Next Article in Journal
Low-Altitude Remote Sensing Inversion of River Flow in Ungauged Basins
Previous Article in Journal
Rapid Urbanization in Ethiopia: Lakes as Drivers and Its Implication for the Management of Common Pool Resources
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Trichoderma: Advent of Versatile Biocontrol Agent, Its Secrets and Insights into Mechanism of Biocontrol Potential

1
Plant Pathology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Maunathbhanjan 275103, India
2
Molecular Biology Lab, ICAR-National Bureau of Agriculturally Important Microorganisms, Maunatbhanjan 275103, India
3
School of Life Sciences, Jawaharlal Nehru University, New Mehrauli Road, New Delhi 110067, India
4
Department of Biochemistry, Institute of Cell Differentiation and Aging, College of Medicine, Hallym University, Chuncheon 24252, Korea
5
ICAR-National Institute of Biotic Stress Management, Baronda 493225, India
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Sustainability 2022, 14(19), 12786; https://doi.org/10.3390/su141912786
Submission received: 30 June 2022 / Revised: 26 August 2022 / Accepted: 7 September 2022 / Published: 7 October 2022

Abstract

:
Trichoderma is an important biocontrol agent for managing plant diseases. Trichoderma species are members of the fungal genus hyphomycetes, which is widely distributed in soil. It can function as a biocontrol agent as well as a growth promoter. Trichoderma species are now frequently used as biological control agents (BCAs) to combat a wide range of plant diseases. Major plant diseases have been successfully managed due to their application. Trichoderma spp. is being extensively researched in order to enhance its effectiveness as a top biocontrol agent. The activation of numerous regulatory mechanisms is the major factor in Trichoderma ability to manage plant diseases. Trichoderma-based biocontrol methods include nutrient competition, mycoparasitism, the synthesis of antibiotic and hydrolytic enzymes, and induced plant resistance. Trichoderma species may synthesize a variety of secondary metabolites that can successfully inhibit the activity of numerous plant diseases. GPCRs (G protein-coupled receptors) are membrane-bound receptors that sense and transmit environmental inputs that affect fungal secondary metabolism. Related intracellular signalling pathways also play a role in this process. Secondary metabolites produced by Trichoderma can activate disease-fighting mechanisms within plants and protect against pathogens. β- Glucuronidase (GUS), green fluorescent protein (gfp), hygromycin B phosphotransferase (hygB), and producing genes are examples of exogenous markers that could be used to identify and track specific Trichoderma isolates in agro-ecosystems. More than sixty percent of the biofungicides now on the market are derived from Trichoderma species. These fungi protect plants from harmful plant diseases by developing resistance. Additionally, they can solubilize plant nutrients to boost plant growth and bioremediate environmental contaminants through mechanisms, including mycoparasitism and antibiosis. Enzymes produced by the genus Trichoderma are frequently used in industry. This review article intends to provide an overview update (from 1975 to 2022) of the Trichoderma biocontrol fungi, as well as information on key secondary metabolites, genes, and interactions with plant diseases.

1. Introduction

It is anticipated that there will be 9.1 billion people living on the planet by the year 2050, according to current population projections. As a consequence of this, there needs to be a seventy percent increase in the amount of food that is produced by agriculture in order to sustainably feed the rising population throughout the world. Challenges, such as global warming and environmental pollution, have pushed plants toward various forms of biotic and abiotic stress, which has caused significant reductions in yield. This will lead to issues of food shortages for future generations [1]. Plant diseases play a direct role in the destruction of agricultural crops. The loss was estimated in fruit crops (78%), vegetables (54%), and cereals (32%) [2]. Specifically, disease caused by soil-borne pathogens is destructive and spreads quickly, causing a huge economic loss of important crops. The application of pesticides was considered an excellent solution to manage soil-borne pathogens, but their excessive use has led to the development of pathogen resistance to fungicides. However, it was realized that applying these pesticides is harmful to the environment and unsafe for human health [3]. It also kills the non-target organisms present in the soil and also fertilizers were used extensively around the globe since the Green Revolution, due to the high subsidies. However, extensive fertilizer use exacerbates soil degradation and causes yield stagnation and, as a result, threatens food security and soil sustainability, especially in developing countries, such as India [4]. Hence, the utility of certain microorganisms that can antagonize the target pathogen has been explored. Bioagents use a host-specific pathogen, a microbial antagonist, to inhibit diseases and control weed populations [5,6]. Biocontrol agents comprise fungi, bacteria, viruses, nematodes, and protozoa [7]. Plants treated with biocontrol agents may become more vigorous, robust, healthier, and yield more than untreated plants. Bioagents are microbial agents that suppress the growth of other microorganisms associated with them. Bioagents can hinder the life process of other phytopathogens, including fungi, bacteria, viruses, and other microorganisms. Biocontrol fungi are mostly saprophytic. They improve plant growth and development, enable the plant to resist abiotic stresses, improve nutrient uptake from the soil, and reduce the effect of plant diseases. A fungus genus called Trichoderma can be found as saprotrophs, mycoparasites, degrading the cell wall components of harmful pathogens by producing chitinase or cellulase enzyme soil inhabitants and plant symbionts [8]. Different strains of Trichoderma account for approximately ninety percent of all fungal biocontrol agents used to combat deleterious microorganisms [9]. In 1794, soil and decomposing organic matter were used to isolate Trichoderma for the first time [10]. Trichoderma is currently the source of more than 60% of the world’s most effective bio-fungicides [11]. Trichoderma has been broadly studied among biocontrol agents due to its ability to antagonize plant pathogenic species. Trichoderma is a widely distributed ubiquitous hypomycetus fungi occurring nearly in all soil types and root ecosystems, especially in those rich in organic matter. Trichoderma, considered a potent biocontrol agent, can be attributed to the following characteristics: high reproductive capacity, ability to survive even in stressed conditions, efficiency in utilization of nutritional capacity to alter the rhizosphere, aggressiveness against phytopathogenic fungi, helps in plant growth promotion, induced defense mechanism as well as providing plants several secondary metabolites [12], enzymes [13], and PR proteins [14]. Because of these characteristics, the genus Trichoderma can be found in a diverse environment with a significant population density. The most common species of Trichoderma as biocontrol agents are Trichoderma virens, Trichoderma viride, and Trichoderma harzianum [15]. The potential of Trichoderma as a biocontrol agent in plant disease management was first recognized in the early 1930s and, in subsequent years, control of many diseases has been reported [16]. Root rot disease, fruit rot, damping-off, wilt, and other common plant diseases can be managed by Trichoderma spp. In recent studies [17], it has been observed that Trichoderma spp. release secondary metabolites that inhibit the growth of plant pathogens and encourage the growth of plants [18]. In addition, in the plant Trichoderma spp. interaction, they efficiently modulate root architecture and enhance the length of lateral and primary roots, which results in the feasibility of nutrient uptake by the plant [19]. Numerous species of Trichoderma under soil microbiome can produce enzymes that degrade the target pathogenic fungi or produce several toxic compounds, which restrict the pathogens. The antagonistic properties of these are based on multiple mechanisms. Trichoderma strains exert biocontrol action against fungal phytopathogens, either indirectly or by competing for nutrients and space, mycoparasitism, production of antibiotics, induction of resistance in host plants, and promoting plant growth [18,20]. Mycoparasitism is a process in which fungi primarily locate target hyphae by probing with persistently synthesized cell wall degrading enzymes (CWDEs) paired with precise detection of cell wall pieces produced from target fungi. This cell wall degrading enzyme complex produced from Trichoderma spp. is composed of chitinases, β-glucanases, cellulases, and proteases. These enzymes can decompose the cell wall of phytopathogens, making it possible for hyphae to penetrate, colonise, and activate myoparasitism in plants [21,22]. Chitinases are potent enzymes that showed the highest antagonistic potential against plant diseases [23]. In order to obtain a new formulation for its efficient biocontrol activity, these metabolites can either be overproduced or mixed with the suitable biocontrol strain [24]. Excellent results have been attained with T. virens and metalaxyl against Pythium ultimum infecting cotton [25]. This has resulted in commercial production of Trichoderma species for the protection of several plant diseases and growth enhancement of several crops in India, Israel, New Zealand, and Sweden. In 1997, it was shown that Trichoderma colonisation of roots could minimize foliar pathogen symptoms. This discovery gave rise to the term "induced systemic resistance" (ISR), which is also used to refer to all types of induced resistance, both local and systemic. [26]. Trichoderma research over the following two decades was dominated by IDR as a plant disease control method [27]. Though synergistic actions in these processes may occur, the degree of disease suppression caused by mycoparasitic activity is greater than that caused by IDR or antibiosis [28].
Due to a lack of reliable characteristics, morphological and cultural characteristics alone have proven difficult to use to distinguish individuals within the genus Trichoderma. The effectiveness of various biochemical and molecular approaches was assessed to distinguish among isolates of the genus Trichoderma. Information was also collected on ITS sequence data, RAPD, or RFLP to differentiate between morphologically indistinguishable isolates [29]. According to a new taxonomic approach, individuals of the genus Trichoderma are currently identified by combining cultural, biochemical, morphological, and molecular characteristics. The accuracy of sequence and RAPD data in determining Trichoderma phylogeny is also assessed. The ITS region of sequence data was the most reliable for predicting the phylogeny of morphologically distinct species, while RAPD and RFLP data were the most beneficial for predicting the overall phylogeny of morphologically similar strains [30,31,32,33,34].
The compilation of basic information about the biocontrol potential of Trichoderma strain and their capabilities to colonise, persist, and disseminate under environmental conditions is vital in the journey of bioformulation development [35]. Orr and Knudsen 2004 developed a method to monitor the variation in biomass of biocontrol agents in native soil by using GFP and GUS labeled T. harzianum ThzID1-M3 strain, an environment in which the presence of local bacteria and fungus impedes the use of conventional methods for determining biomass [36]. It was shown that epifluorescence microscopy tracking of GFP-labeled Trichoderma harzianum was a helpful tool in identifying biocontrol-active hyphal biomass from inactive conidia and chlamydospores, which were measured using plate counts. The GUS and GFP marker genes were intended to distinguish between BCA and native Trichoderma populations. Genes that produce a green fluorescent protein (gfp), hygromycin B phosphotransferase (hygB), and β-glucuronidase (GUS) are examples of exogenous markers that can be utilized to genetically change BCAs in order to track and analyze various strains of Trichoderma on field crops [37,38,39]. This review presents a compilation of studies regarding molecular characterization and the mechanism of Trichoderma species as biocontrol agents, along with a detailed description of genes involved in biocontrol activity, enzyme production, and secondary metabolites/bioactive compounds produced by Trichoderma and findings that discover the potentiality of Trichoderma spp. as a plant growth promoter agent are discussed in this review.

2. Insight on Trichoderma and Its Mechanism

2.1. Morphological Studies on Trichoderma

Trichoderma produces numerous spores with varied shades of color, such as white green, light green, dark green to dull green [40], and on the backside of the plate, colony color varies from yellow, buff, amber, or uncolored [41]. It proliferates; therefore, it is also characterized by the radial growth rate. Most of the Trichoderma spp. produces chlamydospores. Phialide lengths vary from 3.5 to 10.0 × 1.3 − 3.3 µm and the shape of phialides is flask shaped, but the length of phialides varies considerably depending on the species [42]. T. harzianum Rifai, Trichoderma virens [43] von Arx, Beih, and T. viride Pers.:Fr [44,45] were reported as the best effective BCAs against plant pathogenic fungi. T. harzianum is an assemblage of species defined by the presence of short side branches on the conidiophore, short inflated phialides, and smooth and small conidia. Based on the strains and characteristics studied, T. harzianum has been classified into three, four, or five subspecific groupings [46]. Gams and Meyer [47] neotypified T. harzianum and divided it into two main groups based on molecular analysis: T. harzianum sensu lato (s.l.) and T. viride-T. atroviride complex. Th1 and T. inhamatum are some of the most prevalent strains utilised as BCAs [48] in T. harzianum s.l. [49,50]. Colombian T. harzianum isolates were formerly categorised as T. inhamatum due to the lack of sterile appendages on the conidiophores and the globose shape of the conidia [51]. Th1 and T. inhamatum were previously thought to be two separate species due to physical distinctions and two base sequence changes in the ITS1 gene. As per molecular data, Th2 and Th4 strains are still not BCAs and are likewise distinct from T. harzianum s.l. T. viride-T. atroviride complex isolates, with rapidly darkening conidia identified by particular restriction fragment length polymorphism (RFLP) pattern. T. viride is a genus of bacteria having globose or subglobose to ellipsoidal warted conidia, most of which generate antibiotics and have a coconut-like odor. For many years, the morphology of T. viride was unknown until two forms of conidial ornamentation were identified [52]. Recent research has shown that T. viride is a paraphyletic group and a combined morphological and genomic approach has confirmed the redefinition of T. viride types I and II in two species. Type I includes the genuine T. viride species in addition to the Hypocrea rufa anamorph and strains of T. atroviride and T. koningii [53]. Ovoidal instead of globose conidiation, as well as darker and rapid conidiation, characterise the new species T. asperellum [53,54].

2.2. Molecular Studies on Trichoderma

The advent of molecular tools for investigations in fungal taxonomy prompted research in the mid-1990s to re-assess the morphology-based taxonomy in Trichoderma. For the species of bioagents that share common ecology or morphology, rDNA sequencing is a valuable tool to differentiate such species within particular groups of strains or isolates [55,56,57]. These can also be distinguished by randomly amplified polymorphic DNA (ISSR)—PCR, restriction fragment length polymorphisms in mitochondrial and ribosomal DNA, and sequence analysis of ribosomal DNA. Ribosomal DNA sequence analysis, RAPD, and RFLP [30,32,32,33,34,58,59,60] are effective methods to distinguish isolates from the same genera. RAPD helps decide species diversity by molecular identification and characterization of the potent biocontrol agents [61]. The laboratories of G.J. Samuels (Beltsville, MD, USA), T. Borner (Berlin, Germany), and C.P. Kubicek (Vienna, Austria) collaboratively pioneered a revision of Bissett’s section Longibrachiatum. They combined the use of molecular markers (ITS1 and ITS2 sequence analysis, RAPD), physiological (isoenzyme analysis) and phenetic characters, and also, for the first time, included an analysis of potential teleomorphs of the Trichoderma spp. from this section [46,51,57,62,63,64,65].
The total number of phylogenetically recognised species in the Trichoderma and Hypocrea genus reached over one hundred in the year 2006 [64,65]. Many reports of new species of Trichoderma and Hypocrea are listed in Table 1. Misidentifications of particular species have happened in some cases, particularly in earlier publications, such as the name Trichoderma harzianum, which has been used to describe various species [66]. However, it is difficult to safely fix these inaccuracies analysing the strains that were first utilised. As a result, we will summarise the findings using the originally published names. In recent years, the safe identification of novel species has been substantially facilitated by creating an oligonucleotide barcode known as TrichoKEY and a specialised matching search engine known as TrichoBLAST. These tools are available online at www.isth.info accessed on 5 June 2022 [67,68]. Detailed documentations of the genus Trichoderma/Hypocrea have been produced due to ongoing efforts to elucidate the diversity and geographical occurrence of Trichoderma/Hypocrea [69,70,71,72,73,74,75,76,77,78,79,80]. The Index Fungorum (http://www.indexfungorum.org/Names/Names.asp accessed on 5 April 2022) now includes 165 records for Trichoderma and 471 different names for Hypocrea species. Currently, the International Subcommission on Trichoderma/Hypocrea compiled a list of 104 species that have been characterised at the molecular level (http://www.isth.info/biodiversity/index.php accessed on 20 April 2022). Even this, a huge proportion of the potential Hypocrea strains and an even larger portion of the Trichoderma strains, for which sequences have been deposited in GenBank, have not yet been identified [67] and must be investigated further. Trichoderma taxonomy has been greatly improved by the use of molecular phylogenetic markers and phylogenetic study of the many Trichoderma species is still an active research area.

2.2.1. Universal Marker-Based Identification

ITS is a reliable marker for the barcoding of fungal DNA. In environmental samples, ITS of the ribosomal DNA region is used to evaluate fungal diversity. The favored DNA barcoding marker is the ITS region of nuclear ribosomal DNA for molecular identification of mixed templates of single taxa [81]. The most promising method is molecular analysis of the ITS region of rDNA for identification of species [82]. Based on DNA sequence analysis and phylogenetic studies, 290 species of Trichoderma have been identified and characterised [83]. In eukaryotes, variable sequences with the larger subunit or smaller unit of rRNA genes are suitable for analysis of the subgeneric relationship. In many of the plant pathogenic fungal genera, the phylogenetic relationship is determined by the D2 region of the LSU [84]. Bisset concluded that T. pseudokoningii, T. parceramosum, T. citrinoviride, and T. longibrachiatum were allocated under Longibrachiatum section based onmorphological data [85,86]. Rehner and Samuels and Samuels conducted a phylogenetic analysis of Trichoderma ITS region sequences and reported that T. virens showed similarity with T. harzianum, it is distinct from Gliocladium, and the above result supported the Vonrox and Bisset taxonomic studies [87]. The DNA oligonucleotide barcode method is a quick method through which Trichoderma and Hypocrea can be identified [88]. Oligonucleotide barcode combines many oligonucleotides (hallmarks), mainly distributed among the rDNA region of ITS1 and 2 sequences. The genus species hallmark was defined as oligonucleotide barcodes that are consistent in all Trichoderma and Hypocrea rDNA regions of ITS1 and ITS2 and differ in related fungal genera. Harmosa et al. described 16 Trichoderma harzianum Rifai strains and 1 T. viride strain previously recognised as T. harzianum Rifai. A certain level of polymorphism was found in hybridizations using a mitochondrial DNA probe. Three different lengths of ITS and four sequence types were confirmed by sequencing ITS1 and ITS2 [89]. Manzar et al., 2020 reported that tef-1α gene and ITS1 and ITS4 gene sequence analysis were able to identify and differentiate 20 Trichoderma isolates. Based on the sequence analysis of tef-1α and ITS1 and ITS4 gene, these isolates were divided into two species, with 19 isolates belonging to T. asperellum and 1 isolate belonging to T. harzianum [90]. Oskiera et al. identified 104 strains of Trichoderma based on the sequences of translation elongation factor 1 alpha (tef-1α), internal transcribed spacers 1 and 2 regions, as T. simmonsii, T. harzianum, T. atroviride, T. lentiforme, and T. virens. Thus, the comparative nucleotide sequence analysis of ITS1 and ITS4 and tef-1α gene provides better resolution to distinguish different Trichoderma species from the sorghum rhizosphere [91].

