Next Article in Journal
Study of Androgenic Plant Families of Alloplasmic Introgression Lines (H. vulgare) –T. aestivum and the Use of Sister DH Lines in Breeding
Next Article in Special Issue
Essential Oil Enriched with Oxygenated Constituents from Invasive Plant Argemone ochroleuca Exhibited Potent Phytotoxic Effects
Previous Article in Journal
More than Scales: Evidence for the Production and Exudation of Mucilage by the Peltate Trichomes of Tillandsia cyanea (Bromeliaceae: Tillandsioideae)
Previous Article in Special Issue
Evaluation of Allelopathic Activity of Chinese Medicinal Plants and Identification of Shikimic Acid as an Allelochemical from Illicium verum Hook. f.
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

Trichoderma: The “Secrets” of a Multitalented Biocontrol Agent

School of Bioengineering and Biosciences, Lovely Professional University, Jalandhar-Delhi G.T. Road (NH-1), Phagwara, Punjab 144411, India
School of Agriculture, Lovely Professional University, Delhi-Jalandhar Highway, Phagwara, Punjab 144411, India
Department of Agronomy, Faculty of Agriculture, Mansoura University, Mansoura 35516, Egypt
State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou 311300, China
Department of Agriculture, University of Pisa, I-56124 Pisa, Italy
CIRSEC, Centre for Climatic Change Impact, University of Pisa, Via del Borghetto 80, I-56124 Pisa, Italy
Dipartimento AGRARIA, Università Mediterranea di Reggio Calabria, Località Feo di Vito, SNC I-89124 Reggio Calabria, Italy
Authors to whom correspondence should be addressed.
Authors contributed equal.
Plants 2020, 9(6), 762;
Submission received: 25 May 2020 / Revised: 13 June 2020 / Accepted: 16 June 2020 / Published: 18 June 2020


The plant-Trichoderma-pathogen triangle is a complicated web of numerous processes. Trichoderma spp. are avirulent opportunistic plant symbionts. In addition to being successful plant symbiotic organisms, Trichoderma spp. also behave as a low cost, effective and ecofriendly biocontrol agent. They can set themselves up in various patho-systems, have minimal impact on the soil equilibrium and do not impair useful organisms that contribute to the control of pathogens. This symbiotic association in plants leads to the acquisition of plant resistance to pathogens, improves developmental processes and yields and promotes absorption of nutrient and fertilizer use efficiency. Among other biocontrol mechanisms, antibiosis, competition and mycoparasitism are among the main features through which microorganisms, including Thrichoderma, react to the presence of other competitive pathogenic organisms, thereby preventing or obstructing their development. Stimulation of every process involves the biosynthesis of targeted metabolites like plant growth regulators, enzymes, siderophores, antibiotics, etc. This review summarizes the biological control activity exerted by Trichoderma spp. and sheds light on the recent progress in pinpointing the ecological significance of Trichoderma at the biochemical and molecular level in the rhizosphere as well as the benefits of symbiosis to the plant host in terms of physiological and biochemical mechanisms. From an applicative point of view, the evidence provided herein strongly supports the possibility to use Trichoderma as a safe, ecofriendly and effective biocontrol agent for different crop species.

1. Introduction

It is predicted that by 2050, the world’s overall population will reach 9.1 billion people approximately. Therefore, to feed this increasing world population, a raise of about 70% in agricultural food production is necessary [1]. The substantial increase in food grain production helped in meeting the world food security needs, but problems like global warming, environmental pollution and population explosion has pushed plants towards various kinds of biotic and abiotic stresses which are responsible for yield loss to a large extent and it is an issue of great concern for the wellbeing of our future generations. Biotic stress factors involve fungi, bacteria, virus, nematodes weeds, and insects, which cause a yield loss up to 31–42% [2]. Among them, fungal pathogens are the most severe limiting factor for crop production worldwide. Greater than 10,000 spp. of fungi are considered as responsible for a plethora of plant diseases. Consequently, chemical fungicides are still employed injudiciously as a primary means of disease control. These chemicals are not only expensive, but their application results in the build-up of harmful level of toxins in human beings and in our ecosystem [3,4].
Moreover, the indiscriminate use of fungicides compels the pathogens to undergo genetic mutations which are eventually ascribed to the selection of fungicide resistant biotypes. For instance, Venturia inequalis [5], Phytophthora infestans [6], Colletotrichum musae [7] and Colletotrichum gloeosporioides, Diplodia natalensis, Phomopsis citri [8,9] turn resistant to dodine, metalaxyl, benomyl and benzimidazole, respectively. Recently, agronomist and commercial sectors have shown keen interest towards the development of ecofriendly and cost-effective strategies for plant disease management [10].
Biological control mechanisms are contemplated as significant measures for disease management because chemical fungicides adversely affect other non-target organisms [11]. There are several bodies of evidence which support the fact that some microorganisms cause growth inhibition of pathogenic spp. by impairing their metabolisms and/or establishing a parasitic relationship [10]. Additionally, the application of biological control agents (BCAs) with reduced concentrations of chemicals stimulates disease suppression in a similar manner to high doses of chemical fungicide treatments [12]. Around 90% of fungal biocontrol agents against pathogenic microorganisms belong to different strains of Trichoderma [13]. Trichoderma was isolated for the first time in 1794 from soil and decomposing organic matter [14]. Throughout the world, currently greater than 60% efficacious bio-fungicides are obtained from Trichoderma [15]. For example, in India approximately 250 Trichoderma-derived bio fungicides products are employed, but in comparison to biological control, Indian farmers are still relying on synthetic chemical fungicides to a greater extent [16].
Different strains of Trichoderma (telomorph Hypocrea) belong to fungi imperfecti as they do not possess any known sexual stage in their life cycle [17]. These fungi are rapid colonizers, invasive, filamentous, opportunistic, avirulent and exhibit a symbiotic relationship with plants. In pathogen-contaminated soils they not only improve plant growth but also inhibit pathogen growth through several antagonistic mechanisms [18,19,20]. Trichoderma exhibit antagonistic behavior against several phytopathogenic organisms, including bacteria, nematodes and especially fungi, by inhibiting their growth either by direct interactions (e.g., hyperparasitism, competition for nutrient and space, and antibiosis) [21] or indirectly by improving plant growth and vigor and enhancing stress tolerance, active uptake of nutrients and bioremediation of contaminated rhizosphere, as well as providing plants several secondary metabolites, enzymes and PR proteins [22].

2. Trichoderma-Plants Interactions

In recent years, Trichoderma has acquired high importance because of its fungicidal and fertilizing potential. In exchange for sucrose from plants, fungi exert numerous advantageous influences on plants. Among them should be mentioned the induction of rapid plant development and production, an increase in nutrient absorption, rhizosphere modification and tolerance improvement to both biotic and abiotic stresses (Figure 1) [13,20,23]. Trichoderma is attracted by chemical signals released by a plant’s root. The initial steps of symbiosis establishment involve attachment and penetration and colonization of Trichoderma within the plant roots. Plant root anchoring is facilitated by cysteine-rich proteins known as hydrophobin, e.g., TasHyd1 and Qid74 hydrophobins were obtained from T. asperellum and T. harzianum, respectively [24,25]. After successful attachment, root invasion is promoted by emission of expansin-like proteins. They exhibit cellulose binding modules as well as express endopolygalacturonase activity [26,27]. Furthermore, successful penetration of Trichoderma is followed by a rapid colonization of root tissues, which is achieved by lowering plant defenses, such as phytoalexin production, as previously observed in Lotus japonicus roots during T. koningii penetrations [28]. Moreover, in pathogen contaminated soil, Trichoderma spp. cooperate with other beneficial microbial populations, improving plant growth and survival [29,30].

2.1. Impacts on Plant Morphology

A lot of evidence indicates that the application of Trichoderma spp. to plant rhizosphere promotes plant morphological traits such as root-shoot length, biomass, height, number of leaves, tillers, branches, fruits, etc. [31,32]. For instance, inoculation of soil with T. atrovirde enhanced root hair numbers as well as lateral roots in A. thaliana [33]. Similarly, application of T. harzianum to cucumber roots increased biomass [34] and lateral root formation [35]. Likewise, application of T. longipile and T. tomentosum significantly enhanced the total leaf area as well as fresh weight in cabbage seedlings as compared to untreated plants grown in a greenhouse [36].

2.2. Impacts on Plant Physiology

It has been proven that Trichoderma spp. positively regulates several physiological processes in plants such as photosynthesis, stomatal conductance, gas exchange, nutrient absorption and assimilation, water use efficiency, etc. As previously described, Trichoderma spp. improved both root growth and the uptake of mineral nutrients from soil. Trchoderma spp. treatment significantly improved Mg uptake, a key chlorophyll constituent also involved in catalyzing enzymatic activity as well as in regulating genes engaged in photosynthesis. Moreover, in rice plants treated with Trichoderma, the photosynthetic rate (three-folds), stomatal conductance (three-folds) and water use efficiency (two-folds) were significantly stimulated in comparison to plants treated with the classical NPK (Nitrogen, Phosphorus and Potassium) fertilization [37]. In addition, treatment of rice plants with T. harzianum increased water holding capacity, enhanced drought stress resistance and delayed plant senescence phenomenon [38]. A similar senescence delay was observed in rice after application of Trichoderma spp. [39].

2.3. Impacts on Nutrient Solubilization and Absorption

Roots of Trichoderma-treated plants have exhibited a higher ability to explore the soil and an improved uptake of minerals. According to Harman et al. [40] different strains of Trichoderma emit several acids such as coumaric, glucuronic and citric acids, which assist in the discharge of phosphorus ions, which seem to be inaccessible to plants in most soils [41]. The presence of T. harzianum strain 1295-22 in soil increases the availability of P as well as Fe and Zn in liquid medium [42]. Similarly, application of strain T-203, also known as T. asperelloides, enhanced the available amount of Fe and P in the rhizosphere to an amount of 30% and 90%, respectively. Moreover, root and shoot growth, in response to Trichoderma inoculation, leads to an increase of Cu, Na and Zn uptake as well as other micronutrients [43]. Iron deficiency in alkaline soil is a major drawback for crop production in agriculture. The potential ability of Trichoderma for siderophore production can be used to cope with this problem. It has been reported that the application of T. asperellum (T-6) to cucumber roots increased Fe2+ and siderophore content in soil as well as the activity of Fe2+ and Fe3+ chelate reductase [40]. Furthermore, [44] Colla et al. [44] reported that two kinds of siderophores (hydroxamate and catechol) were produced by the MUCL45632 strain of T. atroviride. These studies highlight that Trichoderma application in soil assists the plant in reduction of Fe3+ to Fe2+, which consequently boosts its solubilization and uptake.

2.4. Yield Improvement

Treatment with different species of Trichoderma guarantees high yield production in the case of crops like mustard, wheat, corn, tuberose, sugarcane, tomato, okra, etc. [45,46,47,48,49,50]. Similarly, seed biopriming with Trichoderma spp. spores substantially improve crop yield in greenhouses conditions [51]. Likewise, T. harzianum and T. viride treatments applied to marigold, petunia and verbena induced a significant increase in the number and weight of the flowers [52]. Moreover, treatment of chili seeds with T. harzianum IMI-3924332 enhances the germination rate [53].

2.5. Impacts on Abiotic Stress Tolerance

Being sessile organisms, plants are frequently exposed to various abiotic stresses. Inoculation of soil with different strains of Trichoderma improves plant growth and reproduction under stressful conditions. For example, biopriming of rice with T. harzianum reduced the harmful effects of salinity stress on plants and improved the plant growth [54]. Similar findings were also obtained in plants exposed to salinity stress, e.g., T. asperellum Q1-treated cucumber [55] and seedlings of Arabidopsis thaliana remedied with T. asperelloides T203 [56]. During heat and cold stresses, Trichoderma spp. also play a crucial role in their mitigation. For example, chilling stress in tomato plants was mitigated when plants were treated with T. harzianum AK20G strains [57]. Similarly, transgenic plants of A. thaliana exhibited a greater tolerance to heat stress when transformed with T. harzianum T34 hsp70 genes [58]. Furthermore, various species of Trichoderma are also known for their roles in amelioration of oxidative stress in plants. In fact, in wheat plants inoculated with T. longibrachiatum and subjected to salinity, a significant increase in antioxidants like SOD (superoxide dismutase), CAT (catalase) and POD (peroxidase) gene expression was observed [59].

2.6. Induction of Disease Resistance

It has been reported that the addition of different species of Trichoderma in a plant’s rhizosphere improved plant defense against several pathogenic organisms such as viruses, bacteria and fungi, by stimulating the initiation of different resistance mechanisms mainly encompassing induced systemic resistance (ISR), hypersensitive response (HR) and systemic acquired resistance (SAR) [40]. Based on several reports (Table 1), an inference in favor of different classes of metabolites can be outlined, which emphasizes their significance as elicitors or resistance inducers in the Trichoderma-plants interactions [60]. These metabolites incorporate proteins displaying enzymatic activity such as xylanases and chitinases, protein-like gene products expressed by non-virulent genes and low molecular composites produced because of hydrolytic enzymatic degradation of fungal or plant cells [60].
Induction of resistance is due to the rise in the amounts of defensive metabolites as well as enzymes. These mainly include phytoalexin biosynthesis (HR), which involves the participation of enzymes of phenylpropanoid metabolism, i.e., phenylalanine ammonialyase (PAL) and chalcone synthase (CHS) [61]. Other enzymes which enhance resistance in plants also include chitinases and glucanases [62]. They also encompass pathogenesis-related proteins (PR) (SAR response), and enzymes play a part in antioxidative defense response [61]. For example, Hordeum spp., exhibiting Trichoderma atroviride endochitinase Ech42 activity, revealed improved resistance for Fusarium infection [62]. Likewise, T. harzianum-derived chitinase (Chit42), expressed in tobacco and potato plants, led to the development of extremely tolerant or totally resistant transgenic lines towards soil-borne pathogen like Rhizoctonia solani as well as foliar pathogens such as Alternaria alternata, A. solani and Botrytis cinerea [63]. Yedidia et al. [64] confirmed that cucumber roots inoculated with T. harzianum were characterized by a higher expression of peroxidase and chitinase activities, which improved plant resistance to pathogenic attacks.

