Submitted Successfully!
To reward your contribution, here is a gift for you: A free trial for our video production service.
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Version Summary Created by Modification Content Size Created at Operation
1
Bhupendra Koul
 -- 3337 2023-11-09 06:50:53 |
2 layout
Jessie Wu
 Meta information modification 3337 2023-11-09 09:59:39 |

Video Upload Options

Do you have a full video?
Send video materials Upload full video

Confirm

Are you sure to Delete?
Yes No
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Kumar, V.; Koul, B.; Taak, P.; Yadav, D.; Song, M. Trichoderma. Encyclopedia. Available online: https://encyclopedia.pub/entry/51323 (accessed on 07 May 2024).
Kumar V, Koul B, Taak P, Yadav D, Song M. Trichoderma. Encyclopedia. Available at: https://encyclopedia.pub/entry/51323. Accessed May 07, 2024.
Kumar, Vipul, Bhupendra Koul, Pooja Taak, Dhananjay Yadav, Minseok Song. "Trichoderma" Encyclopedia, https://encyclopedia.pub/entry/51323 (accessed May 07, 2024).
Kumar, V., Koul, B., Taak, P., Yadav, D., & Song, M. (2023, November 09). Trichoderma. In Encyclopedia. https://encyclopedia.pub/entry/51323
Kumar, Vipul, et al. "Trichoderma." Encyclopedia. Web. 09 November, 2023.
Trichoderma
Edit
This entry is adapted from the peer-reviewed paper 10.3390/agriculture13102022

Trichoderma spp. has the ability to inhibit fungal plant pathogens through several mechanisms like the production of hydrolytic enzymes, mycoparasitism, coiling, and antibiosis and is therefore recommended as a potential and native biocontrol agent for effective control of soil-transmitted diseases. Various species of Trichoderma, like T. virens, T. asperellum, T. harzianum, etc., have been explored for their biocontrol activity against phytopathogens. There are different Trichoderma species and strains with respect to plant pathogens. Efforts have been made to develop effective and efficient methods, such as microencapsulation use of different polymers, adjuvants, or carriers, to increase the shelf-life and efficacy of Trichoderma formulations.

biocontrol phytopathogen mycoparasitism soil-borne bio-pesticide

1. Introduction

Biological control of plant diseases has emerged as a promising area in phytopathology. These methods not only minimize reliance on synthetic pesticides but are also comparatively economical, feasible, robust, and sustainable [1][2]. Among the commercial biofungicides/fungal antagonists, Trichoderma has been broadly acknowledged as a source of potential biocontrol agent, particularly for lowering soil-borne phytopathogens such as Fusarium oxysproum, Rhizoctonia solani [3], Macrophomina phaseolina [4], Sclerotinia rolfsii, and others [5][6][7]. Trichoderma spp. are saprophytic, avirulent, and soil-inhabiting fungi, and they control pathogens with various biocontrol methods such as mycoparasitism [8], retard the pathogen growth by secreting cell-wall-destroying enzymes [9][10], nutrient uptake competition, and rhizospheric competence [2]. Because of its effectiveness against phytopathogens, its market demand is increasing yearly [11].
According to Harman (1991), [12] key points that are required for the production of any biological control system are (1) a potential biocontrol agent, (2) viable propagule with amplified shelf-life, (3) bioprotective delivery mechanisms that may offer the biocontrol agent an advantage to compete against existing microflora, and (4) steady field performance [13]. As mentioned above, the first and most principal step before mass production of a biocontrol agent is the identification of a robust propagule (hyphae, chlamydospores, and/or conidia) [14]. Once a reliable and efficient biocontrol agent is identified, large-scale production, design, and application ideas need to be performed cautiously for the product’s stability during storage and later use. Both liquid and solid formulations are utilized in developing sufficient amounts of viable and active Trichoderma inoculums. Conidia and chlamydospores are the preferred propagules for formulations since they can withstand rigorous treatment procedures, whereas hyphae cannot be used because they are not dehydration-resistant [12][15]. Several reports (Table 1) related to the effectiveness of Trichoderma strains and their formulations have been published periodically [13]; however, reports concerning advancements in mass production, persistent viability, and related field performance of Trichoderma species are fragmentary. Furthermore, the challenges related to the isolation and development methods for elevating the effectiveness and sustainable use of Trichoderma formulations in the field of health security and food also need to be addressed. In this research, researchers intend to fill this gap and unravel the recent developments regarding isolation, identification, preservation, substrates, consortium, quality control, mass production, delivery approaches, field performance, and registration and commercialization of Trichoderma formulations.
Table 1. Timeline of historical events in Trichoderma research.
Decades Year Landmarks in Trichoderma Research References
1700s 1794 In this year, the name Trichoderma was introduced. [16]
1800s 1865 The sexual stage of Trichoderma viride (Hypocrea rufa) was reported. [17]
1900s 1932 First evidence that Trichoderma lignorum (Hypocrea virens) has mycoparasitic and biocontrol abilities. [18]
1934 The invention of the first anti-microbial compound (e.g., gliotoxin). [19]
1957 Discovery of the effect of light on T. viride; syn. T. reesei. [20]
1972 Demonstration of biocontrol activity of T. harzianum against Sclerotium rolfsii in field conditions. [21]
1979 RUT C30, a carbon catabolite mutant of T. reesei, was isolated using ultraviolet (UV) mutagenesis. [22]
1983 Cloning of the first Trichoderma species (e.g., T. reesei). [23]
1984 The first international workshop was held on Trichoderma. -
1985 Papavizas wrote the first review on biology, ecology, and potential for biocontrol by Trichoderma. [15]
1986 Report on the expression of growth promotion in the root. [24]
1987 Successful transformation of T. reesei. [25]
1989 First registration of commercial formulation (e.g., Binab T). [26]
1992 Evidence of cloning of lectin-coated fibers by Trichoderma species. [27]
1993 prb1 gene cloning related to mycoparasitism and induced by cell wall. [28]
1997 Expression of enhanced plant immunity (ISR) by application of Trichoderma spp. [29]
1998 Identification of factors that induce genes for mycoparasitism. [30]
1999 Trichoderma internal colonization of plant roots demonstrated. [31]
2000s 2002 Role of signaling pathways and G protein in mechanism of biocontrol and conidia formation. [32]
2003 Role of mitogen-activated protein kinase (MAPK), which negatively regulates conidiation in T. virens. [33][34]
2004 Identification of photoreceptors (Brl1 and Brl2) in T. atroviride. [35]
2005 Function of Trichoderma MAPK (mitogen-activated protein kinase) in Induce systemic resistance (ISR). [36]
2006 Purification of the first true elicitor protein (Sm1/EplI) of Hypocreaatro viridis on glucose. [37]
2006 Cellulases and xylanases regulators identified in T. reesei (XYR1). [38]
2008 First genome sequenced of Trichoderma species (e.g., T. reesei). [39]
2009 Endophytic Trichoderma for stress tolerance in plants. [40]
2010 Discovery of VELVET protein (Vel1) as a key regulator in biocontrol agents (e.g., T. virens) and Trichoderma spp. peptide pheromone precursor genes have been identified. [41]
2011 Genome comparison of three species of Trichoderma. [42]
2012 Next-generation sequencing and high-throughput procedures were used for the sequencing of Trichoderma spp. (T. asperellum, T. harzianum, T. citrinoviride, T. longibrachiatum) genome. [43]
2022 Five new Trichoderma species were reported. [44]
2014–2022 144 Trichoderma strains were registered in 40 countries. [45]