2.2.2. DNA-Fingerprinting Techniques

Many DNA-fingerprinting techniques, such as polymerase chain reaction (PCR), Southern hybridization, and restriction enzyme digestion (RED), are used by scientists to locate strain-specific DNA strands. These methods generate band patterns that can be compared. Trichoderma species can be identified in agro-conditions using species-specific primers. In order to distinguish between T. harzianum biotypes Th2 and Th4, a species-specific primer-based test was devised by Samuels et al., and then redescribed as T. aggressivum f. europaeum and T. aggressivum f. aggressivum [72]. For Schlick and colleagues, they used DNA fingerprinting to demonstrate that oligonucleotides as hybridization probes could differentiate distinct T. harzianum patent-protected strains. All strains could be distinguished from one another using fingerprint patterns [92]. The first approach to separate a commercially available biocontrol strain from the other Trichoderma strains was established by Zimand et al. and it was used to identify T. harzianum T-39 as a BCA against B. cinerea All of the Trichoderma strains studied could be distinguished using a set of 10 mer primers in a random amplified polymorphic DNA (RAPD). It is clear that this idea has many benefits beyond morphological feature approaches [93]. The technique can be completed in less time and with less DNA. To follow the distribution and longevity of T. atroviride C65 on kiwifruit leaves, Dodd et al. (2004) used an isolate-specific RFLP marker in association with a dot-blot test [94].
Cross dot-blot hybridization with UP-PCR amplification products investigated T. polysporum, G. roseum, T. hamatum, T. viride, T. virens, and T. koningii isolates to find commonalities among the strains. The findings show that UP-PCR and ITS-ribotyping could be useful for identifying various species within a single species [95]. Using random, minisatellite, and microsatellite primers, Fanti et al. fingerprinted two strains of Trichoderma, which were potent against Cytospora canker of peach in the environment. The M13 minisatellite demonstrated that each strain has its own fingerprint. The antagonists were collected four months after being applied to the soil under the canopy of peach trees; however, they were not recovered from the soil itself and, after a year, they were no longer there [96]. Although there is a wide variety of PCR-based fingerprinting techniques, not all of them are strain specific. These procedures are also very easy to utilise. Both a lower annealing temperature and a shorter primer length can have an adverse effect on the precision of their results [97]. On the other hand, strain-specific fragments may be utilised as monitoring markers in accordance with SCARs (sequence-characterised-amplified regions) [98,99,100,101,102].

2.2.3. OMICS Approaches in the Service of Trichoderma Monitoring

Biofertilisers and biocontrol agents developed from Trichoderma spp. are commonly utilised in agriculture (BCAs) [103]. Information about Trichoderma strains’ ability to colonise and stay in natural environments is critical for developing a useful Trichoderma strain for a BCA [104]. Trichoderma strains released as BCAs into the environment must be monitored for their destiny, behavior, and population dynamics. A need for the registration of new biocontrol agents based on Trichoderma is the capability to reliably assess and monitor the strain that has been released, as well as to monitor the changing population dynamics of that strain over time [105]. As a consequence, it is becoming increasingly important to differentiate naturally occurring Trichoderma populations found in agricultural areas from newly introduced Trichoderma strains [106]. In classic microbiological methods, colony forming units (CFU) can be estimated by diluting samples using Trichoderma-selective or semi-selective media [107]. A sample collected for dilution plating from the environment does not distinguish between indigenous strains of the Trichoderma population’s existence in the environment and artificially introduced ones by the experimenter. For this, morphological or physiological characteristics are insufficient to identify the colonies [107]. The omics approach is a promising tool and is used for monitoring and differentiating the potent biocontrol agent activity, which is artificially introduced from the native biocontrol agent that is already present in the soil [108]. T. harzianum was monitored and quantified using a primer set and a TaqMan probe for the ITS region [109]. ITS copies were quantified using real-time PCR. The ITS copy number and the fungus biomass were found to have a 0.76 correlation. According to scientists, real-time PCR data can be used to quantify fungi in soil samples. T. harzianum could be detected and measured in soils and other organic materials using primers and probes designed for pure fungus cultures. Beaulieu et al. utilized this method to monitor T. harzianum populations in green compost and peat, which worked well [109,110]. Cultivation-dependent Trichoderma species identification and observation were described by Hagn, et al. using ITS-based primers. Arable soil samples were used to create a library of clones. Its results demonstrated that the primer set selected to amplify the Trichoderma gene encompassed a wide range of species relevant to biocontrol [111]. Trichoderma-specific primers targeting the ITS region were produced by Meincke et al. (2010) to study Trichoderma diversity. On the other hand, the reverse primer binds to an area of ITS2 that is still polymorphic, making it impossible to identify many species [112]. The ITS-based metabarcoding technique by Friedl and Druzhinina eliminated this problem by amplifying the full diagnostic ITS1 and 2 regions from all members of the genus, using six reverse primers and the forward primer ITS5. This culture-independent PCR-based method demonstrated the limited Trichoderma diversity in the soil of a riparian forest. Two types of Trichoderma populations can be incorrectly estimated using PCR methods: active and inactive hyphae and mycelia, as well as dormant conidia and spores [113]. Furthermore, the isolation of total RNA, its reverse transcription, and the subsequent detection of cDNA allow for the identification of active Trichoderma communities by transcriptomic techniques.
Geistlinger et al. employed Touchdown PCR to track and quantify T. virens using simple sequence repeats (SSRs). There were 12 distinct loci for which primers were created. According to findings, this species lives as an endophyte in the roots of tomato plants. Numerous strains of T. virens had their fungal biomass quantified in plant tissues and co-colonization of the roots has also been discovered [99]. Utilizing cleaved amplified polymorphic sequence (CAPS) markers, the genetic diversity of T. atroviride isolates was investigated [114]. Following amplification of RAPD regions, the amplicons were digested to restrict enzyme digestion with BslI, DraI, and TaqI. T. atroviride was distinguished from other species by three CAPS markers, which can be used to assess and monitor T. atroviride, particularly in environmental specimens. Meena et al. provided a strategy for detecting T. harzianum and T. hamatum species. SCAR primers were created based on the sequence of species-specific RAPD fragments [115]. Perez et al. developed a procedure to monitor the growth and colonisation of T. harzianum in experimental communities similar to the method described earlier [100]. Because of the pervasive and diversified nature of T. harzianum, scientists did not suggest using this method for detecting the species in complicated ecological samples such as soil.
Using microarray technology, it is possible to investigate Trichoderma populations in natural surroundings, which track gene expression changes. To monitor active Trichoderma populations, new field-portable microarray analysis systems are now available [101]. These systems provide data on microbial community composition, dynamics, and the physiological status of Trichoderma populations in soil. When conducting comparative transcriptome analyses in vitro or in soil microcosm systems, researchers can use the transcriptomic data from Trichoderma–fungus [102] and Trichoderma–plant interactions to choose target genes for microarray monitoring. After using Trichoderma as a biocontrol agent, a metatranscriptome investigation of agricultural habitats can reveal significant alterations in the active microbiome. On the other hand, this method is time consuming and expensive due to the need for high-throughput sequencing and computing systems.
Now, it is easy to select Trichoderma strains, develop BCA implementation strategies, and establish monitoring strategies for detecting specific cells, secreted proteins, or secondary metabolites; hence, volumes of information are available on the metabolome, proteome, and secretome of Trichoderma strains from multiple species. Because each Trichoderma species produces a unique peptaibiome, non-ribosomally produced peptaibols could be used to build mass spectrometry-based, species-specific monitoring systems [116].

2.2.4. Exogenous Marker Genes

Utilizing exogenous markers, such as glucuronidase (GUS), green fluorescent protein (gfp), hygromycin B phosphotransferase (hygB), or producing genes, certain Trichoderma strains in agroecosystems might be identified and tracked [117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132,133,134,135,136,137,138,139,140,141,142,143,144,145]. Orr and Knudsen employed the gfp-labeled and GUS, T. harzianum strain ThzID1-M3 to quantify the biomass changes in a fungal BCA in unsterilised soil. Indigenous bacterial and fungal populations in unsterilised soil interfere with biomass determination procedures. GUS and gfp were used to distinguish between the BCA-introduced marker genes and the indigenous Trichoderma populations [146,147]. It was demonstrated that epifluorescence microscopy could discriminate active hyphal biomass useful for biological control among dormant chlamydospores and conidia counted by plate counts while observing gfp-labeled T. harzianum [148]. Propiconazole-resistant Trichoderma harzianum TF3 is antagonistic to Botrytis cinerea and can survive at high population densities in tomato, grapevine, and phylloplane. This strain was changed to be resistant to hygromycin B using high-voltage electric pulses and the vector pHAT (an offspring of pAN7-1), which was then used to select strains with high levels of resistance [149]. When grown on tomato phylloplane, all transformants outperformed the wild-type strain, thrived for 2 weeks in the presence of hygromycin B or propiconazole, and were mitotically stable after many passages without selection pressure.
Utilising cucumber plants cultivated in sphagnum peat, Green and Jensen evaluated the population trends and durability of the transformed T. harzianum strain T3a. A T. harzianum strain inoculated into the rhizosphere was studied for the first time using the GUS marker to track its existence, population structure, and behaviors [150]. pAN7-l and pNOM102 plasmids were used by Bowen et al. to transform the T. harzianum strain M1057 against Sclerotium rolfsii [59]. Two transformants had mitotic stability and their growth rates matched wild-type ones. The co-transformant mitotic stability and ability to colonise Sclerotinia sclerotiorum resting sclerotia in soil were studied [129]. T. harzianum ThzID1-M3 strain was found to colonise about 60% of the sclerotia, suggesting that the strains can be co-transformed with GUS and gfp to assess and monitor specific strains introduced into soil [151]. ThzID1-M3 significantly reduces S. sclerotiorum colonisation in soil by inhibiting the growth of fungivorous and other nematode populations when applied to soil. Fungivorous nematodes seek out nutrient-rich areas in the soil. A larger hyphal net produced by a Trichoderma strain and fed to the soil as a pellet formulation attracts worms by providing food. To release into the environment, various countries, including those in the European Union, require authorization [152]. Therefore, it is crucial to monitor distinct, genetically unaltered biocontrol Trichoderma strains in agricultural contexts utilising molecular techniques based on endogenous DNA markers.

3. Mechanisms of Trichoderma

Trichoderma spp. uses numerous antagonistic strategies against plant diseases. These include antibiosis, mycoparasitism, competition for nutrients and space, stimulation of plant growth, and induced plant defense mechanisms (Figure 1) [113].

3.1. Mycoparasitism

Mycoparasitism is an essential antagonistic character of Trichoderma, which is responsible for its efficiency against the plant pathogenic fungi [153]. The complex process of mycoparasitism entails various events. In a biotrophic mycoparasitism, the hyperparasite relies on the host fungus and obtains nutrition from it via haustoria without causing the host cell to die out. Equilibrium is maintained between the host and the mycoparasitic fungus (136). For commercial biocontrol purposes, these species-specific interactions may be essential but are unlikely to be utilized due to the need for host mycelium as a substrate for synthesizing hyperparasite. This category of hyperparasites is significantly better suited for commercial use as MBCA compared to biotrophic hyperparasites since they can grow on artificial substrates in large quantities, allowing for mass production.
Trichoderma and Clonostachys are the most explored mycoparasites. Most antagonistic isolates from these genera exhibit a wide spectrum of plant pathogenic hosts among their antagonistic isolates. CWDEs (cell wall degrading enzymes) and antimicrobial secondary metabolites are typically used in tandem to kill their hosts, which develop structures for attachment and infection [121,122,123,124,125]. Chitinolytic enzymes produced from T. harzianum, such as endochitinase, β-1, 3 glucanase, and chitobiosidase, are more effective against plant pathogenic fungus than chitinolytic enzymes isolated from plants or bacteria. The concentration of cell wall degrading enzymes (CWDEs) viz. chitinase and β-1, 3-glucanase produced by Trichoderma isolate was high. The cellulase and protease amounts were low and the polygalacturonase produced by the pathogen was significantly reduced. The mixture of endochitinase or β 1-3 glucanase showed antifungal activity by lysis of spore cell walls, thallus, and hyphal tips and combining chitobiosidase and endochitinases inhibited the plant pathogenic fungal spore germination and hyphal lysis more than singly [126].
After recognising the host, complicated signaling triggers the production of these lytic enzymes, which are not constitutive [124]. Recognizing the fungal host triggers transcriptional reprogramming and the development of “molecular weapons”, such as CWDEs (cell wall degrading enzymes) that are used in host attack and lysis. The host releases oligosaccharides and oligopeptides that are then recognised by Trichoderma receptors and function as inducers due to the early activities of cell wall degrading enzymes (CWDEs) [124]. Mycoparasites that are necrotrophic can cause more excellent permeability and disintegration of host cell walls, leading to the death of the host. Several Trichoderma mycoparasitism-related gene families are upregulated during mycoparasitism, including ech42 and prb1. Trichothecene, produced by T. harzianum gene tri5, inhibits protein and DNA synthesis, limiting pathogen growth. Trichothecene has a phytotoxic effect on Fusarium species [127]. Trichoderma virens TvBgn2 and TvBgn3 genes release a cell wall disintegrating enzyme, which aids in biocontrol activities [128]. T. harzianum mycoparasitic activity has been boosted by the cloning and expression of genes from five T. harzianum isolates encoding chitinase (chit42), N-acetyl-ß-D-glucosomidase (exc1, and exc2), β-glucanase (bgn 13.1), and protease (prb1) (T 30, 31, 32, 57, and 78) [154]. A gene aids mycoparasitic activity from T. harzianum CECT 2413 that provides adhesion to hydrophobic surfaces and shields plant cells from R. solani infections, according to previous research [155]. The T. atroviride G protein component, responsible for degrading pathogenic fungi cell walls, produces chitinase and other antifungal compounds through the Tga1 gene [156]. B. cinerea and Phytophthora capsici were found to have a synergistic effect on Trichoderma atroviride transcription of genes involved in cell wall breakdown [156]. The genes identified from these biocontrol agents have been discovered to have an essential role in biocontrol activity and their detailed function is discussed in Table 1.
Table 1. List of genes involved in biocontrol activity and enzyme production.
Table 1. List of genes involved in biocontrol activity and enzyme production.
S.No.GeneProteinFunctionReference
1endoglucanase I (EG I)Endoglucanasecellulose hydrolysis[157]
2erg1Squalene epoxidaseactivation of plant defense system[145]
3tri3Trichothecene O-acetyltransferase TRI3trichodermin biosynthesis[149]
4tri4Cytochrome P450 monooxygenasetrichodermin biosynthesis[149]
5tri5Trichodiene synthasetrichothecene biosynthesis[100]
6tri6Trichothecene biosynthesis transcription regulator TRI6transcriptional activator of genes involved in harzianum A (HA) biosynthesis[150,158]
7tri11Trichothecene C-4 hydroxylasetrichodermin biosynthesis[149]
8tri22Cytochrome P450 monooxygenasetrichothecene biosynthesis[151]
9tri10Trancription factorregulation of trichothecene biosynthetic genes[152]
10tri11Trichothecene C-4 hydroxylasetrichodermin biosynthesis[149]
11ACEIRepressor proteincellulase biosynthesis[153]
12AceIITranscription factorcellulase biosynthesis[154,159]
13CbhICellobiohydrolase Icellulase hydrolysis[155]
14cbhII Cellobiohydrolase IIcellulase hydrolysis[148]
15bgl1β-glucosidasecellulose hydrolysis[156]
16prb1Basic proteinaseMycoparasitism[157]
17ech42EndochitinaseMycoparasitism[160]
18chit33Endochitinase 33Mycoparasitism[161]
19chit42Chitinase 42biocontol activity against fungus[162]
20cre1Carbon catabolite repressor Mycoparasitism[163,164]
21xyr1Xylanase regulator 1systemic resistance induction in plants[165,166]
22Rce1Transcriptional repressor proteinregulation of cellulase biosynthesis[167,168]
23nag1N-acetylglucosaminidaseessential for chitinase induction by chitin[169,170]
24egl1β-1,4-EndoglucanaseMycoparasitism[171]
25tvsp1Extracellular serine proteaseMycoparasitism[172,173]
26Sm1Cerato-platanin proteinactivation of plant defense mechanisms[174]
27Sm2Cerato-platanin proteinactivation of plant defense system[175,176]
28SS10Subtilisin-like proteaseBroad-spectrum antifungal activity[177]
29SA76Aspartic proteaseBiocontrol activity against fungus[178]
30SL41Serine proteasebiocontrol activity against fungus[179]
31Tas-acdSACC deaminasePlant root growth-promotion[180]
32TgaAG-protein α subunitmycoparasitism against Sclerotium rolfsii[181,182]
33TmkAmitogen-activated protein kinasemycoparasitism against Sclerotium rolfsii[183]
34ThPG1Endopolygalacturonaseplant defense induction by T. harzianum[184,185]
35TvPG2EndopolygalacturonaseInduction of Plant Systemic Resistance[186]
36ThPTR2Di/tri-peptide transporterMycoparasitic process[187]
37tac1Adenylate cyclaseGrowth, germination, mycoparasitism and secondary metabolism[188]
38Vel1VELVET proteinRegulator of biocontrol as well as morphogenetic traits in Trichoderma virens[189]
39PPT14-phosphopantetheinyl transferaseRole in antibiosis and induction of SA and camalexin-dependent plant defense responses[190]
40Taabc2ABC Transporter Membrane PumpRole in antagonism and biocontrol against Pythium ultimum and Rhizoctonia solani[191]
41epl1 Eliciting plant response-like proteinModulation of Systemic Disease Resistance in SolanumLycopersicum[192]
42epl2Eliciting plant response-like proteinTrichoderma mediated promotion of plant protechion[176]
43Thctf1Transcription factorProduction of secondary metabolites and in the antifungal activity of T. harzianum[193]
44Pgy1Proline-glycine-tyrosine-rich proteinRole in antagonism against soil-borne pathogens of plants[194]
45Ecm33GPI-anchored cell wall proteinRole in antagonism against soil-borne pathogens of plants[194]
46Pac1 Transcription factorRole in antifungal activity of Trichoderma harzianum[195]
47Tvbgn3Beta-1,6-glucanaseMycoparasitism[174]
48tvhydii1Class II hydrophobinMycoparasitism and plant-fungus interaction[196]
49Ste12Transcription factorMycoparasitism[197]
50LaeAMethyltransferase proteinTrichoderma atroviride defense and parasitism[198]