3. Trichoderma-Pathogen Interactions

Disease control, as facilitated by biocontrol mediators, is an outcome of the interactions among the plant’s symbiont and pathogenic communities. Because of their capability to defend plants and control pathogen populations, under various soil circumstances, Trichoderma spp. have been extensively analyzed and exploited commercially as biocontrol agents, soil improvers and biofertilizers, placing Trichoderma spp. amongst the most explored fungal BCAs [20,40,65]. Several species of this genus are ‘rhizosphere competent’ and can also decompose polysaccharides, hydrocarbons, chlorophenolic compounds and the xenobiotic pesticides employed in cultivation [66]. The key biocontrol strategies that Trichoderma develops in direct conflict with fungal pathogens are mycoparasitism [67,68], competition [60] and antibiosis [69,70].

3.1. Mycoparasitism

Mycoparasitism implies the direct strike of one fungal species on another and is among the most important antagonistic mechanisms expressed by Trichoderma spp. About 75 Hypocrea/Trichoderma species with mycoparasitic potential have been previously reported. There are several investigations which indicate that numerous strains of Trichoderma attack and disintegrate plant pathogenic fungi, e.g., Rhizoctonia solani, Alternaria alternata, Sclerotinia sclerotiorum, Fusarium spp., Botrytis cinerea, Pythium spp. and Ustilago maydis [40,70,71].
About 70 years ago, Weindling [72] was the first to note this mycoparasitic reaction. This complex process includes sequential events. Firstly, identification between Trichoderma and the target fungus is mediated by the binding of carbohydrates present in the cell wall of Trichoderma to the lectins of the other one. This is followed by the hyphal twirling and appresoria development, which encompasses a greater number of osmotic compounds like glycerol. After successful penetration, Trichoderma initiate the attack on the host’s cellular machinery via generating numerous fungitoxic cell wall degrading enzymes (CWDEs), such as glucanases, chitinases and proteases [40]. The cumulative action of these compounds causes dissolution of the host cell walls, which ultimately results in parasitism of the target fungus. It has been observed that gaps can be generated at the location of appressoria formation which facilitate the direct access of Trichoderma hyphae into the lumen of the target fungus, which then proceeds to kill the pathogenic fungus [22]. Furthermore, biocontrol agents not only degrade the cell wall of target fungus, but also inactivate its enzymes (e.g., pectinases etc.), which are essential for pathogenic fungus to colonize and penetrate the plant tissues [40].
As we know, fungal cell walls are mainly composed of chitin and β-1,3-glucan [73]. Chitinases (EC and β-1,3-glucanases (EC lytic enzymes synthesized by Trichoderma spp. are supposed to be responsible for their mycoparasitic actions leading to the degradation of phytopathogenic fungal cell walls [74,75,76]. In addition, other CWDEs including those hydrolyzing minor polymers (like proteins, β-1,6-glucans, α-1,3-glucans, etc.) further ensure the complete and effective disintegration of fungal mycelial or conidial walls by Trichoderma spp. [77]. A chitin induced subtilisin-type serine proteinase has previously been depicted in a Trichoderma harzianum mycoparasitic strain [76]. Moreover, β-1,6-glucanases (EC have been reported to degrade cell walls in yeast, filamentous fungi [78,79] and bacteria [80] (Table 1).
Zeilinger et al. [81] previously reported that Trichoderma can sense the existence of pathogenic mycelium in the rhizosphere and proliferate towards the direction of the pathogen area. Recently, the green fluorescent protein encoding gene was incorporated downstream to the regulatory sequence of an endo- and an exochitinase encoding gene. This study revealed that, during the Trichoderma-fungal interaction, the endochitinase gene is stimulated prior to contact with the target fungus. On the contrary, exochitinase activation took place only after the contact was established [82]. Distinct forms may pursue separate patterns of stimulation, however, Trichoderma in fact constantly emit small amounts of exochitinase. Transmission of this enzyme stimulates the generation of cell wall pieces from target fungi. These fragments apparently interact with receptors on the cell wall or plasma membrane of Trichoderma and consequently promote the expression of fungitoxic CWDEs [83]. These CWDEs in turn diffuse and initiate the attack on the target fungi before the actual contact has been made [80,84]. As soon as the contact has been established, Trichoderma spp. coil and form appressoria on the exterior of the host. In addition to CWDEs, Trichoderma emits fungitoxic peptaibol antibiotics [85]. The collective action of these ingredients is essential for dissolution of the cell walls and parasitism of the target fungus. Approximately 20–30 known genes, proteins or metabolites are clearly engaged in this activity [86,87].

3.2. Competition

The limited availability of and competition for nutrients lead to the natural management of fungal communities and phytopathogen development [51]. Competition for micro- and macronutrients such as C, N and Fe plays a pivotal role during interactions of advantageous and disadvantageous fungi and is coupled with the biocontrol systems [18]. It has been well established that Trichoderma species compete for nutrients, biological niches or infection spots with pathogens in plant rhizosphere [60]. Trichoderma exhibits a better capability to mobilize and absorb nutrients from the soil in comparison to other rhizospheric microorganisms; therefore, the control management of some pathogens (e.g., B. cinerea) by using Trichoderma involves the coordination of numerous strategies, such as the competition for nutrients, which is considered amongst the most important [88].
The effective utilization of nutrients depends upon the ability of Trichoderma spp. to get energy derived from the metabolism of carbohydrates like cellulose, chitin, glucan and glucose, which are often present in the mycelial environment [51]. The function of the glucose transport system has yet to be discovered, but it is conceivable that its competence in Trichoderma competition performs a pivotal role [89]. Root exudates and the rhizosphere are particularly rich in nutrients like carbohydrates, amino acids, organic acids, vitamins, Fe, etc., but the competition for C between Trichoderma and pathogenic fungi like Rhizoctonia solani, F. oxysporium, etc. was considered to be most noteworthy [90,91].
As compared to other microbes in the soil, the competent mobilization of immobile nutrients and their use provides superiority to Trichoderma. For this purpose, Trichoderma induces the reduction of soil pH via the biosynthesis and release of organic acids like gluconic, citric and fumaric. Moreover, these organic acids further facilitate the solubilization of micronutrients and mineral cations such as phosphates, Fe, Mn and Mg [18]. Interestingly, it has been reported that T. harzianum CECT 2413 encodes a glucose transporter (Gtt1) which expresses a high affinity for glucose even at an exceptionally low concentration [89,92]. Moreover, Vargas et al. [93] recognized an intracellular invertase enzyme from T. virens (TvInv) which seems to be responsible for the degradation of plant-derived sucrose.
Fe ions serve as cofactor for multiple classes of enzymes and play a key role as a nutrient for the growth and development of plants [94]. Iron occurs primarily as Fe3+ under the conditions of neutral pH and in the presence of oxygen. In the aerobic environment, Fe tends to develop insoluble ferric oxide, which ultimately makes it not available for root absorption [94]. A Fe-chelating complex, known as siderophore, is secreted by Trichoderma spp. [95]. This complex first binds to the insoluble iron (Fe3+) and then transforms it into the easily absorbable soluble form, i.e., (Fe2+) (Figure 2). While increasing the availability of Fe to plants, siderophore simultaneously depletes the Fe sources of the soil and thereby inhibits the growth of target fungi [95]. Most of the fungal siderophores derived so far relate to the hydroxamate class and can be classified into three families: fusarinines, coprogens and ferrichromes [96,97].

3.3. Antibiosis

Antibiosis is the process by which diffusible low-molecular weight compounds interact and reduce the growth of other microorganisms. Mainly, antibiosis is centered on the production of secondary metabolites, which display an inhibitory or deadly consequence on a parasitic fungus. More than 180 secondary metabolites indicating distinct classes of chemical products have been isolated from fungal species belonging to genus Trichoderma [98,99]. Depending upon their biosynthetic origins, these compounds can be grouped into peptaibol, polyketide and terpene [100]. Various spp. of Trichoderma are known to produce non-proteinogenic amino acid (especially α-aminoisobutyric) composed peptaibols, which are polypeptide antibiotics with a molecular weight ranging from 500 to 2200 Da. The peculiar feature of these compounds is that their N-terminal is acetylated, while the C-terminal has amino alcohols [101]. Therefore, their chemical nature is amphipathic, and they arrange themselves in the membrane to form voltage-gated ion channels. These peptides are synthesized by non-ribosomal peptide synthetases (NRPSs).
In addition to this, Trichoderma spp. express the capability to synthesize a different class of defensive metabolite, termed polyketides, through sequential events catalyzed by a complex of enzymes called as polyketide synthases (PKSs). Different strains of Trichoderma synthesize a huge variety of antibiotics [99], e.g., T. viride produces trichotoxins A and B, trichodecenins, trichorovins and trichocellins. Similarly, trichorzianins A and B, trichorzins, HA and MA were isolated from culture filtrate of T. harzianum. T. longibrachiatum produces tricholongins BI and BII, whereas longibrachins and trichokonins were isolated from T. koningii; atroviridins A-C and neoatroviridins A-D derive from T. atroviride cultures. Further, other antibacterial and fungicidal metabolites, e.g., koningins, viridin, dermadin, trichoviridin, lignoren and koningic acid were isolated from T. koningii, T. harzianum, T. aureoviride, T. viride, T. virens, T. hamatum and T. lignorum cultures [99]. Gliotoxin and gliovirin are among the most significant secondary metabolites of Trichoderma related to the P and Q group strain, respectively (Table 1). P group strains of Trichoderma (Gliocladium) virens adversely affect P. ultimum, but not R. solani. On the other hand, Q group is more active against R. solani [102]. The T. virens gene veA ortholog vel1 encoded the VELVET protein, which regulates both the biosynthesis and the biocontrol activity of gliotoxin as well as other genes participating in the secondary metabolism [103].
Growth of soil-borne pathogens like R. solani, Phytophthora cinnamomi, Pythium middletonii, Fusarium oxysporum and Bipolaris sorokiniana was observed to be negatively affected in the presence of Koninginin D [104]. In a similar way, viridins obtained from Trichoderma spp. like T. koningii, T. viride, and T. virens contained the spore germination of Botrytis allii, Colletotrichum lini, Fusarium caeruleum, Penicillium expansum, Aspergillus niger and Stachybotrys atra [105]. T. harzianum-derived harzianic acid showed antibiotic activity against Pythium irregulare, Sclerotinia sclerotiorum and R. solani in in-vitro culture [106]. Two asperelines (i.e., A and E) and 5 trichotoxins designated as T5D2, T5E, T5F, T5G and 1717A with antibiotic features were produced by the T. asperellum strain [107]. In general, antibiotic activity is combined cooperatively with lytic enzymes. Their dual action offers a more advanced level of antagonism than the activity of either antibiotics or enzymes acting alone [108]. As observed by Howell et al. [63], initial disintegration of cell walls in the case of B. cinerea and F. oxysporum by lytic enzymes enhanced the antibiotic penetration into the target hypha.

4. Effect of Trichoderma Inoculation

4.1. Destruction of Pathogenic Organism

This complex process includes sequential events, which initially involve recognition between Trichoderma and the target fungus, the coiling around the fungal hyphae, which is followed by appresoria development [40]. After this collective action, lytic enzymes cause the dissolution of target fungal cell walls. Furthermore, Vel1 of Trichoderma virens participates in the expression of hydrophobin, which facilitates the adhesion of Trichoderma to the host [24]. Interestingly, seven transmembrane G protein coupled receptors (Gpr1) are engaged in perceiving the target fungus in the adjacent neighborhood [109,110]. Binding of ligands with such receptors causes the downstream signaling cascade via stimulation of G proteins and mitogen-activated protein kinase (MAPK). Three MAPK (i.e., MAPKKK, MAPKK and MAPK) are known in different species of Trichoderma [111]. These signaling pathways might play an important role during mycoparasitism and biocontrol of pathogens [111,112] (Table 1). Manufacture and discharge of CWDEs and antibiotics are extremely valuable members of the chemical resources used by Trichoderma to eradicate the pathogens (Figure 3).
Trichoderma also owns glucan and chitin synthases, which are enzymes involved in the healing of the Trichoderma cell wall, which might be damaged during Trichoderma–pathogen contact. Simultaneously, hydrolytic enzymes like chitinases and glucanases, as well as those for secondary metabolism like the NRPSs (non-ribosomal peptide synthetases) pathway, are expressed, inducing pathogen death [98]. Participation of chit42, chit3, bgn13.1, Bgn2, Bgn3 and prb1 genes in biocontrol of deleterious fungi through the activities of chitinases, glucanases and proteases were demonstrated [113].
Certain Trichoderma species (e.g., T. atroviride) produce 6-pentyl-2H-pyran-2-one (6-PP), a volatile metabolite which plays a key role during Trichoderma–fungal interactions [106,114]. Recently, genetic investigations unveiled that NRPS Tex2 of T. virens causes the assemblage of 11- and 14-module peptaibols [115], and these peptaibiotics strongly exhibit antimicrobial activities. For instance, a T. pseudokoningii peptaibol, called trichokonin VI, is known to form voltage-gated channels in membrane, and it ultimately induces programmed cell death (PCD) in Fusarium oxysporum [116]. Similarly, trichokonins VI, a peptaibol isolated from T. pseudokoningii SMF2, displays antibiotic actions by stimulating wide-ranging apoptotic PCD in a range of fungal pathogen species [117]. In a mutant of T. brevicompactum, namely Tb41tri5, the promoted expression of the tri5 (trichodiene synthase) gene amplified the synthesis of trichodermin. Additionally, it enhanced the antifungal activity against Aspergillus fumigatus and Fusarium spp. [115,117].