2. Trichoderma Serves as a Biocontrol Agent

Trichoderma was initially reported as a biocontrol agent in the 1930s [18][19]. Since the discovery of mycoparasitic activity of Trichoderma by Weindling against Rhizoctonia solani and other phytopathogens, several other researchers have also obtained positive results with Trichoderma isolates as biocontrol agents of plant pathogens [46]. Trichoderma continues to hold a significant position among commercial biological control agents (BCAs) in a wide range of crop and disease management, either as a single ingredient or in combination with other ingredients [6][45][47][48]. Up till now, more than 80 species of Trichoderma have been reported [13], and among these, T. harzianum, T. virens, and T. viride are frequently deployed biocontrol agents. In India, commercialization of Trichoderma is limited to only two species, namely T. viride and T. harzianum [13]. However, there are ample reports on the effectiveness of T. virens and T. asperellum, but these are still unregistered under the Central Insecticide Board and Registration Committee (CIBRC) in India. This may be due to several hurdles, such as toxicity assessment, environmental effects of microbes and their formulation, and optimization of technology for mass-scale production [49]. Apart from these, some other constraints include multi-location trials for the purpose of proving its safety, followed by registration. In addition, some other challenges are inconsistent field presentation and low shelf-life of formulation, lack of patent protection, preliminary testing, high registration cost, alertness about the beneficial effect of Trichoderma formulations, and training and education shortfalls. Registration also requires good and effective documentation and other confirmations. Moreover, the evaluation process itself (compilation and analysis of data) can be prolonged and costly. In the past, high registration fees were clearly seen as a delay or barrier to BCA market growth, especially for medium and small enterprises that are the chief manufacturers of biocontrol agents. Due to these reasons, there are now diverse products in the market that claim to be plant growth promoters or biofertilizers for managing plant diseases but are not yet registered. The biocontrol activity of Trichoderma spp. is represented in Table 2.
However, their safe use cannot be guaranteed without toxicological and efficacy data [50]. Combined with the competitive pesticide industry, BCA companies are finding it hard to generate enough revenue from product sales to justify the registration cost. Unluckily, this has led to some products being removed from the stores. For instance, T. harzianum T-39 (Trichodex) was launched in Europe and Israel in 1993 for the control of Botrytis fruit rot through biological methods but was detached from the market. It went bankrupt in 2005 due to low sales and the rising cost of registration. Table 3 contains information on gene identification in Trichoderma species.
Table 2. Biocontrol activity of Trichoderma spp.
Name of Trichoderma Species Name of Plant Pathogens Crop Name Inhibition/Efficacy (%) Experiment Condition References
T. harzianum Sclerotium rolfsii and Rhizoctonia solani Ryegrass 42–47 Greenhouse and field condition [51]
T. harzianum Phytophthora cinnamon Pine 28.5–37.5 Greenhouse [52]
T. hamatum and T. harzianum P. cinnamomi Avocado   Greenhouse [53]
T. viride, T. virens T. harzianum, T. pseudokoningii T. koningii Aspergillus niger, Rhizoctonia solani and Geotrichum candidum Sapodilla (Manilkara zapota L.) 54–74 Laboratory [54]
T. harzianum strain Ths97 F. solani Olive trees 25–50 - [55]
Trichoderma viride 1433 Mutant strains Pythium aphanidermatum Mustard 85 Lab and field [56]
Trichoderma spp. Pythium aphanidermatum Chilli 88.00 Lab and field [57]
Trichoderma harzianumRifai, Trichoderma viride Pythium aphanidermatum Tobacco 100 Lab and greenhouse [58]
Trichoderma virens Trichoderma harzianum, Trichoderma viride Phomopsis vexans Brinjal 38–49 Lab [59]
Trichoderma harzianum T22 Alternaria alternata Sunflower 75 Lab [60]
T. atrobrunneum Armillaria mellea Strawberry 91 Field [61]
Trichoderma harzianum Fusarium moniliforme Maize 73.33 Lab [62]
T. viride, Gliocladium virens Rhizoctonia solani Rice 67.94% and 68.62% respectively Lab [63]
Table 3. Reports on gene identification in Trichoderma species.
S.No. Identified Genes Trichoderma Species Function References
1 Tvsp1 T. virens This gene protects cotton seedlings against Rhizoctonia solani. [64][65]
2 Tag3 T. asperellum Responsible for glucanase production for cell wall degradation. [66]
3 TgaA and TgaB T. virens Bicontrol efficacy for management of R. solani and Sclerotium rolfsii. [67]
4 ThPG1 T. harzianum This gene is required for beneficial interaction between Trichoderma harzianum and the host. [68]
5 ThPRT2 T. harzianum Mycoparasitism activity for Botrytis cinerea. [69]
6 tri5 T. brevicompactum IBT40841 Production of antifungal activity and trichodermin against fungus causing infection in the human body (Candida spp. and Aspergillus fumigatus). [70]
7 erg1 T. harzianum CECT 2413 Ergosterol biosynthetic pathway (EBP). [71]
8 TvGST T. virens This gene provides enhanced tolerance against cadmium stress. [72]
9 TrCCD1 T. reesei This gene facilitates pigment production and hyphal growth. [73]
10 egl1 T. longibrachiatum Exhibits antagonistic activity against Pythium ultimum. [74]
11 qid74 T. harzianum Plant biofertilization and root architecture. [75]
12 Taabc2 T. atroviride ATP binding cassette transporter plays a major role in cell membranes. [76]
13 tac1 T. virens IMI 304061 This gene shows mycoparasitism against S. rolfsii and R. solani. [77]
14 TrCCD1 T. reesei This gene promotes condia formation and elongation of fungal hyphae. [73]
15 gluc78 w T. atroviride Cell wall disintegartion of Pythium and Rhizoctonia spp. [78]
16 SL41 T. harzinum Showed mycoparasitic action. [79]
17 Taabc2 T. atroviride This gene is important for biological control of necrotrophs (B. cinerea and R. solani). [76]
18 Monooxygenase T. hamatum This gene shows antagonistic activity against Sclerotinia sclerotiourum and S. cepivorum. [80]
19 Xl1 Trichoderma strain Y This gene is helpful in hemicellulose breakdown. [81]
20 eg1, β-1,4 glucanase T longibrachiatum This gene shows antagonistic activity against Pythium ultimum in cucumber. [82]
21 pacC T. virens This gene acts as myctorphy. [83]
22 tvhydii1 T. reesei Important in mycoparasitism and plant-fungus interaction. [84]
23 hmgR T. koningii These genes inhibit the pathogen Rhizoctonia solani. [85]
24 Tasx1 T. asperellum This gene plays a key role in morphological development, mycoparasitism, and antibiosis. [86]
25 gpr1 T. atroviride This gene is required for the stability of cell walls and hyphal growth. [87]
26 TvCyt2 T. virens Trichoderma–Arabidopsis interaction [88]
27 gluc31 T. harzianum Mycoparasitism ability and influence cell wall organization. [89]
28 ipa-1 T. virens Antibiosis of R. solani. [90]
29 TasXyn24.2, TasXyn29.4 T. asperellum Induced resistance and promoted growth in seedlings. [91]
30 agl1 T. atroviride Biological control of plant pathogen. [92]