3.2. Competition of Ecological Niche

For maintaining the dynamics of the microbial population, where microorganisms belong to the same community and share the exact physiological needs, the availability of nutrients is limited and, therefore, nutrient competition is essential for their survival. The Trichoderma is a ubiquitous fungus, which is present throughout the world in agricultural and natural soils due to its excellent competitive capability. Trichodema can compete with pathogens in plants for nutritional sources, viz. nitrogen, carbon, and iron and acts as a biocontrol agent against soil-borne plant pathogens. The rhizosphere competence of Trichoderma strains enables them to colonise the root surface and compete with other microorganisms for nutrients secreted by roots in rhizospheric soil [199]. The term rhizosphere competence was coined by Ahmad and Baker in 1987 [200]. Trichoderma spp. not only controls many soil-borne pathogens but also promotes plant growth [201,202]. Trichoderma spp. releases siderophores that sequester iron ions, thereby making them unavailable to the pathogen. It has been established that plant pathogens produce low binding siderophore coefficients or fewer siderophores as compared to Trichoderma. Iron is present in the Fe3+ state and it is not available for the growth of microorganisms because Ferric ion is not soluble. Trichoderma spp. produces siderophores, which chelate Fe3+ and receptor protein of microbial membrane recognise the complex of siderophore–Fe. Thus, the siderophore–Fe3+ complex makes Fe unavailable to the microorganisms, including plant pathogens present in the rhizosphere, ultimately resulting in suppressing pathogenic infection and, hence, Trichoderma acts as a biological control, contributing to managing the plant pathogen colonisation [203,204]. This shows the importance of competition for nutrients between Trichoderma and pathogenic fungi. Trichoderma is more competitive than other rhizospheric microorganisms because it can mobilise and take up nutrients from the soil [202]. T35 strain of T. harzianum, due to its rhizosphere competence, outcompetes Fusariumoxysporum f. sp. melonis for nutrients and can colonise the rhizosphere well, resulting in decreased concentration of nutrients and rhizospheric space for colonization of F. oxysporum f. sp. meloni [205].
In addition, Trichoderma has an advantage over many other soil microbes due to its ability to mobilise and take up soil nutrient sufficiently. Competition for nutrients is the primary mechanism utilised by T. harzianum against Fusarium oxysporum f. sp. melonis. Microorganisms, such as Trichoderma spp., mediate the solubility of nutrients in the soil and make them available at the root surface. Soil microorganisms cause changes in soil pH, a result of which being that equilibrium of many chemical and biochemical reactions is modified [206]. There is scant evidence that Trichoderma can enhance the bioavailability of insoluble or sparingly soluble elements viz. P, Fe, Mn, Cu, and Zn. However, results have been yielded by previous research [207,208,209]. Significant increases in concentrations of P, Fe, Mn, Cu, Zn, and Na in roots of cucumber inoculated with Trichoderma were reported by Yedidia et al. [210]. Fiorentino et al. demonstrated that T. virens GV41 improved the growth of lettuce and rocket and enhanced nutrient uptake by them and, hence, is the best performing microbial biostimulant. It enhanced the use efficiency of N and favored the uptake of native soil N by both the crops. The uptake of N by roots was enhanced under low-N-availability conditions. It has been revealed that Trichoderma acts as a nutrient solubiliser. However, the detailed effects of Trichoderma inoculation remain to be deciphered [211].

3.3. Antibiosis

Trichoderma strains produce low-molecular-weight volatile or nonvolatile antibiotics or diffusible compounds that interact and restrict the growth of deleterious plant pathogenic fungi. This process is called antibiosis. The metabolites viz. antibiotics, mycotoxins, and phytotoxins produced by Trichoderma helped in antagonism by either antibiosis or competition or through hyperparasitism. The fungus releases, viz. glucanases, chitobioses, and chitinase enzymes, or antibiotics, such as viridin, gliotoxin, or peptaibols [88]. Trichoderma produces a broad range of secondary metabolites, such as trichodermin, gliotoxin, viridin, and peptide antibiotics, which is described in detail in Table 2 [212]. Antibiosis plays a vital part in managing Pythium ultimum and Rhizoctonia solani, which causes the damping of zinnias. Gliotoxin antibiotic produced by biocontrol agent Gliocladium virens prevents R. solani and P. ultimum growth by affecting the membrane and the leakage of metabolites from the respective pathogen [213]. Antibiotics, including gliovirin, viridin, and massilactone, and toxic nonvolatile and volatile metabolites, such as tricholin, alamethicins, and harzianic acid, are produced by Trichoderma strains [214]. Mendoza et al. observed that in an interaction between the Trichoderma spp. HTE815 strain and M. phaseolina, the antibiosis phenomenon is involved. There is formation of an intermediate band without growth between colonies. The culture medium changes color and growth of inhibition zone exist due to secondary metabolite excretion. Filizola et al. presented a study on antibiosis and degree of antagonism and reported that the fungi belonging to Trichoderma genus could potentially prevent the growth of the Fusarium strain [201]. This indicates the specificity between the antagonist and the potential phytopathogen determined by various genes and genetic factors that interact with the environment. Gębarowska et al. investigated the volatile secondary metabolites and biometric parameters from coriander (Coriandrum sativum L.) inoculated with T. harzianum strain T22 and T. asperellum strain. The treatment with liquid suspension spores of Trichoderma increased the yield of essential oil by about 36% without affecting the composition of essential oils, leaving it to the upper limits of pharmacopoeial standards [215]. Moreover, the treatment with Trichoderma spp. limited plant pathogenic fungi belonging to the genus Fusarium. Volatile compounds and proteins secreted by Trichoderma strongly inhibited the growth of bacterial isolates. This observation clarifies that Trichoderma significantly modifies rhizosphere bacterial communities due to the fumigant’s nature of volatile compounds [216]. Gliovirin that is produced by P strains of T. virens is potent against P. ultimum. The Q strains of T. virens also produce gliotoxin that is effective against Rhizoctonia solani [217]. Antimicrobial compounds produced by T. koningii SMF2 have been shown to be active against Gram-positive bacterial and fungal plant pathogens. Trichokonin VI, VII, and VIII are the peptaibols that make up the metabolites. Over a broad pH range and at different temperatures, the Trichokonins remain stable and biologically active [218]. The secondary metabolites produced by the T. harzianum strains T22 and T39 have been investigated. They identified and analysed the chemicals T39 butenolide, harzianopyridone, and harzianopyridone. T39 butenolide and harzianopyridone demonstrated strong activity against G. graminis var. tritici, even at low doses [219]. The mutant of T. virens, deficient in mycoparasitism and antibiotic activity, retained its biocontrol efficacy equivalent to that of the parent strain against Pythium ultimum and R. solani, causing cotton seedling disease [220]. However, it was assumed that this was due to the synergistic effect of enzymes and antibiotic compounds [163]. Several authors have reported the involvement of lytic enzymes in biocontrol agent activity with cellulose and chitin degradation characteristics in Trichoderma spp. [126]. Trichoderma spp. produces extracellular metabolites, which are nonvolatile diffusible chemicals that have an inhibitory impact against fungal pathogens, such as Colletotrichum graminicola. Shorter main roots are a result of higher pyrone concentrations, as shown by Garnica-Vergara et al. [221]. Used concentrations are not always present in nature. Additionally, Lee et al. discovered no association between 6-PP generation and growth stimulation [222]. Gliovirin suppresses the Phytophthora and P. ultimum activity, but it is ineffective in managing the diseases caused by Bacillus thuringenesis, Rhizopus arrhizus, and Rhizoctonia solani [223].

3.4. Biochemical and Molecular Defense Response Induced by Trichoderma

A type of active resistance, known as induced systemic resistance, depends on plant anatomy, such as structural and biochemical barriers. Different physical and biochemical alterations that are indicative of the development of plant-induced systemic resistance occur in plants that are co-cultivated with diverse Trichoderma strains. Callose deposition, cell wall thickening, and tylose development in xylem vessels or cork layers are examples of structural alterations [250]. The accumulation of local and systemic reactive oxygen species (ROS), as well as an increase in the production of signaling molecules and secondary metabolites, such as phytoalexins and PR proteins, was among the biochemical reactions seen in plants. In analyses of experimental Trichoderma strain–plant–pathogen systems, these substances are regarded as indicators of the defense response in plants [251,252,253,254,255]. Hydrogen peroxide (H2O2), an ROS implicated in numerous defensive mechanisms, such as cell wall expansion and lignification, is given a lot of attention. The chemical transmits signals and has the potential to activate calcium channels and peroxidases in cell walls [250]. Oxidative burst enzymes, such as NADPH oxidases attached to the plasma membrane, peroxidases bound to the cell wall, and apoplastic amine oxidases, can either directly or indirectly generate H2O2. It is crucial to note that the accumulation of ROS was not accompanied by cell damage processes, as indicated by the concentration of lipid peroxides. This suggests the activation of mechanisms that suppress the production of hydroxyl radicals (OH) as well as the use of ROS by enzymes, such as peroxidase or catalases, to initiate a biochemical defense response [253,256]. Application with Trichoderma induces the synthesis and accumulation of enzymes, as well as a range of secondary metabolites and signaling molecules, such as salicylic acid (SA), ethylene (ET), and jasmonic acid (JA) (SA) [250,251]. Ethylene and Jasmonic acid are the signaling molecules of ISR, which ultimately are responsible for producing different defense enzymes, such as polyphenol oxidase, peroxidase, catalase, β1-3glucanase, β1-4-glucanase, N-acetylglucosaminidases, and chitinases [106,107]. Trichoderma strains, after colonization, penetration, and establishment inside the root tissue or attachment with the root tissue, lead to an array of enzymatic and morphological changes inside the host plant that finally help in the production of defensive enzymes and, lastly, end with the induction of induced systemic resistance in the plant [108]. Elicitation of ISR response in plants begins with recognising specific components from microbial cell surfaces, known as microbe-associated molecular patterns (MAMPs) by plant receptors [257]. MAMPs from various biocontrol agents have been linked with ISR (Baker et al., 2007; Van Wees et al., 2008). MAMP responses start with generation ion fluxes, reactive oxygen species (ROS), nitric oxide, and ethylene (ET) and later involve the accumulation of callose and the biosynthesis of antimicrobial substances. The first MAMP identified from Trichoderma was ET-inducing xylanase (Xyn2/Eix consisting of five surface-exposed amino acids), eliciting plant defense responses in tomato and tobacco (Rotblat et al., 2002). Trichoderma-activated cellulases also trigger defence response by activating ET and SA pathways (Matinez et al., 2001). Trichoderma proteins involved in root colonization, such as swollen in TasSwo, also trigger defense response in cucumbers (Brotman et al., 2008). Another protein, endopolygalacturonase ThPG1, stimulates the resistance response in Arabidopsis (Moran-Diez et al., 2009). During the colonisation of maize and cotton roots by Trichoderma atroviride and Trichoderma virens, protein Ep11 and Sm1 accumulated in hyphae and act as MAMPs, respectively. Root colonisation by Trichoderma leads to the systemic alteration in the proteome, transcriptome, and MAMP interaction in leaves. Trichoderma interaction with plants leads to elicitor’s production. These elicitors induce the production of signaling molecules, such as jasmonic acid (JA) and ethylene (ET), bind the receptors, and after a series of enzymatic reactions, lead to the induction of defensive genes inside the host plant. These defensive genes are directly responsible for plant pathogen suppression and strengthen the morphological and biochemical barrier of the plants [109]. In vitro inoculation of Trichoderma isolates against Sclerotium rolfsii, Colletotrichum gloeosporioides, and C. capsica inhibits mycelial growth and significantly increases the chitinase and β-1, 3-glucanase activities [39]. This enabled them to promote the plant growth and stimulate defense system against plant pathogens. JA/ET-dependent pathways elicit ISR by Trichoderma and trigger priming responses in plants, such as other beneficial microbes. The interaction of Trichoderma with the plant is dynamic. During this interaction, overlapping the expression of defense-related genes of the JA/ET and SA pathways may occur [102]. It depends on the strains of Trichoderma, the concentrations used, the plant material, the developmental stage of the plant, and the time of interaction. The Trichoderma produces plant hormones ET and IAA. These hormones play a vital part in interconnecting development of plants and their defense responses [103]. The Trichoderma is endowed with genes whose expression in plants helps them manage diseases and imparts resistance to stressed environmental conditions. The experimental evidence shows that interactions of Trichoderma with plants have traits in common with other beneficial microbial associations and they also show their particular lifestyle characteristics of Trichoderma spp. However, more investigations are required to decipher the signaling transduction pathways of defense and development. These pathways result from Trichoderma–plant interactions in the presence of biotic and abiotic stresses [102]. Biotrophs trigger the SA route, whereas necrotrophic pathogens stimulate both the ET and JA pathways [177]. In this defense, PDF1.2 (Plant defensin 1.2), Thi2.1 (Thionin), or Chib (Chitinase B) are commonly used as marker genes [235]. The systemic acquired resistance (SAR) mediated by salicylic acid (SA) results in the expression of pathogenesis-related genes (PR) [236]. These signaling pathways are tightly connected, allowing for fine control of resource allocation between plant development and response to environmental stress agents. To avoid or actively decrease defense barriers, plant enemies frequently modify the underlying network of cross-modulating channels. The necessity to prioritise the response against a specific type of biotic stress has been demonstrated. Then, to comprehend plant defense responses against pests and in the context of a beneficial microbes, molecular pathways must be studied at the metaorganism level. Such research will shed light on the co-evolutionary mechanisms that shape pest and disease communities on plants and provide useful information for creating new pest and pathogen control tactics that mimic and alter plant defensive responses (Figure 2).

3.5. Regulatory Mechanisms Triggering the Defense of Trichoderma

Much research has been conducted on the signal transduction pathways that trigger the genes involved in biocontrol and mycoparasitism. These signal transduction pathways include heterotrimeric G-protein signaling, mitogen-activated protein kinase (MAPK) cascades, and the cAMP pathway. These pathways are all interconnected with one another [258]. The MAP-kinase TVK1, which has been identified in T. virens, including its orthologs in T. asperellum (TmkA) and T. atroviride (TMK1), is particularly important in the regulation of signaling processes that target output pathways important for successful biocontrol [259,260]. T. atroviride tmk1 deletion results in increased antifungal activity and resistance against Rhizoctonia solani but decreased mycoparasitic activity [261]. According to this study, T. virens TVK1 deficiency significantly boosts the fungus biocontrol efficacy [259]. As a result, even though deletion of the corresponding genes reduces mycoparasitic efficacy, the mutant strain biocontrol skills are improved [259].
In terms of the action of the heterotrimeric G-protein signaling pathway in Trichoderma spp., two genes have been studied so far in terms of biocontrol-related mechanisms: the class I (adenylate cyclase inhibiting) G-alpha subunits TGA1 of T. atroviride and TgaA of T. virens, as well as the class III (adenylate cyclase activating) G-alpha subunits TGA3 of T. atroviride and GNA3 of T. reesei. TGA1 is known to regulate coiling around host hyphae as well as the synthesis of antifungal metabolites. The absence of TGA1 causes host fungus to develop more slowly [262,263]. TgaA has been linked to a host-specific role, similar to that seen with MAP-kinases [264]. On the other hand, TGA3 is essential for biocontrol, as the absence of the corresponding gene led to the development of non-pathogenic strains [265]. Because it has been hypothesised that mycoparasitism can be favorably affected by the constitutive activation of GNA3 in T. reesei, a similar mechanism is at work on this fungus [266]. These findings are consistent with the analysis of cAMP signaling components, which show that cAMP has a beneficial function in biocontrol [267].
Efforts were made to identify characteristics among each of these genes and enzymes that were regulated upon the interaction of Trichoderma with a pathogen. These characteristics could be used to differentiate efficient biocontrol strains isolated from nature that were less effective [268,269]. However, the effectiveness of standardised marker gene assays for the assessment of the potential biocontrol strains will not be known until after additional and more in-depth research has been conducted.

3.6. Plant Growth Promotion

A plant’s root system is colonised by microbial organisms, which simultaneously protect the plant from soil-borne diseases and stimulate growth [270]. These positive plant–microbe interactions frequently occur in the rhizosphere, enhancing plant growth or aiding the plant in resisting abiotic or biotic stresses [271]. Trichoderma spp. multiplies in the rhizosphere, forming a mutual association that naturally enhances plant nutrition and growth. It can colonise roots, boosting plant nutrition, growth, and development, as well as abiotic stress resistance. Plant growth is typically attributed to an indirect effect of plant disease management when biological control agents are used. T. harzianum was also found to enhance the concentration of trace and essential elements, such as Zn, Fe, Cu, Mn, Cu, Ca, Mg, P, N, K, and Na, in the shoots and roots of cucumber and tomato seedlings [272]. It has the ability to produce a number of phytohormones, siderophores, and phosphate-solubilizing enzymes [273]. Phytohormones enhance the absorptive surface of plant roots by stimulating root development. It has been established that plant antimicrobial chemicals produced by Trichoderma can stimulate plant growth. Isolated compounds, such as Trichocereus A-D, Harzianopyridone, koninginins, 6PP, cyclonerodiol, harzianic acid (HA), and harzianolide, that helped plant growth promotion are dependent on the concentration of compounds. Cerinolactone, a novel secondary metabolite identified from Trichoderma cerinums, was found to have a beneficial impact on tomato seedling growth 3 days after treatment. Similarly, the iron-binding properties of HA and iso-harzianic acid reported in T. harzianum metabolites are known to enhance plant growth [274]. T. virens and T. atroviride have also produced indole-3-acetic acid-related indoles (IAA-related indoles). The incorporation of L-tryptophan into Trichoderma liquid cultures increased the IAA-related indoles production. This finding suggested that Trichoderma production of IAA-related indoles may be one of the processes used by the fungus to enhance plant development and secondary root number, resulting in increased biomass in Arabidopsis [275]. Trichoderma plant-growth-promoting action could be due to these pathways [16]. Trichoderma spp. application results in enhanced vegetative growth on various crop plants. Trichoderma spp. interactions with plants resulted in increased resistance against plant diseases [276]. Increased productivity, biomass, nutrient uptake, and stress tolerance are signs of improved plant growth [277]. Trichoderma isolates from the rhizosphere of the mangrove Avicennia marina solubilize P from insoluble Ca3(PO4)2—an extracellular phytase activity and acidic phosphatase had been exclusively enhanced in the presence of Ca3(PO4)2 [278]. Furthermore, it has been found that using Trichoderma spp. in a consortium improves the physical strength and durability of the plant’s cell wall in the presence of cell wall degrading plant pathogenic fungi [279,280]. The improvement in root growth is likely the result of one or more mechanisms, including an increase in the rate of carbohydrate photosynthetic activities, a higher rate of plant growth regulation, an increase in rooting depth, and, thus, greater tolerance to drought environments [281]. When there are rich inorganic soil substrates, such as bioorganic fertilisers, Trichoderma spp. is more successful in colonising and boosting plant growth [282].