4.2. Plant Growth Promotion

Root colonization by Trichoderma in both mono- and dicotyledonous plants might cause noteworthy variations in plant metabolism. These mainly include alteration in the biosynthesis of growth regulators, compatible osmolytes, amino acids and phenolic components, as well as other physiological processes like photosynthesis, transpiration and leaf water potential [118,119]. Many lytic enzymes such as cellulase, xylanase, pectinase, endopolygalacturonase, glucanase, lipase, amylase, arabinase and protease have been isolated from different strains of Trichoderma [120,121]. A cellulose-binding protein termed swollenin can disrupt the crystalline structure of cellulose in plant cell walls [26]. It possesses a sequence similarity with plant protein expansins, which simplifies expansion of the plant cell wall in roots, as well as in root hairs. Via swollenin production, Trichoderma may enhance the surface area of plant roots, improving its establishment in the rhizosphere [26,70].
In general, an immune-like system is exhibited by plants which has the potential to perceive domains/motifs with preserved structural characters distinctive of a family of microbes termed as microbe-associated molecular patterns (MAMPs) (Figure 4) [13]. The ability of Trichoderma spp. hyphae to release MAMPs for molecular recognition may contribute to signal cascade by signaling molecules within the plant. Trichoderma acts locally and systemically, involving signaling cascade and activation as well as accumulation of defense-related antimicrobial compounds and enzymes such as phenyl ammonia lyase (PAL), peroxidase, polyphenol oxidase and lipoxygenase. In addition, PR proteins, terpenoid, phytoalexins (rishitin, lubimin, phytotuberol, coumarin, solevetivone, resveratrol, etc.) and antioxidants (ascorbic acid, glutathione, etc.) are also synthetized [102]. Consequent upon fungal invasion, plants respond to Trichoderma colonization by producing and concentrating defensive compounds like phytoalexins, flavonoids, terpenoids, phenolic byproducts, aglycones and additional antimicrobial compounds. Interestingly, Trichoderma strains are normally resistant to such compounds. This resistance is regarded as a crucial prerequisite to colonize the plant roots, and it has mainly been contributed by ABC (ATP-binding cassette) transport systems present in Trichoderma strains [122].
Reactive oxygen species (ROS) like H2O2, nitric oxide, etc., produced by glucose oxidase enzymes, are linked to Trichoderma-intermediated immunity in cotton, rice and A. thaliana [123,124,125]. Defense signaling in plants involves the participation of mitogen-activated protein (MAP) kinases, which convey information from receptors to initiate a cascade of cellular responses in plants (Figure 4) [126]. As reported in the case of cucumber, a MAPK exhibiting similarity with MPK3 of A. thaliana is stimulated via inoculation of the root with T. asperellum [127]. In a similar manner, an increase of concentration of the phytoalexin camalexin was detected in the T. virens- and T. atroviride-colonized root system of A. thaliana [128].
Molecular studies in A. thaliana revealed that colonization of roots by T. asperelloides T203 activated a quick upsurge in transcription factor (WRKY18, WRKY40, WRKY60 and WRKY33) expression, which further suppresses salicylic acid (SA) signaling and triggers jasmonic acid (JA)-pathway responses. These genes are induced by pathogens and their expression encodes three WRKY structurally linked proteins that play a key role in JA-arbitrated defense [56]. The expression of PR-1a (pathogenesis-related) and SA regulated genes, as well as the LOX2 gene, were upregulated by the application of T. atroviride and T. virens to A. thaliana [128,129]. Moreover, T. harzianum amplified the levels of SA and JA in melon and thereby changed the plant reactions against F. oxysporum [130]. Likewise, expression of LOX and PAL1 genes (involved respectively in the biosynthesis of jasmonic acid and salicylic acid) and ETR1 and CTR1 genes (participating in ethylene signaling pathways) were observed to increase after the application of T. asperellum T203 [131] (Table 1).
Cellulysin, isolated from T. viride, stimulates the octadecanoid signaling pathway, which subsequently activates the discharge of several volatile compounds in plants [132]. As reported in the case of leaves of lima bean, cellulysin together with JA induce the synthesis of dimethyl nonatriene, hexenyl acetate, germacrene, ocimene, caryophyllene and copaene. Another resemblance between JA- and cellulysin-induced actions causes the discharge of ethylene [132]. Beside degradation of xylan, β-1,4- endoxylanase (EIX) activity from T. viride provoked ethylene emission and the plant defensive system in tobacco [133]. A rise in ethylene levels is supplemented by buildup of ACC (1-aminocyclopropane-1-carboxylic acid) due to enhancement in ACC synthase activity as well as increase in ACC oxidase transcripts [134]. In addition, it has been observed in rice plants that EIX behaved as fungal elicitors, controlling phytoalexin biosynthesis and the expression of defensive genes via calcineurin B-like protein-interacting protein kinases (OsCIPK14/15) [135]. Similarly, SM1, a fungal elicitor obtained from T. virens, encourages the expression of the CAD1- C gene in cotton petioles, which encodes the enzyme (+)-δ-cadinene synthase. This enzyme serves as a primary inducer for phytoalexin synthesis in response to pathogen invasion [122,136].
Table 1. Compounds synthesized by Trichoderma spp. involved in plant interaction.
Table 1. Compounds synthesized by Trichoderma spp. involved in plant interaction.
Sr. No.CategorySub-CategoryFunction PerformedTrichoderma SpeciesReferences
IAAGrowth and development of plants and their root system.T. virens[35]
GA3Growth promotion by degradation of growth repressing DELLA proteins and reduction in ethylene level.Trichoderma spp.[13,137]
ABAAlteration in transpiration and regulation of stomatal aperture via induction of an ABA receptor. T. virens and T. atroviride[33]
Ethylene Improved tolerance to biotic as well as abiotic stresses by regulation of levels of SA and JA as well as their signaling pathways. T. atroviride[138,139,140]
JA JA and/or ET are the signaling molecule for Tichoderma-induced ISR. T. asperellum[141]
SAEnhances disease resistance in plants through induction of SAR.T. atroviride[26,142,143]
Cellulolytic enzymesCleavage of β-1,4-D-glycosidic bonds in cellulose molecule. [120]
Exo-β-1,4-glucanases Breakdown of cellulose by forming a cellobiose molecule either from the reducing or nonreducing terminals.T. viride, T. harzianum, T. reesei, T. koningii[144]
Endo-β-1,4-glucanasesAt the time of enzymatic lysis of cellulose, break the β-1,4- glycosidic bonds in a random way probably in the amorphous areas of cellulose and thereby cause formation of cellulodextrines with variable chain lengths.T. viride, T. longibrachiatum, T. pseudokoningii and T. reesei[145,146,147]
β-GlucosidasesPromote lysis of short length oligosaccharides and cellobiose into glucose.T. viride, T. harzianum, T. reesei and T. longibrachiatum.[148,149]
XylanaseCatalyze breakdown of xylans to form xylo-oligomers, xylobiose and xylose.T. harzianum, T. koningii, T. lignorum, T. longibrachiatum, T. pseudokoningii, T. reesei, T. viride
Trichoderma harzianum,
T. virens, T. asperellum, T. atroviride
Chitinase Catalyze degradation of chitin to chitooligomers of low molecular weight. [83,151,152,153,154]
Endochitinases Randomly hydrolyses chitin at internal sites and form dimer of diacetylchitobiose and low molecular weight multimers of GlcNAc like chitotriose and chitotetraose.
ExochitinasesDivided into 2 subcategories: 1. Chitobiosidases, involved in catalyzing the sequential release of diacetylchitobiose starting from the non-reducing end of the chitin microfibril
2. 1-4-β-glucosaminidases, splitting the oligomeric products of endochitinases and chitobiosidases, thereby producing GlcNAc monomers.
ExopeptidasesCause the cleaving of peptide bond either at the amino or carboxy terminal.T. viride, T. harzianum, T. aureoviride, T. atroviride[155,156]
EndopeptidasesSplit the peptide bonds away from the ends.
LipaseLipase hydrolyses ester bonds of triacylglycerols, resulting in the formation of mono- and diacylglycerols, free fatty acids and, in some cases, glycerol also.T. lanuginosus, Trichoderma reesei, Trichoderma koningii, T. harzianum, T. virens, m T. viride[157]
Glucose oxidaseCause generation of reactive oxygen species (ROS). T. virens, T. asperelloides[123,124,125]
Antioxidative enzymes
(e.g., SOD, CAT, POD etc.)
Enhance antioxidative defense mechanism in plants.Trichoderma spp.[59,158]
Biosynthetic and signaling
PAL & CHSProduction of phytoalexins.Trichoderma spp.[60]
Glucan and Chitin synthasesProduced by the Trichoderma to repair their self-cell wall damage by pathogen during Trichoderma–pathogen interaction.Trichoderma spp.[159]
MAPKConvey information from receptor to generate cellular signaling and defense responses.Trichoderma spp.[126,131]
ETR1 and CTR1 Involved in ethylene (ET) signaling. Trichoderma spp.[131]
LOX1 (Lipoxygenase 1) PAL1 (phenylalanine ammonia lyase),Participate in jasmonic acid (JA) biosynthetic pathway.
Involved in biosynthetic pathway for salicylic acid (SA)
Trichoderma spp.[160]
ACC synthase ACC oxidasePromote ethylene biosynthesis.Trichoderma spp.[134]
δ-cadinene synthaseAct as precursor for phytoalexin synthesis. T. virens[123,136]
3.Soil modifiers
Gluconic, citric and fumaric acidsReduce the pH of soil and facilitate the solubilization of phosphates and micronutrients. Trichoderma spp.[18,41]
SiderophoreChelate with insoluble Fe (III) and convert them to soluble Fe (II).Trichoderma spp.[44,94,95]
4.Secondary metabolites
PyronesAntimicrobialTrichoderma spp.[161]
LactonesParticipate in IAA and ethylene-mediated signaling and improve plant growth and root architecture. T. harzianum, Trichoderma cremeum[162]
KoningininsAntimicrobialT. koningii, T. harzianum,
T. aureoviride
Trichodermamides Antifungal and exhibit cytotoxicity to human colon carcinoma. T. virens[165,166]
ViridinsAntifungalTrichoderma virens, T. koningii, T. viride[99,167,168]
Nitrogen heterocyclic compounds
(harzianopyridone, harzianic acid)
AntifungalT. harzianum[169,170,171]
AzaphilonesAntifungalT. harzianum T22[171,172]
Butenolides and hydroxy-Lactones
(cerinolactone, trichosordarin A, harzianol A and harzianone)
AntifungalT. cerinum, Trichoderma cremeum, Trichoderma
longibrachiatum A-WH-20-2
Isocyano metabolites
(dermadin and trichoviridin)
AntifungalT. viride T. koningii and T. hamatum[164,175,176]
(gliotoxin and gliovirin)
AntifungalTrichoderma (Gliocladium) virens[177]
Peptaibol (alamethicin, trichokonin VI) Non-ribosomal short peptides, rich in 2-amino-isobutyric acid involved in plant defense and antimicrobial in nature.T. virens, T. longibrachiatum[178,179]
PolyketidesParticipate in SA mediated signaling pathway and exhibit antimicrobial activities.T. virens, Trichoderma sp. SCSIO41004[180,181]
cyclonerane sesquiterpenoids, trichocitrin, trichosordarin A
AntimicrobialT. virens, Trichoderma harzianum P1-4, Trichoderma citrinoviride cf-27, Trichoderma harzianum R5[182,183,184,185]
Volatile organic compounds (VOCs) (trichodiene)Facilitate the plant-microbe interactions in rhizosphereT. arundinaceum, T. atroviride[186,187,188]
HydrophobinsPlant growth promotion, signaling and defense T. virens and T. atroviride, T. asperellum [189,190]

5. Other Applications of Trichoderma

Besides the aforementioned roles of Trichoderma spp., their extreme versatility in terms of metabolite production makes fungi from the genus Trichoderma potentially interesting for different applications, as detailed below.

5.1. Bioremediation

Several deleterious organic pollutants like phenols, cyanides and nitrates are frequently degraded via T. harzianum [191]. There are several reports which show the involvement of Trichoderma spp. strains in detoxification of polycyclic aromatic hydrocarbons (PAHs). Katayama and Matsumura [192] verified the degradative efficacy of Trichoderma spp. against several artificial dyes like pentachlorophenol, endosulfan and dichlorodiphenyl trichloroethane (DDT). Capability of immobilized T. viride biomass along with cell-free Ca-alginate beads in biosorption of Cr (VI) has already been reported [193]. Similarly, T. inhamatum displayed an extraordinary capability to stand and totally reduce Cr (VI) concentrations, playing a significant role in bioremediation of Cr (VI)-contaminated wastewaters [194]. Likewise, Trichoderma harzianum express various adaptive strategies in detoxification of Cd contaminated soil [195].

5.2. Animal Feed

Lytic enzymes, like cellulases, hemicellulases and pectinases, produced by Trichoderma spp. can be employed in partial hydrolysis of plant cell walls in feeds. This process increases the digestibility of the feed and increases its nutritive value. Therefore, an increase in animal body weight as well as a higher milk yield was observed [196].

5.3. Industrial Applications

Cellulases produced by Trichoderma are also used to soften textiles. Moreover, the enzymes attained from Trichoderma are employed to modify fiber properties as well as to reduce lignin contents [197]. T. harzianum-derived mutanase may be added in toothpaste to avoid the development of plaque [198]. In the food industry, additional metabolites obtained from the different species of Trichoderma are also used along with their enzymes. For example, nut aroma producing compounds, obtained initially from T. viride and afterward from T. atroviride, express useful antibiotic properties [199]. Brewery industries also use the enzymes attained from Trichoderma spp. They may also be employed as food additives and escalate maceration of raw materials for the manufacturing of fruit and vegetable juices. These enzymes can also be employed to improve wine tang and increase the fermentation, filtration and excellence of beer. Above all, the potential of Trichoderma-derived bioactive compounds could be exploited in the pharmaceutical industry because of their several curative properties [200,201,202,203].

5.4. Second Generation Biofuels

Improved conservational understanding of whole communities as well as growing concerns in alternative resources of energy make it feasible to use fungi from the genus Trichoderma in the manufacturing of self-styled second-generation biofuels [204]. For instance, cellulases and hemicellulases supplied by T. reesei are used in the production of bioethanol from farm wastes. These enzymes indeed catalyze the biodegradation of substrates to simple sugars, and afterwards, these are exposed to yeast (Saccharomyces cerevisiae)-induced fermentation [205,206].

5.5. Wood Preservation

Wood preservation by chemicals is relatively cheap and effectively prolongs the service life of wood [207]. By contrast, the toxicity of heavy metals and other chemicals used as wood preservatives are also a matter of serious health and environmental concern [208,209,210,211]. The intense research activities on developing and testing less problematic protective systems demonstrate the urgent need for innovation in this field [212,213,214,215,216,217,218,219,220]. As the antagonistic properties were evolved in competition with other wood destroyers—such as wood-rotting and sap-staining fungi, or other molds—the expectation is justified that the Trichoderma isolated from wood does have the ability to effectively inhibit wood-damaging fungi. Interestingly, Ejechi [221] researched the capability of Trichoderma viride to prevent the fungal (Gloeophyllum sp. and G. sepiarium) decay of obeche (Triplochiton sceleroxylon) wood via deterioration of decaying fungi under field conditions. Similarly, Tucker et al. [222] observed that isolates of Trichoderma spp. were involved in effective protection of wood against certain basidiomycetes.