3. Biocontrol Properties of Trichoderma against Phytopathogens

Trichoderma spp. have the ability to produce metabolites, modulate the plant defense responses, and act as a hyperparasite [93][94]. Moreover, Trichoderma strains are effective BCAs because of their high reproductive potential, resilience to harsh environments, efficiency in utilizing nutrients, ability to alter the rhizosphere, aggressiveness against phytopathogenic fungi, and effectiveness in fostering plant growth and defense mechanisms. Due to these characteristics, Trichoderma may be found in all habitats and at high population densities [95]. Trichoderma BCAs can even have a beneficial impact on plants by promoting biofertilization, which increases plant development and enhances plant defense systems [96]. Trichoderma uses indirect and direct methods to control plant pathogens. The power of these mechanisms in the biocontrol method relies upon the type of Trichoderma strain, the antagonized pathogen, including its host, and the ecological situation [96]. The direct mechanism includes mycoparasitism and coiling, whereas the indirect mechanism includes challenges for nutrients and space, systemic acquired resistance, and antibiosis. Among them, mycoparasitism, competition, and antibiosis play a major role in Trichoderma-mediated biological control.

3.1. Mycoparasitism

Parasitism is one of the important mechanisms of fungal antagonist, where one fungus parasitizes (mycoparasite) another fungus (host), and this process is known as mycoparasitism. It has been observed that mycoparasitism involves four sequential steps: chemotaxis, recognition, attachment, and wrapping, as well as penetration of the pathogen cell wall and host digestion [97][98][99]. Trichoderma is widely used as a biofungicide against phytopathogens such as B. cinerea as well as the soil-borne pathogens Rhizoctonia, Sclerotinia, Pythium, and Fusarium spp. [14][100].
Trichoderma species employ several mechanisms to antagonize and mycoparasitize other pathogenic fungi, which includes competing for nutrients [101], releasing antibiotic metabolites, and activities like encircling the host and enlargement of the appressorium-like structure [51][102][103]. The degradation of host tissues containing pathogenic organisms occurs due to the enzymatic breakdown of cell walls facilitated by hydrolytic enzymes (such as chitinase, β-1,3-glucanase, and cellulase) that are synthesized by Trichoderma spp [104]. In T. atroviride, the nag1 gene coding for N-acetylglucosaminidase has a significant effect on chitinase induction, followed by biocontrol [105]. In the parasite interaction between Trichoderma and R. solani, host-released dispersal factors are responsible for inducing ech42 (encoding endochitinase 42) gene transcription prior to physical touch [30][106]. Lectins present in the host cell wall cause the parasites to cover the hyphae of the host after direct contact [27][100][106].

3.2. Antibiosis

Antibiosis is a phenomenon where one organism is prevented/inhibited by another microorganism through secondary metabolites (SMs). Trichoderma spp. synthesizes SMs (pyrone, heterocyclic compounds, terpenoids, polyketides, etc.) [107] and also produces specific low molecular weight compounds/antibiotics for combatting plant pathogens [108]. Antibiosis has been reported to occur during contact among pathogen, plant, and Trichoderma spp., which triggers Trichoderma to produce antibiotics and SMs to reduce the growth of phytopathogens. More than 180 secondary metabolites have been extracted from Trichoderma spp., showing different classes of chemical compounds [109][110]. On the basis of their biosynthetic origin, these compounds can be classified as peptaiboles, polyketides, and terpenes [111]. Many species of Trichoderma genus are known to synthesize peptidols that are non-proteinogenic amino acids (α-aminoisobutyric acid, a polypeptide antibiotic with a 500 to 2200 Da molecular weight). These compounds are acetylated at the N-terminus and contain an aminoalcohol at the C-terminus [112].
Different types of Trichoderma produce different antibiotics; for example, T. viride produces mucortoxins A and B, mucorin, trichophyton, and mucorin. Similarly, mucorin A and B were isolated from T. mucorin. T. harzianum produces tricholongins BI and BII, while longibrachins and trichokonins were extracted from T. koningii. Atroviridines A-C and neoatroviridines A-D have been obtained from T. atroviride culture. In addition, other antibiotics and fungicidal compounds have been isolated from T. harzianum, T. koningii, T. aureoviride, T. virens, T. hamatum, and T. lignorum [110].
Growth of soil pathogens such as Phytophthora solani, P. middletonii, P. cinnamomi, Bipolaris sorokiniana, and Fusarium oxysporum was adversely affected in the vicinity of Koninginin D [113]. Similarly, viridins obtained from Trichoderma spp. like T. viride, T. koningii, and T. virens inhibit the spore germination of Colletotrichum lini, Botrytis allii, Penicillium expansum, Fusarium caeruleum, Stachybotry satra, and Aspergillus niger [114]. Harzianic acids derived from T. harzianum show antimicrobial activity against Sclerotinia sclerotiorum, R. solani, and Pythium irregulare [115]. It has been found that Trichoderma spp. And Gliocladium suppressed the growth of various soil-borne plant pathogens (Fusarium spp., Macrophomina, Sclerotium rolfsii, and Sclerotinia spp.) [116][117]. Silva et al. (1998) studied the antibiosis mechanism of Trichoderma against Colletotrichum spp. [118].