4. Conclusions and Future Prospects

The Trichoderma—plant—pathogen interaction is a multi-dependent and dynamic system. A thorough understanding of Trichoderma mechanisms with plants and pathogens can significantly improve the efficacy of their actions. Trichoderma employs a wide range of complex direct and indirect biocontrol mechanisms to protect itself from biotic stresses, such as pathogenic microbes (bacteria, fungi, and nematodes). This review explains why Trichoderma spp. has earned its well-deserved track record as a powerful plant growth promoter, with the added benefit of enhancing localised and systemic resistance in plants. This is because Trichoderma spp. is capable of producing a broad range of antibiotic substances and synthesising so many secondary metabolites, each of which has the possibility to parasitise a broad range of pathogenic fungi inside the rhizosphere. Trichoderma elicitors and effectors are recognised by plant receptors, which begin the signaling process and govern the genetic composition of the host. This provides the foundation for these symbionts to trigger the defensive metabolism in their host. To verify a database for the responsible and long-term usage of Trichoderma, it is necessary to examine the ecological impact of extensive applications of biocontrol agents and their secondary metabolites. Because of this, Trichoderma genomes are a valuable source of gene candidates for creating transgenic plants resistant to both biotic and abiotic stresses. Finally, in the age of a green economy focused on protecting both human health and the environment, the use of Trichoderma species should be encouraged as a viable alternative to pesticides in light of the information presented in this research. Additionally, the current, thorough, developed, and yet affordable, quick, and successful ways of detecting and evaluating antagonists, integrating multiple mechanisms of action with cascade reactions, must be developed and used in Trichoderma research. The research will also focus on determining the risk of using BCAs based on Trichoderma, as well as their toxicity and ecotoxicity, not only in vitro but also in natural farming practices in vitro and in situ, before they are commercialised as biostimulations, biocontrols, or bioremediation preparations. In conclusion, it can be said that more research must be conducted to know the mechanism of Trichoderma spp. in detail so that potent Trichoderma biofungicides can flourish in any type of environment. The social anxiety of implementing new antifungal and antibacterial microbes into the environment must be overcome.

Author Contributions

Conceptualization, writing—original draft preparation, N.M.; Writing—review and editing, A.S.K. and N.M.; writing—original draft preparation, investigation, A.S.K., N.M., M.V.S.R. and R.S.G.; supervision, funding acquisition, H.V.S., S.K.S. and P.K.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by ICAR-NBAIM, Maunath Bhanjan, Uttar Pradesh.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Acknowledgments