5.6. Agricultural and Horticultural Applications

Numerous Trichoderma spp. have also been used to protect fruits and vegetables of commercial significance throughout post-harvest storage. For example, Mortuza and Ilag [223] employed 10 isolates of T. harzianum and T. viride against Lasiodiplodia theobromae (fruit rot pathogen of banana). Similarly, Batta [224,225] applied the invert-emulsion formulation of T. harzianum Rifai in opposition to apple blue mold infection to prevent post-harvest decay of fruit. Trichoderma spp. are well-recognized fungal antagonists of crop/seed pathogens. Management of Colletotrichum truncatum, causing brown blotch of cowpea, has been done via the pre-treatment of seeds in T. viride spore suspension [226].

6. Conclusions and Future Perspectives

Biocontrol might be well-described as the practice of biological organisms or genetically altered genes or their products to lessen the consequences of unwanted organisms and to support organisms, which seems to be beneficial for human beings. As discussed in this review, Trichoderma spp. are correctly renowned for their capacity to generate a broad range of antibiotic substances that have the potential to parasitize a wide array of pathogenic fungi in the rhizosphere. In addition, Trichoderma spp. synthesize several metabolites which have a substantial influence on plant growth, along with stimulation of localized and systemic resistance and stress tolerance in plants. The recognition of Trichoderma elicitors and effectors by plant receptors initiates the signaling and regulation of host genetic apparatus, which serves as a basis for these symbionts to induce the defense metabolism in their host.
Further research dealing with the biochemical and physiological bases through which Trichoderma spp. act as biocontrol agent against several lethal fungi is necessary for a wide, in-depth knowledge of this multitalented biocontrol agent. Moreover, for the purpose of integrated disease management, the compatibility of Trichoderma with chemical fungicides should be evaluated. The popularity of Trichoderma-based formulations among farmers for ecofriendly management of diseases should be enhanced. The ecological influence of comprehensive applications of a fungal species as well as their secondary metabolites for biocontrol should be assessed to confirm a database for the secure and sustainable usage of Trichoderma. Consequently, Trichoderma genomes can also serve as an extremely useful source of candidate genes for producing transgenic plants exhibiting tolerance to both biotic and abiotic stresses. Lastly, by taking into consideration all the information provided in this review, the use of Trichoderma species should be promoted as a valid alternative to pesticides in the era of a green economy which aims at promoting human health and environmental safeguarding.

Author Contributions

M.S., D.K., V.K. wrote initial draft; M.S.S., M.R., F.A., were involved in revision of initial draft. A.S. and M.L. designed the outline and revised the initial draft. All authors have read and agreed to the published version of the manuscript.