3.3. Competition

Limitation and competition for nutrient sources can lead to the natural control of fungal pathogens [119]. Trichoderma is a cosmopolitan fungus and is found in all kinds of soils because of its outstanding competitive potential. It can fight with phytopathogens for nutritive sources, such as C, N, and Fe, and also acts as a biological antagonist towards soil-borne pathogens. It is also an aggressive competitor that grows rapidly and quickly colonizes its substrate and controls slow-growing pathogens [120]. Trichoderma is more competitive with other microorganisms due to certain abilities, such as a higher growth rate and enhanced aptitude to mobilize and utilize nutrients from soil/substrate [121][122]. Thus, competition for macro and micronutrients plays a key role in the interaction between Trichoderma-plant pathogen [123] because Trichoderma species compete with bacteria in the rhizosphere of crops for nutrients and sites of infection [124]. Compared to other rhizosphere bacteria, Trichoderma shows a better ability to produce and take up nourishment from soil; therefore, the management of certain disease-causing entities, such as Botrytis cinerea, using Trichoderma through food competition is possible [125]. It is observed that there are four major features of any organism that contribute to its saprophytic ability and inoculum potential: (i) fast germination of fungal propagule, rapid hyphal growth towards nutrients, (ii) production of suitable enzymes for carbon constituents of the host plant, (iii) secretion of growth inhibitor compounds (fungistatic and bacteriostatic), and (iv) tolerance to fungistatic substances produced by competing microorganisms. Antagonistic fungi can compete with the pathogens for food and space by colonizing the normal environment, i.e., plant tissue, rhizosphere, or phyllosphere [126]. It depends on the colonization level of the host plant and acclimatization to the environmental situations in which they are living [127]. In order to successfully compete with other fungal phytopathogens for food and space, Trichoderma should exhibit efficient strategies for colonization of the plant and should be plentiful in an area where competition with other microorganisms occurs [126].
Trichoderma spp. produces iron chelating agents and siderophores, which make iron unobtainable for rhizospheric bacteria, which eventually leads to the extinction of the disease. Thus, Trichoderma acts as a competitor that helps control plant diseases [128]. Apart from this, due to its ability to colonize the rhizosphere and outcompete for nutrients, T. harzianum (T35 Strain) reduces the availability of nutrients and the amount of rhizospheric space available for the fungal wilt agent of watermelon (Fusarium oxysproum f.sp. meloni) to colonize [129]. Srinivasan et al. (1995) demonstrated the importance of competition between siderophore-producing Trichoderma strains and wood decay Basidiomycetes fungi [130].
Mokhtar et al. 2013 studied the interaction between T. harzianum and a few fungal species, such as Alternaria alternata, Fusarium acuminatum, and A. infectoria. The results revealed that lack of nutrients caused death of the pathogenic fungi [131]. It has also been found that Trichoderma can compete with plant pathogens, including Colletotrichum sp., Botrytis sp., and Phytophthora sp., for complex and simple substrates of carbon [132]. In order to successfully compete with other fungal phytopathogens for food and space, Trichoderma should exhibit efficient strategies for colonization of the plant and should be plentiful in an area where competition with other microorganisms occurs [126].
Trichoderma colonization of roots commonly improves nutrient absorption and utilization, crop yield, tolerance to abiotic stressors, and root growth and development [133]. Trichoderma hamatum or Trichoderma koningii can boost crop production up to 300% after addition in the field. In greenhouse experiments, a substantial increase in yield was reported after treating the seedlings with Trichoderma spores [95]. The ability of Trichoderma BCAs to produce metabolites that either prevent spore germination (fungistatic), kill cells (antibiosis), or alter the rhizosphere, for example, making the soil acidic, leads to biocontrol that is unsuitable for pathogen proliferation [96]. Trichoderma strains quickly proliferate when introduced to the soil because they are inherently resistant to a wide range of hazardous substances, including insecticides, fungicides, and herbicides like DDT [95].

3.4. Production of Antibiotics and Other Antifungal Compounds

It has been shown that the Trichoderma species produce a large number of secondary metabolites, about 370 of which are members of several chemical compound classes with potent antagonistic activities [126][134]. Peptaibols and polyketides are the most significant non-volatile and volatile organic compounds (VOCs) produced by the majority of Trichoderma strains [2]. The volatile antibiotic 6-phenyl-pyrone (6PAP), responsible for the distinctive coconut scent and the biological control of F. oxysporum, is produced by the T. viride, T. harzianum, and T. koningii species [135]. In addition, T. harzianum also produces harzianic acid, a tetramic acid that has strong antifungal action as well as the capacity to stimulate plant development and function as a chelator [136].

3.5. Induced Systemic Resistance

Trichoderma can trigger a host plant’s defensive mechanism while preventing harmful pathogens from proliferating and growing, and it can also encourage crops to build self-defense mechanisms to gain local or systemic disease resistance [137]. Two methods are used to achieve Trichoderma-induced plant disease resistance: first, control the elicitors or elicitors that trigger the plant disease resistance response; and second, release oligosaccharides from the cell-wall-degrading enzymes produced by Trichoderma to cause plant resistance [138]. Saravanakumar et al. (2016) found that Trichoderma coated corn seeds dramatically increased the peroxidase (POD) and phenylalanine ammonia lyase (PAL) activity, and the plants were resistant to Curvularia leaf spot of corn [139].