The authors extend their gratitude to the Indian Council of Agricultural Research, New Delhi, ICAR-National Bureau of Agriculturally Important Microorganisms, Maunath Bhanjan, U.P India, for providing financial assistance during the study. The authors wish to express their sincere thanks to Faheem Ahamad and Pusparaj for assistance during the time period of these studies.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. 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. [Google Scholar] [CrossRef] [PubMed]
  2. Velásquez, A.C.; Castroverde, C.D.M.; He, S.Y. Plant-Pathogen Warfare under Changing Climate Conditions. Curr. Biol. 2018, 28, R619–R634. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Hashimi, M.H.; Hashimi, R.; Ryan, Q. Toxic effects of pesticides on humans, plants, animals, pollinators and beneficial organisms. Asian Plant Res. J. 2020, 5, 37–47. [Google Scholar] [CrossRef]
  4. Kohl, 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] [PubMed] [Green Version]
  5. Pazini, W.C.; Galli, J.C. Reduction of insecticides applications through the adoption of integrated management tactics of Triozoida limbata (Enderlein, 1918) (Hemiptera: Triozidae) in guava tree. Rev. Bras. Frutic. 2011, 33, 66–72. [Google Scholar] [CrossRef] [Green Version]
  6. Lahlali, R.; Ezrari, S.; Radouane, N.; Kenfaoui, J.; Esmaeel, Q.; El Hamss, H.; Belabess, Z.; Barka, E.A. Biological Control of Plant Pathogens: A Global Perspective. Microorganisms 2022, 10, 596. [Google Scholar] [CrossRef]
  7. Thambugala, K.M.; Daranagama, D.A.; Phillips, A.J.L.; Kannangara, S.D.; Promputtha, I. Fungi vs. Fungi in Biocontrol: An Overview of Fungal Antagonists Applied Against Fungal Plant Pathogens. Front. Cell. Infect. Microbiol. 2020, 10, 604923. [Google Scholar] [CrossRef] [PubMed]
  8. Alfiky, A.; Weisskopf, L. Deciphering Trichoderma–Plant–Pathogen Interactions for Better Development of Biocontrol Applications. J. Fungi 2021, 7, 61. [Google Scholar] [CrossRef] [PubMed]
  9. Ghasemi, S.; Safaie, N.; Shahbazi, S.; Askari, H. Enhancement of Lytic Enzymes Activity and Antagonistic Traits of Trichoderma harzianum Using γ-Radiation Induced Mutation. J. Agric. Sci. Technol. 2019, 21, 1035–1048. [Google Scholar]
  10. Persoon, C.H. Disposita methodical fungorum. Romers. Neues. Mag. Bot. 1794, 1, 81–128. [Google Scholar]
  11. 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]
  12. Poveda, J. Trichoderma as biocontrol agent against pests: New uses for a mycoparasite. Biol. Control 2021, 159, e104634. [Google Scholar] [CrossRef]
  13. Elad, Y. Biological Control of Foliar Pathogens by Means of Trichoderma harzianum and Potential Modes of Action. Crop Prot. 2000, 19, 709–714. [Google Scholar] [CrossRef]
  14. Yadav, M.; Dubey, M.K.; Upadhyay, R.S. Systemic Resistance in Chilli Pepper against Anthracnose (Caused by Colletotrichum truncatum) Induced by Trichoderma harzianum, Trichoderma asperellum and Paenibacillus dendritiformis. J. Fungi 2021, 7, 307. [Google Scholar] [CrossRef] [PubMed]
  15. Zin, N.A.; Badaluddin, N.A. Biological functions of Trichoderma spp. for agriculture applications. Ann. Agric. Sci. 2020, 65, 168–178. [Google Scholar] [CrossRef]
  16. Tyśkiewicz, R.; Nowak, A.; Ozimek, E.; Jaroszuk-Ściseł, J. Trichoderma: The Current Status of Its Application in Agriculture for the Biocontrol of Fungal Phytopathogens and Stimulation of Plant Growth. Int. J. Mol. Sci. 2022, 23, 2329. [Google Scholar] [CrossRef] [PubMed]
  17. Bahadur, A.; Dutta, P. Trchoderma Spp.: Their Impact in Crops Diseases Management. In Trichoderma—Technology and Uses; IntechOpen: London, UK, 2022. [Google Scholar]
  18. Zhao, Y.; Chen, X.; Cheng, J.; Xie, J.; Lin, Y.; Jiang, D.; Fu, Y.; Chen, T. Application of Trichoderma Hz36 and Hk37 as Biocontrol Agents against Clubroot Caused by Plasmodiophora brassicae. J. Fungi 2022, 8, 777. [Google Scholar] [CrossRef] [PubMed]
  19. Khan, R.A.A.; Najeeb, S.; Hussain, S.; Xie, B.; Li, Y. Bioactive Secondary Metabolites from Trichoderma spp. against Phytopathogenic Fungi. Microorganisms 2020, 8, 817. [Google Scholar] [CrossRef]
  20. Fiorentino, N.; Ventorino, V.; Woo, S.L.; Pepe, O.; De Rosa, A.; Gioia, L.; Romano, I.; Lombardi, N.; Napolitano, M.; Colla, G.; et al. Trichoderma-Based Biostimulants Modulate Rhizosphere Microbial Populations and Improve N Uptake Efficiency, Yield, and Nutritional Quality of Leafy Vegetables. Front. Plant Sci. 2018, 9, 743. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  21. 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] [Green Version]
  22. Ghasemi, S.; Safaie, N.; Shahbazi, S.; Shams-Bakhsh, M.; Askari, H. The Role of Cell Wall Degrading Enzymes in Antagonistic Traits of Trichoderma virens Against Rhizoctonia solani. Iran J. Biotechnol. 2020, 18, e2333. [Google Scholar] [CrossRef] [PubMed]
  23. Silva, J. A novel Trichoderma reesei mutant RP698 with enhanced cellulase production. Braz. J. Microbiol. 2020, 51, 537–545. [Google Scholar] [CrossRef] [PubMed]
  24. Aoki, Y.; Haga, S.; Suzuki, S.; Llorens, E. Direct antagonistic activity of chitinase produced by Trichoderma sp. SANA20 as biological control agent for grey mould caused by Botrytis cinerea. Cogent Biol. 2020, 6, 1. [Google Scholar] [CrossRef]
  25. Schalamun, M.; Schmoll, M. Trichoderma—Genomes and genomics as treasure troves for research towards biology, biotechnology and agriculture. Front. Fungal Biol. 2022, 3, 1002161. [Google Scholar] [CrossRef]
  26. Wu, W.; Ogawa, F.; Ochiai, M.; Yamada, K.; Fukui, H. Common Strategies to Control Pythium Disease. Rev. Agric. Sci. 2020, 8, 58–69. [Google Scholar] [CrossRef]
  27. Escudero-Leyva, E.; Alfaro-Vargas, P.; Muñoz-Arrieta, R.; Charpentier-Alfaro, C.; Granados-Montero, M.D.M.; Valverde-Madrigal, K.S.; Pérez-Villanueva, M.; Méndez-Rivera, M.; Rodríguez-Rodríguez, C.E.; Chaverri, P.; et al. Tolerance and Biological Removal of Fungicides by Trichoderma Species Isolated From the Endosphere of Wild Rubiaceae Plants. Front. Agron. 2022, 3, 772170. [Google Scholar] [CrossRef]
  28. Mendoza, A.M.; Zaid, R.; Lawry, R.; Hermosa, R.; Monte, E.; Horwitz, B.A.; Mukherjee, P.K. Molecular dialogues between Trichoderma and roots: Role of the fungal secretome. Fungal Biol. Rev. 2018, 32, 62–85. [Google Scholar] [CrossRef]
  29. Mukherjee, P.K.; Mendoza-Mendoza, A.; Zeilinger, S.; Horwitz, B.A. Mycoparasitism as a mechanism of Trichoderma-mediated suppression of plant diseases. Fungal Biol. Rev. 2022, 39, 15–33. [Google Scholar] [CrossRef]
  30. Kredics, L.; Chen, L.; Kedves, O.; Büchner, R.; Hatvani, L.; Allaga, H.; Nagy, V.D.; Khaled, J.M.; Alharbi, N.S.; Vágvölgyi, C. Molecular Tools for Monitoring Trichoderma in Agricultural Environments. Front. Microbiol. 2018, 9, 1599. [Google Scholar] [CrossRef] [PubMed]
  31. Hewedy, O.A.; Abdel Lateif, K.S.; Seleiman, M.F.; Shami, A.; Albarakaty, F.M.; El-Meihy, M.R. Phylogenetic Diversity of Trichoderma Strains and Their Antagonistic Potential against Soil-Borne Pathogens under Stress Conditions. Biology 2020, 9, 189. [Google Scholar] [CrossRef] [PubMed]
  32. Raja, H.A.; Miller, A.N.; Pearce, C.J.; Oberlies, N.H. Fungal identification using molecular tools: A primer for the natural products research community. J. Nat. Prod. 2017, 80, 756–770. [Google Scholar] [CrossRef] [PubMed]
  33. Al-Ani, L.K.T. Trichoderma from extreme environments: Physiology, diversity, and antagonistic activity. In Extremophiles in Eurasian Ecosystems: Ecology, Diversity, and Applications; Springer: Singapore, 2018; Volume 8, pp. 389–403. [Google Scholar]
  34. Gu, X.; Wang, R.; Sun, Q.; Wu, B.; Sun, J.-Z. Four new species of Trichoderma in the Harzianum clade from northern China. MycoKeys 2020, 73, 109–132. [Google Scholar] [CrossRef] [PubMed]
  35. Jang, S.; Kwon, S.L.; Lee, H.; Jang, Y.; Park, M.S.; Lim, Y.W.; Kim, C.; Kim, J.-J. New Report of Three Unrecorded Species in Trichoderma harzianum Species Complex in Korea. Mycobiology 2018, 46, 177–184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Chammem, H.; Antonielli, L.; Nesler, A.; Pindo, M.; Pertot, I. Effect of a Wood-Based Carrier of Trichoderma atroviride SC1 on the Microorganisms of the Soil. J. Fungi 2021, 7, 751. [Google Scholar] [CrossRef]
  37. Chauhan, A.; Modgil, M.; Rajam, M. Establishment of Agrobacterium tumefaciens—Mediated genetic transformation of apple pathogen Marssonina coronaria using marker genes under the control of CaMV 35S promoter. Microbiol. Res. 2021, 253, 126878. [Google Scholar] [CrossRef]
  38. Nogueira-López, G.; Padilla-Arizmendi, F.; Inwood, S.; Lyne, S.; Steyaert, J.M.; Nieto-Jacobo, M.F.; Stewart, A.; Mendoza-Mendoza, A. TrichoGate: An Improved Vector System for a Large Scale of Functional Analysis of Trichoderma Genes. Front. Microbiol. 2019, 10, 2794. [Google Scholar] [CrossRef]
  39. Scandella, V.; Paolicelli, R.C.; Knobloch, M. A novel protocol to detect green fluorescent protein in unfixed, snap-frozen tissue. Sci. Rep. 2020, 10, 14642. [Google Scholar] [CrossRef]
  40. Nichols, N.N.; Quarterman, J.C.; Frazer, S.E. Use of green fluorescent protein to monitor fungal growth in biomass hydrolysate. Biol. Methods Protoc. 2018, 3, bpx012. [Google Scholar] [CrossRef] [Green Version]
  41. Moreno-Ruiz, D.; Fuchs, A.; Missbach, K.; Schuhmacher, R.; Zeilinger, S. Influence of Different Light Regimes on the Mycoparasitic Activity and 6-Pentyl-alpha-pyrone Biosynthesis in Two Strains of Trichoderma atroviride. Pathogens 2020, 9, 860. [Google Scholar] [CrossRef]
  42. Speckbacher, V.; Ruzsanyi, V.; Martinez-Medina, A.; Hinterdobler, W.; Doppler, M.; Schreiner, U.; Böhmdorfer, S.; Beccaccioli, M.; Schuhmacher, R.; Reverberi, M. The lipoxygenase Lox1 is involved in light-and injury-response, conidiation, andvolatile organic compound biosynthesis in the Mycoparasitic fungus Trichoderma atroviride. Front. Microbiol. 2020, 11, 2004. [Google Scholar] [CrossRef]
  43. Zhang, G.-Z.; Yang, H.-T.; Zhang, X.-J.; Zhou, F.-Y.; Wu, X.-Q.; Xie, X.-Y.; Zhao, X.-Y.; Zhou, H.-Z. Five new species of Trichoderma from moist soils in China. MycoKeys 2022, 87, 133–157. [Google Scholar] [CrossRef] [PubMed]
  44. Miller, J.H.; Giddens, J.E.; Foster, A.A. A survey of the fungi of forest and cultivated soils of Georgia. Mycologia 1975, 49, 779–808. [Google Scholar] [CrossRef]
  45. Alwadai, A.S.; Perveen, K.; Alwahaibi, M. The Isolation and Characterization of Antagonist Trichoderma spp. from the Soil of Abha, Saudi Arabia. Molecules 2022, 27, 2525. [Google Scholar] [CrossRef] [PubMed]
  46. Bustamante, D.E.; Calderon, M.S.; Leiva, S.; Mendoza, J.E.; Arce, M.; Oliva, M. Three new species of Trichoderma in the Harzianum and Longibrachiatum lineages from Peruvian cacao crop soils based on an integrative approach. Mycologia 2021, 113, 1056–1072. [Google Scholar] [CrossRef] [PubMed]
  47. Gams, W.; Meyer, W. What exactly is Trichoderma harzianum? Mycologia 1998, 90, 904–915. [Google Scholar] [CrossRef]
  48. Ospina-Giraldo, M.D.; Royse, D.J.; Chen, X.; Romaine, C.P. Molecular phylogenetic analyses of biological control strains of Trichoderma harzianum and other biotypes of Trichoderma spp. associated with mushroom green mold. Phytopathology 1999, 89, 308–313. [Google Scholar] [CrossRef] [Green Version]
  49. Kuhls, K.; Lieckfeldt, E.; Samuels, G.J.; Meyer, W.; Kubicek, C.P.; Borner, T. Revision of Trichoderma sec. Longibrachiatum including related teleomorphs based on analysis of ribosomal DNA internal transcribed spacer regions. Mycologia 1997, 89, 442–460. [Google Scholar]
  50. Kindermann, J.; El-Ayouti, Y.; Samuels, G.J.; Kubicek, C.P. Phylogeny of the genus Trichoderma based on sequence analysis of the internal transcribed spacer region 1 of the rDNA cluster. Fungal Genet. Biol. 1998, 24, 298–309. [Google Scholar] [CrossRef] [Green Version]
  51. Matas-Baca, M.Á.; Urías García, C.; Pérez-Álvarez, S.; Flores-Córdova, M.A.; Escobedo-Bonilla, C.M.; Magallanes-Tapia, M.A.; Sánchez Chávez, E. Morphological and molecular characterization of a new autochthonous Trichoderma sp. isolate and its biocontrol efficacy against Alternaria sp. Saudi J. Biol. Sci. 2022, 29, 2620–2625. [Google Scholar] [CrossRef]
  52. Meyer, R.; Plaskowitz, J.S. Scanning electron microscopy of conidia and conidial matrix of Trichoderma. Mycologia 1989, 81, 312–317. [Google Scholar] [CrossRef]
  53. Lieckfeldt, E.; Samuels, G.J.; Helgard, H.I.; Petrini, O. A morphological and molecular perspective of Trichoderma viride: Is it one or two species? Appl. Environ. Microbiol. 1999, 65, 2418–2428. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Samuels, G.J.; Lieckfeldt, E.; Nirenberg, H.I. Description of T. asperellum sp. nov. and comparison to T. viride. Sydowia 1999, 51, 71–88. [Google Scholar]
  55. Cai, F.; Druzhinina, I.S. In honor of John Bissett: Authoritative guidelines on molecular identification of Trichoderma. Fungal Divers. 2021, 107, 1–69. [Google Scholar] [CrossRef]
  56. Wang, R.; Liu, C.; Jiang, X.; Tan, Z.; Li, H.; Xu, S.; Zhang, S.; Shang, Q.; Deising, H.B.; Behrens, S.-E.; et al. The Newly Identified Trichoderma harzianum Partitivirus (ThPV2) Does Not Diminish Spore Production and Biocontrol Activity of Its Host. Viruses 2022, 14, 1532. [Google Scholar] [CrossRef]
  57. 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]
  58. Arisan-Atac, I.; Heidenreich, E.; Kubicek, C.P. Randomly amplified polymorphic DNA fingerprinting identifies subgroups of Trichoderma viride and other Trichoderma sp. capable of chestnut blight biocontrol. FEMS Microbiol. Lett. 1995, 126, 249–255. [Google Scholar] [CrossRef] [PubMed]
  59. Bowen, J.; Franicevic, S.; Crowhurst, R.; Templeton, M.; Stewart, A. Differentiation of a specific Trichoderma biological control agent by restriction fragment length polymorphism (RFLP) analysis. N. Z. J. Crop Hortic. Sci. 1996, 24, 207–217. [Google Scholar] [CrossRef]
  60. Turoczi, G.; Fekete, C.; Kerényi, Z.; Nagy, R.; Pomázi, A.; Hornok, L. Biological and molecular characterisation of potential biocontrol strains of Trichoderma. J. Basic Microbiol. 1996, 36, 63–72. [Google Scholar] [CrossRef] [PubMed]
  61. Chakraborty, B.; Chakraborty, U.; Saha, A.; Dey, P.; Sunar, K. Molecular characterization of Trichoderma viride and Trichoderma harzianum isolated from soils of North Bengal based on rDNA markers and analysis of their PCR-RAPD profiles. Glob. J. Biotechnol. Biochem. 2010, 5, 55–61. [Google Scholar]
  62. An, X.-Y.; Cheng, G.-H.; Gao, H.-X.; Li, X.-F.; Yang, Y.; Li, D.; Li, Y. Phylogenetic Analysis of Trichoderma Species Associated with Green Mold Disease on Mushrooms and Two New Pathogens on Ganoderma sichuanense. J. Fungi 2022, 8, 704. [Google Scholar] [CrossRef]
  63. Turner, D.; Kovacs, W.; Kuhls, K.; Lieckfeldt, E.; Peter, B.; Arisan-Atac, I.; Strauss, J.; Samuels, G.J.; Börner, T.; Kubicek, C.P. Biogeography and phenotypic variation in Trichoderma sect. Longibrachiatum and associated Hypocrea species. Mycol. Res. 1997, 101, 449–459. [Google Scholar]
  64. 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. Nature Reviews. Microbiology 2011, 9, 749–759. [Google Scholar]
  65. Kullnig-Gradinger, C.M.; Szakacs, G.; Kubicek, C.P. Phylogeny and evolution of the genus Trichoderma: A multigene approach. Mycol. Res. 2002, 106, 757–767. [Google Scholar] [CrossRef]
  66. Kullnig, C.M.; Krupica, T.; Woo, S.L.; Mach, R.L.; Rey, M.; Benítez, T.; Lorito, M.; Kubicek, C.P. Confusion abounds over identities of Trichoderma biocontrol isolates. Mycol. Res. 2001, 105, 769–772. [Google Scholar] [CrossRef]
  67. Druzhinina, I.S.; Kopchinskiy, A.G.; Komon, M.; Bissett, J.; Szakacs, G.; Kubicek, C.P. An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genet. Biol. 2005, 42, 813–828. [Google Scholar] [CrossRef]
  68. Kopchinskiy, A.; Komon, M.; Kubicek, C.P.; Druzhinina, I.S. TrichoBLAST: A multilocus database for Trichoderma and Hypocrea identifications. Mycol. Res. 2005, 109, 658–660. [Google Scholar] [CrossRef]
  69. Samuels, G.J.; Chaverri, P.; Farr, D.F.; McCray, E.B. Trichoderma Online. Systematic Mycology and Microbiology Laboratory, ARS, USDA. 2002. Available online: http://nt.ars-grin.gov/taxadescriptions/keys/TrichodermaIndex.cfm (accessed on 16 April 2010).
  70. Chaverri, P.; Castlebury, L.A.; Samuels, G.J.; Geiser, D. Multilocus phylogenetic structure within the Trichoderma harzianum/Hypocrea lixii complex. Mol. Phylogenet. Evol. 2003, 27, 302–313. [Google Scholar] [CrossRef]
  71. Dou, K.; Gao, J.X.; Zhang, C.L.; Yang, H.T.; Jiang, X.L.; Li, J.S.; Li, Y.Q.; Wang, W.; Xian, H.Q.; Li, S.G.; et al. Trichoderma biodiversity in major ecological systems of China. J. Microbiol. 2019, 57, 668–675. [Google Scholar] [CrossRef]
  72. Samuels, G.J.; Dodd, S.L.; Gams, W.; Castlebury, L.A.; Petrini, O. Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia 2002, 94, 146. [Google Scholar] [CrossRef] [PubMed]
  73. Filizola, P.R.B.; Luna, M.A.C.; de Souza, A.F.; Coelho, I.L.; Laranjeira, D.; Campos-Takaki, G.M. Biodiversity and phylogeny of novel Trichoderma isolates from mangrove sediments and potential of biocontrol against Fusarium strains. Microb. Cell Factories 2019, 18, 89. [Google Scholar] [CrossRef] [PubMed]
  74. Kullnig, C.; Szakacs, G.; Kubicek, C.P. Molecular identification of Trichoderma species from Russia, Siberia and the Himalaya. Mycol. Res. 2000, 104, 1117–1125. [Google Scholar] [CrossRef]
  75. Felix, C.R.; Noronha, E.F.; Miller, R.N. Trichoderma: A dual function fungi and their use in the wine and beer industries. In Biotechnology and Biology of Trichoderma; Elsevier: Amsterdam, The Netherlands, 2014; pp. 345–349. [Google Scholar]
  76. Chaverri, P.; Branco-Rocha, F.; Jaklitsch, W.; Gazis, R.; Degenkolb, T.; Samuels, G.J. Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia 2015, 107, 558–590. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  77. Qiao, M.; Du, X.; Zhang, Z.; Xu, J.; Yu, Z. Three new species of soil-inhabiting Trichoderma from southwest China. MycoKeys 2018, 44, 63. [Google Scholar] [CrossRef] [Green Version]
  78. Jaklitsch, W.M.; Voglmayr, H. Biodiversity of Trichoderma (Hypocreaceae) in Southern Europe and Macaronesia. Stud. Mycol. 2015, 80, 1–87. [Google Scholar] [CrossRef] [Green Version]
  79. Ru, Z.; Di, W. Trichoderma spp. from rhizosphere soil and their antagonism against Fusarium sambucinum. Afr. J. Biotechnol. 2012, 11, 4180–4186. [Google Scholar]
  80. Kumar, K.; Amaresan, N.; Bhagat, S.; Madhuri, K.; Srivastava, R. Isolation and characterization of Trichoderma spp. for antagonistic activity against root rot and foliar pathogens. Indian J. Microbiol. 2012, 52, 137–144. [Google Scholar] [CrossRef] [Green Version]