This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Raney, T. The State of Food and Agriculture: Livestock in the Balance; Food and Agriculture Organization of the United Nations: Rome, Italy, 2009.
  2. Moustafa-Farag, M.; Almoneafy, A.; Mahmoud, A.; Elkelish, A.; Arnao, M.B.; Li, L.; Ai, S. Melatonin and Its Protective Role against Biotic Stress Impacts on Plants. Biomolecules 2020, 10, 54. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Raju, N.S.; Niranjana, S.R.; Shetty, H.S. Effect of Pseudomonas fluoriescens and Trichoderma harzianum on head moulds and seed qualitites of Sorghum. Crop Improv. (India) 2003, 30, 6–12. [Google Scholar]
  4. Atreya, K.; Sitaula, B.K.; Bajracharya, R.M. Pesticide use in agriculture: The philosophy, complexities and opportunities. Sci. Res. Essays 2012, 7, 2168–2173. [Google Scholar]
  5. Meszka, B.; Broniarek-Niemiec, A.; Bielenin, A. The status of dodine resistance of Venturia inaequalis populations in Poland. Phytopathol. Pol. 2008, 47, 57–61. [Google Scholar]
  6. Matson, M.E.H.; Small, I.M.; Fry, W.E.; Judelson, H.S. Metalaxyl resistance in Phytophthora infestans: Assessing role of RPA190 gene and diversity within clonal lineages. Phytopathology 2015, 105, 1594–1600. [Google Scholar] [CrossRef] [Green Version]
  7. Slabaugh, W.R.; Grove, M.D. Postharvest diseases of bananas and their control. Plant Dis. 1982, 66, 746–750. [Google Scholar] [CrossRef]
  8. Spalding, D.H. Resistance of mango pathogens to fungicides used to control postharvest diseases. Plant Dis. 1982, 66, 1185–1186. [Google Scholar] [CrossRef]
  9. Farungsang, U.; Farungsang, N. Benomyl resistance of Colletotrichum spp. Associated with rambutan and mango fruit rot in Thailand. Front. Trop. Fruit Res. 1991, 321, 891–897. [Google Scholar] [CrossRef]
  10. Panth, M.; Hassler, S.C.; Baysal-Gurel, F. Methods for Management of Soilborne Diseases in Crop Production. Agriculture 2020, 10, 16. [Google Scholar] [CrossRef] [Green Version]
  11. Köhl, J.; Kolnaar, R.; Ravensberg, W.J. Mode of action of microbial biological control agents against plant diseases: Relevance beyond efficacy. Front. Plant Sci. 2019, 10, 845. [Google Scholar] [CrossRef] [Green Version]
  12. Hyder, S.; Inam-ul-Haq, M.; Bibi, S.; Humayun, A.; Ghuffar, S.; Iqbal, S. Novel potential of Trichoderma spp. as biocontrol agent. J. Entomol. Zool. Stud. 2017, 5, 214–222. [Google Scholar]
  13. Hermosa, R.; Viterbo, A.; Chet, I.; Monte, E. Plant-beneficial effects of Trichoderma and of its genes. Microbiology 2012, 158, 17–25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Persoon, C.H. Disposita methodical fungorum. Romers. Neues. Mag. Bot. 1794, 1, 81–128. [Google Scholar]
  15. Abbey, J.A.; Percival, D.; Abbey, L.; Asiedu, S.K.; Prithiviraj, B.; Schilder, A. Biofungicides as alternative to synthetic fungicide control of grey mould (Botrytis cinerea)–prospects and challenges. Biocontrol. Sci. Technol. 2019, 29, 207–228. [Google Scholar] [CrossRef]
  16. Singh, H.B.; Singh, B.N.; Singh, S.P.; Singh, S.R.; Sarma, B.K. Biological control of plant diseases: Status and prospects. In Recent Advances in Biopesticides: Biotechnological Applications; New India Pub.: New Delhi, India, 2009; Volume 322. [Google Scholar]
  17. Van Wees, S.C.M.; der Ent, S.; Pieterse, C.M.J. Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 2008, 11, 443–448. [Google Scholar] [CrossRef] [Green Version]
  18. Vinale, F.; Sivasithamparam, K.; Ghisalberti, E.L.; Marra, R.; Woo, S.L.; Lorito, M. Trichoderma–plant–pathogen interactions. Soil Biol. Biochem. 2008, 40, 1–10. [Google Scholar] [CrossRef]
  19. Wilson, P.S.; Ketola, E.O.; Ahvenniemi, P.M.; Lehtonen, M.J.; Valkonen, J.P.T. Dynamics of soilborne Rhizoctonia solani in the presence of Trichoderma harzianum: Effects on stem canker, black scurf, and progeny tubers of potato. Plant Pathol. 2008, 57, 152–161. [Google Scholar] [CrossRef]
  20. Lorito, M.; Woo, S.L.; Harman, G.E.; Monte, E. Translational research on Trichoderma: From’omics to the field. Ann. Rev. Phytopathol. 2010, 48, 395–417. [Google Scholar] [CrossRef] [Green Version]
  21. Zhang, J.; Chen, G.-Y.; Li, X.-Z.; Hu, M.; Wang, B.-Y.; Ruan, B.-H.; Zhou, H.; Zhao, L.-X.; Zhou, J.; Ding, Z.-T.; et al. Phytotoxic, antibacterial, and antioxidant activities of mycotoxins and other metabolites from Trichoderma sp. Nat. Prod. Res. 2017, 31, 2745–2752. [Google Scholar] [CrossRef]
  22. Kumar, S. Trichoderma: A biological weapon for managing plant diseases and promoting sustainability. Int. J. Agric. Sci. Med. Vet. 2013, 1, 106–121. [Google Scholar]
  23. López-Bucio, J.; Pelagio-Flores, R.; Herrera-Estrella, A. Trichoderma as biostimulant: Exploiting the multilevel properties of a plant beneficial fungus. Sci. Hortic. 2015, 196, 109–123. [Google Scholar] [CrossRef]
  24. Viterbo, A.D.A.; Chet, I. TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization. Mol. Plant Pathol. 2006, 7, 249–258. [Google Scholar] [CrossRef] [PubMed]
  25. Samolski, I.; Rincón, A.M.; Pinzón, L.M.; Viterbo, A.; Monte, E. The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiology 2012, 158, 129–138. [Google Scholar] [CrossRef] [PubMed]
  26. Meng, X.; Miao, Y.; Liu, Q.; Ma, L.; Guo, K.; Liu, D.; Ran, W.; Shen, Q. TgSWO from Trichoderma guizhouense NJAU4742 promotes growth in cucumber plants by modifying the root morphology and the cell wall architecture. Microb. Cell Factories 2019, 18, 148. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Morán-Diez, E.; Hermosa, R.; Ambrosino, P.; Cardoza, R.E.; Gutiérrez, S.; Lorito, M.; Monte, E. The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum–plant beneficial interaction. Mol. Plant-Microbe Interact. 2009, 22, 1021–1031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Masunaka, A.; Hyakumachi, M.; Takenaka, S. Plant growth-promoting fungus, Trichoderma koningi suppresses isoflavonoid phytoalexin vestitol production for colonization on/in the roots of Lotus japonicus. Microbes Environ. 2009, 1102230277. [Google Scholar] [CrossRef] [Green Version]
  29. Lace, B.; Genre, A.; Woo, S.; Faccio, A.; Lorito, M.; Bonfante, P. Gate crashing arbuscular mycorrhizas: In vivo imaging shows the extensive colonization of both symbionts by Trichoderma atroviride. Environ. Microbiol. Rep. 2015, 7, 64–77. [Google Scholar] [CrossRef]
  30. Omomowo, O.I.; Babalola, O.O. Bacterial and Fungal Endophytes: Tiny Giants with Immense Beneficial Potential for Plant Growth and Sustainable Agricultural Productivity. Microorganisms 2019, 7, 481. [Google Scholar] [CrossRef] [Green Version]
  31. Halifu, S.; Deng, X.; Song, X.; Song, R. Effects of Two Trichoderma Strains on Plant Growth, Rhizosphere Soil Nutrients, and Fungal Community of Pinus sylvestris var. mongolica Annual Seedlings. Forests 2019, 10, 758. [Google Scholar] [CrossRef] [Green Version]
  32. Sajeesh, P.K. Cu-Chi-Tri: A Triple Combination for the Management of Late Blight Disease of Potato (Solanum tuberosum L.). Ph.D. Thesis, GB Pant University of Agriculture and Technology, Pantnagar, India, 2015. [Google Scholar]
  33. Contreras-Cornejo, H.A.; Macías-Rodríguez, L.; Vergara, A.G.; López-Bucio, J. Trichoderma modulates stomatal aperture and leaf transpiration through an abscisic acid-dependent mechanism in Arabidopsis. J. Plant Growth Regul. 2015, 34, 425–432. [Google Scholar] [CrossRef]
  34. Yedidia, I.; Srivastva, A.K.; Kapulnik, Y.; Chet, I. Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant Soil 2001, 235, 235–242. [Google Scholar] [CrossRef]
  35. Contreras-Cornejo, H.A.; Macías-Rodríguez, L.; Cortés-Penagos, C.; López-Bucio, J. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol. 2009, 149, 1579–1592. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Rabeendran, N.; Moot, D.J.; Jones, E.E.; Stewart, A. Inconsistent growth promotion of cabbage and lettuce from Trichoderma isolates. New Zeal. Plant Prot. 2000, 53, 143–146. [Google Scholar] [CrossRef] [Green Version]
  37. Doni, F.; Isahak, A.; Zain, C.R.C.M.; Ariffin, S.M.; Mohamad, W.N.W.; Yusoff, W.M.W. Formulation of Trichoderma sp. SL2 inoculants using different carriers for soil treatment in rice seedling growth. Springerplus 2014, 3, 532. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Shukla, N.; Awasthi, R.P.; Rawat, L.; Kumar, J. Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiol. Biochem. 2012, 54, 78–88. [Google Scholar] [CrossRef]
  39. Mishra, A.; Salokhe, V.M. Rice root growth and physiological responses to SRI water management and implications for crop productivity. Paddy Water Environ. 2011, 9, 41–52. [Google Scholar] [CrossRef]
  40. Harman, G.E.; Howell, C.R.; Viterbo, A.; Chet, I.; Lorito, M. Trichoderma species—opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2004, 2, 43–56. [Google Scholar] [CrossRef]
  41. Zhao, K.; Penttinen, P.; Zhang, X.; Ao, X.; Liu, M.; Yu, X.; Chen, Q. Maize rhizosphere in Sichuan, China, hosts plant growth promoting Burkholderia cepacia with phosphate solubilizing and antifungal abilities. Microbiol. Res. 2014, 169, 76–82. [Google Scholar] [CrossRef]
  42. Altomare, C.; Norvell, W.A.; Björkman, T.; Harman, G.E. Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295-22. Appl. Environ. Microbiol. 1999, 65, 2926–2933. [Google Scholar] [CrossRef] [Green Version]
  43. Li, R.-X.; Cai, F.; Pang, G.; Shen, Q.-R.; Li, R.; Chen, W. Solubilisation of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS ONE 2015, 10, e0130081. [Google Scholar] [CrossRef] [Green Version]
  44. Colla, G.; Nardi, S.; Cardarelli, M.; Ertani, A.; Lucini, L.; Canaguier, R.; Rouphael, Y. Protein hydrolysates as biostimulants in horticulture. Sci. Hortic. 2015, 196, 28–38. [Google Scholar] [CrossRef]
  45. Haque, M.M.; Ilias, G.N.M.; Molla, A.H. Impact of Trichoderma-enriched biofertilizer on the growth and yield of mustard (Brassica rapa L.) and tomato (Solanum lycopersicon Mill.). Agriculturists 2012, 10, 109–119. [Google Scholar] [CrossRef] [Green Version]
  46. El-Katatny, M.H.; Idres, M.M. Effects of single and combined inoculations with Azospirillum brasilense and Trichoderma harzianum on seedling growth or yield parameters of wheat (Triticum vulgaris L., Giza 168) and corn (Zea mays L., hybrid 310). J. Plant Nutr. 2014, 37, 1913–1936. [Google Scholar] [CrossRef]
  47. Naznin, A.; Hossain, M.M.; Ara, K.A.; Hoque, A.; Islam, M. Influence of organic amendments and bio-control agent on yield and quality of tuberose. J. Hort. 2015, 2, 1–8. [Google Scholar]
  48. Srivastava, S.N.; Singh, V.; Awasthi, S.K. Trichoderma induced improvement in growth, yield and quality of sugarcane. Sugar Tech. 2006, 8, 166–169. [Google Scholar] [CrossRef]
  49. Tucci, M.; Ruocco, M.; de Masi, L.; de Palma, M.; Lorito, M. The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol. Plant Pathol. 2011, 12, 341–354. [Google Scholar] [CrossRef]
  50. Idowu, O.O.; Olawole, O.I.; Idumu, O.O.; Salami, A.O. Bio-control effect of Trichoderma asperellum (Samuels) Lieckf. and Glomus intraradices Schenk on okra seedlings infected with Pythium aphanidermatum (Edson) Fitzp and Erwinia carotovora (Jones). J. Exp. Agric. Int. 2016, 1–12. [Google Scholar] [CrossRef]
  51. Mahmood, A.; Kataoka, R. Potential of biopriming in enhancing crop productivity and stress tolerance. In Advances in Seed Priming; Springer: Berlin/Heidelberg, Germany, 2018; pp. 127–145. [Google Scholar]
  52. Ousley, M.A.; Lynch, J.M.; Whipps, J.M. The effects of addition of Trichoderma inocula on flowering and shoot growth of bedding plants. Sci. Hortic. 1994, 59, 147–155. [Google Scholar] [CrossRef]
  53. Asaduzzaman, M.; Alam, M.J.; Islam, M.M. Effect of Trichoderma on seed germination and seedling parameters of chili. J. Sci. Found. 2010, 8, 141–150. [Google Scholar] [CrossRef]
  54. Rawat, L.; Singh, Y.; Shukla, N.; Kumar, J. Seed biopriming with salinity tolerant isolates of Trichoderma harzianum alleviates salt stress in rice: Growth, physiological and biochemical characteristics. J. Plant Pathol. 2012, 94, 353–365. [Google Scholar]
  55. Qi, W.; Zhao, L. Study of the siderophore-producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. J. Basic Microbiol. 2013, 53, 355–364. [Google Scholar] [CrossRef] [PubMed]
  56. Brotman, Y.; Landau, U.; Cuadros-Inostroza, A.; Takayuki, T.; Fernie, A.R.; Chet, I.; Viterbo, A.; Willmitzer, L. Trichoderma-plant root colonization: Escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog. 2013, 9. [Google Scholar] [CrossRef]
  57. Ghorbanpour, A.; Salimi, A.; Ghanbary, M.A.T.; Pirdashti, H.; Dehestani, A. The effect of Trichoderma harzianum in mitigating low temperature stress in tomato (Solanum lycopersicum L.) plants. Sci. Hortic. 2018, 230, 134–141. [Google Scholar] [CrossRef]
  58. Montero-Barrientos, M.; Hermosa, R.; Cardoza, R.E.; Gutierrez, S.; Nicolas, C.; Monte, E. Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses. J. Plant Physiol. 2010, 167, 659–665. [Google Scholar] [CrossRef] [PubMed]
  59. Zhang, S.; Gan, Y.; Xu, B. Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Front. Plant Sci. 2016, 7, 1405. [Google Scholar] [CrossRef] [Green Version]
  60. Ahluwalia, V.; Kumar, J.; Rana, V.S.; Sati, O.P.; Walia, S. Comparative evaluation of two Trichoderma harzianum strains for major secondary metabolite production and antifungal activity. Nat. Prod. Res. 2015, 29, 914–920. [Google Scholar] [CrossRef]
  61. Stacey, G.; Keen, N.T. (Eds.) Plant-Microbe Interactions Vol 4; American Phytopathological Society Press: St. Paul Minnesota, MN, USA, 1999. [Google Scholar]
  62. McIntyre, M.; Nielsen, J.; Arnau, J.; van der Brink, H.; Hansen, K.; Madrid, S. Proceedings of the 7th European Conference on Fungal Genetics, Copenhagen, Denmark, 7–20 April 2004.
  63. Howell, C.R. Mechanisms employed by Trichoderma species in the biological control of plant diseases: The history and evolution of current concepts. Plant Dis. 2003, 87, 4–10. [Google Scholar] [CrossRef] [Green Version]
  64. Yedidia, I.; Benhamou, N.; Chet, I. Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl. Environ. Microbiol. 1999, 65, 1061–1070. [Google Scholar] [CrossRef] [Green Version]
  65. Harman, G.E. Myths and dogmas of biocontrol changes in perceptions derived from research on Trichoderma harzinum T-22. Plant Dis. 2000, 84, 377–393. [Google Scholar] [CrossRef] [Green Version]