References

  1. He, D.C.; He, M.H.; Amalin, D.M.; Liu, W.; Alvindia, D.G.; Zhan, J. Biological Control of Plant Diseases: An Evolutionary and Eco-Economic Consideration. Pathogens 2021, 10, 1311.
  2. 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.
  3. Zin, N.A.; Badaluddin, N.A. Biological functions of Trichoderma spp. for agriculture applications. Ann. Agric. Sci. 2020, 65, 168–178.
  4. Larralde-Corona, C.P.; Santiago-Mena, M.R.; Sifuentes-Rincón, A.M.; Rodríguez-Luna, I.C.; Rodríguez-Pérez, M.A.; Shirai, K.; Narváez-Zapata, J.A. Biocontrol potential and polyphasic characterization of novel native Trichoderma strains against Macrophomina phaseolina isolated from sorghum and common bean. Appl. Microbiol. Biotechnol. 2008, 80, 167–177.
  5. Bueno, V.H.P.; Parra, J.R.P.; Bettiol, W.; Lenteren, J.v. Biological control in Brazil. In Biological Control in Latin America and the Caribbean: Its Rich History and Bright Future; CABI: Wallingford, UK, 2020; pp. 78–107.
  6. Thambugala, K.M.; Daranagama, D.A.; Phillips, A.J.; 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.
  7. 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.
  8. Guzmán-Guzmán, P.; Kumar, A.; de Los Santos-Villalobos, S.; Parra-Cota, F.I.; Orozco-Mosqueda, M.D.C.; Fadiji, A.E.; Hyder, S.; Babalola, O.O.; Santoyo, G. Trichoderma species: Our best fungal allies in the biocontrol of plant diseases—A review. Plants 2023, 12, 432.
  9. Druzhinina, I.S.; Seidl-Seiboth, V.; Herrera-Estrella, A.; Horwitz, B.A.; Kenerley, C.M.; Monte, E.; Mukherjee, P.K.; Zeilinger, S.; Grigoriev, I.V.; Kubicek, C.P. Trichoderma: The genomics of opportunistic success. Nat. Rev. Microbiol. 2011, 9, 749–759.
  10. Monte, E.; Bettiol, W.; Hermosa, R. Trichoderma e seus mecanismos de ação para o controle de doenças de plantas. In Trichoderma: Usos na Agricultura; Meyer, M.C., Mazaro, S.M., da Silva, J.C., Eds.; Embrapa Soja: Brasília, Brazil, 2019; pp. 181–200.
  11. De Rezende, L.C.; de Andrade Carvalho, A.L.; Costa, L.B.; de Almeida Halfeld-Vieira, B.; Silva, L.G.; Pinto, Z.V.; Morandi, M.A.B.; de Medeiros, F.H.V.; Mascarin, G.M.; Bettiol, W. Optimizing mass production of Trichoderma asperelloides by submerged liquid fermentation and its antagonism against Sclerotinia sclerotiorum. World J. Microbiol. Biotechnol. 2020, 36, 113.
  12. Harman, G.; Jin, X.; Stasz, T.; Peruzzotti, G.; Leopold, A.; Taylor, A. Production of conidial biomass of Trichoderma harzianum for biological control. Biol. Control 1991, 1, 23–28.
  13. Mawar, R.; Manjunatha, B.; Kumar, S. Commercialization, diffusion and adoption of bioformulations for sustainable disease management in indian arid agriculture: Prospects and challenges. Circ. Econ. Sust. 2021, 1, 1367–1385.
  14. Howell, C. Mechanisms employed by Trichoderma species in the biological control of plant diseases: The history and evolution of current concepts. Plant Dis. 2003, 87, 4–10.
  15. Papavizas, G. Trichoderma and Gliocladium: Biology, ecology, and potential for biocontrol. Annu. Rev. Phytopathol. 1985, 23, 23–54.
  16. Persoon, C.H. Disposita methodical fungorum. Romers. Neues. Mag. Bot. 1794, 1, 81–128.
  17. Tulasne, L.-R.; Tulasne, C. Selecta Fungorum Carpologia, 2; Imperial: Paris, France, 1863.
  18. Weindling, R. Trichoderma lignorum as a parasite of other soil fungi. Phytopathology 1932, 22, 837–845.
  19. Weindling, R. Studies on a lethal principle effective in the parasitic action of Trichoderma lignorum on Rhizoctonia solani and other soil fungi. Phytopathology 1934, 24, 1153–1179.
  20. Gutter, Y. Effect of light in sporulation of Trichoderma viride. Bull. Res. Council Israel Sect. D 1957, 5, 273–286.
  21. Wells, H.D. Efficacy of Trichoderma harzianum as a biocontrol for Sclerotium rolfsii. Phytopathology 1972, 62, 442.
  22. Montenecourt, B.S.; Eveleigh, D.E. Selective screening methods for the isolation of high yielding cellulase mutants of Trichoderma reesei. Adv. Chem. 1979, 181, 289–301.
  23. Shoemaker, S.; Schweickart, V.; Ladner, M.; Gelfand, D.; Kwok, S.; Myambo, K.; Innis, M. Molecular cloning of exo–cellobiohydrolase I derived from Trichoderma reesei strain L27. Biotechnology 1983, 1, 691–696.
  24. Chang, Y.-C.; Chang, Y.-C.; Baker, R. Increased growth of plants in the presence of the biological control agent Trichoderma harzianum. Plant Dis. 1986, 70, 145–148.
  25. Penttilä, M.; Nevalainen, H.; Rättö, M.; Salminen, E.; Knowles, J. A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei. Gene 1987, 61, 155–164.
  26. Harkki, A.; Uusitalo, J.; Bailey, M.; Penttilä, M.; Knowles, J.K. A novel fungal expression system: Secretion of active calf chymosin from the filamentous fungus Trichoderma reesei. Biotechnology 1989, 7, 596–603.
  27. Inbar, J.; Chet, I. Biomimics of fungal cell-cell recognition by use of lectin-coated nylon fibers. J. Bacteriol. 1992, 174, 1055–1059.
  28. 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.
  29. Bigirimana, J.; De Meyer, G.; Poppe, J.; Elad, Y.; Höfte, M. Induction of systemic resistance on bean (Phaseolus vulgaris) by Trichoderma harzianum. Meded. Fac. Landbouwkd. Toegepaste Biol. Wet. Univ. Gent. 1997, 62, 1001–1007.
  30. 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.
  31. Yedidia, I.; Benhamou, N.; Chet, I. Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl. Environ. Microbiol. 1999, 65, 1061–1070.
  32. Rocha-Ramírez, V.; Omero, C.; Chet, I.; Horwitz, B.A.; Herrera-Estrella, A. Trichoderma atroviride G-protein α-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryot. Cell 2002, 1, 594–605.
  33. Mendoza-Mendoza, A.; Pozo, M.J.; Grzegorski, D.; Martínez, P.; García, J.M.; Olmedo-Monfil, 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.
  34. 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.
  35. Casas-Flores, S.; Rios-Momberg, M.; Bibbins, M.; Ponce-Noyola, P.; Herrera-Estrella, A. BLR-1 and BLR-2, key regulatory elements of photoconidiation and mycelial growth in Trichoderma atroviride. Microbiology 2004, 150, 3561–3569.
  36. Viterbo, A.; Harel, M.; Horwitz, B.A.; Chet, I.; Mukherjee, P.K. Trichoderma mitogen-activated protein kinase signaling is involved in induction of plant systemic resistance. Appl. Environ. Microbiol. 2005, 71, 6241–6246.
  37. 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.
  38. Stricker, A.R.; Grosstessner-Hain, K.; Würleitner, E.; Mach, R.L. Xyr1 (xylanase regulator 1) regulates both the hydrolytic enzyme system and D-xylose metabolism in Hypocrea jecorina. Eukaryot. Cell 2006, 5, 2128–2137.
  39. Martinez, D.; Berka, R.M.; Henrissat, B.; Saloheimo, M.; Arvas, M.; Baker, S.E.; Chapman, J.; Chertkov, O.; Coutinho, P.M.; Cullen, D.; et al. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat. Biotechnol. 2008, 26, 553–560.
  40. Bae, H.; Sicher, R.C.; Kim, M.S.; Kim, S.-H.; Strem, M.D.; Melnick, R.L.; Bailey, B.A. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J. Exp. Bot. 2009, 60, 3279–3295.
  41. 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.
  42. Kubicek, C.P.; Herrera-Estrella, A.; Seidl-Seiboth, V.; Martinez, D.A.; Druzhinina, I.S.; Thon, M.; Zeilinger, S.; Casas-Flores, S.; Horwitz, B.A.; Mukherjee, P.K. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 2011, 12, R40.
  43. Schuster, A.; Bruno, K.S.; Collett, J.R.; Baker, S.E.; Seiboth, B.; Kubicek, C.P.; Schmoll, M. A versatile toolkit for high throughput functional genomics with Trichoderma reesei. Biotechnol. Biofuels 2012, 5, 1–10.
  44. 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.
  45. Woo, S.L.; Hermosa, R.; Lorito, M.; Monte, E. Trichoderma: A multipurpose, plant-beneficial microorganism for eco-sustainable agriculture. Nat. Rev. Microbiol. 2023, 21, 312–326.
  46. 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.
  47. Collinge, D.B.; Jensen, D.F.; Rabiey, M.; Sarrocco, S.; Shaw, M.W.; Shaw, R.H. Biological control of plant diseases—What has been achieved and what is the direction? Plant Pathol. 2022, 71, 1024–1047.
  48. Sarrocco, S. Biological Disease Control by Beneficial (Micro)Organisms: Selected Breakthroughs in the Past 50 Years. Phytopathology 2023, 113, 732–740.
  49. Zeilinger, S.; Omann, M. Trichoderma biocontrol: Signal transduction pathways involved in host sensing and mycoparasitism. Gene Regul. Syst. Bio. 2007, 1, 227–234.
  50. Cook, R.J.; Bruckart, W.L.; Coulson, J.R.; Goettel, M.S.; Humber, R.A.; Lumsden, R.D.; Maddox, J.V.; McManus, M.L.; Moore, L.; Meyer, S.F. Safety of microorganisms intended for pest and plant disease control: A framework for scientific evaluation. Biol. Control 1996, 7, 333–351.
  51. Elad, Y.; Chet, I.; Boyle, P.; Henis, Y. Parasitism of Trichoderma spp. on Rhizoctonia solani and Sclerotium rolfsii-scanning electron microscopy and fluorescence microscopy. Phytopathology 1983, 73, 85–88.
  52. Kelley, W.D. Interactions of Phytophthora cinnamomi and Trichoderma spp. in relation to propagule production in soil cultures at 26 °C. Can. J. Microbiol. 1977, 23, 288–294.
  53. McLeod, A.; Labuschagne, N.; Kotzé, J. Evaluation of Trichoderma for biological control of avocado root rot in bark medium artificially infested with Phytophthora cinnamomi. S. Afr. Avocado Grow. Assoc. Yearb. 1995, 18, 32–37.
  54. Bhale, U.; Wagh, P.; Rajkonda, J. Antagonistic confrontation of Trichoderma spp. against fruit rot pathogens on Sapodilla (Manilkara zapota L.). J. Yeast Fungal Res. 2013, 4, 5–11.
  55. Ben Amira, M.; Lopez, D.; Triki Mohamed, A.; Khouaja, A.; Chaar, H.; Fumanal, B.; Gousset-Dupont, A.; Bonhomme, L.; Label, P.; Goupil, P.; et al. Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrolling Fusarium solani causal agent of root rot disease in olive trees. Biol. Control 2017, 110, 70–78.
  56. Khare, A.; Singh, B.; Upadhyay, R. Biological control of Pythium aphanidermatum causing damping-off of mustard by mutants of Trichoderma viride 1433. J. Agric. Technol. 2010, 6, 231–243.
  57. Muthukumar, A.; Eswaran, A.; Sanjeevkumas, K. Exploitation of Trichoderma species on the growth of Pythium aphanidermatum in chilli. Braz. J. Microbiol. 2011, 42, 1598–1607.
  58. Fajola, A.; Alasoadura, S. Antagonistic effects of Trichoderma harzianum on Pythium aphanidermatum causing the damping-off disease of tobacco in Nigeria. Mycopathologia 1975, 57, 47–52.
  59. Thesiya, M.; Rakholiya, K.; Lokesh, R.; Shekhda, M. Comparative Efficacy of Fungicides and Biocontrol Agents against Stem Blight and Fruit Rot Disease of Brinjal under Pot Culture Conditions. Int. J. Curr. Microbiol. Appl. Sci. 2020, 9, 2020.
  60. Arzanlou, M.; Khodaei, S.; Narmani, A.; Babai-Ahari, A.; Azar, A.M. Inhibitory effect of Trichoderma isolates on growth of Alternaria alternata, the causal agent of leaf spot disease on sunflower, under laboratory conditions. Arch. Phytopathol. Plant Prot. 2014, 47, 1592–1599.
  61. Naher, L.; Yusuf, U.K.; Ismail, A.; Hossain, K. Trichoderma spp.: A biocontrol agent for sustainable management of plant diseases. Pak. J. Bot. 2014, 46, 1489–1493.
  62. Bhandari, C.; Karuna, V. Screening of different isolates of Trichoderma harzianum and Pseudomonas fluorescens against Fusarium moniliforme infecting maize. Pantnagar J. Res. 2013, 11, 243–247.
  63. Lenka, S.; Mishra, S.; Mohanty, S.; Das, K.; Medhi, B. Bio-control of rice sheath blight through antagonists. ORYZA-Int. J. Rice 2012, 49, 68–69.
  64. 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.
  65. Emani, C.; Garcia, J.M.; Lopata-Finch, E.; Pozo, M.J.; Uribe, P.; Kim, D.-J.; Sunilkumar, G.; Cook, D.R.; Kenerley, C.M.; Rathore, K.S. Enhanced fungal resistance in transgenic cotton expressing an endochitinase gene from Trichoderma virens. Plant Biotechnol. J. 2003, 1, 321–336.
  66. Marcello, C.M.; Steindorff, A.S.; da Silva, S.P.; do Nascimento Silva, R.; Bataus, L.A.M.; Ulhoa, C.J. Expression analysis of the exo-β-1, 3-glucanase from the mycoparasitic fungus Trichoderma asperellum. Microbiol. Res. 2010, 165, 75–81.
  67. 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.
  68. 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.
  69. 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.
  70. Tijerino, A.; Cardoza, R.E.; Moraga, J.; Malmierca, M.G.; Vicente, F.; Aleu, J.; Collado, I.G.; Gutiérrez, S.; Monte, E.; Hermosa, R. Overexpression of the trichodiene synthase gene tri5 increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Fungal Genet. Biol. 2011, 48, 285–296.
  71. Cardoza, R.E.; Malmierca, M.G.; Gutiérrez, S. Overexpression of erg1 gene in Trichoderma harzianum CECT 2413: Effect on the induction of tomato defence-related genes. J. Appl. Microbiol. 2014, 117, 812–823.
  72. Dixit, P.; Mukherjee, P.K.; Ramachandran, V.; Eapen, S. Glutathione transferase from Trichoderma virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS ONE 2011, 6, e16360.
  73. Zhong, Y.H.; Wang, T.H.; Wang, X.L.; Zhang, G.T.; Yu, H.N. Identification and characterization of a novel gene, TrCCD1, and its possible function in hyphal growth and conidiospore development of Trichoderma reesei. Fungal Genet. Biol. 2009, 46, 255–263.
  74. Migheli, Q. Biodiversity of the Genus Trichoderma and Identification of Marker Genes Involved in the Antagonism between Trichoderma spp. and Plant Pathogenic Fungi. Ph.D. Thesis, University of Sassari, Sassari, Italy, 2008.
  75. Samolski, I.; Rincon, A.M.; Pinzon, L.M.; Viterbo, A.; Monte, E. The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiology 2012, 158, 129–138.
  76. 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.
  77. 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.
  78. Donzelli, B.G.G.; Lorito, M.; Scala, F.; Harman, G. Cloning, sequence and structure of a gene encoding an antifungal glucan 1, 3-β-glucosidase from Trichoderma atroviride (T. harzianum). Gene 2001, 277, 199–208.
  79. Liu, Y.; Yang, Q.; Song, J. A new serine protease gene from Trichoderma harzianum is expressed in Saccharomyces cerevisiae. Appl. Biochem. Microbiol. 2009, 45, 22–26.
  80. Carpenter, M.A.; Ridgway, H.J.; Stringer, A.M.; Hay, A.J.; Stewart, A. Characterisation of a Trichoderma hamatum monooxygenase gene involved in antagonistic activity against fungal plant pathogens. Curr. Genet. 2008, 53, 193–205.
  81. Min, S.Y.; Kim, B.-G.; Lee, C.; Hur, H.-G.; Ahn, J.-H. Purification, characterization, and cDNA cloning of xylanase from fungus Trichoderma strain SY. J. Microbiol. Biotechnol. 2002, 12, 890–894.
  82. 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.
  83. Trushina, N.; Levin, M.; Mukherjee, P.K.; Horwitz, B.A. PacC and pH–dependent transcriptome of the mycotrophic fungus Trichoderma virens. BMC Genom. 2013, 14, 138.
  84. 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.
  85. Gajera, H.; Hirpara, D.G.; Katakpara, Z.A.; Patel, S.; Golakiya, B. Molecular evolution and phylogenetic analysis of biocontrol genes acquired from SCoT polymorphism of mycoparasitic Trichoderma koningii inhibiting phytopathogen Rhizoctonia solani Kuhn. Infect. Genet. Evol. 2016, 45, 383–392.
  86. Yang, P. The gene task1 is involved in morphological development, mycoparasitism and antibiosis of Trichoderma asperellum. Biocontrol. Sci. Technol. 2017, 27, 620–635.
  87. Atanasova, L.; Gruber, S.; Lichius, A.; Radebner, T.; Abendstein, L.; Münsterkötter, M.; Stralis-Pavese, N.; Łabaj, P.P.; Kreil, D.P.; Zeilinger, S. The Gpr1-regulated Sur7 family protein Sfp2 is required for hyphal growth and cell wall stability in the mycoparasite Trichoderma atroviride. Sci. Rep. 2018, 8, 12064.
  88. Ramírez-Valdespino, C.A.; Porras-Troncoso, M.D.; Corrales-Escobosa, A.R.; Wrobel, K.; Martínez-Hernández, P.; Olmedo-Monfil, V. Functional characterization of TvCyt2, a member of the p450 monooxygenases from Trichoderma virens relevant during the association with plants and mycoparasitism. Mol. Plant Microbe Interact. 2018, 31, 289–298.
  89. Suriani Ribeiro, M.; Graciano de Paula, R.; Raquel Voltan, A.; de Castro, R.G.; Carraro, C.B.; José de Assis, L.; Stecca Steindorff, A.; Goldman, G.H.; Silva, R.N.; Ulhoa, C.J. Endo-β-1, 3-glucanase (GH16 family) from Trichoderma harzianum participates in cell wall biogenesis but is not essential for antagonism against plant pathogens. Biomolecules 2019, 9, 781.
  90. Estrada-Rivera, M.; Hernández-Oñate, M.Á.; Dautt-Castro, M.; Gallardo-Negrete, J.d.J.; Rebolledo-Prudencio, O.G.; Uresti-Rivera, E.E.; Arenas-Huertero, C.; Herrera-Estrella, A.; Casas-Flores, S. IPA-1 a putative chromatin remodeler/helicase-related protein of Trichoderma virens plays important roles in antibiosis against Rhizoctonia solani and induction of Arabidopsis systemic disease resistance. Mol. Plant Microbe Interact. 2020, 33, 808–824.
  91. Guo, R.; Ji, S.; Wang, Z.; Zhang, H.; Wang, Y.; Liu, Z. Trichoderma asperellum xylanases promote growth and induce resistance in poplar. Microbiol. Res. 2021, 248, 126767.
  92. Dubey, M.; Jensen, D.F.; Karlsson, M. Functional characterization of the AGL1 aegerolysin in the mycoparasitic fungus Trichoderma atroviride reveals a role in conidiation and antagonism. Mol. Genet. Genom. 2021, 296, 131–140.
  93. Harman, G.E. Overview of Mechanisms and Uses of Trichoderma spp. Phytopathology 2006, 96, 190–194.
  94. 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.
  95. Chet, I.; Inbar, J.; Hadar, I. Fungal antagonists and mycoparasites. In The Mycota IV: Environmental and Microbial Relationships; Springer: Berlin/Heidelberg, Germany, 1997; pp. 165–184.
  96. Benítez, T.; Rincón, A.M.; Limón, M.C.; Codon, A.C. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 2004, 7, 249–260.
  97. Chet, I.; Benhamou, N.; Haran, S. Trichoderma and Gliocladium. In Mycoparasitism and Lytic Enzymes; Taylor and Francis: London, UK, 1998; pp. 153–172.
  98. 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.
  99. 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.
  100. Barak, R.; Chet, I. Determination, by fluorescein diacetate staining, of fungal viability during mycoparasitism. Soil Biol. Biochem. 1986, 18, 315–319.
  101. Elad, Y.; Chet, I. Possible role of competition for nutrients in biocontrol of Pythium damping-off by bacteria. Phytopathology 1987, 77, 190–195.
  102. Dennis, C.; Webster, J. Antagonistic properties of species-groups of Trichoderma: I. Production of non-volatile antibiotics. Trans. Br. Mycol. Soc. 1971, 57, 25–39.
  103. Lu, Z.; Tombolini, R.; Woo, S.; Zeilinger, S.; Lorito, M.; Jansson, J.K. In vivo study of Trichoderma-pathogen-plant interactions, using constitutive and inducible green fluorescent protein reporter systems. Appl. Environ. Microbiol. 2004, 70, 3073–3081.
  104. Hjeljord, L.; Tronsmo, A.; Harman, G.; Kubicek, C. Trichoderma and gliocladium. Biological control: An overview. In Trichoderma & Gliocladium: Enzymes, Biological Control and Commercial Applications; Harman, G.E., Kubice, C.P., Eds.; CRC Press: Boca Raton, FL, USA, 1998; Volume 2, pp. 131–151.
  105. 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.
  106. Zeilinger, S.; Galhaup, C.; Payer, K.; Woo, S.L.; Mach, R.L.; Fekete, C.; Lorito, M.; Kubicek, C.P. Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host. Fungal Genet. Biol. 1999, 26, 131–140.
  107. Mukherjee, P.K.; Buensanteai, N.; Moran-Diez, M.E.; Druzhinina, I.S.; Kenerley, C.M. Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize. Microbiology 2012, 158, 155–165.
  108. Gajera, H.; Domadiya, R.; Patel, S.; Kapopara, M.; Golakiya, B. Molecular mechanism of Trichoderma as bio-control agents against phytopathogen system–a review. Curr. Res. Microbiol. Biotechnol. 2013, 1, 133–142.
  109. Masi, M.; Nocera, P.; Reveglia, P.; Cimmino, A.; Evidente, A. Fungal metabolites antagonists towards plant pests and human pathogens: Structure-activity relationship studies. Molecules 2018, 23, 834.
  110. Reino, J.L.; Guerrero, R.F.; Hernández-Galán, R.; Collado, I.G. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem. Rev. 2008, 7, 89–123.
  111. Hu, M.; Li, Q.-L.; Yang, Y.-B.; Liu, K.; Miao, C.-P.; Zhao, L.-X.; Ding, Z.-T. Koninginins RS from the endophytic fungus Trichoderma koningiopsis. Nat. Prod. Res. 2017, 31, 835–839.
  112. Ramachander Turaga, V. Peptaibols: Antimicrobial peptides from fungi. In Bioactive Natural Products in Drug Discovery; Springer: Singapore, 2020; pp. 713–730.
  113. Dunlop, R.W.; Simon, A.; Sivasithamparam, K.; Ghisalberti, E.L. An Antibiotic from Trichoderma Koningii Active Against Soilborne Plant Pathogens. J. Nat. Prod. 1989, 52, 67–74.
  114. Singh, S.; Dureja, P.; Tanwar, R.; Singh, A. Production and antifungal activity of secondary metabolites of Trichoderma virens. Pestic. Res. J. 2005, 17, 26–29.
  115. Manganiello, G.; Sacco, A.; Ercolano, M.R.; Vinale, F.; Lanzuise, S.; Pascale, A.; Napolitano, M.; Lombardi, N.; Lorito, M.; Woo, S.L. Modulation of tomato response to Rhizoctonia solani by Trichoderma harzianum and its secondary metabolite harzianic acid. Front. Microbiol. 2018, 9, 1966.
  116. Ragab, M.M.; Abada, K.; Abd-El-Moneim, M.L.; Abo-Shosha, Y.Z. Effect of different mixtures of some bioagents and Rhizobium phaseoli on bean damping-off under field condition. Int. J. Sci. Eng. Res. 2015, 6, 1009–1106.
  117. Chen, J.-L.; Sun, S.-Z.; Miao, C.-P.; Wu, K.; Chen, Y.-W.; Xu, L.-H.; Guan, H.-L.; Zhao, L.-X. Endophytic Trichoderma gamsii YIM PH30019: A promising biocontrol agent with hyperosmolar, mycoparasitism, and antagonistic activities of induced volatile organic compounds on root-rot pathogenic fungi of Panax notoginseng. J. Ginseng Res. 2016, 40, 315–324.
  118. De Sousa Rocha, J.d.R.; de Oliveira, N.T. In vitro antagonistic potential of Trichoderma spp. against Colletotrichum gloeosporoides agent of anthracnose in the passion fruit (passiflora). Boletín Micológico 1998, 13, 103–110.
  119. Mahmood, A.; Kataoka, R. Potential of biopriming in enhancing crop productivity and stress tolerance. In Advances in Seed Priming; Springer: Berlin/Heidelberg, Germany, 2018; pp. 127–145.
  120. Da Costa, A.C.; de Miranda, R.F.; Costa, F.A.; Ulhoa, C.J. Potential of Trichoderma piluliferum as a biocontrol agent of Colletotrichum musae in banana fruits. Biocatal. Agric. Biotechnol. 2021, 34, 102028.
  121. Fu, S.-F.; Wei, J.-Y.; Chen, H.-W.; Liu, Y.-Y.; Lu, H.-Y.; Chou, J.-Y. Indole-3-acetic acid: A widespread physiological code in interactions of fungi with other organisms. Plant Signal. Behav. 2015, 10, e1048052.
  122. Jaroszuk-Ściseł, J.; Tyśkiewicz, R.; Nowak, A.; Ozimek, E.; Majewska, M.; Hanaka, A.; Tyśkiewicz, K.; Pawlik, A.; Janusz, G. Phytohormones (auxin, gibberellin) and ACC deaminase in vitro synthesized by the mycoparasitic Trichoderma DEMTkZ3A0 strain and changes in the level of auxin and plant resistance markers in wheat seedlings inoculated with this strain conidia. Int. J. Mol. Sci. 2019, 20, 4923.
  123. Vinale, F.; Sivasithamparam, K.; Ghisalberti, E.L.; Marra, R.; Woo, S.L.; Lorito, M. Trichoderma–plant–pathogen interactions. Soil Biol. Biochem. 2008, 40, 1–10.
  124. Ahluwalia, V.; Kumar, J.; Rana, V.S.; Sati, O.P.; Walia, S. Comparative evaluation of two Trichoderma harzianum strains for major secondary metabolite production and antifungal activity. Nat. Prod. Res. 2015, 29, 914–920.
  125. Bargaz, A.; Lyamlouli, K.; Chtouki, M.; Zeroual, Y.; Dhiba, D. Soil microbial resources for improving fertilizers efficiency in an integrated plant nutrient management system. Front. Microbiol. 2018, 9, 1606.
  126. Ghorbanpour, M.; Omidvari, M.; Abbaszadeh-Dahaji, P.; Omidvar, R.; Kariman, K. Mechanisms underlying the protective effects of beneficial fungi against plant diseases. Biol. Control 2018, 117, 147–157.
  127. Oskiera, M.; Szczech, M.; Bartoszewski, G. Molecular identification of Trichoderma strains collected to develop plant growth-promoting and biocontrol agents. J. Hortic. Res. 2015, 23, 75–86.
  128. Saber, W.I.; Ghoneem, K.M.; Rashad, Y.M.; Al-Askar, A.A. Trichoderma harzianum WKY1: An indole acetic acid producer for growth improvement and anthracnose disease control in sorghum. Biocontrol Sci. Technol. 2017, 27, 654–676.
  129. Woźniak, M.; Gałązka, A.; Tyśkiewicz, R.; Jaroszuk-Ściseł, J. Endophytic bacteria potentially promote plant growth by synthesizing different metabolites and their phenotypic/physiological profiles in the Biolog GEN III MicroPlateTM Test. Int. J. Mol. Sci. 2019, 20, 5283.
  130. Srinivasan, U.; Highley, T.; Bruce, A. In The role of siderophore production in the biological control of wood decay fungi by Trichoderma spp. In Proceedings of the 9th International Biodeterioration and Biodegradation Symposium; Institution of Chemical Engineers: Rugby, UK, 1995; pp. 226–231.
  131. Mokhtar, H.; Aid, D. Contribution in isolation and identification of some pathogenic fungi from wheat seeds, and evaluation of antagonistic capability of Trichoderma harzianum against those isolated fungi in vitro. Agric. Biol. J. N. Am. 2013, 4, 145–154.
  132. Oszust, K.; Cybulska, J.; Frąc, M. How do Trichoderma genus fungi win a nutritional competition battle against soft fruit pathogens? A report on niche overlap nutritional potentiates. Int. J. Mol. Sci. 2020, 21, 4235.
  133. Boominathan, K.; Reddy, C.; Arora, D.; Bharat, R.; Mukerji, K.; Knudsen, G. Handbook of Applied Mycology: Fungal Biotechnology 4; Marcel Dekker, Inc.: New York, NY, USA, 1992.
  134. Chowdappa, S.; Jagannath, S.; Konappa, N.; Udayashankar, A.C.; Jogaiah, S. Detection and characterization of antibacterial siderophores secreted by endophytic fungi from Cymbidium aloifolium. Biomolecules 2020, 10, 1412.
  135. Blaszczyk, L.; Siwulski, M.; Sobieralski, K.; Lisiecka, J.; Jedryczka, M. Trichoderma spp.—Application and prospects for use in organic farming and industry. J. Plant Prot. Res. 2014, 54, 309–317.
  136. Vinale, F.; Flematti, G.; Sivasithamparam, K.; Lorito, M.; Marra, R.; Skelton, B.W.; Ghisalberti, E.L. Harzianic acid, an antifungal and plant growth promoting metabolite from Trichoderma harzianum. J. Nat. Prod. 2009, 72, 2032–2035.
  137. Singh, S.P.; Keswani, C.; Singh, S.P.; Sansinenea, E.; Hoat, T.X. Trichoderma spp. mediated induction of systemic defense response in brinjal against Sclerotinia sclerotiorum. Curr. Res. Microb. Sci. 2021, 2, 100051.
  138. Gomes, E.V.; Costa, M.d.N.; de Paula, R.G.; Ricci de Azevedo, R.; da Silva, F.L.; Noronha, E.F.; José Ulhoa, C.; Neves Monteiro, V.; Elena Cardoza, R.; Gutiérrez, S. The Cerato-Platanin protein Epl-1 from Trichoderma harzianum is involved in mycoparasitism, plant resistance induction and self cell wall protection. Sci. Rep. 2015, 5, 17998.
  139. Saravanakumar, K.; Fan, L.; Fu, K.; Yu, C.; Wang, M.; Xia, H.; Sun, J.; Li, Y.; Chen, J. Cellulase from Trichoderma harzianum interacts with roots and triggers induced systemic resistance to foliar disease in maize. Sci. Rep. 2016, 6, 35543.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
Upload a video for this entry
Information
Subjects: Agriculture, Dairy & Animal Science
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Vipul Kumar
,
Bhupendra Koul
,
Pooja Taak
,
Dhananjay Yadav
,
Minseok Song
View Times: 120
Revisions: 2 times (View History)
Update Date: 09 Nov 2023
Table of Contents
    1000/1000
    Hot Most Recent
    Feedback