  81. Bellemain, E.; Carlsen, T.; Brochmann, C.; Coissac, E.; Taberlet, P.; Kauserud, H. ITS as an environmental DNA barcode for fungi: An in silico approach reveals potential PCR biases. BMC Microbiol. 2010, 10, 189. [Google Scholar] [CrossRef] [Green Version]
  82. Bubici, G.; Kaushal, M.; Prigigallo, M.I.; Gómez-Lama Cabanás, C.; Mercado-Blanco, J. Biological control agents against fusarium wilt of banana. Front. Microbiol. 2019, 10, 616. [Google Scholar] [CrossRef] [PubMed]
  83. Du Plessis, I.L.; Druzhinina, I.S.; Atanasova, L.; Yarden, O.; Jacobs, K. The diversity of Trichoderma species from soil in South Africa, with five new additions. Mycologia 2018, 110, 559–583. [Google Scholar] [CrossRef]
  84. Logrieco, A.; Moretti, A.; Ritieni, A.; Bottalico, A.; Corda, P. Occurrence and toxigenicity of Fusarium proliferatum from preharvest maize ear rot, and associated mycotoxins, in Italy. Plant Dis. 1995, 79, 727–731. [Google Scholar] [CrossRef]
  85. Bissett, J. A revision of the genus Trichoderma. I. Section Longibrachiatum sect. nov. Can. J. Bot. 1984, 62, 924–931. [Google Scholar] [CrossRef]
  86. Bissett, J. A revision of the genus Trichoderma. IV. Additional notes on section Longibrachiatum. Can. J. Bot. 1991, 69, 2418–2420. [Google Scholar] [CrossRef]
  87. Samuels, G.J. Trichoderma: A review of biology and systematics of the genus. Fungal Biol. 1996, 100, 923–935. [Google Scholar] [CrossRef]
  88. Dou, K.; Lu, Z.; Wu, Q.; Ni, M.; Yu, C.; Wang, M.; Li, Y.; Wang, X.; Xie, H.; Chen, J.; et al. MIST: A multilocus identification system for Trichoderma. Appl. Environ. Microbiol. 2020, 86, e01532-20. [Google Scholar] [CrossRef]
  89. Hermosa, M.; Grondona, I.; Iturriaga, E.T.; Diaz-Minguez, J.; Castro, C.; Monte, E.; Garcia-Acha, I. Molecular characterization and identification of biocontrol isolates of Trichoderma spp. Appl. Environ. Microbiol. 2000, 66, 1890–1898. [Google Scholar] [CrossRef] [Green Version]
  90. Manzar, N.; Singh, Y.; Kashyap, A.S.; Sahu, P.K.; Rajawat, M.V.S.; Bhowmik, A.; Sharma, P.K.; Saxena, A.K. Biocontrol potential of native Trichoderma spp. against anthracnose of great millet (Sorghum bicolour L.) from Tarai and hill regions of India. Biol. Control 2020, 152, 104474. [Google Scholar] [CrossRef]
  91. Oskiera, M.; Szczech, M.; Bartoszewski, G. Molecular identification of Trichoderma strains collected to develop plant growth-promoting and biocontrol agents. J. Hort. Res. 2015, 23, 75–86. [Google Scholar] [CrossRef] [Green Version]
  92. Schlick, A.; Kuhls, K.; Meyer, W.; Lieckfeldt, E.; Börner, T.; Messner, K. Fingerprinting reveals gamma-ray induced mutations in fungal DNA: Implications for identification of patent strains of Trichoderma harzianum. Curr. Genet. 1994, 26, 74–78. [Google Scholar] [CrossRef]
  93. Zimand, G.; Valinsky, L.; Elad, Y.; Chet, I.; Manulis, S. Use of the RAPD procedure for the identification of Trichoderma strains. Mycological Research 1994, 98, 531–534. [Google Scholar] [CrossRef]
  94. Dodd, S.L.; Hill, R.A.; Stewart, A. A duplex-PCR bioassay to detect a Trichoderma virens biocontrol isolate in non-sterile soil. Soil Biol. Biochem. 2004, 36, 1955–1965. [Google Scholar] [CrossRef]
  95. Freeman, S.; Barbul, O.; David, D.R.; Nitzani, Y.; Zveibil, A.; Elad, Y. Trichoderma spp. for biocontrol of Colletotrichum acutatum and Botrytis cinerea in strawberry. Eur. J. Plant Pathol. 2004, 110, 361–370. [Google Scholar] [CrossRef]
  96. Fanti, S.; Barbieri, A.; Vannacci, G. Environmental Monitoring of Antagonistic Trichoderma. In Proceedings of the First FEMS Congress of European Microbiologists, Ljubljana, Slovenia, 29 June–3 July 2003; p. 390. [Google Scholar]
  97. Zhang, Y.; Wang, X.; Pang, G.; Cai, F.; Shen, Q. Two-step genomic sequence comparison strategy to design Trichoderma strain-specific primers for quantitative PCR. AMB Express 2019, 9, 179. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  98. Paran, I.; Michelmore, R.W. Development of reliable PCR-based markers linked to downy mildew resistance genes in lettuce. Theor. Appl. Genet. 1993, 85, 985–993. [Google Scholar] [CrossRef] [PubMed]
  99. Geistlinger, J.; Zwanzig, J.; Heckendorff, S.; Schellenberg, I. SSR markers for Trichoderma virens: Their evaluation and application to identify and quantify root-endophytic strains. Diversity 2015, 7, 360–384. [Google Scholar] [CrossRef] [Green Version]
  100. Perez, G.; Verdejo, V.; Gondim-Porto, C.; Orlando, J.; Caru, M. Designing a SCAR molecular marker for monitoring Trichoderma harzianum in experimental communities. J. Zhejiang Univ. Sci. 2014, 15, 966–978. [Google Scholar] [CrossRef] [Green Version]
  101. Chandler, D.P.; Kukhtin, A.; Mokhiber, R.; Knickerbocker, C.; Ogles, D.; Rudy, G.; Golova, J.; Long, P.; Peacock, A. Monitoring microbial community structure and dynamics during in situ U (VI) bioremediation with a field-portable microarray analysis system. Environ. Sci. Technol. 2010, 44, 5516–5522. [Google Scholar] [CrossRef]
  102. Atanasova, L.; Crom, S.L.; Gruber, S.; Coulpier, F.; Seidl-Seiboth, V.; Kubicek, C.P.; Druzhinina, I.S. Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genom. 2013, 14, 121. [Google Scholar] [CrossRef] [Green Version]
  103. Hatvani, L. Mushroom Pathogenic Trichoderma Species: Occurrence, Biodiversity, Diagnosis and Extracellular Enzyme Production. Ph.D. Thesis, University of Szeged, Szeged, Hungary, 2008. [Google Scholar]
  104. Longa, C.M.O.; Savazzini, F.; Tosi, S.; Elad, Y.; Pertot, I. Evaluating the survival and environmental fate of the biocontrol agent Trichoderma atroviride SC1 in vineyards in northern Italy. J. Appl. Microbiol. 2009, 106, 1549–1557. [Google Scholar] [CrossRef]
  105. Savazzini, F.; Longa, C.M.O.; Pertot, I.; Gessler, C. Real-time PCR for detection and quantification of the biocontrol agent Trichoderma atroviride strain SC1 in soil. J. Microbiol. Methods 2008, 73, 185–194. [Google Scholar] [CrossRef]
  106. Peng, Y.; Li, S.J.; Yan, J.; Tang, Y.; Cheng, J.P.; Gao, A.J.; Yao, X.; Ruan, J.J.; Xu, B.L. Research Progress on Phytopathogenic Fungi and Their Role as Biocontrol Agents. Front. Microbiol. 2021, 12, 670135. [Google Scholar] [CrossRef]
  107. Vargas Gil, S.; Meriles, J.; Conforto, C.; Figoni, G.; Basanta, M.; Lovera, E.; March, G.J. Field assessment of soil biological and chemical quality in response to crop management practices. World J. Microbiol. Biotechnol. 2009, 25, 439–448. [Google Scholar] [CrossRef]
  108. Sherriff, C.; Whelan, M.J.; Arnold, G.M.; Lafay, J.-F.; Brygoo, Y.; Bailey, J.A. Ribosomal DNA sequence analysis reveals new species groupings in the genus Colletotrichum. Exp. Mycol. 1994, 18, 121–138. [Google Scholar] [CrossRef]
  109. López-Mondéjar, R.; Antón, A.; Raidl, S.; Ros, M.; Pascual, J.A. Quantification of the biocontrol agent Trichoderma harzianum with real-time TaqMan PCR and its potential extrapolation to the hyphal biomass. Bioresour. Technol. 2010, 101, 2888–2891. [Google Scholar] [CrossRef] [PubMed]
  110. Beaulieu, R.; López-Mondéjar, R.; Tittarelli, F.; Ros, M.; Pascual, J.A. qRT-PCR quantification of the biological control agent Trichoderma harzianum in peat and compost-based growing media. Bioresour. Technol. 2011, 102, 2793–2798. [Google Scholar] [CrossRef] [PubMed]
  111. Hagn, A.; Wallisch, S.; Radl, V.; Munch, J.C.; Schloter, M. A new cultivation independent approach to detect and monitor common Trichoderma species in soils. J. Microbiol. Methods 2007, 69, 86–92. [Google Scholar] [CrossRef]
  112. Meincke, R.; Weinert, N.; Radl, V.; Schloter, M.; Smalla, K.; Berg, G. Development of a molecular approach to describe the composition of Trichoderma communities. J. Microbiol. Methods 2010, 80, 63–69. [Google Scholar] [CrossRef]
  113. Druzhinina, I.S.; Shelest, E.; Kubicek, C.P. Novel traits of Trichoderma predicted through the analysis of its secretome. FEMS Microbiol. Lett. 2012, 337, 1–9. [Google Scholar] [CrossRef] [Green Version]
  114. Skoneczny, D.; Oskiera, M.; Szczech, M.; Bartoszewski, G. Genetic diversity of Trichoderma atroviride strains collected in Poland and identification of loci useful in detection of within-species diversity. Folia Microbiol. 2015, 60, 297–330. [Google Scholar] [CrossRef]
  115. Meena, S. Development of Species-Specific SCAR Markers for the Identification of Trichoderma Species. Master’s Thesis, Dharwad University of Agricultural Sciences, Dharwad, India, 2009. [Google Scholar]
  116. Marik, T.; Urbán, P.; Tyagi, C.; Szekeres, A.; Leitgeb, B.; Vágvölgyi, M.; Manczinger, L.; Druzhinina, I.S.; Vágvolgyi, C.; Kredics, L. Diversity profile and dynamics of peptaibols produced by green mould Trichoderma species in interactions with their hosts Agaricus bisporus and Pleurotus ostreatus. Chem. Biodivers. 2017, 14, e1700033. [Google Scholar] [CrossRef]
  117. Bae, Y.-S.; Knudsen, G.R. Cotransformation of Trichoderma harzianum with β-glucuronidase and green fluorescent protein genes provides a useful tool for monitoring fungal growth and activity in natural soils. Appl. Environ. Microbiol. 2000, 66, 810–815. [Google Scholar] [CrossRef] [Green Version]
  118. Bae, Y.-S.; Knudsen, G.R. Influence of a fungus-feeding nematode on growth and biocontrol efficacy of Trichoderma harzianum. Phytopathology 2001, 91, 301–306. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  119. Cherif, M.; Benhamou, N. Cytochemical aspects of chitin breakdown during the parasitic action of a Trichoderma sp. on Fusarium oxysporum f. sp. radicis-lycopersici. Phytopathology 1990, 80, 1406–1414. [Google Scholar] [CrossRef]
  120. Jeffries, P. Biology and ecology of mycoparasitism. Can. J. Bot. 1995, 73, S1284–S1290. [Google Scholar] [CrossRef]
  121. 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] [PubMed]
  122. Harman, G.E. Overview of mechanisms and uses of Trichoderma spp. Phytopathology 2006, 96, 190–194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  123. Mukherjee, M.; Mukherjee, P.K.; Horwitz, B.A.; Zachow, C.; Berg, G.; Zeilinger, S. Trichoderma–plant–pathogen interactions: Advances in genetics of biological control. Indian J. Microbiol. 2012, 52, 522–529. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  124. Karlsson, M.; Atanasova, L.; Jensen, D.F.; Zeilinger, S. Necrotrophic mycoparasites and their genomes. Microbiol. Spectr. 2017, 5, 1005–1026. [Google Scholar] [CrossRef]
  125. Nygren, K.; Dubey, M.; Zapparata, A.; Iqbal, M.; Tzelepis, G.D.; Durling, M.B.; Jensen, D.F.; Karlsson, M. The mycoparasitic fungus Clonostachys rosea responds with both common and specific gene expression during interspecific interactions with fungal prey. Evol Appl. 2018, 11, 931–949. [Google Scholar] [CrossRef]
  126. Lorito, M.; Harman, G.; Hayes, C.; Broadway, R.; Tronsmo, A.; Woo, S.; Di Pietro, A. Chitinolytic enzymes produced by Trichoderma harzianum: Antifungal activity of purified endochitinase and chitobiosidase. Phytopathology 1993, 83, 302–307. [Google Scholar] [CrossRef]
  127. Gallo, A.; Mule, G.; Favilla, M.; Altomare, C. Isolation and characterisation of a trichodiene synthase homologous gene in Trichoderma harzianum. Physiol. Molec. Plant Pathol. 2004, 65, 11–20. [Google Scholar] [CrossRef]
  128. Djonović, S.; Vargas, W.A.; Kolomiets, M.V.; Horndeski, M.; Wiest, A.; Kenerley, C.M. A proteinaceous elicitor sm1 from the beneficial fungal Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol. 2007, 145, 875–889. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  129. Reino, J.L.; Guerrero, R.F.; Hernandez-Galan, R.; Collado, I.G. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem. Rev. 2008, 7, 89–123. [Google Scholar] [CrossRef]
  130. 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]
  131. Henrissat, B.; Driguez, H.; Viet, C.; Schülein, M. Synergism of cellulases from Trichoderma reesei in the degradation of cellulose. Bio/Technology 1985, 3, 722–726. [Google Scholar] [CrossRef]
  132. Endo, A.; Hasumi, K.; Yamada, A.; Shimoda, R.; Takeshima, H. The synthesis of compactin (ML-236B) and monacolin K in fungi. J. Antibiot. 1986, 39, 1609–1610. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  133. Andrade, R.; Ayer, W.A.; Mebe, P.P. The metabolites of Trichoderma longibrachiatum. Part 1. Isolation of the metabolites and the structure of trichodimerol. Can. J. Chem. 1992, 70, 2526–2535. [Google Scholar] [CrossRef] [Green Version]
  134. Kontani, M.; Sakagami, Y.; Marumo, S. First β-1, 6-glucan biosynthesis inhibitor, bisvertinolone isolated from fungus, Acremonium strictum and its absolute stereochemistry. Tetrahedron Lett. 1994, 35, 2577–2580. [Google Scholar] [CrossRef]
  135. Qian-Cutrone, J.; Huang, S.; Chang, L.-P.; Pirnik, D.M.; Klohr, S.E.; Dalterio, R.A.; Hugill, R.; Lowe, S.; Alam, M.; Kadow, K.F. Harziphilone and fleephilone, two new HIV REV/RRE binding inhibitors produced by Trichoderma harzianum. J. Antibiot. 1996, 49, 990–997. [Google Scholar] [CrossRef] [PubMed]
  136. Mazzucco, C.E.; Warr, G. Trichodimerol (BMS-182123) inhibits lipopolysaccharide-induced eicosanoid secretion in THP-1 human monocytic cells. J. Leukoc. Biol. 1996, 60, 271–277. [Google Scholar] [CrossRef] [PubMed]
  137. Macías, F.A.; Varela, R.M.; Simonet, A.M.; Cutler, H.G.; Cutler, S.J.; Eden, M.A.; Hill, R.A. Bioactive Carotanes from Trichoderma v irens. J. Nat. Prod. 2000, 63, 1197–1200. [Google Scholar] [CrossRef]
  138. Evidente, A.; Cabras, A.; Maddau, L.; Serra, S.; Andolfi, A.; Motta, A. Viridepyronone, a new antifungal 6-substituted 2 h-pyran-2-one produced by Trichoderma viride. J. Agric. Food Chem. 2003, 51, 6957–6960. [Google Scholar] [CrossRef] [PubMed]
  139. Wu, Y.W.; Ouyang, J.; Xiao, X.H.; Gao, W.Y.; Liu, Y. Antimicrobial properties and toxicity of anthraquinones by microcalorimetric bioassay. Chin. J. Chem. 2006, 24, 45–50. [Google Scholar] [CrossRef]
  140. 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]
  141. 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] [PubMed] [Green Version]
  142. Kubicek, C.; Herrera, E.; Seidl, S.; Martinez, D. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Boil. 2011, 12, R40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  143. Vinale, F.; Sivasithamparam, K.; Ghisalberti, E.; Ruocco, M.; Woo, S.; Lorito, M. Trichoderma secondary metabolites that affect plant metabolism. Nat. Prod. Commun. 2012, 7, 1545–1550. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  144. Lin, Y.-R.; Lo, C.-T.; Liu, S.-Y.; Peng, K.-C. Involvement of pachybasin and emodin in self-regulation of Trichoderma harzianum mycoparasitic coiling. J. Agric. Food Chem. 2012, 60, 2123–2128. [Google Scholar] [CrossRef] [PubMed]
  145. Malmierca, M.G.; Cardoza, R.E.; Alexander, N.J.; McCormick, S.P.; Collado, I.G.; Hermosa, R.; Monte, E.; Gutiérrez, S. Relevance of trichothecenes in fungal physiology: Disruption of tri5 in Trichoderma arundinaceum. Fungal Genet. Biol. 2013, 53, 22–33. [Google Scholar] [CrossRef] [PubMed]
  146. Orr, K.; Knudsen, G. Use of green fluorescent protein and image analysis to quantify proliferation of Trichoderma harzianum in nonsterile soil. Phytopathology 2004, 94, 1383–1389. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  147. Migheli, Q.; Herrera-Estrella, A.; Avataneo, M.; Gullino, M.L. Fate of transformed Trichoderma harzianum in the phylloplane of tomato plants. Mol. Ecol. 1994, 3, 153–159. [Google Scholar] [CrossRef]
  148. Meng, J.; Wang, B.; Cheng, W. Study on the secondary metabolites of Thichoderma sturnisporum. Chin. J. Mar. Drugs 2017, 36, 27–31. [Google Scholar]
  149. Shentu, X.; Yao, J.; Yuan, X.; He, L.; Sun, F.; Ochi, K.; Yu, X. Tri11, tri3, and tri4 genes are required for trichodermin biosynthesis of Trichoderma brevicompactum. AMB Express 2018, 8, 58. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  150. Lindo, L.; McCormick, S.P.; Cardoza, R.E.; Brown, D.W.; Kim, H.-S.; Alexander, N.J.; Proctor, R.H.; Gutiérrez, S. Effect of deletion of a trichothecene toxin regulatory gene on the secondary metabolism transcriptome of the saprotrophic fungus Trichoderma arundinaceum. Fungal Genet. Biol. 2018, 119, 29–46. [Google Scholar] [CrossRef] [PubMed]
  151. Proctor, R.H.; McCormick, S.P.; Kim, H.-S.; Cardoza, R.E.; Stanley, A.M.; Lindo, L.; Kelly, A.; Brown, D.W.; Lee, T.; Vaughan, M.M. Evolution of structural diversity of trichothecenes, a family of toxins produced by plant pathogenic and entomopathogenic fungi. PLoS Pathog. 2018, 14, e1006946. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  152. Lindo, L.; McCormick, S.P.; Cardoza, R.E.; Kim, H.-S.; Brown, D.W.; Alexander, N.J.; Proctor, R.H.; Gutiérrez, S. Role of Trichoderma arundinaceum tri10 in regulation of terpene biosynthetic genes and in control of metabolic flux. Fungal Genet. Biol. 2019, 122, 31–46. [Google Scholar] [CrossRef] [PubMed]
  153. Aro, N.; Ilmén, M.; Saloheimo, A.; Penttilä, M. ACEI of Trichoderma reesei is a repressor of cellulase and xylanase expression. Appl. Environ. Microbiol. 2003, 69, 56–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  154. Aro, N.; Saloheimo, A.; Ilmén, M.; Penttilä, M. ACEII, a novel transcriptional activator involved in regulation of cellulase and xylanase genes of Trichoderma reesei. J. Biol. Chem. 2001, 276, 24309–24314. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  155. Heitz, H.J.; Witte, K.; Wartenberg, A. Amorphous-cellulose dispersing activity of cellobiohydrolase I of trichoderma reesei, suggestion for an interpretation of the C1-effect. Acta Biotechnol. 1990, 10, 277–282. [Google Scholar] [CrossRef]
  156. Xia, Y.; Yang, L.; Xia, L. High-level production of a fungal β-glucosidase with application potentials in the cost-effective production of Trichoderma reesei cellulase. Process Biochem. 2018, 70, 55–60. [Google Scholar] [CrossRef]
  157. 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] [PubMed]
  158. Green, H.; Jensen, D.F. A tool for monitoring Trichoderma harzianum: II. The use of a GUS transformant for ecological studies in the rhizosphere. Phytopathology 1995, 85, 1436–1440. [Google Scholar] [CrossRef]
  159. Li, X.-H.; Yang, H.-J.; Roy, B.; Park, E.Y.; Jiang, L.-J.; Wang, D.; Miao, Y.-G. Enhanced cellulase production of the Trichoderma viride mutated by microwave and ultraviolet. Microbiol. Res. 2010, 165, 190–198. [Google Scholar] [CrossRef] [PubMed]
  160. Cortes, C.; Gutierrez, A.; Olmedo, V.; Inbar, J.; Chet, I.; Herrera-Estrella, A. The expression of genes involved in parasitism by Trichoderma harzianum is triggered by a diffusible factor. Mol. Gen. Genet. 1998, 260, 218–225. [Google Scholar] [CrossRef] [PubMed]