  66. Li, G.-H.; Zheng, L.-J.; Liu, F.-F.; Dang, L.-Z.; Li, L.; Huang, R.; Zhang, K.-Q. New cyclopentenones from strain Trichoderma sp. YLF-3. Nat. Prod. Res. 2009, 23, 1431–1435. [Google Scholar] [CrossRef]
  67. Karuppiah, V.; Li, T.; Vallikkannu, M.; Chen, J. Co-cultivation of Trichoderma asperellum GDFS1009 and Bacillus amyloliquefaciens 1841 causes differential gene expression and improvement in the wheat growth and biocontrol activity. Front. Microbiol. 2019, 10, 1068. [Google Scholar] [CrossRef] [PubMed]
  68. Howell, C.R. Understanding the mechanisms employed by Trichoderma virens to effect biological control of cotton diseases. Phytopathology 2006, 96, 178–180. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  69. Juliatti, F.C.; Rezende, A.A.; Juliatti, B.C.M.; Morais, T.P. Trichoderma as a Biocontrol Agent against Sclerotinia Stem Rot or White Mold on Soybeans in Brazil: Usage and Technology. In Trichoderma-The Most Widely Used Fungicide; IntechOpen: London, UK, 2019. [Google Scholar]
  70. Druzhinina, I.S.; Seidl-Seiboth, V.; Herrera-Estrella, A.; Horwitz, B.A.; Kenerley, C.M.; Monte, E.; Mukherjee, P.K.; Zeilinger, S.; Grigoriev, I.V.; Kubicek, C.P. Trichoderma: The genomics of opportunistic success. Nat. Rev. Microbiol. 2011, 9, 749–759. [Google Scholar] [CrossRef] [PubMed]
  71. Harwoko, H.; Daletos, G.; Stuhldreier, F.; Lee, J.; Wesselborg, S.; Feldbrügge, M.; Müller, W.E.G.; Kalscheuer, R.; Ancheeva, E.; Proksch, P. Dithiodiketopiperazine derivatives from endophytic fungi Trichoderma harzianum and Epicoccum nigrum. Nat. Prod. Res. 2019, 1–9. [Google Scholar] [CrossRef]
  72. Weindling, R. Trichoderma lignorum as a parasite of other soil fungi. Phytopathology 1932, 22, 837–845. [Google Scholar]
  73. Fesel, P.H.; Zuccaro, A. β-glucan: Crucial component of the fungal cell wall and elusive MAMP in plants. Fungal Genet. Biol. 2016, 90, 53–60. [Google Scholar] [CrossRef] [Green Version]
  74. de La Cruz, J.; Hidalgo-Gallego, A.; Lora, J.M.; Benitez, T.; Pintor-Toro, J.A.; Llobell, A. Isolation and characterization of three chitinases from Trichoderma harzianum. Eur. J. Biochem. 1992, 206, 859–867. [Google Scholar] [CrossRef]
  75. Elad, Y.; Chet, I.; Henis, Y. Degradation of plant pathogenic fungi by Trichoderma harzianum. Can. J. Microbiol. 1982, 28, 719–725. [Google Scholar] [CrossRef]
  76. Sivan, A.; Chet, I. Degradation of fungal cell walls by lytic enzymes of Trichoderma harzianum. Microbiology 1989, 135, 675–682. [Google Scholar] [CrossRef] [Green Version]
  77. Geremia, R.A.; Goldman, G.H.; Jacobs, D.; Ardrtes, W.; Vila, S.B.; van Montagu, M.; Herrera-Estrella, A. Molecular characterization of the proteinase-encoding gene, prb1, related to mycoparasitism by Trichoderma harzianum. Mol. Microbiol. 1993, 8, 603–613. [Google Scholar] [CrossRef]
  78. Yamamoto, S.; Kobayashi, R.; Nagasaki, S. Purification and Properties of an Endo β-1, 6-Glucanase from Rhizopus chinensis R-69. Agric. Biol. Chem. 1974, 38, 1493–1500. [Google Scholar] [CrossRef] [Green Version]
  79. Chet, I.; Harman, G.E.; Baker, R. Trichoderma hamatum: Its hyphal interactions with Rhizoctonia solani and Pythium spp. Microb. Ecol. 1981, 7, 29–38. [Google Scholar] [CrossRef] [PubMed]
  80. Rombouts, F.M.; Phaff, H.J. Lysis of Yeast Cell Walls Lytic β-(1→ 6)-Glucanase from Bacillus circulans WL-12: Lytic β-(1→ 6)-Glucanase from Bacillus circulans WL-12. Eur. J. Biochem. 1976, 63, 109–120. [Google Scholar] [CrossRef] [PubMed]
  81. Zeilinger, S.; Galhaup, C.; Payer, K.; Woo, S.L.; Mach, R.L.; Fekete, C.; Lorito, M.; Kubicek, C.P. Chitinase Gene Expression during Mycoparasitic Interaction of Trichoderma harzianum with Its Host. Fungal Genet. Biol. 1999, 26, 131–140. [Google Scholar] [CrossRef] [PubMed]
  82. Brunner, K.; Peterbauer, C.K.; Mach, R.L.; Lorito, M.; Zeilinger, S.; Kubicek, C.P. The Nag1 N-acetylglucosaminidase of Trichoderma atroviride is essential for chitinase induction by chitin and of major relevance to biocontrol. Curr. Genet. 2003, 43, 289–295. [Google Scholar] [PubMed]
  83. Viterbo, A.; Montero, M.; Ramot, O.; Friesem, D.; Monte, E.; Llobell, A.; Chet, I. Expression regulation of the endochitinase chit36 from Trichoderma asperellum (T. harzianum T-203). Curr. Genet. 2002, 42, 114–122. [Google Scholar] [CrossRef]
  84. Inbar, J.; Menendez, A.N.A.; Chet, I. Hyphal interaction between Trichoderma harzianum and Sclerotinia sclerotiorum and its role in biological control. Soil Biol. Biochem. 1996, 28, 757–763. [Google Scholar] [CrossRef]
  85. Dotson, B.R.; Soltan, D.; Schmidt, J.; Areskoug, M.; Rabe, K.; Swart, C.; Widell, S.; Rasmusson, A.G. The antibiotic peptaibol alamethicin from Trichoderma permeabilises Arabidopsis root apical meristem and epidermis but is antagonized by cellulase-induced resistance to alamethicin. BMC Plant Biol. 2018, 18, 165. [Google Scholar] [CrossRef]
  86. Benitez, T.; Limon, C.; Delgado-Jarana, J.; Rey, M. Glucanolytic and other enzymes and their genes. Trichoderma Gliocladium 1998, 2, 101–127. [Google Scholar]
  87. Lorito, M. Chitinolytic enzymes and their genes. Trichoderma Gliocladium 1998, 2, 73–99. [Google Scholar]
  88. Bargaz, A.; Lyamlouli, K.; Chtouki, M.; Zeroual, Y.; Dhiba, D. Soil microbial resources for improving fertilizers efficiency in an integrated plant nutrient management system. Front. Microbiol. 2018, 9, 1606. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  89. Delgado-Jarana, J.; Moreno-Mateos, M.A.; Benítez, T. Glucose uptake in Trichoderma harzianum: Role of gtt1. Eukaryot. Cell 2003, 2, 708–717. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  90. Alabouvette, C.; Olivain, C.; Migheli, Q.; Steinberg, C. Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt-inducing Fusarium oxysporum. New Phytol. 2009, 184, 529–544. [Google Scholar] [CrossRef]
  91. Sarrocco, S.; Guidi, L.; Fambrini, S.; Degl’Innocenti, E.; Vannacci, G. Competition for cellulose exploitation between Rhizoctonia solani and two Trichoderma isolates in the decomposition of wheat straw. J. Plant Pathol. 2009, 91, 331–338. [Google Scholar]
  92. Benítez, T.; Rincón, A.M.; Limón, M.C.; Codon, A.C. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 2004, 7, 249–260. [Google Scholar]
  93. Vargas, W.A.; Mandawe, J.C.; Kenerley, C.M. Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiol. 2009, 151, 792–808. [Google Scholar] [CrossRef] [Green Version]
  94. Miethke, M. Molecular strategies of microbial iron assimilation: From high-affinity complexes to cofactor assembly systems. Metallomics 2013, 5, 15–28. [Google Scholar] [CrossRef]
  95. Srivastava, M.P.; Gupta, S.; Sharm, Y.K. Detection of siderophore production from different cultural variables by CAS-agar plate assay. Asian J. Pharm. Pharmacol. 2018, 4, 66–69. [Google Scholar] [CrossRef]
  96. Renshaw, J.C.; Robson, G.D.; Trinci, A.P.J.; Wiebe, M.G.; Livens, F.R.; Collison, D.; Taylor, R.J. Fungal siderophores: Structures, functions and applications. Mycol. Res. 2002, 106, 1123–1142. [Google Scholar] [CrossRef]
  97. Kubicek, C.P.; Herrera-Estrella, A.; Seidl-Seiboth, V.; Martinez, D.A.; Druzhinina, I.S.; Thon, M.; Zeilinger, S.; Casas-Flores, S.; Horwitz, B.A.; Mukherjee, P.K.; et al. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 2011, 12, R40. [Google Scholar] [CrossRef] [Green Version]
  98. Masi, M.; Nocera, P.; Reveglia, P.; Cimmino, A.; Evidente, A. Fungal metabolites antagonists towards plant pests and human pathogens: Structure-activity relationship studies. Molecules 2018, 23, 834. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  99. Reino, J.L.; Guerrero, R.F.; Hernández-Galán, R.; Collado, I.G. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem. Rev. 2008, 7, 89–123. [Google Scholar] [CrossRef]
  100. Hu, M.; Li, Q.-L.; Yang, Y.-B.; Liu, K.; Miao, C.-P.; Zhao, L.-X.; Ding, Z.-T. Koninginins RS from the endophytic fungus Trichoderma koningiopsis. Nat. Prod. Res. 2017, 31, 835–839. [Google Scholar] [CrossRef]
  101. Turaga, V.N.R. Peptaibols: Antimicrobial Peptides from Fungi. In Bioactive Natural Products in Drug Discovery; Springer: Berlin/Heidelberg, Germany, 2020; pp. 713–730. [Google Scholar]
  102. Howell, C.R.; Hanson, L.E.; Stipanovic, R.D.; Puckhaber, L.S. Induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. Phytopathology 2000, 90, 248–252. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  103. Mukherjee, P.K.; Horwitz, B.A.; Kenerley, C.M. Secondary metabolism in Trichoderma–a genomic perspective. Microbiology 2012, 158, 35–45. [Google Scholar] [CrossRef] [Green Version]
  104. Dunlop, R.W.; Simon, A.; Sivasithamparam, K.; Ghisalberti, E.L. An antibiotic from Trichoderma koningii active against soilborne plant pathogens. J. Nat. Prod. 1989, 52, 67–74. [Google Scholar] [CrossRef]
  105. Singh, S.; Dureja, P.; Tanwar, R.S.; Singh, A. Production and antifungal activity of secondary metabolites of Trichoderma virens. Pestic. Res. J. 2005, 17, 26–29. [Google Scholar]
  106. Manganiello, G.; Sacco, A.; Ercolano, M.R.; Vinale, F.; Lanzuise, S.; Pascale, A.; Napolitano, M.; Lombardi, N.; Lorito, M.; Woo, S.L. Modulation of tomato response to Rhizoctonia solani by Trichoderma harzianum and its secondary metabolite harzianic acid. Front. Microbiol. 2018, 9, 1966. [Google Scholar] [CrossRef]
  107. Brito, J.P.C.; Ramada, M.H.S.; de Magalhães, M.T.Q.; Silva, L.P.; Ulhoa, C.J. Peptaibols from Trichoderma asperellum TR356 strain isolated from Brazilian soil. SpringerPlus 2014, 3, 1–10. [Google Scholar] [CrossRef] [Green Version]
  108. Monte, E. Understanding Trichoderma: Between biotechnology and microbial ecology. Int. Microbiol. 2001, 4, 1–4. [Google Scholar]
  109. Zeilinger, S.; Reithner, B.; Scala, V.; Peissl, I.; Lorito, M.; Mach, R.L. Signal transduction by Tga3, a novel G protein α subunit of Trichoderma atroviride. Appl. Environ. Microbiol. 2005, 71, 1591–1597. [Google Scholar] [CrossRef] [Green Version]
  110. Omann, M.R.; Lehner, S.; Rodr\’\iguez, C.E.; Brunner, K.; Zeilinger, S. The seven-transmembrane receptor Gpr1 governs processes relevant for the antagonistic interaction of Trichoderma atroviride with its host. Microbiology 2012, 158, 107. [Google Scholar] [CrossRef] [PubMed]
  111. Reithner, B.; Schuhmacher, R.; Stoppacher, N.; Pucher, M.; Brunner, K.; Zeilinger, S. Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk1 differentially affects mycoparasitism and plant protection. Fungal Genet. Biol. 2007, 44, 1123–1133. [Google Scholar] [CrossRef] [Green Version]
  112. Kumar, A.; Scher, K.; Mukherjee, M.; Pardovitz-Kedmi, E.; Sible, G.V.; Singh, U.S.; Kale, S.P.; Mukherjee, P.K.; Horwitz, B.A. Overlapping and distinct functions of two Trichoderma virens MAP kinases in cell-wall integrity, antagonistic properties and repression of conidiation. Biochem. Biophys. Res. Commun. 2010, 398, 765–770. [Google Scholar] [CrossRef]
  113. Singh, A.; Shukla, N.; Kabadwal, B.; Tewari, A.; Kumar, J. Review on plant-Trichoderma-pathogen interaction. Int. J. Curr. Microbiol. Appl. Sci. 2018, 7, 2382–2397. [Google Scholar] [CrossRef]
  114. El-Hasan, A.; Walker, F.; Buchenauer, H. Trichoderma harzianum and its metabolite 6-pentyl-alpha-pyrone suppress fusaric acid produced by Fusarium moniliforme. J. Phytopathol. 2008, 156, 79–87. [Google Scholar] [CrossRef]
  115. Mukherjee, P.K.; Wiest, A.; Ruiz, N.; Keightley, A.; Moran-Diez, M.E.; McCluskey, K.; Pouchus, Y.F.; Kenerley, C.M. Two classes of new peptaibols are synthesized by a single non-ribosomal peptide synthetase of Trichoderma virens. J. Biol. Chem. 2011, 286, 4544–4554. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  116. Shi, M.; Chen, L.; Wang, X.-W.; Zhang, T.; Zhao, P.-B.; Song, X.-Y.; Sun, C.-Y.; Chen, X.-L.; Zhou, B.-C.; Zhang, Y.-Z. Antimicrobial peptaibols from Trichoderma pseudokoningii induce programmed cell death in plant fungal pathogens. Microbiology 2012, 158, 166–175. [Google Scholar] [CrossRef] [Green Version]
  117. Tijerino, A.; Cardoza, R.E.; Moraga, J.; Malmierca, M.G.; Vicente, F.; Aleu, J.; Collado, I.G.; Gutiérrez, S.; Monte, E.; Hermosa, R. Overexpression of the trichodiene synthase gene tri5 increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Fungal Genet. Biol. 2011, 48, 285–296. [Google Scholar] [CrossRef]
  118. Brotman, Y.; Lisec, J.; Méret, M.; Chet, I.; Willmitzer, L.; Viterbo, A. Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 2012, 158, 139–146. [Google Scholar] [CrossRef] [Green Version]
  119. Bae, H.; Sicher, R.C.; Kim, M.S.; Kim, S.-H.; Strem, M.D.; Melnick, R.L.; Bailey, B.A. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J. Exp. Bot. 2009, 60, 3279–3295. [Google Scholar] [CrossRef] [PubMed]
  120. Strakowska, J.; Błaszczyk, L.; Chełkowski, J. The significance of cellulolytic enzymes produced by Trichoderma in opportunistic lifestyle of this fungus. J. Basic Microbiol. 2014, 54, S2–S13. [Google Scholar] [CrossRef] [PubMed]
  121. Kour, D.; Rana, K.L.; Kaur, T.; Singh, B.; Chauhan, V.S.; Kumar, A.; Rastegari, A.A.; Yadav, N.; Yadav, A.N.; Gupta, V.K. Extremophiles for Hydrolytic Enzymes Productions: Biodiversity and Potential Biotechnological Applications. Bioprocess. Biomol. Prod. 2019, 321–372. [Google Scholar] [CrossRef]
  122. Khatabi, B.; Molitor, A.; Lindermayr, C.; Pfiffi, S.; Durner, J.; von Wettstein, D.; Kogel, K.-H.; Schäfer, P. Ethylene supports colonization of plant roots by the mutualistic fungus Piriformospora indica. PLoS ONE 2012, 7, e35502. [Google Scholar] [CrossRef]
  123. Djonović, S.; Pozo, M.J.; Dangott, L.J.; Howell, C.R.; Kenerley, C.M. Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol. Plant-Microbe Interact. 2006, 19, 838–853. [Google Scholar] [CrossRef] [Green Version]
  124. Gupta, K.J.; Mur, L.A.J.; Brotman, Y. Trichoderma asperelloides suppresses nitric oxide generation elicited by Fusarium oxysporum in Arabidopsis roots. Mol. Plant-Microbe Interact. 2014, 27, 307–314. [Google Scholar] [CrossRef] [Green Version]
  125. Contreras-Cornejo, H.A.; Macías-Rodríguez, L.; López-Bucio, J.S.; López-Bucio, J. Enhanced plant immunity using Trichoderma. In BioTechnology and Biology of Trichoderma; Elsevier: Amsterdam, The Netherlands, 2014; pp. 495–504. [Google Scholar]
  126. Jagodzik, P.; Tajdel-Zielinska, M.; Ciesla, A.; Marczak, M.; Ludwikow, A. Mitogen-activated protein kinase cascades in plant hormone signaling. Front. Plant Sci. 2018, 9, 1387. [Google Scholar] [CrossRef]
