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Trichoderma and its role in biological control of plant fungal and nematode disease

Xin Yao, Hailin Guo, Kaixuan Zhang and 3 more

Frontiers in Microbiology · 2023 · Review · CC BY

doi:10.3389/fmicb.2023.1160551

Abstract

Trichoderma is mainly used to control soil-borne diseases as well as some leaf and panicle diseases of various plants. Trichoderma can not only prevent diseases but also promotes plant growth, improves nutrient utilization efficiency, enhances plant resistance, and improves agrochemical pollution environment. Trichoderma spp. also behaves as a safe, low-cost, effective, eco-friendly biocontrol agent for different crop species. In this study, we introduced the biological control mechanism of Trichoderma in plant fungal and nematode disease, including competition, antibiosis, antagonism, and mycoparasitism, as well as the mechanism of promoting plant growth and inducing plant systemic resistance between Trichoderma and plants, and expounded on the application and control effects of Trichoderma in the control of various plant fungal and nematode diseases. From an applicative point of view, establishing a diversified application technology for Trichoderma is an important development direction for its role in the sustainable development of agriculture.

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From PubMed Central, U.S. National Library of Medicine, as current on Oct 21, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

1In the traditional crop cultivation process, the excessive use of pesticides and chemical fertilizers, as well as the long-term large-scale planting of a single crop, has led to the destruction of the farmland ecological environment, plant diseases, insect pest problems, crop pesticide residues, and soil and water environment pollution. With green agricultural development, people are urgently seeking safe, effective, and environmentally friendly plant disease control measures. Biological control is mainly used to control harmful organisms in plants through beneficial organisms and their products to control plant diseases and effectively reduce the application of chemical fertilizers and pesticides. Trichoderma, a biological fungus widely used for plant pest control, mainly exists in the soil, air, plant surface, and other ecological environments and can effectively control a variety of plant diseases. Trichoderma is mainly used to control soil-borne diseases in various plants and some leaf and spike diseases. Trichoderma can prevent disease, promote plant growth, improve nutrient utilization efficiency, enhance plant resistance, and repair agrochemical pollution.

2Trichoderma belonging to Eumycota, Deuteromycotina, Hyphomycetes, Hyphomycetales, and Moniliaceae. Its sexual stage includes the Ascomycota, Sordariomycetes, Hypocreales, Hypocreaceae, and Trichoderma ssp.. There are more than 370 Trichoderma spp. including T. harzianum, T. viride, T. asperellum, T. hamatum, T. atroviride, T. koningii, T. longibrachiatum, and T. aureoviride. Trichoderma has been used in biological control research, including T. harzianum, T. hamatum, T. longibrachiatum, T. koningii, T. viride, T. polysporum, and T. asperellum. Many studies have shown that most Trichoderma spp. can produce bioactive substances and have antagonistic effects on plant-pathogenic fungi and plant-pathogenic nematodes. These bioactive substances, including secondary metabolites and cell wall-degrading enzymes, can effectively improve crop resistance, reduce plant diseases, and promote plant growth. Professor Harman of Cornell University isolated and purified T. harzianum T22 strain and systematically studied its application in biological control of plant pests and commercial development of biological control technology. This study systematically and comprehensively elaborated on the research progress on Trichoderma spp. and its role in plant disease control, its application as a biological control and its mechanism, as well as preliminarily discussed the problems and prospects of Trichoderma as a biological control agent, providing a reference for future research and application.

Application of Trichoderma in biological control of plant fungal diseases

3Trichoderma is a biocontrol fungus widely distributed worldwide. Trichoderma has a huge application value and potential in the field of biological control of plant diseases. Research on the use of Trichoderma to control plant diseases has been reported worldwide. T. viride and T. harzianum have different degrees of inhibitory effects on 29 species of plant pathogenic fungi belonging to 18 genera, including Botrytis, Fusarium, and Rhizoctonia. Trichoderma has control effects on a variety of plant pathogenic fungi, such as Rhizoctonia solani, Pythium ultimum, Fusarium oxysporum, Sclerotinia sclerotiorum, Botrytis cinerea, Pseudocercospora spp. and Colletotrichum spp.. Trichoderma has been widely used for the biological control of cotton verticillium wilt, crop gray mold, tomato gray mold, melon wilt, potato dry rot, tobacco root rot, and other plant diseases. T. longibrachiatum T6 biocontrol agent has a good control effect on pepper damping off and can effectively control the spread of pepper disease. The control effect was up to 54.8%, which is 12.5% higher than that of the chemical pesticide carbendazim. T. harzianum has a good control effect on pepper and potato Phytophthora blight. It can inhibit the growth of Phytophthora blight in soil, reduce the number of pathogenic fungi, and effectively reduce the rate of dead seedlings and disease index of plants. The control effect of 50× T. asperellum fungal fluid on apple canker reached 88.24%, which was significantly higher than that of benziothiazolinone. T. asperellum has different effects on different pathogenic fungi, among which its inhibitory effect on the pathogen causing corn leaf spot is the best, at up to 77.91%, followed by Pythium and Fusarium; and the worst inhibition effect is on corn sheath blight. Therefore, using Trichoderma to prevent and control plant diseases can not only inhibit the growth of pathogenic fungi, which is conducive to plant growth but can also reduce the use of chemical pesticides, which is conducive to protecting the ecological environment.