  161. De las Mercedes Dana, M.; Limón, M.C.; Mejías, R.; Mach, R.L.; Benítez, T.; Pintor-Toro, J.A.; Kubicek, C.P. Regulation of chitinase 33 (chit33) gene expression in Trichoderma harzianum. Curr. Genet. 2001, 38, 335–342. [Google Scholar] [CrossRef] [PubMed]
  162. Ataei, A.; Zamani, M.; Motallebi, M.; Haghbeen, K.; Ziaei, M.; Jourabchi, E. Increased antifungal activity of Chit42 from Trichoderma atroviride by addition of a chitin binding domain. Trop. Plant Pathol. 2016, 41, 350–356. [Google Scholar] [CrossRef]
  163. Lorito, M.; Mach, R.L.; Sposato, P.; Strauss, J.; Peterbauer, C.K.; Kubicek, C.P. Mycoparasitic interaction relieves binding of the Cre1 carbon catabolite repressor protein to promoter sequences of the ech42 (endochitinase-encoding) gene in Trichoderma harzianum. Proc. Natl. Acad. Sci. USA 1996, 93, 14868–14872. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  164. Kong, Z.; Jing, R.; Wu, Y.; Guo, Y.; Geng, Y.; Ji, J.; Qin, L.; Zheng, C. Trichodermadiones A and B from the solid culture of Trichoderma atroviride S361, an endophytic fungus in Cephalotaxus fortunei. Fitoterapia 2018, 127, 362–366. [Google Scholar] [CrossRef] [PubMed]
  165. Reithner, B.; Mach-Aigner, A.R.; Herrera-Estrella, A.; Mach, R.L. Trichoderma atroviride transcriptional regulator Xyr1 supports the induction of systemic resistance in plants. Appl. Environ. Microbiol. 2014, 80, 5274–5281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  166. Nawrocka, J.; Małolepsza, U. Diversity in plant systemic resistance induced by Trichoderma. Biol. Control 2013, 67, 149–156. [Google Scholar] [CrossRef]
  167. Jiang, X.; Du, J.; He, R.; Zhang, Z.; Qi, F.; Huang, J.; Qin, L. Improved Production of Majority Cellulases in Trichoderma reesei by Integration of cbh1 Gene From Chaetomium thermophilum. Front. Microbiol. 2020, 11, 1633. [Google Scholar] [CrossRef] [PubMed]
  168. Cao, Y.; Zheng, F.; Wang, L.; Zhao, G.; Chen, G.; Zhang, W.; Liu, W. Rce1, a novel transcriptional repressor, regulates cellulase gene expression by antagonizing the transactivator Xyr1 in Trichoderma reesei. Mol. Microbiol. 2017, 105, 65–83. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  169. López-Mondejar, R.; Bernal-Vicente, A.; Ros, M.; Tittarelli, F.; Canali, S.; Intrigiolo, F.; Pascual, J.A. Utilisation of citrus compost-based growing media amended with Trichoderma harzianum T-78 in Cucumis melo L. seedling production. Bioresour. Technol. 2010, 101, 3718–3723. [Google Scholar] [CrossRef] [PubMed]
  170. 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]
  171. Migheli, Q.; González-Candelas, L.; Dealessi, L.; Camponogara, A.; Ramón-Vidal, D. Transformants of Trichoderma longibrachiatum Overexpressing the β-1,4-Endoglucanase Gene egl1 Show Enhanced Biocontrol of Pythium ultimum on Cucumber. Phytopathology 1998, 88, 673–677. [Google Scholar] [CrossRef] [Green Version]
  172. Rosado, I.; Rey, M.; Codón, A.C.; Govantes, J.; Moreno-Mateos, M.; Benítez, T. QID74 cell wall protein of Trichoderma harzianum is involved in cell protection and adherence to hydrophobic surfaces. Fungal Genet. Biol. 2007, 44, 950–964. [Google Scholar] [CrossRef]
  173. Pozo, M.J.; Baek, J.-M.; Garcıa, J.M.; Kenerley, C.M. Functional analysis of tvsp1, a serine protease-encoding gene in the biocontrol agent Trichoderma virens. Fungal Genet. Biol. 2004, 41, 336–348. [Google Scholar] [CrossRef]
  174. 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]
  175. Heil, M.; Bostock, R.M. Induced Systemic Resistance (ISR) Against Pathogens in the Context of Induced Plant Defences. Ann. Bot. 2002, 89, 503–512. [Google Scholar] [CrossRef] [Green Version]
  176. Gaderer, R.; Lamdan, N.L.; Frischmann, A.; Sulyok, M.; Krska, R.; Horwitz, B.A.; Seidl-Seiboth, V. Sm2, a paralog of the Trichoderma cerato-platanin elicitor Sm1, is also highly important for plant protection conferred by the fungal-root interaction of Trichoderma with maize. BMC Microbiol. 2015, 15, 2. [Google Scholar] [CrossRef]
  177. Yan, L.; Qian, Y. Cloning and heterologous expression of SS10, a subtilisin-like protease displaying antifungal activity from Trichoderma harzianum. FEMS Microbiol. Lett. 2009, 290, 54–61. [Google Scholar] [CrossRef] [Green Version]
  178. Liu, Y.; Yang, Q. Cloning and heterologous expression of aspartic protease SA76 related to biocontrol in Trichoderma harzianum. FEMS Microbiol. Lett. 2007, 277, 173–181. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  179. Liu, Y.-X.; Liu, X.-M.; Nin, L.-F.; Shi, L.; Chen, S.-R. Serine protease and ovarian paracrine factors in regulation of ovulation. Front. Biosci. 2013, 18, 650–664. [Google Scholar] [CrossRef] [Green Version]
  180. Viterbo, A.; Landau, U.; Kim, S.; Chernin, L.; Chet, I. Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol. Lett. 2010, 305, 42–48. [Google Scholar] [CrossRef] [PubMed]
  181. Do Nascimento Silva, R.; Steindorf, A.S.; Ulhoa, C.J.; Felix, C.R. Involvement of G-alpha protein GNA3 in production of cell wall-degrading enzymes by Trichoderma reesei (Hypocrea jecorina) during mycoparasitism against Pythium ultimum. Biotechnol. Lett. 2009, 31, 531–536. [Google Scholar] [CrossRef] [PubMed]
  182. Mukherjee, A.; Sampath Kumar, A.; Kranthi, S.; Mukherjee, P. Biocontrol potential of three novel Trichoderma strains: Isolation, evaluation and formulation. 3 Biotech 2014, 4, 275–281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  183. Mukherjee, P.K.; Latha, J.; Hadar, R.; Horwitz, B.A. TmkA, a mitogen-activated protein kinase of Trichoderma virens, is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot. Cell 2003, 2, 446–455. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  184. 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]
  185. Mukherjee, M.; Mukherjee, P.K.; Kale, S.P. cAMP signalling is involved in growth, germination, mycoparasitism and secondary metabolism in Trichoderma virens. Microbiology 2007, 153, 1734–1742. [Google Scholar] [CrossRef] [Green Version]
  186. Sarrocco, S.; Matarese, F.; Baroncelli, R.; Vannacci, G.; Seidl-Seiboth, V.; Kubicek, C.P.; Vergara, M. The constitutive endopolygalacturonase TvPG2 regulates the induction of plant systemic resistance by Trichoderma virens. Phytopathology 2017, 107, 537–544. [Google Scholar] [CrossRef]
  187. Vizcaíno, J.; Cardoza, R.; Hauser, M.; Hermosa, R.; Rey, M.; Llobell, A.; Becker, J.; Gutiérrez, S.; Monte, E. ThPTR2, a di/tri-peptide transporter gene from Trichoderma harzianum. Fungal Genet. Biol. 2006, 43, 234–246. [Google Scholar] [CrossRef]
  188. Abbas, A.; Mubeen, M.; Zheng, H.; Sohail, M.A.; Shakeel, Q.; Solanki, M.K.; Iftikhar, Y.; Sharma, S.; Kashyap, B.K.; Hussain, S.; et al. Trichoderma spp. Genes Involved in the Biocontrol Activity Against Rhizoctonia solani. Front. Microbiol. 2022, 13, 884469. [Google Scholar] [CrossRef] [PubMed]
  189. Mukherjee, P.K.; Kenerley, C.M. Regulation of morphogenesis and biocontrol properties in Trichoderma virens by a VELVET protein, Vel1. Appl. Environ. Microbiol. 2010, 76, 2345–2352. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  190. Velázquez-Robledo, R.; Contreras-Cornejo, H.; Macias-Rodriguez, L.; Hernández-Morales, A.; Aguirre, J.; Casas-Flores, S.; López-Bucio, J.; Herrera-Estrella, A. Role of the 4-phosphopantetheinyl transferase of Trichoderma virens in secondary metabolism and induction of plant defense responses. Mol. Plant-Microbe Interact. 2011, 24, 1459–1471. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  191. Ruocco, M.; Lanzuise, S.; Vinale, F.; Marra, R.; Turrà, D.; Woo, S.L.; Lorito, M. Identification of a new biocontrol gene in Trichoderma atroviride: The role of an ABC transporter membrane pump in the interaction with different plant-pathogenic fungi. Mol. Plant-Microbe Interact. 2009, 22, 291–301. [Google Scholar] [CrossRef] [Green Version]
  192. Salas-Marina, M.A.; Isordia-Jasso, M.I.; Islas-Osuna, M.A.; Delgado-Sánchez, P.; Jiménez-Bremont, J.F.; Rodríguez-Kessler, M.; Rosales-Saavedra, M.T.; Herrera-Estrella, A.; Casas-Flores, S. The Epl1 and Sm1 proteins from Trichoderma atroviride and Trichoderma virens differentially modulate systemic disease resistance against different life style pathogens in Solanum lycopersicum. Front. Plant Sci. 2015, 6, 77. [Google Scholar] [CrossRef] [Green Version]
  193. Rubio, M.B.; Hermosa, R.; Reino, J.L.; Collado, I.G.; Monte, E. Thctf1 transcription factor of Trichoderma harzianum is involved in 6-pentyl-2H-pyran-2-one production and antifungal activity. Fungal Genet. Biol. 2009, 46, 17–27. [Google Scholar] [CrossRef]
  194. Bansal, R.; Mukherjee, M.; Horwitz, B.A.; Mukherjee, P.K. Regulation of conidiation and antagonistic properties of the soil-borne plant beneficial fungus Trichoderma virens by a novel proline-, glycine-, tyrosine-rich protein and a GPI-anchored cell wall protein. Curr. Genet. 2019, 65, 953–964. [Google Scholar] [CrossRef]
  195. Moreno-Mateos, M.A.; Delgado-Jarana, J.; Codon, A.C.; Benítez, T. pH and Pac1 control development and antifungal activity in Trichoderma harzianum. Fungal Genet. Biol. 2007, 44, 1355–1367. [Google Scholar] [CrossRef]
  196. 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]
  197. Gruber, S.; Zeilinger, S. The transcription factor Ste12 mediates the regulatory role of the Tmk1 MAP kinase in mycoparasitism and vegetative hyphal fusion in the filamentous fungus Trichoderma atroviride. PLoS ONE 2014, 9, e111636. [Google Scholar]
  198. Aghcheh, R.K.; Druzhinina, I.S.; Kubicek, C.P. The putative protein methyltransferase LAE1 of Trichoderma atroviride is a key regulator of asexual development and mycoparasitism. PLoS ONE 2013, 8, e67144. [Google Scholar] [CrossRef] [PubMed]
  199. Monfil, V.O.; Casas-Flores, S. Molecular mechanisms of biocontrol in Trichoderma spp. and their applications in agriculture. In Biotechnology and Biology of Trichoderma; Elsevier: Amsterdam, The Netherlands, 2014; pp. 429–453. [Google Scholar]
  200. Ahmad, J.S.; Baker, R. Rhizosphere competence of Trichoderma harzianum. Phytopathology 1987, 77, 182–189. [Google Scholar] [CrossRef]
  201. Benítez, T.; Rincón, A.M.; Limón, M.C.; Codon, A.C. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 2004, 7, 249–260. [Google Scholar] [PubMed]
  202. Palmieri, D.; Ianiri, G.; Del Grosso, C.; Barone, G.; De Curtis, F.; Castoria, R.; Lima, G. Advances and Perspectives in the Use of Biocontrol Agents against Fungal Plant Diseases. Horticulturae 2022, 8, 577. [Google Scholar] [CrossRef]
  203. Hemming, B.C. Microbial-iron interactions in the plant rhizosphere. An overview. J. Plant Nutr. 1986, 9, 505–521. [Google Scholar] [CrossRef]
  204. Neilands, J.; Leong, S.A. Siderophores in relation to plant growth and disease. Annu. Rev. Plant Physiol. 1986, 37, 187–208. [Google Scholar] [CrossRef]
  205. Tjamos, E.C.; Papavizas, G.C.; Cook, R.J. Biological Control of Plant Diseases: Progress and Challenges for the Future; Springer: New York, NY, USA, 1992. [Google Scholar]
  206. De Santiago, A.; García-López, A.M.; Quintero, J.M.; Avilés, M.; Delgado, A. Effect of Trichoderma asperellum strain T34 and glucose addition on iron nutrition in cucumber grown on calcareous soils. Soil Biol. Biochem. 2013, 57, 598–605. [Google Scholar] [CrossRef]
  207. Altomare, C.; Tringovska, I. Beneficial soil microorganisms, an ecological alternative for soil fertility management. In Sustainable Agriculture Reviews; Springer: Berlin/Heidelberg, Germany, 2011; pp. 161–214. [Google Scholar]
  208. Adams, P.; Lynch, J.; De Leij, F. Desorption of zinc by extracellularly produced metabolites of Trichoderma harzianum, Trichoderma reesei and Coriolus versicolor. J. Appl. Microbiol. 2007, 103, 2240–2247. [Google Scholar] [CrossRef]
  209. Leong, J. Siderophores: Their biochemistry and possible role in the biocontrol of plant pathogens. Annu. Rev. Phytopathol. 1986, 24, 187–209. [Google Scholar] [CrossRef]
  210. Yedidia, I.; Shrivasta, A.K.; Kapulnik, Y.; Chet, I. Effect of Trichoderma harzianum on microelement concentration and increased growth of cucumber plants. Plant Soil 2001, 235, 235–242. [Google Scholar] [CrossRef]
  211. Fiorentino, N.; Ventorino, V.; Bertora, C.; Pepe, O.; Giancarlo, M.; Grignani, C.; Fagnano, M. Changes in soil mineral N content and abundances of bacterial communities involved in N reactions under laboratory conditions as predictors of soil N availability to maize under field conditions. Biol. Fertil. Soils 2016, 52, 523–537. [Google Scholar] [CrossRef]
  212. Dennis, C.; Webster, J. Antagonistic properties of species-groups of Trichoderma: I. Production of non-volatile antibiotics. Trans. Br. Mycol. Soc. 1971, 57, 25-IN3. [Google Scholar] [CrossRef]
  213. Lumsden, R.; Lewis, J.; Locke, J. Managing soilborne plant pathogens with fungal antagonists. In Pest Management: Biologically Based Technologies; Government Printing Office: Washington, DC, USA, 1993; pp. 196–203. [Google Scholar]
  214. Vey, A.; Hoagland, R.E.; Butt, T.M.; Jackson, C.W.; Magan, N. Toxic Metabolites of Fungal Biocontrol Agents; CABI International: Wallingford, UK, 2001. [Google Scholar]
  215. Gębarowska, E.; Pytlarz-Kozicka, M.; Nöfer, J.; Łyczko, J.; Adamski, M.; Szumny, A. The effect of Trichoderma spp. on the composition of volatile secondary metabolites and biometric parameters of coriander (Coriandrum sativum L.). J. Food Qual. 2019, 2019, 5687032. [Google Scholar] [CrossRef] [Green Version]
  216. Li, M.-F.; Li, G.-H.; Zhang, K.-Q. Non-volatile metabolites from Trichoderma spp. Metabolites 2019, 9, 58. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  217. Howell, C.; Stipanovic, R.; Lumsden, R. Antibiotic production by strains of Gliocladium virens and its relation to the biocontrol of cotton seedling diseases. Biocontrol Sci. Technol. 1993, 3, 435–441. [Google Scholar] [CrossRef]
  218. Song, X.-Y.; Shen, Q.-T.; Xie, S.-T.; Chen, X.-L.; Sun, C.-Y.; Zhang, Y.-Z. Broad-spectrum antimicrobial activity and high stability of Trichokonins from Trichoderma koningii SMF2 against plant pathogens. FEMS Microbiol. Lett. 2006, 260, 119–125. [Google Scholar]
  219. Vinale, F.; Marra, R.; Scala, F.; Ghisalberti, E.; 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]
  220. Hanson, L.E.; Howell, C.R. Biocontrol efficacy and other characteristics of protoplast fusants between Trichoderma koningii and T. virens. Mycol. Res. 2002, 106, 321–328. [Google Scholar] [CrossRef] [Green Version]
  221. Garnica-Vergara, A.; Barrera-Ortiz, S.; Muñoz-Parra, E.; Raya-González, J.; Méndez-Bravo, A.; Macías-Rodríguez, L.; Ruiz-Herrera, L.F.; López-Bucio, J. The volatile 6-pentyl-2H-pyran-2-one from Trichoderma atroviride regulates Arabidopsis thaliana root morphogenesis via auxin signaling and ETHYLENE INSENSITIVE 2 functioning. New Phytol. 2016, 209, 1496–1512. [Google Scholar] [CrossRef] [Green Version]
  222. Lee, S.; Yap, M.; Behringer, G.; Hung, R.; Bennett, J.W. Volatile organic compounds emitted by Trichoderma species mediate plant growth. Fungal Biol. Biotechnol. 2016, 3, 7. [Google Scholar] [CrossRef] [Green Version]
  223. Howell, C.; Hanson, L.; Stipanovic, R.; Puckhaber, L. 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]
  224. 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. In Microorganism for Industrial Enzymes and Biocontrol; Research Signpost: Kerala, India, 2005; pp. 1–22. [Google Scholar]
  225. Kawada, M.; Yoshimoto, Y.; Kumagai, H.; Someno, T.; Momose, I.; Kawamura, N.; Isshiki, K.; Ikeda, D. PP2A inhibitors, harzianic acid and related compounds produced by fungus strain F-1531. J. Antibiot. 2004, 57, 235–237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  226. Parker, S.R.; Cutler, H.G.; Jacyno, J.M.; Hill, R.A. Biological activity of 6-pentyl-2 H-pyran-2-one and its analogs. J. Agric. Food Chem. 1997, 45, 2774–2776. [Google Scholar] [CrossRef]
  227. 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]
  228. Mukherjee, P.K.; Horwitz, B.A.; Kenerley, C.M. Secondary metabolism in Trichoderma—A genomic perspective. Microbiology 2012, 158, 35–45. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  229. Cutler, H.G.; Himmelsbach, D.S.; Arrendale, R.F.; Cole, P.D.; Cox, R.H. Koninginin A: A novel plant growth regulator from Trichoderma koningii. Agric. Biol. Chem. 1989, 53, 2605–2611. [Google Scholar]
  230. Crutcher, F.K.; Parich, A.; Schuhmacher, R.; Mukherjee, P.K.; Zeilinger, S.; Kenerley, C.M. A putative terpene cyclase, vir4, is responsible for the biosynthesis of volatile terpene compounds in the biocontrol fungus Trichoderma virens. Fungal Genet. Biol. 2013, 56, 67–77. [Google Scholar] [CrossRef] [PubMed]
  231. Contreras-Cornejo, H.A.; Macías-Rodríguez, L.; Alfaro-Cuevas, R.; López-Bucio, J. Trichoderma spp. improve growth of Arabidopsis seedlings under salt stress through enhanced root development, osmolite production, and Na+ elimination through root exudates. Mol. Plant-Microbe Interact. 2014, 27, 503–514. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  232. 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. 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] [PubMed] [Green Version]
  233. Rivera-Chávez, J.; Raja, H.A.; Graf, T.N.; Gallagher, J.M.; Metri, P.; Xue, D.; Pearce, C.J.; Oberlies, N.H. Prealamethicin F50 and related peptaibols from Trichoderma arundinaceum: Validation of their authenticity via in situ chemical analysis. RSC Adv. 2017, 7, 45733–45741. [Google Scholar] [CrossRef] [PubMed]
  234. Song, Y.-P.; Miao, F.-P.; Fang, S.-T.; Yin, X.-L.; Ji, N.-Y. Halogenated and nonhalogenated metabolites from the marine-alga-endophytic fungus Trichoderma asperellum cf44-2. Mar. Drugs 2018, 16, 266. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  235. Ding, Z.; Wang, X.; Kong, F.-D.; Huang, H.-M.; Zhao, Y.-N.; Liu, M.; Wang, Z.-P.; Han, J. Overexpression of Global Regulator Talae1 Leads to the Discovery of New Antifungal Polyketides from Endophytic Fungus Trichoderma afroharzianum. Front. Microbiol. 2020, 11, 622785. [Google Scholar] [CrossRef] [PubMed]
  236. Shi, Z. Chemical Structures and Biological Activities of Secondary Metabolites from Five Marine-Alga-Epiphytic Fungi; Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences: Yantai, China, 2018. [Google Scholar]
  237. Ji, Z.; Ma, D.; Miao, F. Chemical constituents from Trichoderma longibrachiatum, an endophytic fungus derived from marine green alga codium fragile. J. Shenyang Univ. 2014, 26, 277–280. [Google Scholar]
  238. Xuan, Q.-C.; Huang, R.; Chen, Y.-W.; Miao, C.-P.; Ma, K.-X.; Wang, T.; Wu, S.-H. Cyclonerol derivatives from Trichoderma longibrachiatum YM311505. Nat. Prod. Commun. 2014, 9, 313–314. [Google Scholar] [CrossRef] [PubMed]