  127. Shoresh, M.; Gal-On, A.; Leibman, D.; Chet, I. Characterization of a mitogen-activated protein kinase gene from cucumber required for Trichoderma-conferred plant resistance. Plant Physiol. 2006, 142, 1169–1179. [Google Scholar] [CrossRef] [Green Version]
  128. Contreras-Cornejo, H.A.; Macías-Rodríguez, L.; Beltrán-Peña, E.; Herrera-Estrella, A.; López-Bucio, J. Trichoderma-induced plant immunity likely involves both hormonal-and camalexin-dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea. Plant Signal. Behav. 2011, 6, 1554–1563. [Google Scholar] [CrossRef] [Green Version]
  129. Salas-Marina, M.A.; Silva-Flores, M.A.; Uresti-Rivera, E.E.; Castro-Longoria, E.; Herrera-Estrella, A.; Casas-Flores, S. Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur. J. Plant Pathol. 2011, 131, 15–26. [Google Scholar] [CrossRef]
  130. Martínez-Medina, A.; Pascual, J.A.; Pérez-Alfocea, F.; Albacete, A.; Roldán, A. Trichoderma harzianum and Glomus intraradices modify the hormone disruption induced by Fusarium oxysporum infection in melon plants. Phytopathology 2010, 100, 682–688. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  131. Shoresh, M.; Yedidia, I.; Chet, I. Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 2005, 95, 76–84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  132. Piel, J.; Atzorn, R.; Gäbler, R.; Kühnemann, F.; Boland, W. Cellulysin from the plant parasitic fungus Trichoderma viride elicits volatile biosynthesis in higher plants via the octadecanoid signalling cascade. FEBS Lett. 1997, 416, 143–148. [Google Scholar] [CrossRef] [Green Version]
  133. Sharon, A.; Fuchs, Y.; Anderson, J.D. The elicitation of ethylene biosynthesis by a Trichoderma xylanase is not related to the cell wall degradation activity of the enzyme. Plant Physiol. 1993, 102, 1325–1329. [Google Scholar] [CrossRef] [PubMed]
  134. Kieber, J.J.; Polko, J.K. 1-aminocyclopropane 1-carboxylic acid and its emerging role as an ethylene-independent growth regulator. Front. Plant Sci. 2019, 10, 1602. [Google Scholar]
  135. Kurusu, T.; Hamada, J.; Nokajima, H.; Kitagawa, Y.; Kiyoduka, M.; Takahashi, A.; Hanamata, S.; Ohno, R.; Hayashi, T.; Okada, K.; et al. Regulation of microbe-associated molecular pattern-induced hypersensitive cell death, phytoalexin production, and defense gene expression by calcineurin B-like protein-interacting protein kinases, OsCIPK14/15, in rice cultured cells. Plant Physiol. 2010, 153, 678–692. [Google Scholar] [CrossRef] [Green Version]
  136. Yoshikuni, Y.; Martin, V.J.J.; Ferrin, T.E.; Keasling, J.D. Engineering cotton (+)-δ-cadinene synthase to an altered function: Germacrene D-4-ol synthase. Chem. Biol. 2006, 13, 91–98. [Google Scholar] [CrossRef] [Green Version]
  137. Guzmán-Guzmán, P.; Porras-Troncoso, M.D.; Olmedo-Monfil, V.; Herrera-Estrella, A. Trichoderma species: Versatile plant symbionts. Phytopathology 2019, 109, 6–16. [Google Scholar] [CrossRef] [Green Version]
  138. Pieterse, C.M.J.; der Does, D.; Zamioudis, C.; Leon-Reyes, A.; van Wees, S.C.M. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 2012, 28, 489–521. [Google Scholar] [CrossRef] [Green Version]
  139. Mukherjee, P.K.; Horwitz, B.A.; Herrera-Estrella, A.; Schmoll, M.; Kenerley, C.M. Trichoderma research in the genome era. Annu. Rev. Phytopathol. 2013, 51, 105–129. [Google Scholar] [CrossRef]
  140. Wang, K.L.-C.; Li, H.; Ecker, J.R. Ethylene biosynthesis and signaling networks. Plant Cell 2002, 14, S131–S151. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  141. Yoshioka, Y.; Ichikawa, H.; Naznin, H.A.; Kogure, A.; Hyakumachi, M. Systemic resistance induced in Arabidopsis thaliana by Trichoderma asperellum SKT-1, a microbial pesticide of seedborne diseases of rice. Pest. Manag. Sci. 2012, 68, 60–66. [Google Scholar] [CrossRef] [PubMed]
  142. Ruocco, M.; Lanzuise, S.; Lombardi, N.; Woo, S.L.; Vinale, F.; Marra, R.; Varlese, R.; Manganiello, G.; Pascale, A.; Scala, V.; et al. Multiple roles and effects of a novel Trichoderma hydrophobin. Mol. Plant-Microbe Interact. 2015, 28, 167–179. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  143. Seyfferth, C.; Tsuda, K. Salicylic acid signal transduction: The initiation of biosynthesis, perception and transcriptional reprogramming. Front. Plant Sci. 2014, 5, 697. [Google Scholar] [CrossRef] [Green Version]
  144. Vázquez-Garcidueñas, S.; Leal-Morales, C.A.; Herrera-Estrella, A. Analysis of the β-1, 3-glucanolytic system of the biocontrol agent Trichoderma harzianum. Appl. Environ. Microbiol. 1998, 64, 1442–1446. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  145. Okada, H.; Tada, K.; Sekiya, T.; Yokoyama, K.; Takahashi, A.; Tohda, H.; Kumagai, H.; Morikawa, Y. Molecular characterization and heterologous expression of the gene encoding a low-molecular-mass endoglucanase from Trichoderma reesei QM9414. Appl. Environ. Microbiol. 1998, 64, 555–563. [Google Scholar] [CrossRef] [Green Version]
  146. Sandgren, M.; Shaw, A.; Ropp, T.H.; Wu, S.; Bott, R.; Cameron, A.D.; Ståhlberg, J.; Mitchinson, C.; Jones, T.A. The X-ray crystal structure of the Trichoderma reesei family 12 endoglucanase 3, Cel12A, at 1.9 Å resolution. J. Mol. Biol. 2001, 308, 295–310. [Google Scholar] [CrossRef]
  147. Li, X.; Zhang, P.; Wang, M.; Zhou, F.; Malik, F.A.; Yang, H.; Bhaskar, R.; Hu, J.; Sun, C.; Miao, Y. Expression of Trichoderma viride endoglucanase III in the larvae of silkworm, Bombyx mori L. and characteristic analysis of the recombinant protein. Mol. Biol. Rep. 2011, 38, 3897–3902. [Google Scholar] [CrossRef]
  148. Chandra, M.; Kalra, A.; Sangwan, N.S.; Sangwan, R.S. Biochemical and proteomic characterization of a novel extracellular β-glucosidase from Trichoderma citrinoviride. Mol. Biotechnol. 2013, 53, 289–299. [Google Scholar] [CrossRef]
  149. Sternberg, D.; Vuayakumar, P.; Reese, E.T. β-Glucosidase: Microbial production and effect on enzymatic hydrolysis of cellulose. Can. J. Microbiol. 1977, 23, 139–147. [Google Scholar] [CrossRef] [PubMed]
  150. Wong, K.K.Y.; Saddler, J.N. Trichoderma xylanases, their properties and application. Crit. Rev. Biotechnol. 1992, 12, 413–435. [Google Scholar] [CrossRef]
  151. Lorito, M.; Harman, G.E.; Hayes, C.K.; Broadway, R.M.; Tronsmo, A.; Woo, S.L.; di Pietro, A. Chitinolytic enzymes produced by Trichoderma harzianum: Antifungal activity of purified endochitinase and chitobiosidase. Phytopathology 1993, 83, 302–307. [Google Scholar] [CrossRef]
  152. Peterbauer, C.K.; Lorito, M.; Hayes, C.K.; Harman, G.E.; Kubicek, C.P. Molecular cloning and expression of the nag1 gene (N-acetyl-β-D-glucosaminidase-encoding gene) from Trichoderma harzianum P1. Curr. Genet. 1996, 30, 325–331. [Google Scholar] [CrossRef] [PubMed]
  153. Kim, D.-J.; Baek, J.-M.; Uribe, P.; Kenerley, C.M.; Cook, D.R. Cloning and characterization of multiple glycosyl hydrolase genes from Trichoderma virens. Curr. Genet. 2002, 40, 374–384. [Google Scholar] [CrossRef]
  154. Harman, G.E.; Hayes, C.K.; Lorito, M.; Broadway, R.M.; di Pietro, A.; Peterbauer, C.; Tronsmo, A. Chitinolytic enzymes of Trichoderma harzianum: Purification of chitobiosidase and endochitinase. Phytopathology 1993, 83, 313–318. [Google Scholar] [CrossRef]
  155. Flores, A.; Chet, I.; Herrera-Estrella, A. Improved biocontrol activity of Trichoderma harzianum by over-expression of the proteinase-encoding gene prb1. Curr. Genet. 1997, 31, 30–37. [Google Scholar] [CrossRef]
  156. Goldman, M.H.S.; Goldman, G.H. Trichoderma harzianum transformant has high extracellular alkaline proteinase expression during specific mycoparasitic interactions. Genet. Mol. Biol. 1998, 21. [Google Scholar] [CrossRef]
  157. Bhale, U.N.; Rajkonda, J.N. Enzymatic activity of Trichoderma species. Nov. Nat. Sci. Res. 2012, 1, 1–8. [Google Scholar]
  158. Mastouri, F.; Björkman, T.; Harman, G.E. Trichoderma harzianum enhances antioxidant defense of tomato seedlings and resistance to water deficit. Mol. Plant-Microbe Interact. 2012, 25, 1264–1271. [Google Scholar] [CrossRef] [Green Version]
  159. Suriani Ribeiro, M.; de Paula, R.; Raquel Voltan, A.; de Castro, R.G.; Carraro, C.B.; de Assis, L.; Stecca Steindorff, A.; Goldman, G.H.; Silva, R.N.; Ulhoa, C.J.; et al. Endo-β-1, 3-glucanase (GH16 Family) from Trichoderma harzianum Participates in Cell Wall Biogenesis but Is Not Essential for Antagonism Against Plant Pathogens. Biomolecules 2019, 9, 781. [Google Scholar] [CrossRef] [Green Version]
  160. Sharma, V.; Salwan, R.; Al-Ani, L.K.T. Molecular Aspects of Plant Beneficial Microbes in Agriculture; Academic Press: Cambridge, MA, USA, 2020. [Google Scholar]
  161. Cardoza, R.-E.; Hermosa, M.-R.; Vizcaíno, J.-A.; Sanz, L.; Monte, E.; Gutiérrez, S. Secondary metabolites produced by Trichoderma and their importance in the biocontrol process. Microorg. Ind. Enzym. Biocontrol 2005, 1–22. [Google Scholar]
  162. Vinale, F.; Girona, I.A.; Nigro, M.; Mazzei, P.; Piccolo, A.; Ruocco, M.; Woo, S.; Rosa, D.R.; Herrera, C.L.; Lorito, M. Cerinolactone, a hydroxy-lactone derivative from Trichoderma cerinum. J. Nat. Prod. 2012, 75, 103–106. [Google Scholar] [CrossRef] [PubMed]
  163. Pyke, T.R.; Dietz, A. U-21,963, a New Antibiotic: I. Discovery and Biological Activity. Appl. Environ. Microbiol. 1966, 14, 506–510. [Google Scholar] [CrossRef] [Green Version]
  164. Almassi, F.; Ghisalberti, E.L.; Narbey, M.J.; Sivasithamparam, K. New antibiotics from strains of Trichoderma harzianum. J. Nat. Prod. 1991, 54, 396–402. [Google Scholar] [CrossRef]
  165. Ghisalberti, E.L.; Rowland, C.Y. Antifungal metabolites from Trichoderma harzianum. J. Nat. Prod. 1993, 56, 1799–1804. [Google Scholar] [CrossRef]
  166. Garo, E.; Starks, C.M.; Jensen, P.R.; Fenical, W.; Lobkovsky, E.; Clardy, J. Trichodermamides A and B, cytotoxic modified dipeptides from the marine-derived fungus Trichoderma virens. J. Nat. Prod. 2003, 66, 423–426. [Google Scholar] [CrossRef]
  167. Liu, R.; Gu, Q.-Q.; Zhu, W.-M.; Cui, C.-B.; Fan, G.-T. Trichodermamide A and aspergillazine A, two cytotoxic modified dipeptides from a marine-derived fungus Spicaria elegans. Arch. Pharm. Res. 2005, 28, 1042–1046. [Google Scholar] [CrossRef]
  168. Brian, P.W.; McGowan, J.G. Viridin: A highly fungistatic substance produced by Trichoderma viride. Nature 1945, 156, 144–145. [Google Scholar] [CrossRef]
  169. Sivasithamparam, K.; Ghisalberti, E.L. Secondary metabolism in Trichoderma. Trichoderma Gliocladium. Vol 1 Basic Biol. Taxon. Genet. 2002, 1, 139. [Google Scholar]
  170. Dickinson, J.M.; Hanson, J.R.; Hitchcock, P.B.; Claydon, N. Structure and biosynthesis of harzianopyridone, an antifungal metabolite of Trichoderma harzianum. J. Chem. Soc. Perkin Trans. 1989, 1, 1885–1887. [Google Scholar] [CrossRef]
  171. Vinale, F.; Marra, R.; Scala, F.; Ghisalberti, E.L.; Lorito, M.; Sivasithamparam, K. Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett. Appl. Microbiol. 2006, 43, 143–148. [Google Scholar] [CrossRef] [PubMed]
  172. Vinale, F.; Flematti, G.; Sivasithamparam, K.; Lorito, M.; Marra, R.; Skelton, B.W.; Ghisalberti, E.L. Harzianic acid, an antifungal and plant growth promoting metabolite from Trichoderma harzianum. J. Nat. Prod. 2009, 72, 2032–2035. [Google Scholar] [CrossRef] [PubMed]
  173. Vinale, F.; Strakowska, J.; Mazzei, P.; Piccolo, A.; Marra, R.; Lombardi, N.; Manganiello, G.; Pascale, A.; Woo, S.L.; Lorito, M. Cremenolide, a new antifungal, 10-member lactone from Trichoderma cremeum with plant growth promotion activity. Nat. Prod. Res. 2016, 30, 2575–2581. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  174. Zou, J.-X.; Song, Y.-P.; Ji, N.-Y. Deoxytrichodermaerin, a harziane lactone from the marine algicolous fungus Trichoderma longibrachiatum A-WH-20-2. Nat. Prod. Res. 2019, 1–6. [Google Scholar] [CrossRef] [PubMed]
  175. Meyer, C.E. U-21,963, a New Antibiotic: II. Isolation and Characterization. Appl. Environ. Microbiol. 1966, 14, 511–512. [Google Scholar] [CrossRef] [Green Version]
  176. Tamura, A.; Kotani, H.; Naruto, S. Trichoviridin and dermadin from Trichoderma sp. TK-1. J. Antibiot. 1975, 28, 161–162. [Google Scholar] [CrossRef] [Green Version]
  177. Howell, C.R. Selective isolation from soil and separation in vitro of P and Q strains of Trichoderma virens with differential media. Mycologia 1999, 91, 930–934. [Google Scholar] [CrossRef]
  178. Rippa, S.; Eid, M.; Formaggio, F.; Toniolo, C.; Béven, L. Hypersensitive-Like Response to the Pore-Former Peptaibol Alamethicin in Arabidopsis Thaliana. ChemBioChem 2010, 11, 2042–2049. [Google Scholar] [CrossRef]
  179. Shi, W.-L.; Chen, X.-L.; Wang, L.-X.; Gong, Z.-T.; Li, S.; Li, C.-L.; Xie, B.-B.; Zhang, W.; Shi, M.; Li, C.; et al. Cellular and molecular insight into the inhibition of primary root growth of Arabidopsis induced by peptaibols, a class of linear peptide antibiotics mainly produced by Trichoderma spp. J. Exp. Bot. 2016, 67, 2191–2205. [Google Scholar] [CrossRef] [Green Version]
  180. Mukherjee, P.K.; Buensanteai, N.; Moran-Diez, M.E.; Druzhinina, I.S.; Kenerley, C.M. Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize. Microbiology 2012, 158, 155–165. [Google Scholar] [CrossRef] [Green Version]
  181. Pang, X.; Lin, X.; Tian, Y.; Liang, R.; Wang, J.; Yang, B.; Zhou, X.; Kaliyaperumal, K.; Luo, X.; Tu, Z.; et al. Three new polyketides from the marine sponge-derived fungus Trichoderma sp. SCSIO41004. Nat. Prod. Res. 2018, 32, 105–111. [Google Scholar] [CrossRef] [PubMed]
  182. Ramírez-Valdespino, C.A.; Porras-Troncoso, M.D.; Corrales-Escobosa, A.R.; Wrobel, K.; Mart\’\inez-Hernández, P.; Olmedo-Monfil, V. Functional characterization of TvCyt2, a member of the p450 monooxygenases from Trichoderma virens relevant during the association with plants and mycoparasitism. Mol. Plant-Microbe Interact. 2018, 31, 289–298. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  183. Fang, S.-T.; Wang, Y.-J.; Ma, X.-Y.; Yin, X.-L.; Ji, N.-Y. Two new sesquiterpenoids from the marine-sediment-derived fungus Trichoderma harzianum P1-4. Nat. Prod. Res. 2019, 33, 3127–3133. [Google Scholar] [CrossRef] [PubMed]
  184. Liang, X.-R.; Miao, F.-P.; Song, Y.-P.; Guo, Z.-Y.; Ji, N.-Y. Trichocitrin, a new fusicoccane diterpene from the marine brown alga-endophytic fungus Trichoderma citrinoviride cf-27. Nat. Prod. Res. 2016, 30, 1605–1610. [Google Scholar] [CrossRef] [PubMed]
  185. Liang, X.-R.; Ma, X.-Y.; Ji, N.-Y. Trichosordarin A, a norditerpene glycoside from the marine-derived fungus Trichoderma harzianum R5. Nat. Prod. Res. 2019, 1–6. [Google Scholar] [CrossRef]