Storage resistance and processing technology of Trichoderma products

4The commercial application of biocontrol Trichoderma depends to a large extent on the stress resistance (such as high temperature, drying, ultraviolet radiation, etc.) and storage resistance (more than 1 year at normal temperature) of the Trichoderma preparation. At present, there are two main technologies: on the one hand, reducing acidity and regulating oxygen utilization to induce Trichoderma to produce stress-resistant chlamydospores; on the other hand, some chemical additives (such as copper) are added to the preparation. increased the resistance of Trichoderma to high temperature (35 ~ 40°C) and ultraviolet radiation by adding trehalose to Trichoderma. added glycerin to the Trichoderma preparation as a humectant to prolong its shelf life. Special packaging design, vacuum drying, and low-density polyethylene packaging materials can extend the shelf-life to 15 months. In the field of Trichoderma preparation form processing, developed the Trichoderma conidia powder agent and obtained a patented technology for inducing Trichoderma to produce chlamydospores. With the increasingly mature biological control technology, the types of commercial preparations for Trichoderma spp. are also becoming diverse. There are four main categories: (1) Wettable powders, which are made by mixing conidia powder, powdery carriers, and humectant. (2) Granules are made by mixing and stirring conidia and carrier. (3) A mixture consisting of spore powder and chemical fungicides mixed in proportion on a suitable carrier. (4) Suspenso-emulsion is prepared by suspending conidia in a lotion composed of vegetable oil, mineral oil, emulsifier, etc. In the current market for Trichoderma biological agents, T. Harzianum is the largest, followed by T. viride and T. koningii. Trichoderma agents widely used in plant disease control mainly include Trichodex (Makhteshim Chemical Works Ltd., Israel), a commercial preparation of T. harzianum T-39; RootShield (Bioworks, USA), a commercial preparation of T. harzianum T-22; Binab TF (Binab Bio Innovation AB, Sweden), a mixed-agent of T. harzianum and T. polyspora; Sentinel (Novozymes, Denmark), a commercial preparation of T. atrovilide; And Supervivit (Borregaard Bioplant, Denmark), a commercial preparation of T. harzianum.

Competitive role of Trichoderma

5Trichoderma are saprophytic fungi with fast mycelial growth and strong adaptability to the environment. It can seize the invasive part of the pathogenic fungi in the root of a plant, thus hindering the invasion of the pathogen fungi. It can also rapidly absorb the nutrients required for the growth of the pathogen fungi, resulting in nutrient deficiency and inhibiting the growth and reproduction of the pathogen fungi (;;; Figure 1A). Trichoderma has strong adaptability to the environment. Through its rapid growth and reproduction, it can seize nutrients and space near the plant rhizosphere, consume oxygen in the air, and weaken the growth of plant pathogenic fungi. The growth rate of Trichoderma is much faster than that of plant-pathogenic fungi; therefore, it can effectively inhibit the growth of plant-pathogenic fungi. After entering the soil for 24 h, Trichoderma can quickly adsorb to the roots of crops for propagation, and the hyphae quickly wrap the roots of crops to form a protective layer, protect the roots of crops from the invasion of pathogens, and kill the nearby pathogens. found that the growth rate of T. harzianum was 2.0 to 4.2 times faster than that of B. cinerea. Trichoderma mycelium competed with Fusarium graminearum by clinging, twining, inter-penetration, and other mechanisms, which caused the mycelium of F. graminearum to deform and eventually disappear. Trichoderma can capture water and nutrients, occupy space, and consume oxygen, etc. through rapid growth and reproduction, to weaken and exclude the gray mold pathogen in the same habitat.

Mycoparasitism of Trichoderma

6Mycoparasitism is one of the important mechanisms in the biological control of Trichoderma (Figure 1B). Trichoderma can parasitize about 18 genera of Pythium, Phytophthora, Rhizoctonia, and Peronospora. They directly invade or wound the mycelium, causing the pathogen cells to expand, deform, shorten, become round, shrink the protoplasm, and break the cell wall. Trichoderma TM can invade the hyphae of Sclerotinia sclerotiorum, attach to and wrap around the hyphae of pathogenic fungi, and break the hyphae of S. sclerotiorum until it disintegrates. found that Trichoderma can form putrescence in a specific environment, which has a mycoparasitic effect on Botrytis cinerea. It forms a large number of branches and sexual structures after entering the host hyphae, thus inhibiting the appearance of grape B. cinerea symptoms. Trichoderma can degrade the cell wall of pathogenic fungi by secreting chitin-degrading enzymes, so as to better invade the interior of pathogenic fungi. Trichoderma mycelium hyperparasitized Fusarium graminearum by clinging, twining, inter-penetration, and other mechanisms, which caused the mycelium of F. graminearum to deform and eventually disappear. Chitinase secreted by T. harzianum plays an important role in promoting cell wall dissolution, mycelial autolysis, chitin assimilation, fungal parasitism, and inhibiting spore germination, mycelial growth, and spore formation. T. koningiopsis can invade the hyphae of Sclerotinia sclerotiorum, attach to and wrap around the hyphae of pathogenic fungi, and break the hyphae of S. sclerotiorum until it disintegrates.

Antibiosis effect of Trichoderma

7Antibiosis mainly refers to the ability of Trichoderma to inhibit the growth of plant pathogenic fungi by secreting antagonistic substances (;;;;; Figure 1C). Trichoderma can produce hundreds of antimicrobial secondary metabolites, including trichomycin, gelatinomycin, chlorotrichomycin, and antibacterial peptides. These secondary metabolites can act as antibacterial agents, promote plant growth, and provide rich materials for the development of agricultural antibiotics. found that the metabolites of T. viride had a significant inhibitory effect on the wilt-specific form of F. oxysporum, with an inhibition rate of 54.81%. found that the volatile secondary metabolites secreted by T. viride TG050 609 can cause the mycelium of P. nicotianae to grow irregularly, break, or even dissolve, proving that T. viride has an antibiosis effect on P. nicotianae. In addition, most Trichoderma strains can produce antimicrobial substances such as pentaibols, which can inhibit a variety of plant pathogenic fungi and can also cooperate with cell wall-degrading enzymes on pathogenic fungi to effectively inhibit their growth. Some studies have shown that some Trichoderma spp. can produce volatile metabolites, which can inhibit the growth of colonies to varying degrees, and some of them can inhibit the growth of colonies by more than 80%.

8In recent years, research on the genome, transcriptome, proteome, and metabolome of Trichoderma has developed rapidly. Genome and EST sequencing, and microarray and microarray based expression profiling have become important tools for exploring Trichoderma genes and studying the mechanism of action. In genomics research, a cDNA library of T. harzianum EST has been constructed, and multiple new genes have been identified. The researchers completed the genome sequencing of T. reesei, T. virens, and T. atroviride. used high-density oligonucleotide (HDO) microarray technology and bioinformatics analysis to detect and analyze: after 20 h of interaction between T. hamatum T7 and tomato, there were 200 differentially expressed genes, of which 166 were up-regulated and 34 were down-regulated; 43.14% of genes are related to molecular function, 56.86% are related to biological processes, and 32.0% are related to cell component formation. identified the changes of 27 endochitinase genes and 4 exochitinase genes in maize after interaction between T. harzianum T22 and maize using proteomic methods and EST libraries and discovered a new specific chitinase. used proteomic techniques to identify proteins related to resistance to root rot in maize, among which chitinase, SOD, isoflavone reductase, and PR protein are associated with resistance to root rot in maize seedlings.

Induced systemic resistance of Trichoderma

9Trichoderma can induce host plants to produce defense responses. While inhibiting the growth and reproduction of pathogenic fungi, it can also induce crops to produce self-defense systems to obtain local or systemic disease resistance (Figure 1D). Trichoderma-induced plant disease resistance is achieved through two approaches: one is to regulate the plant disease resistance response by regulating elicitors or effectors; second, the cell wall-degrading enzyme produced by Trichoderma releases oligosaccharides that can induce plant resistance. At present, there are more than 10 elicitors of Trichoderma that induce plant resistance, including Sm1, QID74 hydrophobic protein, chitin-degrading enzyme, MRSP1, xylanase, cellulase, endopolygalacturonase, sucrase, and antibacterial peptides. These substances are mainly derived from five Trichoderma species: T. asperellum, T. viride, T. atroviride, and T. harzianum. found that the activities of peroxidase (POD) and phenylalanine ammonia lyase (PAL) of corn seeds coated with Trichoderma increased significantly, and the plants were resistant to curvularia leaf spot of corn.

Antagonism of Trichoderma

10The antagonism of Trichoderma is often considered the result of simultaneous or sequential action of more than two mechanisms (;; Figures 1E,F). Based on multiple mechanisms, Trichoderma has synergistic capabilities. found that the synergistic use of T. harzianum and fungicides can effectively inhibit tomato gray mold, and the inhibition rate was higher than that of both fungicides alone. found that the fermentation metabolites of T. viride CCTCC-SWB0199 and brassinolide in a certain proportion had a higher effect on the control of tomato gray mold than when the two were applied separately. found that the biocontrol effect of Trichoderma spp. against plant pathogens fungi are often the result of a combination of multiple mechanisms, and different strains have different emphasis on biocontrol mechanisms. used transcriptology and metabolomics to study the tripartite interactions of Arabidopsis, Trichoderma, and Pseudomonas syringae tomato varieties. The results showed that the treatment of Arabidopsis roots with Trichoderma for 48 h induced more than 300 gene expression changes in the roots, but the changes in leaf genes were different from those in the roots. Trichoderma induces the differential expression of host plant genes, mainly at the level of quantity. A metabolomics study found that 27 compounds were related to induced resistance in Arabidopsis thaliana. The biocontrol effect of Trichoderma on plant pathogenic fungi is often the result of multiple mechanisms, and different strains have different biocontrol mechanisms (;;;; Figure 1).

Application of Trichoderma in the control of plant nematodes

11At present, the reported Trichoderma with nematicidal activity mainly includes T. longibrachiatum, T. viride, T. harzianum, T. Hamatum, T. atroviride, and T. koningii. The fermentation broth of T. longibrachiatum T6 has a strong lethal effect on the eggs and second-instar larvae of cereal cyst nematodes in wheat. The relative inhibition rate of the two concentrated fermentation broths on egg hatching was 46.47%, and the corrected mortality rate for the second-instar larvae was 44.45%. Microscopic observation showed that the fermentation liquid of T. longibrachiatum T6 could digest the contents of nematode eggs and body cavities of the second instar larvae. used inducers to make T. koningiopsis UFSMQ40 produced fermentation broth containing a large amount of chitinase, and its lethal rate to root-knot nematodes of South China and Java was 90.4 and 63.2%, respectively. analyzed the transcriptional activity of chi18-5 and chi18-12 genes of T. harzianum FB10 in Trichoderma egg parasitism. Compared to the control, the expression of chi18-5 and chi18-12 genes during parasitism increased significantly, indicating that the chitinase content increased, which could provide favorable conditions for egg cleavage.

Mechanism of Trichoderma resistance to nematode disease

12The mechanism by which Trichoderma inhibits nematode disease remains unclear. Some studies suggest that the serine protease pr1 of Trichoderma has similar biochemical characteristics to the protein Pr1 of nematicidal fungi, so it has a certain nematode inhibition effect. The antimicrobial peptides produced by Trichoderma also have nematicidal effects.

Mycoparasitism effect of Trichoderma

13Trichoderma mycoparasitism is an important mechanism for controlling nematodes and includes identification, contact, entanglement, penetration, and parasitism (; Figure 2). Trichoderma mycelium penetrates the eggshell or cuticle of larvae and adults of nematodes, colonizes, absorbs nutrients from nematodes, and causes nematode death. Trichoderma mycoparasitic nematode processes involve the production and co-secretion of various degrading enzymes. The induction of Trichoderma activities of β-1, 3-glucanase, chitinase, and protease are increased, which can enhance the immunity of plants to nematodes. The hyperparasitic process is mainly regulated by heterotrimeric G protein, cAMP, and MAPK motif signals, and secretes extracellular chitinase, glucanase, xylanase, cellulase, and protease, among which chitinase and protease are particularly important and can degrade the cyst, egg, larva, and adult body wall of nematodes. Trichoderma secretes glucosidases NAG1 and NAG2, which act on the extracellular and self-cell walls, respectively, and their main function is to degrade chitin so that they can protect their cell walls from degradation during the process of hyperparasitism.

Antibiosis effect of Trichoderma

14Trichoderma can inhibit the growth and reproduction of nematodes by secreting antagonistic substances. Trichoderma produces a variety of secondary metabolites, including trichomycin, gliotoxin, viridin, antibacterial peptide, β-1, 3-glucanase, chitinase, polypeptides, polyketones, butyrolactones, sesquiterpene heptadecarboxylic acid, terpenes, and some volatile substances (hydrocarbons, alcohols, furans, aldehydes, alkanes, olefins, esters, aromatic compounds, heterocyclic compounds, and various terpenoids). reported for the first time that T. harzianum ThzID1-M3 labeled with GFP significantly inhibited the reproduction of potato cyst nematodes, with a cyst decline rate of 60%. The inhibition rates of the fermentation broth of T. hamatum HZ-9 and T. virens HZ-L9 on the hatching of soybean cyst nematode eggs were 80.6 and 79.4%, respectively. The secondary metabolites produced by the same Trichoderma species in different media have different effects on nematode resistance. The inhibition rate of T. viride secondary metabolites on wheat medium and solid medium on egg hatching of southern root knot nematode was 71.6 and 67.3%, respectively. detected and analyzed the T. hamatum FB10 secondary metabolite nematicidal active ingredient; thirteen kinds of chemical substances were obtained, including 6-amyl-α-pyranone. The inhibition rate of egg hatching of Meloidogyne incognita was 78.26%.

Toxicity effect of Trichoderma

15Trichoderma produces toxic secondary metabolites that directly come into contact with nematodes, which is an important direct biological control mechanism. It has been found that the toxic secondary metabolites produced by Trichoderma are divided into two categories, one is small molecules and volatile substances, including aromatic compounds, polyketides, butenolactones, and terpenoids, etc.; the other is macromolecular metabolites, including peptides, enzymes, etc.. It has been reported that the main nematicidal substances isolated from Trichoderma are trichodermin, acetic acid, gliotoxin, and peptide cyclosporin A. Meanwhile, used GC–MS to detect and analyze the nematicidal active components of Trichoderma TUV-13 strain and obtained more than 40 chemical components, among which of which the main alkanes are the most, in addition to organic acids, esters, ketones, steroids, and other organic compounds. summarized and analyzed the secondary metabolites and activities of 20 species of Trichoderma, including T. aureoviride, T. arundinaceum, T. brevicompactum, T. citrinoviride, T. gamsii, T. polysporum, T. saturnisporum, T. spirale, T. cremeum, T. pesudokoningii, and T. lignorum. There were 390 non-volatile secondary metabolites, among which wickerol A, harziandione, trichodermin, and cyclonerodiol exhibited nematicidal activity. The T. virens B3 fermentation broth has strong toxic activity against cereal cyst nematodes, and the killing rate is as high as 86.2%. The fermentation broth can maintain good stability for a long time. The fermentation broth of T. citrinoviride，T. harzianum，T. acroviride, and T. koningiopsis had a strong toxic effect on the southern root-knot nematode J2, with a mortality rate of more than 85%.

Induced resistance effect of Trichoderma

16Induced resistance is the response of plants to stress, which is stimulated by external factors. Trichoderma-colonized plant roots cause physiological and metabolic changes and produce a variety of secondary metabolites that act as elicitors. At present, there are more than 20 elicitors produced by Trichoderma that induce plant resistance, including antitoxins, polypeptides, lipopeptides, cellulases, hydrophobic proteins, non-toxic gene proteins, terpenoids, phenol derivatives, glycosidic ligands, and flavonoids. These secondary metabolites induce plant defense responses and promote plant growth. The interaction between Trichoderma and plants increases the synthesis of defense-related enzymes and substances. T. hamatum can induce the activities of phenylalanine ammonia lyase (PAL), polyphenol oxidase (PPO), and peroxidase (POD), which are related to tobacco defense reaction, to increase significantly. In tomatoes treated with T. harzianum, the control effect against M. incognita was 61.88%. Further studies have shown that the levels of reactive oxygen species (ROS), superoxide (O2−), hydrogen peroxide (H2O2), and malondialdehyde (MDA) in tomatoes were significantly increased, and the defense-related genes PAL, C4H, 4CL, CAD, LPO, CCOMT, Tpx1, and G6PDH were upregulated, thus inducing the defense response of tomatoes to M. incognita. Plant-induced resistance mainly involves signal transduction pathways such as those of salicylic acid (SA), jasmonic acid (JA), and ethylene (ET). In the interaction between Trichoderma and Arabidopsis, tomato, and cucumber, JA, SA, and ET contents increased to varying degrees, indirectly improving plant resistance. This process is also related to activating chitinase and glucanase activities and inhibiting the plant antioxidant enzyme system. The expression of ETR1 and LOX1 genes of jasmonic acid and the ethylene signal pathway increased significantly in T. asperellum DQ-1 irrigated tomato, which enhanced tomato resistance. Some volatile secondary metabolites of Trichoderma are important elicitors that induce plant resistance. The volatile substances produced by T. harzianum and T. asperellum act as elicitors to stimulate the up-regulated expression of Arabidopsis-induced resistance-related transcription factor MYB72, which triggers a JA-regulated defense response. At present, the interaction mechanisms and signal transduction pathways between Trichoderma volatile secondary metabolites and plants have not been thoroughly studied. The active substances produced by Trichoderma are recognized by plants, thus activating the signal transduction pathway and inducing the production of plant system resistance. The microbial determinants recognized by microorganisms are called microbe-associated molecular patterns (MAMPs). After Trichoderma infects plant roots, it releases a variety of MAMPs to activate immune response (MTI), thus inducing plant systemic resistance (ISR). showed that T. hamatum strain Th23 promotes tomato growth and induces systemic resistance against tobacco mosaic virus.

Application of Trichoderma in promoting plant growth and repairing environment

17Trichoderma can produce plant growth stimulators, such as indoleacetic acid (IAA) and harzianolide, to promote the development and growth of plant roots by secreting phytase and ferritin to promote the absorption of P and Fe by plants; decomposes soil organic matter; increases the supply of soil nutrients; improves crop photosynthetic efficiency; improves plant height, stem diameter, and other agronomic traits; and increases production. Many studies have shown that most Trichoderma spp. can produce bioactive substances and have antagonistic effects on plant-pathogenic fungi and plant-pathogenic nematodes. Bioactive substances, including secondary metabolites and cell wall-degrading enzymes, can effectively improve the resistance of crops, reduce plant diseases, and promote plant growth.

18Trichoderma can improve soil nutrient availability and utilization efficiency. The aboveground biomass of cucumber seedlings inoculated with Trichoderma MF-2 increased by 39.07%, with a significant growth-promoting effect, and an increased number of beneficial microorganisms in the soil. Different Trichoderma strains had different degrees of antagonism to F. oxysporum, and the combination of Trichoderma wettable powder treatment significantly increased banana yield. found that the biocontrol agent Trichoderma GYXM-1p1 strain had a strong growth-promoting effect through pot cultivation. After treatment with this strain, the root length, plant height, root fresh weight, dry weight, total fresh weight, and total dry weight of cabbage plants were significantly improved compared to the water control (p < 0.05), and the total fresh weight and total dry weight of cabbage plants were increased by 417. 60% and 762. 69%, respectively, compared with water control. Ruan et al. found that the application of nitrogen fertilizer with Trichoderma promoted the quality of muskmelon. After the application of Trichoderma, the soluble sugar content of muskmelon fruit increases significantly, improving the quality of muskmelon. The application of Trichoderma can increase the SPAD value of chlorophyll in peanut leaves, improve the main agronomic traits of peanuts, significantly increase the activity of protective enzymes in peanut roots, stems, and leaves, and reduce the content of MDA. When 1.5 kg/666.7 m−2 was applied, the number of pods per plant, pod weight, seed kernel weight, 100 fruit quality, 100 fruit kernel quality, and yield per plant of peanut increased by 24.63, 20.22, 14.10, 4.86, 7.63, and 12.85%, respectively, compared with the control.

Mechanism of Trichoderma in promoting plant growth and repairing environment

19Trichoderma can promote plant growth, produce substances that can promote plant growth, improve the solubility of nutrients in the soil, and improve plant rhizosphere microecology, thereby promoting plant absorption and growth (;;; Figure 3). Trichoderma plant interactions can not only induce resistance but also improve the resistance of plants to abiotic stress factors (salt, high temperature, UV). Treatment of cucumber seeds with T. asperellum T203 improved the plant’s salt tolerance, and the activities of Mn/Cu SOD and catalase (CAT), and significantly reduced ascorbic acid in the plant. Trichoderma can significantly enhance the Na+ efflux from the root system of Lycium barbarum and its transport to the upper ground, ensure K+ absorption and maintain the ion balance in the plant, thus reducing the damage of PSII caused by ion toxicity and oxidative stress, protecting photosynthetic pigments, maintaining the photosynthetic performance of L. barbarum under salt stress, and reducing biomass loss.

20The synthesis of plant growth hormones, such as IAA, ABA, ET, GA, and CK is the main mechanism of Trichoderma. T. asperellum induced cucumber to produce IAA, GA, and ABA to promote growth. The height, stem diameter, soluble sugar content, and absorption rate of available nitrogen of tomato seedlings treated with T. asperellum were significantly increased, and the expression of tomato hormone signal transduction-related genes JAR1, MYC2, NPR1, PR1, and GH3 was significantly increased. Another study showed that T. asperellum can upregulate the expression of xylanase genes in poplar and has a significant growth-promoting effect. T. harzianum regulates tricarboxylic acid cycle (TAC) and hexose monophosphate pathway (HMP) to promote tomato growth by enhancing succinate dehydrogenase and glucose-6-phosphate dehydrogenase activities. Trichoderma produces acidic substances that can dissolve insoluble trace elements in soil and provide more nutrition to plants. T. asperellum can transform insoluble phosphate in the soil into effective phosphorus and promote the absorption and utilization of cucumbers (; Figure 3). T. koningiopsis can produce organic acids that dissolve insoluble tricalcium phosphate under high alkaline stress and can also produce alkaline phosphatase under drought stress to solubilize phosphorus and improve the utilization of nutrients by plants. Many experiments have verified that Trichoderma promotes plant growth; under complex field production conditions, the mechanism by which Trichoderma promotes plant growth requires more systematic research.

Conclusion and future perspectives

21At present, chemical control is the main method used for plant disease control and is achieved by spraying pesticides and fungicides. Although the effect of chemical control is good and helpful in increasing agricultural production, the unscientific use of chemical pesticides has caused serious pollution to the environment and enhanced pathogens’ resistance to and chemical pesticides. Several experiments have proven that Trichoderma has good biological control effects and can reduce the use of chemical pesticides. However, there are still few biocontrol agents against Trichoderma on the market, and more effective and suitable strains need to be found to join the biocontrol team. Although Trichoderma has great prospects for agricultural applications, there are still some problems in the development and utilization of Trichoderma. Because the spore preparation of Trichoderma is generally a living fungal preparation, which is often affected by various natural factors such as humidity, temperature, soil acidity, alkalinity, and the soil microbial community when it is applied in the field, the field test performance is unstable, and the biological control effect is weakened. In addition, the shelf life of biological control agents is relatively short, and some microorganisms must be stored at low temperatures to ensure the concentration of live microorganisms when they are applied.

22There are still several problems to be solved in the application of Trichoderma in the biological control of plant diseases. The first is to explore and produce efficient strains, which can be screened through genetic engineering technology to produce Trichoderma biocontrol-engineered strains that are resistant to chemical pesticides and low temperatures. At the same time, it is necessary to develop effective Trichoderma agents suitable for use with various application methods to enhance the control effect and improve the processing technology of Trichoderma agents to extend the shelf life of biological control agents. Second, exploring the combined effects of Trichoderma spp. and other microorganisms is necessary. The development of Pesticides with volatile and non-volatile secondary metabolites secreted by Trichoderma as the main active ingredient will be the focus of future research and the development of new Pesticides. To improve the quality of Trichoderma biopesticides, in addition to monitoring traditional indicators such as pH, dissolved oxygen, and temperature in the fermentation process, it is also necessary to monitor its correlation with the yield of antagonistic substances at the level of the cell metabolic flow, genome, proteome, and metabolome. However, it is necessary to establish more scientific quality standards for Trichoderma products in vivo, such as increasing the content of antagonistic substances or activity indicators. The development of new dosage forms, such as cell microcapsules, water-in-oil emulsions, and other protective dosage forms, should be strengthened, and the molecular mechanism of chlamydospore production should be further studied (Table 1).

23With further study of transgenic Trichoderma, a prospective study on the biological and environmental safety of transgenic Trichoderma should be conducted. At present, the balance regulation of Trichoderma colonizing host and plant immune response, long-distance and trans-growth period transduction mechanism of systematically induced plant disease resistance and its defense signals, identification of Trichoderma elicitors to recognize plant targets or receptors, and mechanism of Trichoderma-induced plant endophytic microbiome to synergistically stimulate plant immune response has become an international research topic of interest. Studies on miRNA regulation of Trichoderma colonization host process and plant immune response, and the regulation mechanism of cross-border miRNA transduction between Trichoderma, plants, and pathogenic microorganisms are emerging. The combination design or co-culture technology of Trichoderma and other microorganisms has become key for tapping new metabolites with specific functions of microorganisms, broadening the target spectrum of microbial metabolites, and developing new biopesticides and biostimulants based on metabolites. It is expected to become a new direction for the development of macromolecular biopesticides by molecular construction or modification of the Trichoderma multi-stimulator fusion protein and the development of new plant immune-activating protein pesticides. At present, it is urgent to reveal the synergistic interactions among Trichoderma, plants, and pathogenic microorganisms in induced disease resistance on a cross-genome scale, develop Trichoderma and other microbial symbiotic agents that can cure both diseases and pests, and develop new biostimulator products based on Trichoderma metabolites.

24Compared with single-life biocontrol fungi, compound biocontrol fungi can better avoid the problems of weak adaptability to the environment, narrow range of disease resistance, and insufficient control effect. At present, there are many preparations containing different kinds of Trichoderma, which are being used in sustainable agricultural crops, but the application of these preparations is still expensive, and not available to all farmers. The application of compatible or affinity multiple microorganisms for compounding has become a trend in the development of biocontrol agents. Trichoderma can form alliances with a variety of microorganisms such as bacteria and fungi to directly or indirectly improve the ability of plants to prevent and control diseases. The following aspects may be the main research focus of Trichoderma as a biocontrol fungus in the future: the molecular mechanism of the specific interaction between Trichoderma and plants; Molecular basis of plant immunity induced by Trichoderma; Improvement of Trichoderma fermentation process; Establishing diversified application technology models of Trichoderma. The commercial application of biocontrol Trichoderma depends largely on the stress resistance (such as high temperature, drying, ultraviolet radiation, etc.) and storage resistance (more than 1 year at normal temperature) of the Trichoderma agent. At present, there are two main technologies. One is to reduce the acidity and regulate the utilization of oxygen to induce Trichoderma to produce stress-resistant chlamydospores, and the other is to add some chemical additives (such as copper) to the inoculum. How the effectors produced by Trichoderma interact with plant cell receptors has become the key to revealing the mechanism of Trichoderma inducing plant immunity. With the deepening of the research on transgenic Trichoderma, prospective research on the biological and environmental safety of transgenic Trichoderma should be carried out.