  239. Wang, C.; Zolotarskaya, O.Y.; Nair, S.S.; Ehrhardt, C.J.; Ohman, D.E.; Wynne, K.J.; Yadavalli, V.K. Real-time observation of antimicrobial polycation effects on Escherichia coli: Adapting the carpet model for membrane disruption to quaternary copolyoxetanes. Langmuir 2016, 32, 2975–2984. [Google Scholar] [CrossRef] [PubMed]
  240. Zhou, P.; Wu, Z.; Tan, D.; Yang, J.; Zhou, Q.; Zeng, F.; Zhang, M.; Bie, Q.; Chen, C.; Xue, Y. Atrichodermones A–C, three new secondary metabolites from the solid culture of an endophytic fungal strain, Trichoderma atroviride. Fitoterapia 2017, 123, 18–22. [Google Scholar] [CrossRef] [PubMed]
  241. Ding, G.; Wang, H.; Li, L.; Chen, A.J.; Chen, L.; Chen, H.; Zhang, H.; Liu, X.; Zou, Z. Trichoderones A and B: Two pentacyclic cytochalasans from the plant endophytic fungus Trichoderma gamsii. Eur. J. Org. Chem. 2012, 2012, 2516–2519. [Google Scholar] [CrossRef]
  242. 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]
  243. Pang, X.; Lin, X.; Tian, Y.; Liang, R.; Wang, J.; Yang, B.; Zhou, X.; Kaliyaperumal, K.; Luo, X.; Tu, Z. Three new polyketides from the marine sponge-derived fungus Trichoderma sp. SCSIO41004. Nat. Prod. Res. 2018, 32, 105–111. [Google Scholar] [CrossRef] [PubMed]
  244. Iida, A.; Sanekata, M.; Fujita, T.; Tanaka, H.; Enoki, A.; Fuse, G.; Kanai, M.; Rudewicz, P.J.; Tachikawa, E. Fungal metabolites. XVI. Structures of new peptaibols, trichokindins I-VII, from the fungus Trichoderma harzianum. Chem. Pharm. Bull. 1994, 42, 1070–1075. [Google Scholar] [CrossRef] [Green Version]
  245. Li, C.-W.; Song, R.-Q.; Yang, L.-B.; Deng, X. Isolation, purification, and structural identification of an antifungal compound from a Trichoderma strain. J. Microbiol. Biotechnol. 2015, 25, 1257–1264. [Google Scholar] [CrossRef] [PubMed]
  246. Gong, B.; Zhang, S.-Q.; Lin, Y.-X.; Wang, X.-F.; Ding, W.-J.; Li, C.-Y. Study on metabolites with antifungal activity against plant pathogens of an endophytic fungus Trichoderma sp. 09 from Myoporum bontioides A. Gray. Guangdong Agric. Sci. 2013, 40, 62–65. [Google Scholar]
  247. Wu, B.; Oesker, V.; Wiese, J.; Schmaljohann, R.; Imhoff, J.F. Two new antibiotic pyridones produced by a marine fungus, Trichoderma sp. strain MF106. Mar. Drugs 2014, 12, 1208–1219. [Google Scholar] [CrossRef] [Green Version]
  248. 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] [PubMed]
  249. Zhang, J.-c.; Chen, G.-Y.; Li, X.-Z.; Hu, M.; Wang, B.-Y.; Ruan, B.-H.; Zhou, H.; Zhao, L.-X.; Zhou, J.; Ding, Z.-T. Phytotoxic, antibacterial, and antioxidant activities of mycotoxins and other metabolites from Trichoderma sp. Nat. Prod. Res. 2017, 31, 2745–2752. [Google Scholar] [CrossRef] [PubMed]
  250. Bolton, D.M.; Thomma, B.P.; Nelson, B.D. Sclerotinia sclerotiorum (lib.) de Bray: Biology and molecular traits of a cosmopolitan pathogen. Mol. Plant Pathol. 2006, 7, 1–16. [Google Scholar] [CrossRef] [PubMed]
  251. Harman, G.E.; Herrera-Estrella, A.H.; Horwitz, B.A.; Lorito, M. Special issue: Trichoderma-from basic biology to biotechnology. Microbiology 2012, 158, 1–2. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  252. 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]
  253. Risoli, S.; Cotrozzi, L.; Sarrocco, S.; Nuzzaci, M.; Pellegrini, E.; Vitti, A. Trichoderma-Induced Resistance to Botrytis cinerea in Solanum Species: A Meta-Analysis. Plants 2022, 11, 180. [Google Scholar] [CrossRef]
  254. Shoresh, M.; Mastouri, F.; Harman, G.E. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu. Rev. Phytopathol. 2010, 48, 21–43. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  255. Sriram, N.; Kalayarasan, S.; Sudhandiran, G. Epigallocatechin-3-gallate exhibits anti-fibrotic effect by attenuating bleomycin-induced glycoconjugates, lysosomal hydrolases and ultrastructural changes in rat model pulmonary fibrosis. Chem. Biol. Interact. 2009, 180, 271–280. [Google Scholar] [CrossRef] [PubMed]
  256. Nawrocka, J.; Snochowska, M.; Gajewska, E.; Pietrowska, E.; Szczech, M.; Malolepsza, U. Activation of defense responses in cucumber and tomato plants by selected polish Trichoderma strains. Veg. Crops Res. Bull. 2011, 75, 105–116. [Google Scholar] [CrossRef]
  257. Schwessinger, B.; Zipfel, C. News from the frontline: Recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 2008, 11, 389–395. [Google Scholar] [CrossRef]
  258. Zeilinger, S.; Omann, M. Trichoderma biocontrol: Signal transduction pathways involved in host sensing and mycoparasitism. Gene Regul. Syst. Biol. 2007, 1, 227–234. [Google Scholar] [CrossRef] [Green Version]
  259. Mendoza-Mendoza, A.; Pozo, M.J.; Grzegorski, D.; Martínez, P.; García, J.M.; Olmedo-Monfi, V.; Cortés, C.; Kenerley, C.; Herrera-Estrella, A. Enhanced biocontrol activity of Trichoderma through inactivation of a mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 2003, 100, 15965–15970. [Google Scholar] [CrossRef]
  260. Mendoza-Mendoza, A.; Rosales-Saavedra, T.; Cortés, C.; Castellanos-Juárez, V.; Martínez, P.; Herrera-Estrella, A. The MAP kinase TVK1 regulates conidiation, hydrophobicity and the expression of genes encoding cell wall proteins in the fungus Trichoderma virens. Microbiology 2007, 153, 2137–2147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  261. 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] [PubMed] [Green Version]
  262. Reithner, B.; Brunner, K.; Schuhmacher, R.; Peissl, I.; Seidl, V.; Krska, R.; Zeilinger, S. The G protein alpha subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites. Fungal Genet. Biol. 2005, 42, 749–760. [Google Scholar] [CrossRef] [PubMed]
  263. Rocha-Ramírez, V.; Omero, C.; Chet, I.; Horwitz, B.A.; Herrera-Estrella, A. Trichoderma atroviride G-protein alpha-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryot. Cell 2002, 1, 594–605. [Google Scholar] [CrossRef] [Green Version]
  264. Mukherjee, P.K.; Latha, J.; Hadar, R.; Horwitz, B.A. Role of two G-protein alpha subunits, TgaA and TgaB, in the antagonism of plant pathogens by Trichoderma virens. Appl. Environ. Microbiol. 2004, 70, 542–549. [Google Scholar] [CrossRef] [Green Version]
  265. Zeilinger, S.; Reithner, B.; Scala, V.; Peissl, I.; Lorito, M.; Mach, R.L. Signal transduction by Tga3, a novel G protein alpha subunit of Trichoderma atroviride. Appl. Environ. Microbiol. 2005, 71, 1591–1597. [Google Scholar] [CrossRef] [Green Version]
  266. Silva, R.N.; da Silva, S.P.; Brandão, R.L.; Ulhoa, C.J. Regulation of N-acetyl-β-D-glucosaminidase produced by Trichoderma harzianum: Evidence that cAMP controls its expression. Res. Microbiol. 2004, 155, 667–671. [Google Scholar] [CrossRef] [PubMed]
  267. Sun, Z.-B.; Yu, S.-F.; Wang, C.-L.; Wang, L. cAMP Signalling Pathway in Biocontrol Fungi. Curr. Issues Mol. Biol. 2022, 44, 2622–2634. [Google Scholar] [CrossRef] [PubMed]
  268. Scherm, B.; Schmoll, M.; Balmas, V.; Kubicek, C.P.; Migheli, Q. Identification of potential marker genes for Trichoderma harzianum strains with high antagonistic potential against Rhizoctonia solani by a rapid subtraction hybridization approach. Curr. Genet. 2009, 55, 81–91. [Google Scholar] [CrossRef] [Green Version]
  269. Nagy, V.; Seidl, V.; Szakacs, G.; Komon-Zelazowska, M.; Kubicek, C.P.; Druzhinina, I.S. Application of DNA bar codes for screening of industrially important fungi: The haplotype of Trichoderma harzianum sensu stricto indicates superior chitinase formation. Appl. Environ. Microbiol. 2007, 73, 7048–7058. [Google Scholar] [CrossRef]
  270. Harman, G.E. Trichoderma-not just for biocontrol anymore. Phytoparasitica 2011, 39, 103–108. [Google Scholar] [CrossRef] [Green Version]
  271. Zamioudis, C.; Pieterse, C.M.J. Modulation of host immunity by benefi cial microbes. Mol. Plant Microbe. Interact. 2012, 25, 139–150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  272. Azarmi, R.; Hajieghrari, B.; Gigloul, A. Effect of Trichoderma isolates on tomato seedling growth response and nutrient uptake. Afr. J. Biotechnol. 2011, 10, 5850–5855. [Google Scholar]
  273. Doni, F.; Isahak, A.; Zain, C.R.C.M.; Yusoff, W.M.W. Physiological and growth response of rice plants (Oryza sativa L.) to Trichoderma spp. inoculants. AMB Express 2014, 4, 45. [Google Scholar] [CrossRef]
  274. Vinale, F.; Arjona Girona, I.; Nigro, M.; Mazzei, P.; Piccolo, A.; Ruocco, M.; Woo, S.; Ruano Rosa, D.; Lopez Herrera, C.; Lorito, M. Cerinolactone, a hydroxy-lactone derivative from Trichoderma cerinum. J. Nat. Prod. 2012, 75, 103–106. [Google Scholar] [CrossRef]
  275. Yuan, M.; Huang, Y.; Ge, W.; Jia, Z.; Song, S.; Zhang, L.; Huang, Y. Involvement of jasmonic acid, ethylene and salicylic acid signaling pathways behind the systemic resistance induced by Trichoderma longibrachiatum H9 in cucumber. BMC Genom. 2019, 20, 144. [Google Scholar] [CrossRef] [Green Version]
  276. Martinez-Medina, A.; Alguacil, M.D.M.; Pascual, J.; Van Wees, S.C. Phytohormone profles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. J. Chem. Ecol. 2014, 40, 804–815. [Google Scholar] [CrossRef] [PubMed]
  277. Hoyos-Carvajal, L.; Orduz, S.; Bissett, J. Growth stimulation in bean (Phaseolus vulgaris L.) by Trichoderma. Biol. Control. 2009, 51, 409–416. [Google Scholar] [CrossRef]
  278. Saravanakumar, K.; Arasu, V.S.; Kathiresan, K. Effect of Trichoderma on soil phosphate solubilization and growth improvement of Avicennia marina. Aquat. Bot. 2012, 104, 101–105. [Google Scholar] [CrossRef]
  279. Joshi, B.B.; Bhatt, R.P.; Bahukhandi, D. Antagonistic and plant growth activity of Trichoderma isolates of Western Himalayas. J. Environ. Biol. 2010, 31, 921–928. [Google Scholar] [PubMed]
  280. Umashankar, N.; Venkateshamurthy, P.; Krishnamurthy, R.; Raveendra, H.R.; SatishI, K.M. Effect of microbial inoculants on the growth of silver oak (Grevillea robusta) in nursery condition. Int. J. Environ. Sci. Dev. 2012, 3, 72–76. [Google Scholar] [CrossRef]
  281. Mastouri, F.; Björkman, T.; Harman, G.E. Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 2010, 100, 1213–1221. [Google Scholar] [CrossRef] [Green Version]
  282. Yang, C.A.; Cheng, C.H.; Lo, C.T.; Liu, S.Y.; Lee, J.W.; Peng, K.H. A novel L-amino acid oxidase from Trichoderma harzianum EST 323 associated with antagonism of R. solani. J. Agric. Food Chem. 2011, 59, 4519–4526. [Google Scholar] [CrossRef]
Figure 1. Biocontrol mechanism used by Trichoderma against plant pathogens and promoting healthy crop.
Figure 1. Biocontrol mechanism used by Trichoderma against plant pathogens and promoting healthy crop.
Sustainability 14 12786 g001
Figure 2. Trichoderma-induced resistance in host plant.
Figure 2. Trichoderma-induced resistance in host plant.
Sustainability 14 12786 g002
Table 2. List of secondary metabolites/bioactive compounds produced by Trichoderma.
Table 2. List of secondary metabolites/bioactive compounds produced by Trichoderma.
Serial NumberCompound (Secondary Metabolites)Biological ActivityProduced ByReferences
1.Trichorzianin TA
Trichorzianin TB
AntifungalT. harzianum[224]
1.Trichorzins TVB I, II, IVAntifungalT. virens[224]
2.HarzianopyridoneAntifungal, Plant growth RegulatorT. harzianum[225]
3.HarzianolideDehydroharzianolideAntifungalT. harzianum[224]
4.6-pentyl-α-pyroneAntifungal,
Antimicrobial,
Plant growth Regulator
T. harzianum
T. koningii
T. viride
[224]
5.6-pentyl-2H-pyran-2-oneAntifungal, anti-nematode and
plant growth-promoting in
tomato and Arabidopsis
thaliana
T. atroviride
T. harzianum
T. koningii
T. viride
[221]
6.6-pent-1-enyl-α-pyroneAntifungalT. harzianum
T. viride
[226]
7.Massoilactone- δ-decenolactoneAntifungalTrichoderma spp.[224]
8.Koninginin E, B, AAntifungal, Plant growth RegulatorT. harzianum
T. koningii
[227]
9.Koniginin D
Hydroxykoninginin B
Seco-koninginin
Antifungal, Plant growth RegulatorT. harzianum[224]
10.Koninginin CAntifungal, Plant growth RegulatorT. koningii[28]
11.3,4-dihydroxycaroteneAntifungalT. virens[224]
12.LignorenAntifungal
Antibacterial
T. lignorum[224]
13.TrichoderminAntifungal
Antitrichomonal
Mycotoxin
T. polysporum
T. sporulosum
T. virens
T. reesei
[224]
14.Harzianum AAntifungalT. harzianum[224]
15.Mycotoxin T2Antifungal
Mycotoxin
T. lignorum[224]
16.Ergokonin AAntifungalT. koningii
T. viride
T. longibrachiatum
[141]
17.Ergokonin BAntifungalT. koningii
T. viride
[224]
18.ViridinAntibiotic
Inhibitor Fungal
Spore germination
Phytotoxic
T. viride
T. virens
T. koningii
[224]
19.Dermadin (U21, 963)AntimicrobialT. koningii
T. viride
[130]
20.CellulasesDegrade cellulose during root colonization to penetrate the plant tissueT. reesei[153]
21.CompactinAct as Cholestrol lowering agentT. longibrachiatum
T. pseudokoningii
[132]
22.5-HydroxyvertinolideFungal antagonistT. longibrachiatum[133]
23.GliovirinAntimicrobialT. virens[217]
24.BisvertinoloneAntifungalT. longibrachiatum[134]
25.FleephiloneInhibitory action against VirionT. harzianum[135]
26.HarziphiloneCytotoxicity against murine tumor cell line M-109T. harzianum[135]
27.TrichodimerolInhibit tumor necrosis factor in human monocytes.T. longibrachiatum[136]
28.Trichocaranes A,B,DGrowth inhibitor of etiolated wheat coleoptilesT. virens[137]
29.ViridepyrononeFungal antagonistT. viride[138]
30.T22azaphiloneAntifungalT. harzianum[219]
31.T39butenolideAntifungalT. harzianum[219]
32.EmodinAntimicrobial and antineoplastic agentT. viride[139]
33.TrichosetinAntibioticT. harzianum[141]
34.Trichoderma mide BDisplays cytotoxicity against
HCT-116 human colon
Carcinoma
T. virens[141]
35.WortmannoloneInhibitor of the
phosphatidylinsitol 3-kinase
T. virens[141]
36.VironeInhibitor of the
phosphatidylinsitol 3-kinase
T. virens[141]
37.Heptelidic acidActivity against Plasmodium
Falciparum
T. virens
T. viride
[141]
38.Indole-3-acetic acid
(IAA)
Growth and development
Regulator
T. atroviride
T. virens
[140]
39.Indole-3-acetaldehydeControl root growth in
Arabidopsis thaliana
T. atroviride
T. virens
[140]
40.Indole-3
Carboxaldehyde
Induces adventitious root
formation in Arabidopsis
thaliana
T. atroviride
T. virens
[141]
41.FerricrocinRequired in the competition of
iron in the rhizosphere
T. atroviride
T. virens,
T. reesei
[142]
42.GliotoxinRequired in the competition of
iron in the rhizosphere
T. hamatum
T. viride
T. virens
[228]
43.CyclonerodiolAntifungalT. harzianum
T. koningii
[153]
44.PachybasinAntifungalT. harzianum[144]
45.Trichovirin IIInduction of resistance in
cucumber plants
T. virens[228]
46.AlamethicinInduction of plant defense in lima and pathogen resistanceT. viride[228]
47.Coprogen BSolubilize iron unavailable for
the plan
Trichoderma spp.[143]
48.Harzianic acidAntimicrobial, plant growth
Regulator
T. arundinaceum,
T. harzianum
[145]
49.cis- and
trans-ß-ocimene
Induce expression of JA defense
responses-related genes in
Arabidopsis. Thaliana
T. virens[229]
50.ß-MyrceneRegulates the expression of
genes (abiotic and biotic
stresses)
T. virens[230]
51.Abscisic acid (ABA)Regulates stomatal aperture in
Arabidopsis thaliana
T. atroviride,
T. virens
[231]
52.Ethylene (ET)Regulates cell differentiation
and defense responses
T. atroviride[227]
53.Trichokonin VIInhibits primary root growth in
Arabidopsis thaliana
T. longibrachiatum[232]
54.Glu(OMe)18-alamethicin F50 (2)Anti-tumorT. arundinaceum[233]
55.trichobrevin BIII-DAnti-tumorT. arundinaceum[233]
56.bisabolan-1,10,11-triolAntibacterial
Growth inhibitoring
T. asperellum[234]
57.12-nor-11-acetoxybisabolen-3,6,7-triolAntibacterial
Growth inhibitoring
T. asperellum[234]
58.Dechlorotrichodenone-CAntibacterial
Growth inhibitoring
T. asperellum[234]
59.3-hydroxytrichodenone CAntibacterial Growth
Inhibitoring
T. asperellum[234]
60.
, 5α, 9α-trihydroxyergosta-7,22-dien- 6-one
AntifungalT. asperellum
T. harzianum
Trichoderma spp.
[235]
61.Isoechinulin AAntimicroalgalT. koningiopsis[236]
62.EchinulineAntimicroalgalT. koningiopsis[236]
63.Fructigenine AAntimicroalgalT. koningiopsis[236]
64.CyclopenolAntibacterialT. koningiopsis[236]
65.Wickerol ANematicidalT. koningiopsis[236]
66.SorbicillinAntibacterialT. longibrachiatum[237]
67.10,11-dihydrocyclonerotriolAntifungalT. longibrachiatum[238]
68.Sohirnone AAntifungalT. longibrachiatum[238]
69.Trichokonin AAntiviral
Anti-tumor
Antimicrobial
Plant resistance
T. longibrachiatum[239]
70.Atrichodermone A,B,CCytotoxic
Anti-inflammatory
T. atroviride[240]
71.Cerebroside A, DAntibacteriaT. saturnisporum
Trichoderma spp.
[239]
72.LignorenAntibacterialT. atroviride S361
T. citrinoviride
T. lignorum
[235]
73.Catenioblin CAntifungalT. atroviride
T. longibrachiatum
[241]
74.Trichocarotin E,HAntimicroalgalT. virens[237]
75.TrichocitrinAntimicroalgalT. citrinoviride[242]
76.NafuredinAntimicroalgal
Antibacterial
T. citrinoviride
Trichodermasp
[235]
77.ChromoneAntifungalT. virens[237]
78.Aspochalasin D, J, ICytotoxicT. gamsii[241]
79.Epicycloneodiol oxideAntibacterialT. harzianum
T. koningiopsis
[235]
80.cycloneodiol oxideAntibacterialT. harzianum
T. koningiopsis
[235]
81.ZSU-H85 AAntiviralTrichoderma spp.[243]
82.Trichokindin I, II, III, IV, V,VI, VIIBioinducerT. harzianum[244]
83.2,5-cyclohexadiene-1,4-dione-2,6-bis(1,1-dimethylethyl)AntifungalTrichoderma spp. T-33[245]
84.N-2′-hydroxy-3′E-octadecenoyl-1-o-
β-D-glucopyranosyl-9-methyl-4E,8E-sphingadiene
AntifungalTrichoderma spp. 09[246]
85.TyrosolAnti-tumor
Hyperplasia-inhibitory
T. harzianum
T. spirale
[235]
86.Trichoderma ketone AAntifungalT. koningi[235]
87.PyridoxatinAntibioticTrichoderma spp. MF106[247]
88.3-(3-oxocyclopent-1-enyl)propanoic acidAntibacterialTrichoderma spp. YLF-3[248]
89.OxosorbicillinolDPPH-radical-scavengingTrichoderma spp. USF-2690[56]
90.α-acetylorcinolGrowth inhibitoringTrichoderma spp. Jing-8[249]
91.DaidzeinAntibacterialTrichoderma spp. YM311505[238]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Manzar, N.; Kashyap, A.S.; Goutam, R.S.; Rajawat, M.V.S.; Sharma, P.K.; Sharma, S.K.; Singh, H.V. Trichoderma: Advent of Versatile Biocontrol Agent, Its Secrets and Insights into Mechanism of Biocontrol Potential. Sustainability 2022, 14, 12786. https://doi.org/10.3390/su141912786

AMA Style

Manzar N, Kashyap AS, Goutam RS, Rajawat MVS, Sharma PK, Sharma SK, Singh HV. Trichoderma: Advent of Versatile Biocontrol Agent, Its Secrets and Insights into Mechanism of Biocontrol Potential. Sustainability. 2022; 14(19):12786. https://doi.org/10.3390/su141912786

Chicago/Turabian Style

Manzar, Nazia, Abhijeet Shankar Kashyap, Ravi Shankar Goutam, Mahendra Vikram Singh Rajawat, Pawan Kumar Sharma, Sushil Kumar Sharma, and Harsh Vardhan Singh. 2022. "Trichoderma: Advent of Versatile Biocontrol Agent, Its Secrets and Insights into Mechanism of Biocontrol Potential" Sustainability 14, no. 19: 12786. https://doi.org/10.3390/su141912786

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