  186. Schenkel, D.; Lemfack, M.C.; Piechulla, B.; Splivallo, R. A meta-analysis approach for assessing the diversity and specificity of belowground root and microbial volatiles. Front. Plant Sci. 2015, 6, 707. [Google Scholar] [CrossRef]
  187. Malmierca, M.G.; McCormick, S.P.; Cardoza, R.E.; Alexander, N.J.; Monte, E.; Gutiérrez, S. Production of trichodiene by Trichoderma harzianum alters the perception of this biocontrol strain by plants and antagonized fungi. Environ. Microbiol. 2015, 17, 2628–2646. [Google Scholar] [CrossRef]
  188. Cruz-Magalhães, V.; Nieto-Jacobo, M.F.; van Zijll de Jong, E.; Rostás, M.; Padilla-Arizmendi, F.; Kandula, D.; Kandula, J.; Hampton, J.; Herrera-Estrella, A.; Steyaert, J.M.; et al. The NADPH oxidases Nox1 and Nox2 differentially regulate volatile organic compounds, fungistatic activity, plant growth promotion and nutrient assimilation in Trichoderma atroviride. Front. Microbiol. 2019, 9, 3271. [Google Scholar] [CrossRef] [Green Version]
  189. Guzmán-Guzmán, P.; Alemán-Duarte, M.I.; Delaye, L.; Herrera-Estrella, A.; Olmedo-Monfil, V. Identification of effector-like proteins in Trichoderma spp. and role of a hydrophobin in the plant-fungus interaction and mycoparasitism. BMC Genet. 2017, 18, 16. [Google Scholar] [CrossRef] [Green Version]
  190. Huang, Y.; Mijiti, G.; Wang, Z.; Yu, W.; Fan, H.; Zhang, R.; Liu, Z. Functional analysis of the class II hydrophobin gene HFB2-6 from the biocontrol agent Trichoderma asperellum ACCC30536. Microbiol. Res. 2015, 171, 8–20. [Google Scholar] [CrossRef]
  191. Huang, Y.; Xiao, L.; Li, F.; Xiao, M.; Lin, D.; Long, X.; Wu, Z. Microbial degradation of pesticide residues and an emphasis on the degradation of cypermethrin and 3-phenoxy benzoic acid: A review. Molecules 2018, 23, 2313. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  192. Katayama, A.; Matsumura, F. Photochemically enhanced microbial degradation of environmental pollutants. Environ. Sci. Technol. 1991, 25, 1329–1333. [Google Scholar] [CrossRef]
  193. Bishnoi, N.R.; Kumar, R.; Bishnoi, K. Biosorption of Cr (VI) with Trichoderma viride immobilized fungal biomass and cell free Ca-alginate beads. Indian J. Exp. Biol. 2007, 45, 657–664. [Google Scholar] [PubMed]
  194. Morales-Barrera, L.; Cristiani-Urbina, E. Hexavalent chromium removal by a Trichoderma inhamatum fungal strain isolated from tannery effluent. Water Air Soil Pollut. 2008, 187, 327–336. [Google Scholar] [CrossRef]
  195. Faedda, R.; Puglisi, I.; Sanzaro, V.; Petrone, G.; Cacciola, S.O. Expression of genes of Trichoderma harzianum in response to the presence of cadmium in the substrate. Nat. Prod. Res. 2012, 26, 2301–2308. [Google Scholar] [CrossRef]
  196. Ying, W.; Shi, Z.; Yang, H.; Xu, G.; Zheng, Z.; Yang, J. Effect of alkaline lignin modification on cellulase–lignin interactions and enzymatic saccharification yield. BioTechnol. Biofuels 2018, 11, 214. [Google Scholar] [CrossRef]
  197. Shafique, S.; Bajwa, R.; Shafique, S. Molecular characterisation of UV and chemically induced mutants of Trichoderma reesei FCBP-364. Nat. Prod. Res. 2010, 24, 1438–1448. [Google Scholar] [CrossRef]
  198. Wiater, A.; Szczodrak, J.; Pleszczyńska, M. Optimization of conditions for the efficient production of mutants in streptococcal cultures and post-culture liquids. Acta Biol. Hung. 2005, 56, 137–150. [Google Scholar] [CrossRef]
  199. Sharma, A.; Sharma, P.; Singh, J.; Singh, S.; Nain, L. Prospecting the Potential of Agroresidues as Substrate for Microbial Flavor Production. Front. Sustain. Food Syst. 2020, 4, 18. [Google Scholar] [CrossRef] [Green Version]
  200. Marra, R.; Nicoletti, R.; Pagano, E.; DellaGreca, M.; Salvatore, M.M.; Borrelli, F.; Lombardi, N.; Vinale, F.; Woo, S.L.; Andolfi, A. Inhibitory effect of trichodermanone C, a sorbicillinoid produced by Trichoderma citrinoviride associated to the green alga Cladophora sp., on nitrite production in LPS-stimulated macrophages. Nat. Prod. Res. 2019, 33, 3389–3397. [Google Scholar] [CrossRef]
  201. Phuwapraisirisan, P.; Rangsan, J.; Siripong, P.; Tip-Pyang, S. 9-epi-Viridiol, a novel cytotoxic furanosteroid from soil fungus Trichoderma virens. Nat. Prod. Res. 2006, 20, 1321–1325. [Google Scholar] [CrossRef] [PubMed]
  202. Zhang, L.; Niaz, S.I.; Wang, Z.; Zhu, Y.; Lin, Y.; Li, J.; Liu, L. α-Glucosidase inhibitory and cytotoxic botryorhodines from mangrove endophytic fungus Trichoderma sp. 307. Nat. Prod. Res. 2018, 32, 2887–2892. [Google Scholar] [CrossRef] [PubMed]
  203. Han, M.; Qin, D.; Ye, T.; Yan, X.; Wang, J.; Duan, X.; Dong, J. An endophytic fungus from Trichoderma harzianum SWUKD3. 1610 that produces nigranoic acid and its analogues. Nat. Prod. Res. 2019, 33, 2079–2087. [Google Scholar] [CrossRef] [PubMed]
  204. Iqtedar, M.; Nadeem, M.; Naeem, H.; Abdullah, R.; Naz, S.; Syed, Q.U.A.; Kaleem, A. Bioconversion potential of Trichoderma viride HN1 cellulase for a lignocellulosic biomass Saccharum spontaneum. Nat. Prod. Res. 2015, 29, 1012–1019. [Google Scholar] [CrossRef]
  205. Arthe, R.; Rajesh, R.; Rajesh, E.M.; Rajendran, R.; Jeyachandran, S. Production of bio-ethanol from cellulosic cotton waste through microbial extracellular enzymatic hydrolysis and fermentation. Electron. J. Environ. Agric. Food chem. 2008, 7, 2948–2958. [Google Scholar]
  206. Schuster, A.; Schmoll, M. Biology and biotechnology of Trichoderma. Appl. Microbiol. Biotechnol. 2010, 87, 787–799. [Google Scholar] [CrossRef] [Green Version]
  207. Rowell, R.M. Chemical modification of wood: Advantages and disadvantages. In Proceedings of the American Wood-Preservers’ Association, San Francisco, CA, USA, 28–30 April 1975; Volume 71, pp. 41–51. [Google Scholar]
  208. Rai, P.K.; Lee, S.S.; Zhang, M.; Tsang, Y.F.; Kim, K.-H. Heavy metals in food crops: Health risks, fate, mechanisms, and management. Environ. Int. 2019, 125, 365–385. [Google Scholar] [CrossRef]
  209. Lebow, S. Leaching of Wood Preservative Components and Their Mobility in the Environment: Summary of Pertinent Literature; (General Technical Report FPL; GTR-93): 36 p.; 28 cm; United States Department of Agriculture: Washington, DC, USA, 1996; Volume 93.
  210. Hingston, J.A.; Collins, C.D.; Murphy, R.J.; Lester, J.N. Leaching of chromated copper arsenate wood preservatives: A review. Environ. Pollut. 2001, 111, 53–66. [Google Scholar] [CrossRef]
  211. Schultz, T.P.; Militz, H.; Freeman, M.H.; Goodell, B.; Nicholas, D.D. Development of Commercial Wood Preservatives: Efficacy, Environmental, and Health Issues. ACS Sympos. Ser. 2008, 982, 655. [Google Scholar]
  212. Namyslo, J.C.; Kaufmann, D.E. Chemical improvement of surfaces. Part 1: Novel functional modification of wood with covalently bound organoboron compounds. Holzforschung 2009, 63, 627–632. [Google Scholar] [CrossRef]
  213. Verma, P.; Junga, U.; Militz, H.; Mai, C. Protection mechanisms of DMDHEU treated wood against white and brown rot fungi. Holzforschung 2009, 63, 371–378. [Google Scholar] [CrossRef]
  214. Lee, M.J.; Cooper, P. Copper monoethanolamine adsorption in wood and its relation with cation exchange capacity (CEC). Holzforschung 2010, 64, 653–658. [Google Scholar] [CrossRef]
  215. Pilgård, A.; Alfredsen, G.; Hietala, A. Quantification of fungal colonization in modified wood: Quantitative real-time PCR as a tool for studies on Trametes versicolor. Holzforschung 2010, 64, 645–651. [Google Scholar] [CrossRef]
  216. Robinson, S.C.; Laks, P.E. The effects of subthreshold loadings of tebuconazole, DDAC, and boric acid on wood decay by Postia placenta. Holzforschung 2010, 64, 537–543. [Google Scholar] [CrossRef]
  217. Chirkova, J.; Andersone, I.; Irbe, I.; Spince, B.; Andersons, B. Lignins as agents for bio-protection of wood. Holzforschung 2011, 65, 497–502. [Google Scholar] [CrossRef]
  218. Freitag, C.; Morrell, J.J.; Love, C.S. Long-term performance of fused borate rods for limiting internal decay in Douglas-fir utility poles. Holzforschung 2011, 65, 429–434. [Google Scholar] [CrossRef]
  219. Pankras, S.; Cooper, P.A. Effect of ammonia addition to alkaline copper quaternary wood preservative solution on the distribution of copper complexes and leaching. Holzforschung 2012, 66, 397–406. [Google Scholar] [CrossRef]
  220. Schultz, T.P.; Nicholas, D.D. Relative fungal efficacy results from the soil block test with a long incubation period of three commercial copper wood preservatives. Holzforschung 2012, 66, 245–250. [Google Scholar] [CrossRef]
  221. Ejechi, B.O. Biological control of wood decay in an open tropical environment with Penicillium sp. and Trichoderma viride. Int. Biodeterior. Biodegrad. 1997, 39, 295–299. [Google Scholar] [CrossRef]
  222. Tucker, E.J.B.; Bruce, A.; Staines, H.J. Application of modified international wood preservative chemical testing standards for assessment of biocontrol treatments. Int. Biodeterior. Biodegrad. 1997, 39, 189–197. [Google Scholar] [CrossRef]
  223. Mortuza, M.G.; Ilag, L.L. Potential for biocontrol of Lasiodiplodia theobromae (Pat.) Griff. & Maubl. in banana fruits by Trichoderma species. Biol. Control. 1999, 15, 235–240. [Google Scholar]
  224. Batta, Y.A. Effect of treatment with Trichoderma harzianum Rifai formulated in invert emulsion on postharvest decay of apple blue mold. Int. J. Food microbiol. 2004, 96, 281–288. [Google Scholar] [CrossRef] [PubMed]
  225. Batta, Y.A. Postharvest biological control of apple gray mold by Trichoderma harzianum Rifai formulated in an invert emulsion. Crop Prot. 2004, 23, 19–26. [Google Scholar] [CrossRef]
  226. Bankole, S.A.; Adebanjo, A. Biocontrol of brown blotch of cowpea caused by Colletotrichum truncatum with Trichoderma viride. Crop Prot. 1996, 15, 633–636. [Google Scholar] [CrossRef]
Figure 1. Depicts pictorially the impacts of Trichoderma spp. on plants in rhizosphere. Presence of Trichoderma improved the plant growth and development at physiological and biochemical levels. Further, Trichoderma spp. raised the plant resistance towards several biotic as well as abiotic stresses through multiple adaptive mechanisms.
Figure 1. Depicts pictorially the impacts of Trichoderma spp. on plants in rhizosphere. Presence of Trichoderma improved the plant growth and development at physiological and biochemical levels. Further, Trichoderma spp. raised the plant resistance towards several biotic as well as abiotic stresses through multiple adaptive mechanisms.
Plants 09 00762 g001
Figure 2. In plant rhizosphere Trichoderma produces a siderophore which chelates insoluble Fe (Fe3+) and facilitate its conversion to soluble Fe (Fe2+) form. By doing this, Trichoderma also make Fe source unavailable to pathogenic fungi and thereby deprive them of Fe.
Figure 2. In plant rhizosphere Trichoderma produces a siderophore which chelates insoluble Fe (Fe3+) and facilitate its conversion to soluble Fe (Fe2+) form. By doing this, Trichoderma also make Fe source unavailable to pathogenic fungi and thereby deprive them of Fe.
Plants 09 00762 g002
Figure 3. Mode of action of Trichoderma spp. in destroying pathogenic fungi. Trichoderma releases the lytic enzymes in the rhizosphere, which catalyzes the cell wall damage to target fungi. After this, a signaling cascade is activated in Trichoderma cells which involves the activation of MAPK (mitogen-activated protein kinase) through G-protein-coupled receptors. Alteration in gene expression ultimately leads to PCD (programmed cell death) of pathogenic fungi.
Figure 3. Mode of action of Trichoderma spp. in destroying pathogenic fungi. Trichoderma releases the lytic enzymes in the rhizosphere, which catalyzes the cell wall damage to target fungi. After this, a signaling cascade is activated in Trichoderma cells which involves the activation of MAPK (mitogen-activated protein kinase) through G-protein-coupled receptors. Alteration in gene expression ultimately leads to PCD (programmed cell death) of pathogenic fungi.
Plants 09 00762 g003
Figure 4. Plant-Trichoderma interaction involves the recognition molecules, i.e., MAMPS (microbe-associated molecular patterns) and effectors. MAMPS and effector molecules bind to the PRRs (pattern recognition receptors) and intracellular receptors and thereby initiate the MTI (MAMPS triggered) and ETI (effector triggered) immunity in plants, respectively. Moreover, this interaction also leads to the production of ROS (reactive oxygen species), which serve as signaling molecules and initiate a defensive response in plants by synthesis of antifungal molecules like phytoalexins, VOCs (volatile organic compounds), PRs (pathogenesis related) proteins such as CWDEs, etc. Trichoderma also improved the plant growth in pathogen-contaminated soil by regulating the expression of genes involved in growth regulation as well as induction of disease resistance.
Figure 4. Plant-Trichoderma interaction involves the recognition molecules, i.e., MAMPS (microbe-associated molecular patterns) and effectors. MAMPS and effector molecules bind to the PRRs (pattern recognition receptors) and intracellular receptors and thereby initiate the MTI (MAMPS triggered) and ETI (effector triggered) immunity in plants, respectively. Moreover, this interaction also leads to the production of ROS (reactive oxygen species), which serve as signaling molecules and initiate a defensive response in plants by synthesis of antifungal molecules like phytoalexins, VOCs (volatile organic compounds), PRs (pathogenesis related) proteins such as CWDEs, etc. Trichoderma also improved the plant growth in pathogen-contaminated soil by regulating the expression of genes involved in growth regulation as well as induction of disease resistance.
Plants 09 00762 g004

Share and Cite

MDPI and ACS Style

Sood, M.; Kapoor, D.; Kumar, V.; Sheteiwy, M.S.; Ramakrishnan, M.; Landi, M.; Araniti, F.; Sharma, A. Trichoderma: The “Secrets” of a Multitalented Biocontrol Agent. Plants 2020, 9, 762.

AMA Style

Sood M, Kapoor D, Kumar V, Sheteiwy MS, Ramakrishnan M, Landi M, Araniti F, Sharma A. Trichoderma: The “Secrets” of a Multitalented Biocontrol Agent. Plants. 2020; 9(6):762.

Chicago/Turabian Style

Sood, Monika, Dhriti Kapoor, Vipul Kumar, Mohamed S. Sheteiwy, Muthusamy Ramakrishnan, Marco Landi, Fabrizio Araniti, and Anket Sharma. 2020. "Trichoderma: The “Secrets” of a Multitalented Biocontrol Agent" Plants 9, no. 6: 762.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop