic> species are influenced by ecological parameters such as moisture and temperature of soil, atmosphere, pH, OM, nutrient content, and plant types (<xref ref-type="bibr" rid="B52">Domsch et&#xa0;al., 1980</xref>). <italic>Trichoderma</italic> species have been reported to grow in a wide range of soil temperatures varying from 0&#xb0;C to as high as 40&#xb0;C favoring <italic>T. viride</italic> and <italic>T. polysporum</italic> in cool temperature regions, whereas <italic>T. harzianum</italic> in warm tropical soils (<xref ref-type="bibr" rid="B112">Klein and Eveleigh, 1998</xref>). In an extensive study by researchers (<xref ref-type="bibr" rid="B237">Zehra et&#xa0;al., 2017a</xref>), variation in temperature attributed to the existence of <italic>Trichoderma</italic> species in particular niches by affecting growth, metabolic activity, enzyme production, and production of volatile antibiotics. The reduction of soil moisture or increase in soil temperature greatly hampered the establishment of <italic>Trichoderma</italic> colonies in soils by reducing the hyphal growth, germination, and spore production (<xref ref-type="bibr" rid="B40">Clarkson et&#xa0;al., 2004</xref>).</p>
<p>In the past, a few studies also concluded that <italic>T. pseudokoningii</italic> and <italic>T. hamatum</italic> are adapted to excessive soil moisture conditions, whereas <italic>T. koningii</italic> and <italic>T. hamatum</italic> are widely distributed in diverse climatic conditions. In general, the optimum growth and development of <italic>Trichoderma</italic> have been reported not only in pH condition ranging from 3.5 to 5.6 but also extended to extreme pH up to 2.1 in several studies (<xref ref-type="bibr" rid="B84">Ghazanfar et&#xa0;al., 2018</xref>). In addition, soil carbon dioxide (CO<sub>2</sub>) atmospheric content also affects growth of <italic>Trichoderma</italic> by affecting soil pH upon combining with water to form weak acid, that is, carbonic acid, which readily dissociates into H<sup>+</sup> ions and <inline-formula>
<mml:math display="inline" id="im1">
<mml:mrow>
<mml:msubsup>
<mml:mrow>
<mml:mtext>HCO</mml:mtext>
</mml:mrow>
<mml:mn>3</mml:mn>
<mml:mo>-</mml:mo>
</mml:msubsup>
</mml:mrow>
</mml:math>
</inline-formula>, thus, decreasing soil pH (<xref ref-type="bibr" rid="B110">Killham, 1994</xref>). <xref ref-type="bibr" rid="B51">Dix and Webster (1995)</xref> also revealed that, under high soil CO<sub>2</sub> concentration, basic substrates positively affect the growth of <italic>Trichoderma</italic> species, by influencing the availability of ions and nutrients in soil through salt solubilization in soil solution. Survivability of <italic>Trichoderma</italic> species in soil after application is basically mediated by hyphae, aggregate, or mycelial fragments, resting structure such as chlamydospores and conidia (<xref ref-type="bibr" rid="B157">Papavizas et&#xa0;al., 1984</xref>). Persistence of conidia lasted up to 110&#x2013;113 days without any amendments or decreased initially, then stabilized up to 1/10<sup>th</sup> of original population in soil for 24 months (<xref ref-type="bibr" rid="B158">Papavizas and Lumsden, 1982</xref>; <xref ref-type="bibr" rid="B1">Abbas et&#xa0;al., 2022</xref>).</p>
</sec>
<sec id="s3_4">
<title>Mode of action of <italic>Trichoderma</italic>
</title>
<p>
<italic>Trichoderma</italic> species operated through mixed mode of action involving more than one mechanism for antagonistic interaction and suppression of plant pathogens either through direct mechanisms <italic>viz.</italic>, mycoparasitism, competition, and antibiosis or complex indirect interaction by stimulating induced systemic resistance (ISR), solubilization and sequestration of nutrients, nutrient uptake, and enhancement of plant growth (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>). <italic>Trichoderma</italic> species have been known for their prolific production of extracellular enzymes, proteins, fungitoxic compounds, antibiotics, and defense-related substances in addition to their ability to enhance shoot and root growth (<xref ref-type="bibr" rid="B60">Dutta and Das, 1999a</xref>), nutrient uptake, resistance to abiotic stresses, and crop productivity (<xref ref-type="bibr" rid="B95">Howell, 2003</xref>).</p>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>Mycoparasitism of <italic>Trichoderma</italic> spp. within the soil community (adopted from <xref ref-type="bibr" rid="B54">Druzhinina et&#xa0;al., 2011</xref>).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fagro-04-932839-g002.tif"/>
</fig>
<sec id="s3_4_1">
<title>Mycoparasitism</title>
<p>Plant pathogenic fungi are sensitive to <italic>Trichoderma</italic> species through direct physical contact, and such biocontrol activity is called mycoparasitism (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3</bold>
</xref>; <xref ref-type="bibr" rid="B51">Dix and Webster, 1995</xref>; <xref ref-type="bibr" rid="B54">Druzhinina et&#xa0;al., 2011</xref>). However, the concept of mycoparasitism <italic>via</italic> mycoparasitism by <italic>Trichoderma</italic> dates back to demonstration of parasitism of <italic>Rhizoctonia solani</italic> by <italic>T. virens</italic> in mitigating citrus seedling disease by <xref ref-type="bibr" rid="B225">Weindling (1932)</xref>. Earlier reports of direct parasitism of <italic>Pythium ultimum</italic> and <italic>Sclerotium rolfsii</italic> by <italic>Trichoderma</italic> species also provide evidence of its mycoparasitic ability (<xref ref-type="bibr" rid="B156">Papavizas, 1985</xref>). <xref ref-type="bibr" rid="B51">Dix and Webster (1995)</xref> suggested that mycoparasitism occurs as the direct mode of antagonism as a sequential process involving three steps, including chemotrophic growth, coiling and interaction of hyphae, and release of lytic enzymes. The mycoparasitic interaction is usually mediated by host-derived chemicals that are detected by <italic>Trichoderma</italic> species through specific signaling mechanisms mediating recognition via diffusible signals such as oligochitins, inducing enzyme secretion, namely, exochitinases, endochitinases, and 1,4-&#x3b2;-<italic>N-</italic>acetylglucosaminidases, extracellular &#x3b2;-(1,3)-glucanases, proteases, and lipases (<xref ref-type="bibr" rid="B219">Viterbo and Horwitz, 2010</xref>). Upon establishment of contact, <italic>Trichoderma</italic> attaches to the fungal cell through formation of papillae/appressoria-like structures, causing mycoparasitic coiling around the target fungus mediated by hydrophobin-like proteins and a lectin complex from the cell wall of <italic>Trichoderma</italic> and target pathogen (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3</bold>
</xref>), respectively (<xref ref-type="bibr" rid="B95">Howell, 2003</xref>). The secretion of particular lytic enzymes from the cell wall of <italic>Trichoderma viz.</italic>, glucanases, chitinases, pectinases, and peptaibol antibiotics induced a cascade of physiological changes within the target fungus facilitating flow of nutrients to the mycoparasite and degeneration of target fungus (<xref ref-type="bibr" rid="B95">Howell, 2003</xref>). Mycoparasitic ability of <italic>Trichoderma</italic> species have been studied against various soilborne pathogens, such as <italic>Fusarium oxysporum</italic>, <italic>F. solani</italic>, <italic>R. solani</italic>, <italic>S. sclerotiorum</italic>, <italic>S. rolfsii</italic>, and <italic>Colletotrichum capsici</italic> in our earlier studies (<xref ref-type="bibr" rid="B60">Dutta and Das, 1999a</xref>; <xref ref-type="bibr" rid="B62">Dutta and Das, 2002</xref>; <xref ref-type="bibr" rid="B63">Dutta and Das, 2009</xref>; <xref ref-type="bibr" rid="B58">Dutta et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B66">Dutta et&#xa0;al., 2020</xref>).</p>
<fig id="f3" position="float">
<label>Figure&#xa0;3</label>
<caption>
<p>Plant-pathogen-antagonist tri-trophic interaction, how <italic>Trichoderma</italic> species can modulate the molecular signaling in the challenge between the <italic>Fusarium</italic> and <italic>Alternaria</italic> and the host (tomato).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fagro-04-932839-g003.tif"/>
</fig>
</sec>
<sec id="s3_4_2">
<title>Antibiosis</title>
<p>
<xref ref-type="bibr" rid="B226">Weindling (1934)</xref> proposed the concept of &#x201c;lethal principle&#x201d; describing influence of certain lethal factors excreted by <italic>T. lingorum</italic> in soil inhibiting growth and development of <italic>R. solani</italic> and <italic>S. americana</italic> displayed a paradigm shift toward involvement of lethal factors apart from mycoparasitism in biocontrol activity. In 1941, the factor causing the &#x201c;lethal principle&#x201d; was identified as gliotoxin, secreted by <italic>Gliocladium virens</italic> (Now <italic>T. virens</italic>). Later, in 1983, <xref ref-type="bibr" rid="B96">Howell and Stipanovic (1983)</xref> reported another antibiotic, that is, gliovirin secreted from <italic>T. virens</italic> known for potential inhibitory effect against <italic>Phytophthora</italic> species and <italic>Pythium ultimum</italic>. The phenomenon of antibiosis, utilized by <italic>Trichoderma</italic>, produces low-molecular weight, diffusible, specific compounds, or an antibiotic possessing antifungal and antibacterial properties. Depending upon the biochemical nature, antibiotics act as metabolic inhibitors or block protein synthesis (translational pathways), penetrate host cells, inhibit cell wall synthesis, growth, uptake of nutrients, sporulation, and metabolite production by target pathogen.</p>
<p>Various species of <italic>Trichoderma</italic> are known for producing a diverse range of secondary metabolites (SMs) including polyketides, pyrones, oxygen heterocyclic compounds, polypeptides, terpenoids, and derivatives of fatty acids and amino acids (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>). The emission of coconut odor in case of few strains of <italic>T. viride</italic> and <italic>T. hamatum</italic> might be due to release of volatile 6-pentyl-&#x3b1;-pyrone, whereas, pigment-related compounds include anthroquinones such as chrysophanol (1,8-dihydroxy-3-methyl-9,10-anthroquinone), paschybasin (1,8-dihydroxy-3-methyl-9,10-anthroquinone), and emodin (1,6,8-trihydroxy-3-methyl-9,10-anthroquinone). Some metabolites attributed to mycotoxic properties of <italic>Trichoderma</italic> include trichothecenes (e.g., trichodermin, which impairs plant growth), cyclic peptides (e.g., suzukacillin, lipophilic alamethicin, trichopolyns, trichotoxins, and trichorianine, which attack the cell membrane of bacteria and eukaryotes promoting lysis), and isocyanide (e.g., trichoviridin). The volatile and non-volatile metabolites produced by various species of <italic>Trichoderma</italic> are described under separate section. In our recent study, cell-free culture filtrate of <italic>T. pseudokoningii</italic> showed efficacy against <italic>C. capsici</italic>, <italic>S. sclerotiorum</italic>, <italic>R. solani</italic>, and <italic>F. oxysporum</italic> due to release of extracellular SMs (<xref ref-type="bibr" rid="B58">Dutta et&#xa0;al., 2018</xref>).</p>
<table-wrap id="T2" position="float">
<label>Table&#xa0;2</label>
<caption>
<p>Different types of secondary metabolites produced by <italic>Trichoderma</italic> species.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Secondary metabolites</th>
<th valign="top" align="center">Compounds</th>
<th valign="top" align="center">Species name</th>
<th valign="top" align="center">Functions</th>
<th valign="top" align="center">Target pathogens</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Pyrones</td>
<td valign="top" align="left">6-pentyl-2H-pyran-2-one</td>
<td valign="top" align="left">
<italic>T. viride</italic>,<break/>
<italic>T. atroviridae</italic>,<break/>
<italic>T. harzianum</italic>,<break/>
<italic>T. koningii</italic>
</td>
<td valign="top" align="left">Antifungal activity</td>
<td valign="top" align="left">&#x2013;</td>
</tr>
<tr>
<td valign="top" align="left">Koninginins</td>
<td valign="top" align="left">Complex pyranes (Koningins A, B, D, E, and G)</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>,<break/>
<italic>T. koningii</italic>,<break/>
<italic>T. aureoviride</italic>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left">
<italic>Gaeumannomyces graminis</italic>var. <italic>tritici, R. solani, P. innamon, F. oxysporum, Pythium</italic>
</td>
</tr>
<tr>
<td valign="top" align="left">Viridins</td>
<td valign="top" align="left">Steroidal metabolite viridin</td>
<td valign="top" align="left">
<italic>T. koningii</italic>,<break/>
<italic>T. viride, T. virens</italic>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left">
<italic>F. caeruleum, P. expansum, A. niger</italic>
</td>
</tr>
<tr>
<td valign="top" align="left">Nitrogen Heterocyclic Compounds</td>
<td valign="top" align="left">Harzianopyridone (Harzianic acid &amp; Pyrrolidindione ring)</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Antibiotic activity</td>
<td valign="top" align="left">
<italic>R. solani, G. graminis</italic> var. <italic>tritici, P. ultimum</italic>
</td>
</tr>
<tr>
<td valign="top" align="left">Azaphilones</td>
<td valign="top" align="left">Highly oxygenated bicyclic core &amp; chiral quaternary center</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>T22</td>
<td valign="top" align="left">Growth inhibition</td>
<td valign="top" align="left">
<italic>R. solani, P. ultimum, G. graminis</italic> var. <italic>tritici</italic>
</td>
</tr>
<tr>
<td valign="top" align="left">Butenolides, Hydroxy-Lactones</td>
<td valign="top" align="left">Harzianolide, Butenolides, dehydro-harzianolide</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Antifungal</td>
<td valign="top" align="left">
<italic>P. ultimum, R. solani</italic>
</td>
</tr>
<tr>
<td valign="top" align="left">Isocyano Metabolites</td>
<td valign="top" align="left">Dermadin</td>
<td valign="top" align="left">
<italic>T. koningii</italic>,<break/>
<italic>T. viride, T. hamatum</italic>
</td>
<td valign="top" align="left">Antibiotic</td>
<td valign="top" align="left">
<italic>Phytopthora</italic> spp.</td>
</tr>
<tr>
<td valign="top" align="left">Diketo-piperazines</td>
<td valign="top" align="left">Gliotoxin (Q strains) &amp; gliovirin (P strains)</td>
<td valign="top" align="left">
<italic>T. virens</italic>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left">
<italic>P. ultimum</italic> (P strains)<break/>
<italic>R. solani</italic> (Q strains)</td>
</tr>
<tr>
<td valign="top" align="left">Peptaibols</td>
<td valign="top" align="left">A-aminoisobutyric acid &amp; isovaline</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Inhibits &#x3b2;-glucan synthase</td>
<td valign="top" align="left">&#x2013;</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
  <p>Information compiled from: <xref ref-type="bibr" rid="B56">Dunne et&#xa0;al. (1996)</xref>.
</p>
</fn>
</table-wrap-foot>
</table-wrap>
</sec>
<sec id="s3_4_3">
<title>Competition</title>
<p>Competition is one of the classical biocontrol mechanisms utilized by the genus <italic>Trichoderma</italic>, indirectly eliminating pathogens <italic>via</italic> reduction of food source and niche exclusion (<xref ref-type="bibr" rid="B130">Lorito et&#xa0;al., 1996</xref>; <xref ref-type="bibr" rid="B70">Elad et&#xa0;al., 2000</xref>). <xref ref-type="bibr" rid="B43">Corke and Hunter (1979)</xref> provided the first evidence of competition exerted by <italic>Trichoderma</italic> as a basis of biocontrol against <italic>Chrondrostereum purpureum</italic>, the silver leaf pathogen of plum trees. <xref ref-type="bibr" rid="B194">Sivan and Chet (1989)</xref> determined expression of antagonism by different <italic>Trichoderma</italic> species against <italic>F. oxysporum</italic> by exhibiting competition for carbon. <italic>Trichoderma</italic> species have been regarded as most aggressive competitors due to their ability to extensively proliferate in soil, competing for nutrients, space, water, or oxygen and capacity to mobilise soil nutrients as compared with other soil fungi. Such competitive ability enhanced by exerting resistance against a variety of toxins or antimicrobial compounds produced by other microorganisms due to the presence of ATP-binding cassettes transporters. Reports of <italic>T. harzianum</italic> CECT 2413 producing <italic>Gtt1</italic> gene encoding for high-affinity glucose transporter expressed at very low glucose concentration and <italic>T. virens</italic> producing <italic>TvInv</italic> encoding for intracellular invertase for sucrose hydrolysis provided evidence for nutrient competition similar to the scenario of competence among microorganisms (<xref ref-type="bibr" rid="B14">Benitez et&#xa0;al., 2004</xref>).</p>
</sec>
<sec id="s3_4_4">
<title>Rhizosphere competence</title>
<p>The term &#x201c;Rhizosphere&#x201d; was coined for the first time for <italic>Trichoderma</italic> strains by <xref ref-type="bibr" rid="B5">Ahmad and Baker (1987)</xref> who attributed the capability of <italic>Trichoderma</italic> to colonize root surfaces to a depth greater than 2 cm (<xref ref-type="bibr" rid="B35">Chao et&#xa0;al., 1986</xref>), proliferate in developing rhizosphere to a concentration exceeding initial population on seed coat (<xref ref-type="bibr" rid="B155">Papavizas, 1982</xref>) and compete with other microorganisms for nutrients secreted by roots in rhizospheric soil. Seed treatment with <italic>T. harzianum</italic> rhizosphere competent strain T-95 of barley, cucumber, pea, radish, and tomato was implicated in reduced damping-off disease incidence caused by <italic>Pythium ultimum</italic> due to the absence of fungal units in up to 8 cm of root segment as compared with 3,000 CFU/g rhizosphere soil in case of untreated seeds (<xref ref-type="bibr" rid="B5">Ahmad and Baker, 1987</xref>). The colonization of roots by <italic>Trichoderma</italic> species is mediated by attachment of the fungus to roots <italic>via</italic> appressoria-like structures (class I hydrophobin encoded by gene TasHyd1), whereas penetration is achieved by release of protease and cellulolytic enzymes (<xref ref-type="bibr" rid="B24">Brotman et&#xa0;al., 2008</xref>). Recent study showed that rhizosphere competence by <italic>Trichoderma</italic> strains is governed by extensive communication <italic>via</italic> exchange and perception of signaling molecules, that is, deposition of fungal elicitors, auxin-like metabolites, and proteinaceous compounds released by <italic>Trichoderma</italic> are perceived by plants rhizosphere (<xref ref-type="bibr" rid="B81">Garnica-Vegara et&#xa0;al., 2015</xref>).</p>
<p>Studies by <xref ref-type="bibr" rid="B137">McLean et&#xa0;al. (2005)</xref> also determined that proliferation of <italic>T. atroviride</italic> C52 in onion rhizosphere and rhizoplane are dependent on the type of formulation used to introduce the fungus into the soil. Results indicated higher fungal concentration of 10<sup>5</sup> cfu/g soil was maintained through pellet formulation with reduced incidence of <italic>Sclerotium cepivorum</italic> as compared to solid-substrate and seed-coating formulations maintaining 10<sup>4</sup> and 10<sup>1</sup> CFU/g soil, respectively. Similarly, <italic>T. viride</italic> as cob-based formulation, when applied in the form of seed coat and soil treatment, imparted enhanced plant growth performance of mungbean, pea, and pigeon pea through better rhizosphere competence and reduced disease incidence of <italic>Fusarium</italic> in <italic>Cajanus</italic> sp. by 86.00% was also document by <xref ref-type="bibr" rid="B159">Pappu (2018)</xref>.</p>
</sec>
<sec id="s3_4_5">
<title>Induced resistance</title>
<p>Induction of local and systemic resistance as indirect mechanism by <italic>Trichoderma</italic> species have been reported for both monocots and dicots involving recognition of the fungus by plants through ISR and systemic acquired resistance (SAR) against many phytopathogens (<xref ref-type="bibr" rid="B89">Harman et&#xa0;al., 2004</xref>). The response is mediated by phytohormones <italic>viz.</italic>, jasmonic acid (JA), and ethylene (ET) as closest analogue of induced resistance activated by rhizobacteria (<xref ref-type="bibr" rid="B211">Van loon, 2007</xref>) and induction of pathogenesis-related (PR) genes expression mediated by salicylic acid (SA), triggered by biotrophic and hemi-biotrophic pathogens. The first demonstration of induced resistance by <italic>Trichoderma</italic> was reported by <xref ref-type="bibr" rid="B18">Bigirimana et&#xa0;al. (1997)</xref> against <italic>Colletotrichum lindemuthianum</italic> and <italic>Botrytis cinerea</italic>, causing foliage diseases of beans.</p>
<p>The concept was further supported by <xref ref-type="bibr" rid="B236">Yedidia et&#xa0;al. (1999)</xref> who studied induced resistance by <italic>T. harzianum</italic> against cucumber seedling disease. Indirect evidence of plant ISR by <italic>Trichoderma</italic> was first described by (<xref ref-type="bibr" rid="B29">Calderon et&#xa0;al., 1993</xref>) through induction of hypersensitive response (HR) and phytoalexin synthesis by <italic>T. viride</italic> cellulase in grapevine cell cultures. Later, <xref ref-type="bibr" rid="B33">Chang et&#xa0;al. (1997)</xref> demonstrated the capability of heat-stable mycelial extracts of <italic>T. longibrachiatum</italic> to induce disease resistance against <italic>Phytophthora parasitica</italic> by induction of higher level of <italic>PR-1b</italic> and <italic>PR-5</italic> in tobacco, <italic>Nicotiana tabacum</italic> (<xref ref-type="bibr" rid="B33">Chang et&#xa0;al., 1997</xref>). In addition, reports on soil inoculation with <italic>T. harzianum</italic>T39 imparted resistance to leaves of bean plants, that is, parts spatially separated from the site of inoculation against <italic>B. cinerea</italic> and <italic>C. lindemuthianum</italic> have also been documented (<xref ref-type="bibr" rid="B18">Bigirimana et&#xa0;al., 1997</xref>; <xref ref-type="bibr" rid="B48">De Meyer et&#xa0;al., 1998</xref>).</p>
</sec>
<sec id="s3_4_6">
<title>Nutrient solubilization and sequestration</title>
<p>The ability of <italic>Trichoderma</italic> species to enhance plant growth and productivity was determined by utilization of indirect mechanism mediated by solubilization of mineral nutrients available in limited amounts for plants in soil, involving chelation and reduction (<xref ref-type="bibr" rid="B89">Harman et&#xa0;al., 2004</xref>). Earlier evidence on solubilization of various plant nutrients such as rock phosphate, Cu<sup>2+</sup>, Fe<sup>3+</sup>, Zn<sup>2+</sup>, and Mn<sup>4+</sup> ions by <italic>T. harzianum</italic> T22 was documented by <xref ref-type="bibr" rid="B9">Altomare et&#xa0;al. (1999)</xref>, possibly due to production of diffusible metabolites capable of reducing Fe (III) and Cu (II) due to the formation of Fe (II)-Na<sub>2</sub>-2,9-batho- and Cu(I)-Na<sub>2</sub>-2,9- dimethyl-4,7-diphenyl-1,10-phenanthrolinedisulfonic acid complexes. <xref ref-type="bibr" rid="B26">Brotman et&#xa0;al. (2012)</xref> described nitrogen use efficiency of <italic>T. asperelloides</italic> T203 through increased amino acid content in colonized plants by allocating, re-used nitrogen, and increased nitrogen uptake as major determinants of transported nitrogen in plants.</p>
<p>A reduction of soil pH, caused by biosynthesis and release of organic acids, such as gluconic, citric, and fumaric acids, facilitates <italic>Trichoderma&#x2019;s</italic> mobilization of immobile nutrients, including phosphates, iron, magnesium, and manganese (<xref ref-type="bibr" rid="B218">Vinale et&#xa0;al., 2008</xref>). <xref ref-type="bibr" rid="B100">Jalal et&#xa0;al. (1986)</xref> identified Fe-chelating complex, that is, siderophores produced by <italic>T. virens</italic> are derivatives of hydroxymate nature classified under three families <italic>viz.</italic>, fusarinines, coprogens, and ferrichrome, which play key role in binding insoluble iron (Fe<sup>3+</sup>), transforms it into a soluble form (Fe<sup>2+</sup>) making it available to plants. In addition, the formation of siderophore-iron complex by <italic>Trichoderma</italic> species participates in depletion of Fe sources from soil inhibiting growth of phytopathogenic fungi (<xref ref-type="bibr" rid="B224">Wallner et&#xa0;al., 2009</xref>). Siderophore production also played role in conidial germination of <italic>T. atroviride</italic> (<xref ref-type="bibr" rid="B212">Velazquez-Robledo et&#xa0;al., 2011</xref>), competitiveness of <italic>T. asperellum</italic>, and suppression of <italic>F. oxysporum</italic> f.sp. <italic>lycopersici</italic> (<xref ref-type="bibr" rid="B184">Segarra et&#xa0;al., 2010</xref>).</p>
</sec>
<sec id="s3_4_7">
<title>Inactivation of pathogen&#x2019;s enzymes</title>
<p>Fungal cell walls are composed of polysaccharides, lipids, proteins, &#x3b2;-glucans, and 90% of chitin. In contrast, cell walls of oomycetes consist of cellulose. Production of hydrolytic enzymes viz., chitinase, glucanase, N-acetylglucosaminidase, and protease by <italic>Trichoderma</italic> sp. causes the breakdown down of polysaccharides, chitin, and &#x3b2;-glucans, which are responsible for rigidity and integrity of fungal cells, and are attributed to successful mycoparasitic relationships. In recent literature, dual culture experiments between <italic>Trichoderma</italic> and <italic>R. solani</italic> <xref ref-type="bibr" rid="B94">Heflish et&#xa0;al. (2021)</xref> unravelled the presence of a diffusible molecule before direct contact, determined to activate transcription of cell wall degrading enzymes (CWDEs) encoding genes. However, under secretome analysis conducted for direct confrontation of <italic>T. harzianum</italic> EST 323 against <italic>R. solani</italic> through two-dimensional gels (2-DE) and liquid chromatography mass spectrometry (LC-MS/MS), seven CWDEs (viz., xylanase, chitinase, &#x3b2;<italic>-</italic>1,6-glucanase, &#x3b2;-1,3-glucanase, mannose, and protease) were identified (<xref ref-type="bibr" rid="B208">Tseng et&#xa0;al., 2008</xref>).</p>
<p>In similar studies, proteomic analysis confirmed a critical role of CWDEs produced by <italic>T. harzianum</italic> in antagonism by deactivating mycelia of <italic>B. cinerea</italic>, indicating cell walls as the primary target during mycoparasitism (<xref ref-type="bibr" rid="B234">Yang et&#xa0;al., 2009</xref>). Several studies identified virulent genes encoding for CWDEs <italic>viz.</italic>, <italic>Eng18B</italic> a gene encoding for typical glycoside hydrolase family enzyme by <italic>T. atroviride</italic>, <italic>Nag1</italic>, and <italic>ech42</italic> gene encoding for <italic>N</italic>-acetyl-glucosaminidase and endochitinase, respectively, by <italic>Trichoderma</italic> species (<xref ref-type="bibr" rid="B121">Kulling et&#xa0;al., 2000</xref>). Recently, the concept of enzyme biosynthesis merged with production with antibiotics unravelled a synergistic mechanism of biological control in <italic>T. harzianum</italic> through a combination endochitinase, gliotoxin, and peptabiols resulted in a detrimental effect on conidial germination and hyphal elongation of <italic>B. cinerea</italic> (<xref ref-type="bibr" rid="B87">Gu et&#xa0;al., 2020</xref>).</p>
</sec>
</sec>
</sec>
<sec id="s4">
<title>
<italic>Trichoderma</italic> species: Chemical profile</title>
<p>
<italic>Trichoderma</italic> species are notable for having the ability to grow rapidly, exploit diverse substrates, and resist harmful chemicals. Among soilborne fungal communities, they are dominant. <italic>Trichoderma</italic> produce a broad range of biologically active compounds that are among the most fascinating and important properties of the organism. In particular, plant defense responses can be mediated by proteins, peptides, and low-molecular-weight compounds produced by <italic>Trichoderma</italic> species (<xref ref-type="bibr" rid="B171">Reino et&#xa0;al., 2008</xref>). Compounds with low molecular weights include aromatic compounds and polyketides such as butenolides and pyrones, isocyanate metabolites, and volatile terpenes. It produces volatile (such as ET, alcohols, hydrogen cyanide, ketones, and aldehydes) and non-volatile (such as peptides) compounds that inhibit microbial growth. <xref ref-type="bibr" rid="B171">Reino et&#xa0;al. (2008)</xref> have shown that <italic>Trichoderma</italic> species can produce a number of volatile (such as pyrones and sesquiterpenes) and non-volatile (such as peptaibols) metabolites. Here are a few examples of the volatile organic compounds (VOCs) and other metabolites released by different species of <italic>Trichoderma</italic>.</p>
<sec id="s4_1">
<title>VOCs and their role in control of plant pathogens</title>
<p>
<italic>Trichoderma</italic> are well-known for their VOCs that make them of interest to the scientific community. Natural products, or SMs, are among these compounds. Often, these compounds do unknown or obscure things in the producing organism that are vital to humankind. Some of these VOCs are beneficial to society, such as ones for medical, industrial, and agricultural purposes. Numerous reports suggest that some VOCs possess antibacterial and immunosuppressive properties as well as phytotoxic and mycotoxin properties. VOCs are low-molecular-weight organic compounds with substantive vapor pressure under ambient conditions. They have diverse chemical structures such as alcohols, ketones, mono- and sesquiterpenes, esters, lactones, or C<sub>8</sub> compounds (<xref ref-type="bibr" rid="B115">Korpi et&#xa0;al., 2009</xref>; <xref ref-type="bibr" rid="B188">Siddiquee et&#xa0;al., 2012</xref>). Chemical ecologists explain VOCs as semiochemicals that attract and deter insect pests and other invertebrates.</p>
<p>VOCs derived from fungi are used for biological control of plant pathogens in agriculture. Moreover, these VOC mixtures have been studied for their ability to promote plant growth. Food companies use the same biological control properties to reduce fungal spoilage of food commodities in postharvest, which is called &#x201c;mycofumigation.&#x201d; The potential role of fungal VOCs has recently been examined. The genus <italic>Trichoderma</italic> is well-known for its production of volatile compounds with potential biological activity. VOC is usually defined as normal saturated hydrocarbons (C7-C30), cyclopentane, cyclohexane, alcohol, fatty acid, sulfur-containing compounds, esters, simple and benzine derivatives, hydroxy, or amino compounds. A compound&#x2019;s production differs based on (1) its specific molecular structure, (2) its strain and species, (3) its presence of microbes, and (4) the balance between its biosynthesis and biotransformation rates (<xref ref-type="bibr" rid="B218">Vinale et&#xa0;al., 2008, 2010</xref>). The important VOCs derived from <italic>Trichoderma</italic> are shown in <xref ref-type="table" rid="T3">
<bold>Table&#xa0;3</bold>
</xref>.</p>
<table-wrap id="T3" position="float">
<label>Table&#xa0;3</label>
<caption>
<p>Volatile and non-volatile metabolites identified from <italic>Trichoderma</italic> species.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Species name</th>
<th valign="top" align="center">Non-volatile metabolites</th>
<th valign="top" align="center">References</th>
<th valign="top" align="center">VOC</th>
<th valign="top" align="center">Reference</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">
<italic>T. arundinaceum</italic>
</td>
<td valign="top" align="left">Prealamethicin F50, alamethicin II, alamethicin F50, atroviridin J</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B36">Chavez et&#xa0;al. (2017)</xref>
</td>
<td valign="top" align="left">Harzianum A</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B135">Malmierca et&#xa0;al. (2012)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">T. asperellum</td>
<td valign="top" align="left">Trichodermaerin, aspereline G</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B38">Chen et&#xa0;al. (2013)</xref>; <xref ref-type="bibr" rid="B34">Chantrapromma et&#xa0;al. (2014)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">6-Amyl alpha-pyrone</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B235">Yang et&#xa0;al. (2014)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Dechlorotrichodenone C</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B196">Song et&#xa0;al. (2018)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. hamatum</italic>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Isonitrin A</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B13">Baldwin et&#xa0;al. (1991)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Viridiol</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B232">Wipf and Kerekes (2003)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Harziandione</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B126">Liang (2016)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. koningiopsis</italic>
</td>
<td valign="top" align="left">Trikoningin KB I</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B138">McMullin et&#xa0;al. (2017)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Konginginin A -M</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B37">Chen et&#xa0;al. (2015)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Lutidonecarboxylic acid, cyclonertriolisoechinulin A, echinuline, cyclopenol 3-o-methylviridicatin</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B186">Shi (2018)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. citrinoviride</italic>
</td>
<td valign="top" align="left">Ergosterol endoperoxide</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B126">Liang (2016)</xref>
</td>
<td valign="top" align="left">Citrantifidiene (hexa-1,3-dienyl ester of acetic acid),<break/>citrantifidiol (cyclohexane-1,3-diol)</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B75">Evidente et&#xa0;al. (2008)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Ergosterol endoperoxide, harzianolide, trichoharzianin, 3-indol acetic acid</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B126">Liang (2016)</xref>, <xref ref-type="bibr" rid="B218">Vinale et&#xa0;al. (2008)</xref>
</td>
<td valign="top" align="left">Harzianum A</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B149">Nielsen et&#xa0;al. (2005)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">&#x3b2;-sitosterol</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B4">Ahluwalia et&#xa0;al. (2015)</xref>
</td>
<td valign="top" align="left">Harziphilone</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B171">Reino et&#xa0;al. (2008)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Hexadecanoic acid, hexatriacontane,<break/>indane</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B188">Siddiquee et&#xa0;al. (2012)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. longibrachiatum</italic>
</td>
<td valign="top" align="left">&#x3b2;-sitosterol</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B203">Tarus et&#xa0;al. (2003)</xref>
</td>
<td valign="top" align="left">Harzianone, harziane diterpene</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B144">Miao et&#xa0;al. (2012)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Cerevisterol ergosterol peroxide, squalene sorbicillin</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B102">Ji et&#xa0;al. (2014)</xref>
</td>
<td valign="top" align="left">Bisvertinolone</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B2">Abe et&#xa0;al. (1998a)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Ergokonin A</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B215">Vicente et&#xa0;al. (2001)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">5-Hydroxyvertinolide</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B11">Andrade et&#xa0;al. (1997)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Bislongiquinolide</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B11">Andrade et&#xa0;al. (1997)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Bislongiquinolide</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B6">Ahmed et&#xa0;al. (2009)</xref>
</td>
<td valign="top" align="left">Trichodermin</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B149">Nielsen et&#xa0;al. (2005)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Trichodecenins, trichorovins, trichocellins</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B79">Fujta et&#xa0;al. (1994)</xref>
</td>
<td valign="top" align="left">Viridenepoxydiol,<break/>Viridepyronone</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B73">Evidente et&#xa0;al. (2006</xref>; <xref ref-type="bibr" rid="B74">2003)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Trichorovin I and II,</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B222">Wada et&#xa0;al. (1995)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. polysporum</italic>
</td>
<td valign="top" align="left">Valinotricin, cyclonerodiol oxide</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B78">Fujita et&#xa0;al. (1984)</xref>
</td>
<td valign="top" align="left">Emodin<break/>Ergosterol</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B78">Fujita et&#xa0;al. (1984)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. atroviride</italic>
</td>
<td valign="top" align="left">Atrichodermone A-D, trichodermone A 1,3-dione-5,5-dimethylcyclohexane</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B105">Kandasamy et&#xa0;al. (2018)</xref>
</td>
<td valign="top" align="left">Chloroform,<break/>Cinnamic acid,<break/>Diterpene B, C, D, E,<break/>Limonene,<break/>Toluene</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B148">Nemcovic et&#xa0;al. (2008)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">40-(4,5-Dimethyl-1,3-dioxolan-2-yl) methylphenol, 30-hydroxybutan-20-yl) 5-oxopyrrolidine-<break/>2-carboxylate, troviridetide</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B132">Lu et&#xa0;al. (2012)</xref>
</td>
<td valign="top" align="left">Ethylbenzene<break/>Iso-menthone,<break/>Isopentyl acetate,<break/>Menthone,<break/>Nerolidol,<break/>&#x3b1;-curcumene,<break/>&#x3b2;-bisabolene</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B165">Polizzi et&#xa0;al. (2011)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">&#x3b1;-Terpinene, &#x3b1;-phellandrene,<break/>&#x3b1;-terpinolene,<break/>&#x3d2;-terpinene</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B199">Stoppacher et&#xa0;al. (2010)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. polysporum</italic>
</td>
<td valign="top" align="left">Trichosporin Bs</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B127">Lida et&#xa0;al. (1993)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. reesei</italic>
</td>
<td valign="top" align="left">Harzialactone A, 3,6-dibenzylpiperazine-2,5-dione,<break/>3-benzyl-8-hydroxyl-pyrrolopiperazine-<break/>2,5-dione</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B200">Sun et&#xa0;al. (2007)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. saturnisporum</italic>
</td>
<td valign="top" align="left">Cerebroside A, sorbicillin B, bisvertinolone, saturnispol A-D</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B142">Meng et&#xa0;al. (2017)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">T. citrinoviride</td>
<td valign="top" align="left">Penicillenol B1, penicillenol B2</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B98">Hu et&#xa0;al. (2014)</xref>
</td>
<td valign="top" align="left">Citrantifidiene, Citrantifidiol</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B75">Evidente et&#xa0;al. (2008)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Citrostadienol, euphorbol, trichocitrin</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B126">Liang (2016)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. virens</italic>
</td>
<td valign="top" align="left">Trichocarane A,14-hydroxy CAF-603 7-&#x3b2;-hydroxy CAF-603, chromone</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B186">Shi (2018)</xref>
</td>
<td valign="top" align="left">Mevalonic acid</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B164">Phuwapraisirisan et&#xa0;al. (2006)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Oleic ester</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B125">Lee et&#xa0;al. (1995a)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Trichocaranes A, B, C and D</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B133">Macias et&#xa0;al. (2000)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Trichodermamides A-B,<break/>Trichodermin</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B82">Garo et&#xa0;al. (2003)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Viridin</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B192">Singh et&#xa0;al. (2005)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Viridiol</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B164">Phuwapraisirisan et&#xa0;al. (2006)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. gamsii</italic>
</td>
<td valign="top" align="left">Trichoderone A, aspochalasin</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B50">Ding et&#xa0;al. (2012)</xref>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">
<italic>T. koningii</italic>
</td>
<td valign="top" align="left">Trichodermaketone C &amp; D, koninginin A-F</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B182">Sawant et&#xa0;al. (1996)</xref>
</td>
<td valign="top" align="left">6-Pentyl- &#x3b1;-pyrone,<break/>dermadin</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B199">Stoppacher et&#xa0;al. (2010)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left">Trichokonin I-IV</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B97">Huang et&#xa0;al. (1995)</xref>
</td>
<td valign="top" align="left">Ergokonin A B</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B170">Reichenbach et&#xa0;al. (1990)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Gliotoxin</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B88">Haggag and Abo-Sedera (2005)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Palmitic acid</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B15">Benoni et&#xa0;al. (1990)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">Trichodermamides A-D</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B195">Song et&#xa0;al. (2010)</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
<p>
<xref ref-type="table" rid="T3">
<bold>Table&#xa0;3</bold>
</xref> revealed that the major compounds produced by <italic>Trichoderma</italic> species include gliotoxin, gliovirin, glisoprenin, viridin, 6-pentyl-&#x3b1;-pyrone, hepteledic acid, koninginins, trichodermamides, peptaibols, anthraquinones, polypeptides, terpenoids, polyketides, trichodermaides, trichothecenes, harzialactones, compounds derived from alpha-amino acids, and azaphilones (<xref ref-type="bibr" rid="B214">Vey et&#xa0;al., 2001</xref>; <xref ref-type="bibr" rid="B171">Reino et&#xa0;al., 2008</xref>). <xref ref-type="bibr" rid="B129">Liu et&#xa0;al. (2009)</xref> reported that crysophanol, pachybasin, &#x3c9;- hydroxypachybasin, emodin, 1, 7-dihydroxy-3-hydroxymethyl-9,10-anthraquinone, and 1,5-dihydroxy-3-hydroxymethyl-9,10-anthraquinone showed potential bioactivity against several plant pathogens. In addition, pchybasin and emodin play major roles in the biocontrol mechanism of <italic>Trichoderma</italic> mycoparasitic coils through cAMP signaling (<xref ref-type="bibr" rid="B128">Lin et&#xa0;al., 2012</xref>). A novel compound, cerinolactone, extracted from <italic>T. cerinum</italic> together with three known butenolides containing harzianolide, 3,4-dialkylfuran-2(5<italic>H</italic>)-one nucleus, T39butenolide, and dehydroharzianolide, both compounds exhibited activities against <italic>B. cinerea</italic>, <italic>R. solani</italic>, and <italic>P. ultimum</italic> (<xref ref-type="bibr" rid="B217">Vinale et&#xa0;al., 2012</xref>). <italic>T. harzianum</italic> ETS 323 exhibits a stimulatory effect and an antagonistic action on <italic>R. solani</italic> by a novel compound of l-amino oxidase (Th-LAAO). Considering these results, <italic>T. harzianum</italic> is a good biocontrol agent due to its ability to provide insight into the function of l-amino acid oxidase (<xref ref-type="bibr" rid="B233">Yang et&#xa0;al., 2011</xref>). Due to these beneficial effects, <italic>T. asperellum</italic>, <italic>T. atroviride</italic>, and <italic>T. harzianum</italic> strains have been used as plant protection agents in agriculture to control molds (<xref ref-type="bibr" rid="B213">Verma et&#xa0;al., 2007</xref>).</p>
<p>Mycoparasitism and interaction of <italic>Trichoderma</italic> with plants are mediated by VOCs (<xref ref-type="bibr" rid="B218">Vinale et&#xa0;al., 2008</xref>). Few research investigations addressed the effect of various culture media on the volatile types produced by <italic>Trichoderma</italic> (<xref ref-type="bibr" rid="B229">Wheatley et&#xa0;al., 1997</xref>) or the function properties of some of these volatiles (<xref ref-type="bibr" rid="B148">Nem&#x10d;ovi&#x10d; et&#xa0;al., 2008</xref>). There have been reports of multiple <italic>Trichoderma</italic> species producing VOCs as shown in <xref ref-type="table" rid="T3">
<bold>Table&#xa0;3</bold>
</xref> (<xref ref-type="bibr" rid="B199">Stoppacher et&#xa0;al., 2010</xref>). VOCs form intermediates and end products of diverse metabolic pathways and include ketones, alcohols, esters, lactones, mono- and sesquiterpenes, and some C<sub>8</sub> compounds (<xref ref-type="bibr" rid="B115">Korpi et&#xa0;al., 2009</xref>; <xref ref-type="bibr" rid="B188">Siddiquee et&#xa0;al., 2012</xref>). These compounds are relatively nonpolar and have high vapor pressures. The compounds with high molecular weight are polar, such as peptaibols.</p>
<p>To determine whether these compounds are significant during the life cycles of their producing species properly, controlled studies are needed. Nevertheless, observing fungal ecology may lead to the development of strategies that have proven effective for the discovery of novel bioactive fungal compounds. The use of biocontrol tactics is one example. Historically, <italic>Trichoderma</italic> species have been used as biological control agents since the 1930s, and numerous field experiments have proven that applications of <italic>Trichoderma</italic> species promote plant growth while limiting pathogen growth. Thus, due to production of VOCs, <italic>Trichoderma</italic> species are effective biofungicides, as they degrade other pathogenic fungi enzymatically, produce antimicrobial compounds that kill pathogenic fungi, and compete with them for nutrients and space.</p>
</sec>
<sec id="s4_2">
<title>Non-volatile metabolites and their role in control of plant pathogens</title>
<p>SMs produced by <italic>Trichoderma</italic> species have a variety of biological activities. There have been a number of reviews published about <italic>Trichoderma</italic> metabolites. These reviews focus on structure, biological activity, or fungal origin. An overview of some of the most important non-volatile compounds in <italic>Trichoderma</italic> has been provided in <xref ref-type="table" rid="T3">
<bold>Table&#xa0;3</bold>
</xref>. Seventeen compounds were isolated from the endophytic fungus <italic>Trichoderma</italic> sp. Xy24: ergosterol, trichodimerol, cyclonerodiol, and trichoacorenol (<xref ref-type="bibr" rid="B240">Zhang, 2015</xref>); 10,11-dihydroxy-cyclonerodiol, trichocage B, harzianone, 14-hydroxy-trichoacorenol; ergokonin B, (9R,10R)-dihydro-harzianone, and methyl stearate (<xref ref-type="bibr" rid="B241">Zhang et&#xa0;al., 2014</xref>), trichoacorenol B, harzianelactone, cyclonerodiol B, and trichoacorenol C (<xref ref-type="bibr" rid="B242">Zhang et&#xa0;al., 2016</xref>). <italic>Trichoderma harzianum</italic> and <italic>T. longibrachiatum</italic> that contain tetracyclic scaffolds, harziandione, have been described as potential microbial biocontrol agents against <italic>C. lagenarium</italic> and <italic>F. oxysporum</italic> (<xref ref-type="bibr" rid="B144">Miao et&#xa0;al., 2012</xref>). There is a potential antagonistic action of <italic>T. saturnisporum</italic> owing to the presence of cerebroside A, sorbicillin B, bisvertinolone, and saturnispol A&#x2013;D (<xref ref-type="bibr" rid="B142">Meng et&#xa0;al., 2017</xref>). The presence of 5-hydroxyvertinolide, bislongiquinolide (<xref ref-type="bibr" rid="B11">Andrade et&#xa0;al., 1997</xref>), and Ergokonin A (<xref ref-type="bibr" rid="B215">Vicente et&#xa0;al., 2001</xref>) in <italic>T. longibrachiatum</italic> also demonstrated antagonistic activity. Likewise, the antagonistic effect of <italic>T. harzianum</italic> was also attributed to non-volatile metabolites such as ergosterol, harzianolide, endoperoxide, and 3-indol acetic acid.</p>
</sec>
</sec>
<sec id="s5">
<title>Compatibility studies</title>
<p>Inorganic pesticides (insecticides, fungicides, and herbicides) and fertilizers have played vital role in supplementing plant nutrients and curbing biotic stresses. The utilization of bioformulations as part of integrated plant disease management strategies involved combination of cultural, physical, chemical, and biological means. <xref ref-type="bibr" rid="B68">Dutta et&#xa0;al. (2017)</xref> studied compatibility of <italic>T. pseudokoningii</italic> with selective fertilizers, insecticides, fungicides, herbicides, and organic stickers. Researchers found that all the tested pesticides inhibited the growth of <italic>T. pseudokoningii</italic>, with the exception of thiamethonaus 25% WG at 0.125% and ritha at the highest test dose found compatible. Urea and MOP were found to be compatible, whereas SSP and CAN inhibited growth. These variations in inhibitory potential are attributed to inherent variations in chemical ingredients within the fungus&#x2019; cellular components. In another study, <italic>T. viride</italic> also showed compatibility with insecticide (imidacloprid), fungicides (mancozeb, tebuconazole, pencycuron, and propineb), and herbicides (imazathafir, 2, 4-D sodium salt, and oxyfluorfen) (<xref ref-type="bibr" rid="B134">Madhavi et&#xa0;al., 2011</xref>). In a recent study, <xref ref-type="bibr" rid="B193">Singh et&#xa0;al. (2019)</xref> tested compatibility of <italic>Trichoderma</italic> species with nematicides such as carbofuran, aldicarb, phorate, and thionazin and found compatibility with carbofuran and phorate for management of root knot nematode in rice. <italic>Trichoderma viride</italic> and <italic>T. harzianum</italic> were also found compatible with azoxystrobin and metalaxyl, respectively (<xref ref-type="bibr" rid="B185">Shashikumar et&#xa0;al., 2019</xref>).</p>
<p>In a view to improve the efficacy of <italic>T. harzianum</italic> application against phytopathogens and plant growth promotion, its compatibility was tested with biosynthesized (27.64 nm) and commercial grades (20 nm, Sigma-Aldrich, St. Louis, Missouri, United States) of silver (Ag) and chemically synthesized zinc oxide (ZnO, 20 nm) nanoparticles (NPs). In this context, <xref ref-type="bibr" rid="B21">Biswas and Dutta (2019)</xref> reported 100% compatibility of <italic>T. harzianum</italic> with commercial grade of AGNPs at 5,000 ppm and slightly lower of 98.94 and 90.00% in case of myco-AgNPs at 1,000 and 5,000 ppm, respectively. In contrast, inhibitory effect on growth of <italic>T. harzianum</italic> was observed under all the tested concentrations of ZnONPs. Recently, in a study by <xref ref-type="bibr" rid="B210">Upamanya et&#xa0;al. (2020)</xref>, compatible reactions of <italic>T. harzianum</italic> and <italic>T. asperellum</italic> were also tested with fungal entomopathogens <italic>viz.</italic>, <italic>Beauveria bassiana s.l.</italic>, and <italic>Metarhizium anisopliae s.l.</italic> (recently named as <italic>M. robertsii</italic>) for development of microbial consortia. Under standard co-culture conditions, combination-I (<italic>B. bassiana s.l.</italic> + <italic>T. harzianum</italic>, <italic>M. anisopliae s.l.</italic> + <italic>T. harzianum</italic>, <italic>B. bassiana s.l. + M. anisopliae s.l. + T. harzianum</italic>) and combination-II (<italic>T. asperellum</italic> + <italic>B. bassiana s.l.</italic>, <italic>T. asperellum + M. anisopliae s.l.</italic>, <italic>T. asperellum + B. bassiana s.l. + M. anisopliae s.l.</italic>) gave compatible reaction. Mixed culture showed mutual growth and overlapping among test microbial biocontrol agents, due to lack of production of SMs by individual organism against another, while growing in the same media.</p>
</sec>
<sec id="s6">
<title>Mass culture, growth, and formulation of <italic>Trichoderma</italic>
</title>
<p>The development of potential <italic>Trichoderma</italic> species as successful microbial biocontrol agents and its effective commercial application depends on production of viable propagules, mass production, formulation strategies, and optimized delivery systems. Fungal spores of <italic>Trichoderma</italic> as active ingredient are formulated using different organic and inorganic carriers (diluents and surfactant), through solid or liquid state fermentation to improve physical characteristics, increase shelf life, and protect against adverse environmental conditions. Different kinds of <italic>Trichoderma</italic> propagules used in formulation includes hyphae, chlamydospores, and conidia, of which both conidia and chlamydospore are highly preferred means due to their ability to withstand adverse environmental conditions as compared with hyphae due to lack of resistance toward dehydration (<xref ref-type="bibr" rid="B95">Howell, 2003</xref>).</p>
<p>Under solid state formulation, <italic>Trichoderma</italic> species are commonly multiplied on boiled rice, sorghum seeds, rice saw dust, wheat bran-saw dust, and agro-waste products such as peels of potato, brinjal, papaya, banana, spinach, guava, used tea leaves, sugarcane, and pea husk used as solid substrate or food base. Solid formulation types <italic>viz.</italic>, wet dust, dry pellets, granules, dry dust, and granules are adjuvated by using adhesive substances such as Arabic gum, carboxymethylcellulose (CMC), clays, compost, talc powder, and so forth. In a study by <xref ref-type="bibr" rid="B63">Dutta and Das (2009)</xref>, the seed treatment of French bean (var. Contender) with talc-based formulation of <italic>T. harzianum</italic> in combination with methylcellulose and carbendazim was found significantly efficient and at par with seed treatment with carbendazim for the management of white mold rot of bean.</p>
<p>Liquid formulations were adopted for multiplication of fungal propagules in soluble materials <italic>viz.</italic>, broth cultures of potato dextrose broth (PDB), and agricultural substrates such as rice water, vegetables juices, and boiled dal. Fully grown mycelial mat along with supernatant imposed with submerged conidia are grounded homogenously and amended with several adjuvants such as carboxymethyl cellulose (CMC), Tween-80, mannitol, peptone, and oil. Sprayable/liquid formulations include soluble liquids (SLs), soluble powders (SPs), soluble granules (SGs), emulsifiable concentrates, and liquid suspension dispersed in water, that is, suspension concentrates (SCs) and aqueous suspension (AS). <xref ref-type="bibr" rid="B45">Das et&#xa0;al. (2006)</xref> tested efficacy of osmoticant (mannitol) amended PDB liquid formulation yielded higher biomass, sporulation, cfu, and dry weight of biomass followed by modified Richard&#x2019;s broth (MRB). In addition, talc-based formulation at 3:1 dose showed higher sporulation as compared with starch-based formulation at 1:1 dose with a shelf life of 60 and 30 days, respectively. However, seed treatment with bioformulation enriched with <italic>T. harzianum</italic> + talc + osmoticant assessed under field condition showed lowest stem rot disease index caused by <italic>R. solani</italic> with higher enhanced percent seed germination, plant vigour, and crop yield.</p>
<p>In North-Eastern region (NER) of India, several locally made liquid-based biopesticides from native strains of <italic>Trichoderma</italic> species were developed such as Org-Trichojal (<italic>T. harzianum</italic>) in Assam, UmTricho (<italic>T. harzianum</italic>), <italic>UmTriv</italic> (<italic>T. viride</italic>), and two <italic>Trichoderma-</italic>based microbial consortia, that is, UmTim <italic>(T. harzianum + Metarhizium anisopliae s.l.</italic>) and UmComb (<italic>T. harzianum + Beauveria bassiana s.l. + M. anisopliae s.l. + Akanthomyces</italic> (<italic>=Lecanicillium</italic>) <italic>lecanii + Pseudomonas fluorescens</italic>) in Meghalaya (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4</bold>
</xref>) and maintained by team workers at Central Agricultural University (Imphal), Umiam and Assam Agricultural University, Jorhat (<xref ref-type="bibr" rid="B59">Dutta et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B57">Dutta, 2020</xref>). The technology was used in preparation were standardized by <xref ref-type="bibr" rid="B57">Dutta et&#xa0;al. (2020)</xref> as mycelial mat centrifuged in PDB, amended with mannitol (osmoticant), sunflower oil (UV protector), Tween-80 (surfactant), CMC (cellulose-enrich), peptone (nitrogen supplier), and glycerol (preservative) with a shelf life of 180 days (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4</bold>
</xref>). Developed bioformulations have been locally accepted by farmers, KVKs, and institutes from the region as well as in different states of India and have been adopted in organic package of practices for cauliflower, cabbage, and spice crops of Assam. Seed treatment with <italic>T. harzianum&#x2013;</italic>based bioformulation, that is, Org-Trichojal@ 5g/L of water + CMC @ 0.02% for 1h followed by shade dried for 2h prior to sowing has been recommended against soilborne disease such as damping off of cabbage and cauliflower. In spice crop cultivation, that is, bhoot jolokia, <italic>Capsicum chinense</italic> Jaqc, and seed treatment with <italic>T. harzianum&#x2013;</italic>based bioformulation, <italic>Org-Trichojal</italic> was recommended at the rate of 5 ml/kg of seed against <italic>R. solani</italic> and <italic>Fusarium</italic> spp. Commercial formulations of <italic>Trichoderma</italic> species available worldwide and in India are listed in <xref ref-type="table" rid="T4">
<bold>Table&#xa0;4</bold>
</xref>.</p>
<fig id="f4" position="float">
<label>Figure&#xa0;4</label>
<caption>
<p>Biopesticides developed from native strains of <italic>Trichoderma</italic> spp. <italic>viz.</italic>, <bold>(A)</bold> <italic>Org-Trichojal</italic> (<italic>T. harzianum</italic>) in Assam and <bold>(B)</bold> <italic>UmTriv</italic> (<italic>T. viride</italic>), <bold>(C)</bold> <italic>UmTricho</italic> (<italic>T. harzianum</italic>), and <italic>Trichoderma</italic>-based consortia, <bold>(D)</bold> <italic>UmComb</italic> and I <bold>(E)</bold> <italic>UmTim</italic> in Meghalaya of NER (Source: <xref ref-type="bibr" rid="B59">Dutta et&#xa0;al., 2020</xref>).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fagro-04-932839-g004.tif"/>
</fig>
<table-wrap id="T4" position="float">
<label>Table&#xa0;4</label>
<caption>
<p>Commercial formulation of <italic>Trichoderma</italic> species.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Commercial products</th>
<th valign="top" align="left">
<italic>Trichoderma</italic> strains</th>
<th valign="top" align="center">Manufactured by</th>
<th valign="top" align="center">Country</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Antagon TV</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Green tech Agro-products</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Anatgon</td>
<td valign="top" align="left">
<italic>Trichoderma</italic> spp.</td>
<td valign="top" align="left">DeCeuster Meststoffen N.V. (DCM)</td>
<td valign="top" align="left">Belgium</td>
</tr>
<tr>
<td valign="top" align="left">Biocon</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Tocklai Experimental Station, Tea Research Association</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Bioguard</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Krishi Rasayan Export Pvt. Ltd.</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Bip T</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left">Poland</td>
</tr>
<tr>
<td valign="top" align="left">Binab T</td>
<td valign="top" align="left">
<italic>T. harzianum, T. polysporum</italic>
</td>
<td valign="top" align="left">BINAB Bio-Innovation AB; Henry Doubleday Research Association</td>
<td valign="top" align="left">Sweden, UK</td>
</tr>
<tr>
<td valign="top" align="left">Bioderma</td>
<td valign="top" align="left">
<italic>T. viride</italic>+ <italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Biotech International Ltd.</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Bio Fit</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Ajay Biotech Ltd.</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Defense SF</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Wockhardt Life Science Ltd.</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Eco fit</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Hoechst Schering Agro Evo Ltd.</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Ecoderma</td>
<td valign="top" align="left">
<italic>T. viride</italic>+ <italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Morgo Biocontrol Pvt. Ltd.</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Funginil</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Crop Health Bioproduct Research Centre, Ghaziabad</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Gliostar</td>
<td valign="top" align="left">
<italic>T. virens</italic>
</td>
<td valign="top" align="left">GBPUAT, Pantnagar</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Monitor</td>
<td valign="top" align="left">
<italic>Trichoderma</italic> spp.</td>
<td valign="top" align="left">Agricultural and Biotech Pvt. Ltd.</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Plant biocontrol agent-1</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">GBPUAT,</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Plant shield</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Bioworks, Inc.</td>
<td valign="top" align="left">USA</td>
</tr>
<tr>
<td valign="top" align="left">PromotPlusWPPromotPlusDD</td>
<td valign="top" align="left">
<italic>T. koningii, T. harzianum</italic>
</td>
<td valign="top" align="left">Tan Quy</td>
<td valign="top" align="left">Vietnam</td>
</tr>
<tr>
<td valign="top" align="left">Trichostar</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Green tech Agro-products</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Trichoguard</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Anu Biotech Int. Ltd.</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">Tricho-X</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">Excel Industries Ltd.</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>Org-Trichojal</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Assam Agricultural University</td>
<td valign="top" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>UmTricho</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" rowspan="4" align="left">CPGS-AS, Central Agricultural University</td>
<td valign="top" rowspan="4" align="left">India</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>UmTriv</italic>
</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>UmTim (Consortia)</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>+ <italic>M. anisopliae s.l.</italic>
</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>UmComb (Consortia)</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum + Beauveria bassiana s.l. + Metarhizium anisopliae s.l. + A. lecanii</italic>
</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
  <p>Information compiled from: <xref ref-type="bibr" rid="B168">Puyam (2016)</xref>; <xref ref-type="bibr" rid="B59">Dutta et&#xa0;al. (2020)</xref>; <xref ref-type="bibr" rid="B57">Dutta (2020)</xref>.
</p>
</fn>
</table-wrap-foot>
</table-wrap>
</sec>
<sec id="s7">
<title>Genetic manipulation</title>
<p>Genetic manipulation of <italic>Trichoderma</italic> species has been achieved by different techniques including protoplast-mediated transformation (PMT), electroporation, biolistic transformation, and <italic>Agrobacterium</italic>-mediated transformation (AMT) leading to alteration of fungal cell by insertion of genetic material into genome. <xref ref-type="bibr" rid="B161">Penttila et&#xa0;al. (1987)</xref> first successfully attempted introduction of DNA in prototrophic strain <italic>T. reesei</italic> along with <italic>arg</italic>B gene as auxotrophic marker and <italic>smd</italic>S as dominant marker from <italic>Aspergillus nidulans</italic> by polyethylene glycol (PEG)/CaCl<sub>2</sub>&#x2013;mediated protoplast transformation technique. Auxotrophic marker genes enable high transformation efficiency, whereas dominant marker genes confer properties <italic>viz.</italic>, antibiotic resistance, nutrition utilization, for example, nitrogen or carbon, allowing transformed cells to thrive as compared with non-transformed cells. Several examples of dominant marker genes include acetamide (acrylamide) as nitrogen source encoded by <italic>amdS</italic> gene of <italic>A. nidulans</italic>, invertase <italic>sucA</italic>gene of <italic>A. niger</italic> using sucrose as carbon source, and pyrithiamine (<italic>ptrA</italic>)&#x2013;resistant gene of <italic>A. oryzae</italic> have been expressed in <italic>T. reesei</italic> (<xref ref-type="bibr" rid="B16">Berges et&#xa0;al., 1993</xref>; <xref ref-type="bibr" rid="B118">Kubodera et&#xa0;al., 2002</xref>). Later, transfer of <italic>Trichoderma</italic> genes in plants was first successfully demonstrated by <xref ref-type="bibr" rid="B131">Lorito et&#xa0;al. (1998)</xref> in tobacco and potato plants expressing 42 kDaendochitinase gene <italic>chit42</italic>, conferred high resistance against <italic>A. alternata</italic>, <italic>A. solani</italic>, <italic>B. cinerea</italic>, and <italic>R. solani.</italic>
</p>
<p>Chitinases genes elevated defense response by involving greater induction of ROS through expression of defense-related genes, PR enzymes, and terpenoid biosynthesis. Numerous studies demonstrated the expression of potential defense genes of <italic>Trichoderma</italic> sp. in plants through genetic transformation techniques have successfully conferred enhanced resistance to phytopathogenic fungi and bacteria (<xref ref-type="table" rid="T5">
<bold>Table&#xa0;5</bold>
</xref>). Recently, marker-free transgenics of <italic>Trichoderma</italic> spp. were also generated <italic>via</italic> marker removal, recycling, and reusing for another transformation, through excision of marker genes mediated by native homologous recombination (HR) machinery or by heterologous site-specific recombinases. Sequential deletions using different cassettes comprising the excision of marker genes <italic>viz.</italic>, direct-repeat-mediated HR for removal of pyr<italic>4</italic> gene (<xref ref-type="bibr" rid="B91">Hartl and Seiboth, 2005</xref>) and site-specific Cre recombinase for removal of <italic>xyn1</italic> promoter (<xref ref-type="bibr" rid="B198">Steiger et&#xa0;al., 2011</xref>) were reported in <italic>T. reesei.</italic> In addition, split-marker systems for successful gene deletions were also used in <italic>T. virens</italic> and <italic>T. atroviride</italic> (<xref ref-type="bibr" rid="B207">Trushina et&#xa0;al., 2013</xref>). Knockout strategies involving RNA interference (RNAi) gene silencing was also used to silence <italic>cel6a</italic> (cellobiohydrolase 2) gene expression in <italic>T. reesei</italic> (<xref ref-type="bibr" rid="B23">Brody and Maiyuram, 2009</xref>).</p>
<table-wrap id="T5" position="float">
<label>Table&#xa0;5</label>
<caption>
<p>Genetic manipulation using <italic>Trichoderma</italic> spp. in different crops conferred disease resistance.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Crop</th>
<th valign="top" align="center">Pathogen</th>
<th valign="top" align="center">
<italic>Trichoderma</italic> species</th>
<th valign="top" align="center">Mechanism and activity</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Onion roots</td>
<td valign="top" align="left">
<italic>Sclerotium cepivorum</italic>
</td>
<td valign="top" align="left">
<italic>T. koningii</italic>
</td>
<td valign="top" align="left">Hyphae penetrated into infected epidermal and cortical tissue of root, destroyed pathogen hyphae <italic>via.</italic>, production of endo- and exo-chitinases</td>
</tr>
<tr>
<td valign="top" align="left">Cotton seedlings</td>
<td valign="top" align="left">
<italic>R. solani</italic>
</td>
<td valign="top" align="left">
<italic>T. virens</italic>
<break/>Gv29-8</td>
<td valign="top" align="left">Over-expression of gene cht42, encoding for chitinase showed enhanced biocontrol activity and reduced cotton seedling disease</td>
</tr>
<tr>
<td valign="top" rowspan="2" align="left">Bean leaves</td>
<td valign="top" rowspan="2" align="left">
<italic>B. cinerea</italic>
</td>
<td valign="top" rowspan="2" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Chitinase activity (ech42) reduced disease symptoms</td>
</tr>
<tr>
<td valign="top" align="left">Proteases inactivate hydrolytic enzymes produced by <italic>B. cinerea</italic>, break down into peptide chains or constituent amino acids, thus destroy their capacity to incite diseases</td>
</tr>
<tr>
<td valign="top" align="left">Tobacco, Potato, Tomato</td>
<td valign="top" align="left">
<italic>Alternaria alternata, A. solani, B. cinerea, R. solani</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum</italic> P1</td>
<td valign="top" align="left">Transfer and expression of 42 kDa gene encoding for endochitinase<italic>chit42</italic> demonstrated high-level, broad-spectrum resistance</td>
</tr>
<tr>
<td valign="top" align="left">Apple</td>
<td valign="top" align="left">
<italic>Venturia inaequalis</italic>
</td>
<td valign="top" align="left">
<italic>T. atroviride</italic> P1</td>
<td valign="top" align="left">Transgenics expressing <italic>chit42</italic> gene encoding both endo- and exo-chitinases showed reduced growth but enhanced resistance</td>
</tr>
<tr>
<td valign="top" align="left">Broccoli</td>
<td valign="top" align="left">
<italic>Alternaria brassicola</italic>
</td>
<td valign="top" align="left">
<italic>Trichoderma</italic> sp.</td>
<td valign="top" align="left">Expression of <italic>chit42</italic> gene increased resistance</td>
</tr>
<tr>
<td valign="top" align="left">Tobacco</td>
<td valign="top" align="left">Fungal and bacterial pathogens</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">Overexpression of two endochitinases (<italic>Chit33</italic> and <italic>Chit42</italic>) conferred broad resistance: synergistic effect</td>
</tr>
<tr>
<td valign="top" rowspan="2" align="left">
<italic>Femminello siracusano</italic> lemon</td>
<td valign="top" align="left">
<italic>Phomatracheiphila</italic>
</td>
<td valign="top" rowspan="2" align="left">
<italic>T. harzianum</italic>(<italic>chit42</italic>)</td>
<td valign="top" align="left">Foliar protein extracts from <italic>chit42</italic> introduced lemon inhibited conidial germination and fungal growth</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>B. cinerea</italic>
</td>
<td valign="top" align="left">Smaller lesion area, enhanced transcript levels of ROS and ISR-related genes</td>
</tr>
<tr>
<td valign="top" align="left">Rice</td>
<td valign="top" align="left">
<italic>Rhizoctonia solani</italic>
</td>
<td valign="top" align="left">
<italic>T. virens</italic>
</td>
<td valign="top" align="left">Expression of <italic>cht42</italic> gene accumulated <italic>cht42</italic> transcript and chitinase activity showed 62.00% reduction in sheath blight disease index</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">
<italic>Meloidogyne incognita</italic>, root knot nematode</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
<break/>T-203</td>
<td valign="top" align="left">Genes encoding protease enzyme drastically reduced root galling and penetrate egg masses</td>
</tr>
<tr>
<td valign="top" align="left">Cucumber</td>
<td valign="top" align="left">
<italic>Pythium ultimum</italic>
</td>
<td valign="top" align="left">
<italic>T. longibrachiatum</italic>CECT2606</td>
<td valign="top" align="left">Transformants with over-expression of gene encoding &#x3b2;-1,4-endoglucanase effective in biocontrol</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>Information compiled from: <xref ref-type="bibr" rid="B95">Howell (2003)</xref>, <xref ref-type="bibr" rid="B183">Schuster and Schmoll (2010)</xref>, <xref ref-type="bibr" rid="B150">Olmedo-Monfil and Casas-Flores (2014)</xref>, <xref ref-type="bibr" rid="B42">Contreras-Cornejo et&#xa0;al. (2016)</xref>.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</sec>
<sec id="s8">
<title>Defense mechanism and their exploitation</title>
<p>The <italic>Trichoderma</italic> species, most commonly <italic>T. atroviride</italic>, <italic>T. harzianum</italic>, <italic>T. virens</italic>, <italic>T. hamatum</italic>, <italic>T. asperellum</italic>, and so forth, are progressively used as efficient microbial biocontrol agents due to their ability to activate local or systemic resistance in plants (<xref ref-type="table" rid="T6">
<bold>Table&#xa0;6</bold>
</xref>). The concept of induced defense responses in plants by <italic>Trichoderma</italic> inoculation was first supported by the work of Yedidia et&#xa0;al. (<xref ref-type="bibr" rid="B236">1999</xref>), inoculated roots of 7-day-old cucumber seedlings with <italic>T. harzianum</italic> T-203 at 10<sup>5</sup> spores/ml. Roots and leaves of treated cucumber seedlings demonstrated initiation of plant defense, exerted increase in peroxidase activity, increase in chitinase, and deposition of callose-enriched appositions in inner surface of callose walls. Different strategies utilized by <italic>Trichoderma</italic> such as production of lytic enzymes, ABC transporter membrane pumps, diffusible or volatile and SMs compromising enzymatic and chemical weapons utilized by plant pathogens, make it efficient mycoparasite and antagonist. The defense mechanism of <italic>Trichoderma</italic> are triggered by regulatory mechanisms utilizing signal transduction pathways including heterotrimeric G-protein signaling, mitogen-activated protein kinase (MAPK) cascades, and cAMP pathway (<xref ref-type="bibr" rid="B239">Zeilinger and Omann, 2007</xref>).</p>
<table-wrap id="T6" position="float">
<label>Table&#xa0;6</label>
<caption>
<p>Defense mechanism induced by <italic>Trichoderma</italic> spp. in various crops against different pathogens.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Crop</th>
<th valign="top" align="center">
<italic>Trichoderma</italic> sp.</th>
<th valign="top" align="center">Pathogens</th>
<th valign="top" align="center">Defense activities</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Beans</td>
<td valign="top" align="left">
<italic>T. atroviride</italic>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left">Early defense response, secondary metabolites induced intracellular Ca<sup>2+</sup> variations</td>
</tr>
<tr>
<td valign="top" align="left">Cucumber</td>
<td valign="top" align="left">
<italic>T. asperellum</italic>T203</td>
<td valign="top" align="left">
<italic>Pseudomonas syringae</italic> pv. <italic>lachrymans</italic>
</td>
<td valign="top" align="left">Activated MAPK, expression of <italic>LOX1</italic> (Lipoxygenase 1), <italic>JA</italic> (Jasmonic acid), <italic>PAL1</italic> (Phenylalanine ammonia lyase), <italic>SA</italic> (Salicyclic acid), <italic>ETR1</italic> (Ethylene receptor 1), <italic>CTR1</italic> (Constitutive triple Response 1), <italic>ET</italic> (Ethylene),</td>
</tr>
<tr>
<td valign="top" align="left">Cotton</td>
<td valign="top" align="left">
<italic>T. asperellum</italic>T203</td>
<td valign="top" align="left">
<italic>Pseudomonas syringae</italic> pv. <italic>lachrymans</italic>
</td>
<td valign="top" align="left">PAL, hydroperoxide lyase (HPL), production of phytoalexins (phenolic secondary metabolites), terpenoids, increased peroxidase and chitinase activity</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">
<italic>T. harzianum</italic> strain</td>
<td valign="top" align="left">
<italic>Alternaria solani</italic>
</td>
<td valign="top" align="left">Local and systemic resistance; rhizosphere competent</td>
</tr>
<tr>
<td valign="top" align="left">Melon</td>
<td valign="top" align="left">
<italic>T. harzianum, T. longibrachiatum</italic>
</td>
<td valign="top" align="left">
<italic>Fusarium oxysporum</italic>
</td>
<td valign="top" align="left">SA and JA signaling pathway, cellulose activated ET and SA pathway, induced peroxidase and chitinase activities</td>
</tr>
<tr>
<td valign="top" align="left">Cotton, rice, <italic>Arabidopsis thaliana</italic>
</td>
<td valign="top" align="left">
<italic>Trichoderma</italic> sp.</td>
<td valign="top" align="left"/>
<td valign="top" align="left">
<italic>Trichoderma-</italic>mediated immunity- reactive oxygen species (ROS), nitric oxide,</td>
</tr>
<tr>
<td valign="top" align="left">Cotton</td>
<td valign="top" align="left">
<italic>T. virens</italic> (G-6, G-11, G6-5)</td>
<td valign="top" align="left">
<italic>R. solani</italic>
</td>
<td valign="top" align="left">Induced terpenoid synthesis <italic>viz.</italic> desoxyhemigossypol (dHG), hemigossypol (HG), gossypol (G)</td>
</tr>
</tbody>
</table>
</table-wrap>
<p>Attempts made by <xref ref-type="bibr" rid="B172">Reithner et&#xa0;al. (2005)</xref> identified heterotrimeric G-protein signaling genes, that is, <italic>TGA</italic> of <italic>T. virens</italic>, <italic>GNA3</italic> of <italic>T. reesei</italic>, and <italic>TGA1</italic> and <italic>TGA3</italic> of <italic>T. atroviride</italic> belonging to classes I and III of adenylate cyclase inhibiting G-alpha subunits, played an important role in the regulation of antifungal metabolites and coiling around host hyphae. MAP-kinase TVK1 characterized in <italic>T. asperellum</italic>, <italic>T. atroviride</italic>, and <italic>T. virens</italic> mediated the transfer of information from sensors, regulate signaling mechanisms, cellular responses in plant roots, and increased biocontrol effectively against <italic>R. solani</italic> (<xref ref-type="bibr" rid="B141">Mendoza-Mendoza et&#xa0;al., 2003</xref>). The perception of signals transmitted by <italic>Trichoderma</italic> in plants facilitated root colonization by swollenin and enhanced systemic resistance by ceratoplatanin family proteins, MAPK functions, indirectly leading to enhanced root proliferation, better growth and protection of plants. In a study, in model plant <italic>A. thaliana</italic>, root inoculation with <italic>T. virens</italic> and <italic>T. atroviride</italic> reported to increase the level of phytoalexin camalexin along with induction of PR-1a and <italic>LOX2</italic> SA-responsive gene expression (<xref ref-type="bibr" rid="B41">Contreras-Cornejo et&#xa0;al., 2011</xref>; Contreras-Cornejo et&#xa0;al., 2016). Similarly, in another study, root inoculation of <italic>A. thaliana</italic> with <italic>T. asperelloides</italic>T203 triggered rapid increase in the expression of transcription factors, that is, <italic>WRKY18</italic>, <italic>WRKY40</italic>, <italic>WRKy60</italic>, and <italic>WRKY33</italic> exerted positive role in JA-mediated defense (<xref ref-type="bibr" rid="B25">Brotman et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B1">Abbas et&#xa0;al., 2022</xref>).</p>
</sec>
<sec id="s9">
<title>Field and industrial applications</title>
<p>The pioneering work on <italic>Trichoderma</italic> species on their field application for disease management was initiated during 1970s, which reported success of several <italic>Trichoderma</italic> species <italic>viz</italic>., <italic>T. harzianum</italic>, <italic>T. hamatum</italic>, and <italic>T. viride</italic> against <italic>Pythium</italic> spp., <italic>F. oxysporum</italic>, <italic>R. solani</italic>, and <italic>Sclerotium rolfsii</italic> (<xref ref-type="bibr" rid="B176">Roy, 1977</xref>). Since then, many researchers from the region have worked on improving the efficacy of <italic>Trichoderma</italic> as potential antagonists against many soilborne and foliar plant pathogens and protectors of plants, as shown in <xref ref-type="table" rid="T7">
<bold>Table&#xa0;7</bold>
</xref>.</p>
<table-wrap id="T7" position="float">
<label>Table&#xa0;7</label>
<caption>
<p>Application of <italic>Trichoderma</italic> species as fungal biocontrol agents against various crop diseases.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="left">Crop</th>
<th valign="top" align="center">Disease</th>
<th valign="top" align="left">
<italic>Trichoderma</italic> spp.</th>
<th valign="top" align="center">References</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Knol-khol</td>
<td valign="top" align="left">
<italic>Sclerotium w</italic>ilt and rot</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B191">Singh et&#xa0;al. (1988)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Soybean</td>
<td valign="top" align="left">Stem rot (<italic>R. solani</italic>)</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B62">Dutta and Das</xref> (<xref ref-type="bibr" rid="B60">1999a</xref>; <xref ref-type="bibr" rid="B61">1999b</xref>), <xref ref-type="bibr" rid="B64">Dutta et&#xa0;al. (2000)</xref>; <xref ref-type="bibr" rid="B45">Das et&#xa0;al. (2006)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Rice</td>
<td valign="top" align="left">Sheath blight (<italic>R. solani</italic>)</td>
<td valign="top" align="left">
<italic>Trichoderma</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B47">Das et&#xa0;al. (1997)</xref>; <xref ref-type="bibr" rid="B46">Das and Hazarika (2000)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">Collar rot (<italic>Sclerotium rolfsii</italic>)</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B62">Dutta and Das (2002)</xref>
</td>
</tr>
<tr>
<td valign="top" rowspan="2" align="left">Potato</td>
<td valign="top" align="left">Black scurf (<italic>R. solani</italic>), Bacterial brown rot (<italic>Fusarium, Phoma</italic> spp.)</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B85">Gogoi et&#xa0;al. (2007)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">
<italic>S. sclerotiorum</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B139">Mech (2004)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">French bean</td>
<td valign="top" align="left">White mold<break/>(<italic>S. sclerotiorum</italic>); Root knot nematode</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B67">Dutta et&#xa0;al. (2008)</xref>; <xref ref-type="bibr" rid="B59">Dutta et&#xa0;al. (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Beans</td>
<td valign="top" align="left">Damping-off (<italic>Pythium aphanidermatum</italic>)</td>
<td valign="top" align="left">
<italic>Trichoderma</italic> spp. (T-105)</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B104">Kamala and Indira (2011)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Beans</td>
<td valign="top" align="left">Damping-off, Wilting<break/>(<italic>R. solani, Fusarium</italic> spp.)</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B103">Kamala and Devi (2012)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Ginger</td>
<td valign="top" align="left">Rhizome rot <italic>(F. oxysporum</italic> f.sp. <italic>zingiberi</italic>)</td>
<td valign="top" align="left">
<italic>T. viride, T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B109">Khatso and Tiameren Ao(2013)</xref></td>
</tr>
<tr>
<td valign="top" align="left">
<italic>Etlingera linguiformis</italic>
</td>
<td valign="top" align="left">Leaf blight (<italic>Curvularia lunata</italic>var. <italic>aeriai)</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B111">Kithan and Daiho (2014)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tea gardens</td>
<td valign="top" align="left">
<italic>Pestalotia theae, Fusarium solani</italic>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B147">Naglot et&#xa0;al. (2015)</xref>
</td>
</tr>
<tr>
<td valign="top" rowspan="3" align="left">Tea</td>
<td valign="top" align="left">Red rust, Poria (<italic>Poria hypobrunea</italic>)</td>
<td valign="top" align="left">
<italic>T. harzianum. T. asperellum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B69">Dutta et&#xa0;al. (2016)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Black rot (<italic>Corticumtheae</italic>)</td>
<td valign="top" align="left">
<italic>T. atroviride, T. citrin</italic> (Aerospore)</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B205">Thoudam and Dutta (2012)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Die back</td>
<td valign="top" align="left">
<italic>T. harzianum, T. viride</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B69">Dutta et&#xa0;al. (2016)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Turmeric</td>
<td valign="top" align="left">Leaf spot (<italic>Colletotrichum capsici</italic>)</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B106">Kangjam et&#xa0;al. (2017)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Carrot</td>
<td valign="top" align="left">
<italic>Sclerotinia</italic> Rot (<italic>S. sclerotiorum</italic>)</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>+ chitosan (1%), zinc (0.25%), boron (0.5%)</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B22">Bora (2017)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">Wilt (<italic>F. oxysporum</italic> f.sp. <italic>lycopersici)</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B237">Zehera et&#xa0;al. 2017a</xref>; <xref ref-type="bibr" rid="B238">2017b</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Lettuce</td>
<td valign="top" align="left">
<italic>R. solanacearum, F. oxysporum</italic> f. sp. <italic>lactucae</italic>
</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B108">Khan et&#xa0;al. (2018)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Cowpea</td>
<td valign="top" align="left">Powdery mildew (<italic>Erysiphe flexuosa</italic>)</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B152">Omomowo et&#xa0;al., 2018</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Ghost pepper</td>
<td valign="top" align="left">Root rot <italic>(R. solani)</italic>
</td>
<td valign="top" align="left">
<italic>Trichoderma</italic> spp.</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B113">Koijam and Sinha (2018)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">Damping off (<italic>Pythium</italic> spp., <italic>R. solani)</italic>
</td>
<td valign="top" align="left">
<italic>Trichoderma</italic> spp. (T55, TR122, TR66, TR136)</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B17">Biam and Majumder (2019)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Banana</td>
<td valign="top" align="left">Fusarium wilt (<italic>F. oxysporum</italic>s.sp. <italic>cubense</italic>)</td>
<td valign="top" align="left">
<italic>T. reesei</italic> (RMF-13, 25), <italic>T. harzianum</italic> (RMF- 28)</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B124">Lalngaihawmi and Bhattacharya (2019)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">
<italic>Fusarium solani</italic>
</td>
<td valign="top" align="left">
<italic>T. hamatum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B107">Kareem and Matloob (2019)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Ground nut</td>
<td valign="top" align="left">
<italic>Colletotrichum</italic> spp</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B65">Dutta et&#xa0;al. (2021)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">Wilt (<italic>F. oxysporum</italic> f.sp. <italic>lycopersici)</italic>
</td>
<td valign="top" align="left">
<italic>T. atroviride</italic> and <italic>T. longibrachiatum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B179">Sallam et&#xa0;al. (2019)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">Pythium damping off (<italic>Pythium aphanidermatum)</italic>
</td>
<td valign="top" align="left">T. <italic>harzianum</italic> (Th), +<break/>T. <italic>asperellum</italic> (Ta), +<break/>T. <italic>virens</italic> (Tvs1), +<break/>T. <italic>virens</italic> (Tvs2) +<break/>T. <italic>virens</italic> (Tvs3)</td>
<td valign="top" align="left">(<xref ref-type="bibr" rid="B72">Elshahawy and Mohamedy2019</xref>)</td>
</tr>
<tr>
<td valign="top" align="left">Ivy gourd</td>
<td valign="top" align="left">Root knot nematode (<italic>Meloidogyne incognita</italic>)</td>
<td valign="top" align="left">
<italic>T. asperellum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B197">Sonowal et&#xa0;al. (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">Wilt (<italic>F. oxysporum</italic> f.sp. <italic>lycopersici)</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B55">Dubey et&#xa0;al. (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Common bean</td>
<td valign="top" align="left">Root rot (<italic>M. Phaseolina, R. solani</italic>)</td>
<td valign="top" align="left">
<italic>T. atroviride</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B71">El-Benawy et&#xa0;al. (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Cucumber</td>
<td valign="top" align="left">
<italic>Powdery mildew (Podosphaera xanthii)</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>, <italic>T. viride</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B181">Sarhan et al. (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Soybean</td>
<td valign="top" align="left">Anthracnose (<italic>Colletotrichum truncatum)</italic>
</td>
<td valign="top" align="left">
<italic>T. koningiopsis</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B189">Silva et&#xa0;al. (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Mungbean</td>
<td valign="top" align="left">Dry root rot (<italic>M. phaseolina</italic>)</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B202">Swehla et&#xa0;al. (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">Rhizoctonia wilt (<italic>R. solani</italic>)</td>
<td valign="top" align="left">
<italic>T. viride</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B3">Aboelmagd (2021)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">Wilt (<italic>F. oxysporum</italic> f.sp. <italic>lycopersici)</italic>
</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
<break/>
<italic>T. viride</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B101">Jamil (2021)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Chickpea</td>
<td valign="top" align="left">Ascochyta blight (<italic>Ascochyta rabiei)</italic>
</td>
<td valign="top" align="left">
<italic>T. hamatum</italic> and <italic>T. koningii</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B166">Poveda (2021)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Mungbean</td>
<td valign="top" align="left">Dry root rot (<italic>Macrophomina phaseolina</italic>)</td>
<td valign="top" align="left">
<italic>T. harzianum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B202">Swehla et al. (2020)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">Pythium damping off (<italic>P. aphanidermatum</italic>)</td>
<td valign="top" align="left">
<italic>T. asperellum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B123">Kumhar et&#xa0;al. (2022)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Potato</td>
<td valign="top" align="left">Early blight (<italic>Alternaria solani</italic>)</td>
<td valign="top" align="left">
<italic>Trichoderma</italic> spp.</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B143">Metz and Hausladen (2022)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Onion</td>
<td valign="top" align="left">Purple blotch (<italic>Alternaria porri</italic>)</td>
<td valign="top" align="left">
<italic>T. asperellum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B30">Camacho-Luna et&#xa0;al. (2021)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Banana</td>
<td valign="top" align="left">Anthracnose (<italic>Colletotrichum musae</italic>
<bold>)</bold>
</td>
<td valign="top" align="left">
<italic>T. piluliferum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B44">Da Costa et&#xa0;al. (2021)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Tomato</td>
<td valign="top" align="left">Early blight (<italic>Alternaria solani</italic>)</td>
<td valign="top" align="left">
<italic>T. asperellum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B7">Ajiboye and Sobowale (2022)</xref>
</td>
</tr>
<tr>
<td valign="top" align="left">Lettuce</td>
<td valign="top" align="left">Cercospora leaf spot (<italic>C. lactucae</italic>-<italic>sativae</italic>)</td>
<td valign="top" align="left">
<italic>T. asperellum</italic>
</td>
<td valign="top" align="left">
<xref ref-type="bibr" rid="B167">Promwee and Intana (2022)</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
<p>In 1976, the discovery of cellulase production efficiency of <italic>T. reesei</italic> QM6a by U.S. army during World War II (<xref ref-type="bibr" rid="B169">Reese, 1976</xref>) focused extensive research toward industrial application of enzymes, SMs, antibiotics and protein produced by <italic>Trichoderma</italic> spp. <italic>T. reesei</italic>, being potent cellulase producer were focused for improvement of enzyme cocktail efficiency resulting in the production of biofuel, that is, bioethanol from cellulosic waste material. Achievement of high level of cellulase and hemicellulase production on cellulose, xylan, plant polymers or lactose and high protein secretion capacity up to 100 g/L for 60.00% major cellulase Cel7a (CBHI) and 20.00% Cel6a (CBHII) attributed to agricultural or paper and pulp industry by-products (<xref ref-type="bibr" rid="B27">Buchert et&#xa0;al., 1998</xref>). Earlier evidences showed that the expression of heterologous protein by <italic>T. reesei</italic> was exploited for the production of calf chymosin followed by expression of immunologically active antibody fragments for production of several enzymes and proteins (<xref ref-type="bibr" rid="B160">Pentilla, 1998</xref>). Safe-scale industrial enzymes produced by <italic>Trichoderma</italic> species are used for brewing processes (&#x3b2;-glucanases), macerating enzymes in fruit juice production (hemicellulases, cellulases, and pectinases), feed additive for livestock farming (xylanases), baking, malting, grain alcohol production (cellulases), and food preservatives (<xref ref-type="bibr" rid="B80">Galante et&#xa0;al., 1998b</xref>).</p>
<p>In a study by <xref ref-type="bibr" rid="B223">Waiter et&#xa0;al. (2005)</xref>, they reported that mutanase enzyme produced by <italic>T. harzianum</italic> can also be used in toothpaste for preventing accumulation of mutan in dental plaque. In wine industry, crude blend preparations of glycosidases and CWDEs produced by <italic>T. reesei</italic> are exploited in wine-making process for improving juice yield, flavor, clarification, filterability, facilitate liberation, and solubilization of phenolic compounds from seeds, skin, and flesh of grapes (<xref ref-type="bibr" rid="B216">Villanueva et&#xa0;al., 2000</xref>). Earlier, <xref ref-type="bibr" rid="B162">Perez-Gonzalez et&#xa0;al. (1993)</xref> also explored beneficial application of endo-&#x3b2;-1,4-glucanases and xylanases genes from <italic>T. longibrachiatum</italic> and <italic>T. reesei</italic> in wine making by developing recombinant yeast strains for improving free flow, different colors, intensity, stability while ageing, sensorial, and tasting capabilities in Pinot Noir and Ruby Cabernet. In addition, chemical such as 2,4,6-trichloroanisole released by <italic>T. longibrachiatum</italic> and <italic>T. viride</italic> have been involved in cork taint and musty-off odors. In addition, the application of <italic>Trichoderma</italic> sp. in beer industry attributed to exploitation of cellulolytic enzymes and recombinant yeast (<italic>Saccharomyces cerevisiae</italic>) constructed from <italic>egl</italic>1 gene from <italic>T. reesei</italic> for glucan hydrolysis, reduction of &#x3b2;-glucan content, enhanced filterability and beer flavor (<xref ref-type="bibr" rid="B76">Faulds et&#xa0;al., 2008</xref>).</p>
</sec>
<sec id="s10">
<title>Challenges and solutions</title>
<p>
<italic>Trichoderma</italic> species are effective biocontrol agents that can replace chemicals in agriculture. It is essential that microbial biocontrol agents succeed or fail as commercial products (<xref ref-type="bibr" rid="B221">Vurukonda et&#xa0;al., 2018</xref>). In order to be successful as a commercial product, it should fulfill farmer&#x2019;s needs such as repeated positive results, realistic prices, easy usage, and long shelf life (<xref ref-type="bibr" rid="B146">Murphy et&#xa0;al., 2018</xref>). Nevertheless, a bioproduct with microbial biocontrol agents and/or SMs has the specific problem that its viability decreases during storage as well as its effectiveness for controlling pathogens and pests (<xref ref-type="bibr" rid="B221">Vurukonda et&#xa0;al., 2018</xref>). Lack of understanding of biocontrol techniques can result in a reduction in application and requirement of the product. Thus, understanding the practical deployment of <italic>Trichoderma</italic> as microbial biocontrol agents for disease management in agriculture is crucial.</p>
<p>Despite this, it is urgent that communication between researchers and the farmers be improved for efficient biocontrol methods. Therefore, it is crucial to ensure that farmers are aware of the correct use of products for a specific pathogen (<xref ref-type="bibr" rid="B63">Dutta and Das, 2009</xref>). There have been many studies investigating <italic>Trichoderma</italic> as efficient microbial biocontrol agents. Most of these research investigations, however, were conducted in lab environments, and their applicability was evaluated in the field. Alternatively, some <italic>Trichoderma</italic> species may be friendly with particular host plants in a narrow range of environmental conditions. The biological efficacy of <italic>Trichoderma</italic> can be affected by changes in agricultural conditions, including soil OM, pH, nutrients, and moisture content (<xref ref-type="bibr" rid="B146">Murphy et&#xa0;al., 2018</xref>). An in-depth analysis of field trials will help to develop strains of <italic>Trichoderma</italic> that are friendly with the crops and environment, as most isolates of <italic>Trichoderma</italic> are unique to their hosts and environments. Therefore, it is best to identify the field-related problems, follow up on continuous <italic>in vivo</italic> and <italic>in vitro</italic> laboratory experiments, and find a solution for that particular problem related to <italic>Trichoderma</italic> antagonists against plant pathogens and diseases. It is anticipated that these products will be in higher demand in the future (<xref ref-type="bibr" rid="B221">Vurukonda et&#xa0;al., 2018</xref>).</p>
</sec>
<sec id="s11">
<title>Conclusions and future</title>
<p>In terms of managing plant diseases, <italic>Trichoderma</italic> species could be a viable alternative to synthetic fungicides. <italic>Trichoderma</italic> species is already widely used against plant diseases as a microbial biocontrol agent. To develop successful commercial products of <italic>Trichoderma</italic>, <italic>in vitro</italic> tests under standardized conditions are routinely conducted to screen potential isolates of the fungus. However, field trials under different environmental conditions must also be conducted. Ecological and physical parameters of microbial biocontrol agents along with their environmental effects should be investigated in field experiments. For the commercialization of <italic>Trichoderma</italic> and their use by farmers in remote areas who do not know about them, further research is vital, as this would significantly reduce economic and environmental costs. We may be able to achieve this by using novel molecular technologies such as metagenomics and statistical advances, as well as environmental dynamics. Future work could integrate screening with antagonistic ability validation in greenhouse and field trials, as well as the production of biomass after the commercialization of <italic>Trichoderma</italic> species required to protect global food security. The following are an outline of the broad future outlook.</p>
<list list-type="bullet">
<list-item>
<p>Phylogenetic diversity of the genus <italic>Trichoderma</italic> needs to be explored by understanding sexual development; the genetic basis of chlamydospore production and the identification of niche-related genes through combined expression analysis and functional genomics can provide a blue print of <italic>Trichoderma</italic> species.</p>
</list-item>
<list-item>
<p>As an opportunistic mycoparasite, investigation on induction and regulation of enzyme expression responsible for improvement of biocontrol abilities and development on potential commercial bio-fungicides need to be focused.</p>
</list-item>
<list-item>
<p>Applications of high-throughput screening of peptaibols produced by <italic>Trichoderma</italic> provide extended scope of research in bio-medical applications beyond agriculture.</p>
</list-item>
<list-item>
<p>Effort should also be made to identify plant receptors for <italic>Trichoderma</italic> elicitors and effectors triggering defense mechanisms in order to reprogramme host&#x2019;s genetic machinery for understanding interaction of avirulent plant symbionts and host defense.</p>
</list-item>
<list-item>
<p>Extensive studies regarding identification of diverse physiological traits to upgrade industrial application of <italic>Trichoderma</italic> for production of antibiotics, enzymes and biofuels as an alternative strategy.</p>
</list-item>
</list>
</sec>
<sec id="s12" sec-type="author-contributions">
<title>Author contributions</title>
<p>PD: Original Draft Preparation review and edit, LD: review and edit, AP: Wrote existing crop management strategies, volatile and not volatile metabolites, challenges and future prospects, review and edit. All authors contributed to the article and approved the submitted version.</p>
</sec>
<sec id="s13" sec-type="funding-information">
<title>Funding</title>
<p>Authors are thankful to Department of Biotechnology, Government of India for providing grant through the sanction no.  BT/KIS/123/SP45224/2022 and BT/NER/143/SP42744/2021.</p>
</sec>
<sec id="s14" sec-type="COI-statement">
<title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
<sec id="s15" sec-type="disclaimer">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
</sec>
</body>
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