Author contributions

25MZ and XY: software. KZ and MZ: data curation. XY: writing – original draft preparation. JR, JC, and KZ: writing, review, and editing. All authors read and agreed to the published version of the manuscript.

Funding

26This research was supported by the National Science Foundation of China (32161143005 and 32160669) and the Guizhou Science and Technology Support Program ([2020]1Y125).

Conflict of interest

27The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

28All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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Complete Genome Sequences and Genome-Wide Characterization of Trichoderma Biocontrol Agents Provide New Insights into their Evolution and Variation in Genome Organization, Sexual Development, and Fungal-Plant Interactions · 2021
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Trichoderma Applications on Strawberry Plants Modulate the Physiological Processes Positively Affecting Fruit Production and Quality · 2020
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Lombardi N. Salzano A. M. Troise A. D. Scaloni A. Vitaglione P. Vinale F.. (2020b ). Effect of Trichoderma bioactive metabolite treatments on the production, quality, and protein profile of strawberry fruits. J. Agric. Food Chem. 68, 7246–7258. doi:, PMID:
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Structural Diversity and Bioactivities of Peptaibol Compounds From the Longibrachiatum Clade of the Filamentous Fungal Genus Trichoderma · 2019
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Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato · 2013
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Calcium-mediated perception and defense responses activated in plant cells by metabolite mixtures secreted by the biocontrol fungus <it>Trichoderma atroviride</it> · 2007
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Nawrocka J. Gromek A. Małolepsza U. (2019 ). Nitric oxide as a beneficial signaling molecule in Trichoderma atroviride TRS25- induced systemic defense responses of cucumber plants against Rhizoctonia solani. Front. Plant Sci. 10:421. doi:, PMID:
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Environmental Growth Conditions of Trichoderma spp. Affects Indole Acetic Acid Derivatives, Volatile Organic Compounds, and Plant Growth Promotion · 2017
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Effects of Foliar Treatment with a Trichoderma Plant Biostimulant Consortium on Passiflora caerulea L. Yield and Quality · 2020
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Scent of a Killer: Microbial Volatilome and Its Role in the Biological Control of Plant Pathogens · 2020
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168.
Tseng Y. H. Rouina H. Groten K. Rajani P. Furch A. Reichelt M.. (2020 ). An endophytic Trichoderma strain promotes growth of its hosts and defends against pathogen attack. Front. Plant Sci. 11:573670. doi:, PMID:
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169.
Trichoderma: The Current Status of Its Application in Agriculture for the Biocontrol of Fungal Phytopathogens and Stimulation of Plant Growth · 2022
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170.
Velasco P. Rodríguez V. M. Soengas P. Poveda J. (2021 ). Trichoderma hamatum increases productivity, glucosinolate content and antioxidant potential of different leafy brassica vegetables. Plan. Theory 10:2449. doi:, PMID:
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Vicente I. Baroncelli R. Morán-Diez M. E. Bernardi R. Puntoni G. Hermosa R.. (2020 ). Combined comparative genomics and gene expression analyses provide insights into the terpene synthases inventory in Trichoderma. Microorganisms 8:1603. doi:, PMID:
Not in our library10.3390/microorganisms8101603
172.
Biological Control of Alternaria Leaf Spot Caused by Alternaria spp. in Jerusalem Artichoke (Helianthus tuberosus L.) under Two Fertilization Regimes · 2019
Not checked
173.
Viterbo A. Harel M. Horwitz B. A. Chet I. Mukherjee P. K. (2005 ). Trichoderma mitogen-activated protein kinase signaling is involved in induction of plant systemic resistance. Appl. Environ. Microbiol. 71, 6241–6246. doi:, PMID:
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174.
Vos C. M. De Cremer K. Cammue B. P. De Coninck B. (2015 ). The toolbox of Trichoderma spp. in the biocontrol of Botrytis cinerea disease. Mol. Plant Pathol. 16, 400–412. doi:, PMID:
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Wang Y. Chen H. Ma L. Gong M. Wu Y. Bao D.. (2022 ). Use of CRISPR-Cas tools to engineer Trichoderma species. Microb. Biotechnol. 15, 2521–2532. doi:, PMID:
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176.
Wang R. Liu C. Jiang X. Tan Z. Li H. Xu S.. (2022 ). The newly identified Trichoderma harzianum partitivirus (ThPV2) does not diminish spore production and biocontrol activity of its host. Viruses 14:1532. doi:, PMID:
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Wang H. Zhang R. Duan Y. Jiang W. Chen X. Shen X.. (2021 ). The endophytic strain Trichoderma asperellum 6S-2: an efficient biocontrol agent against apple replant disease in China and a potential plant-growth-promoting fungus. J. Fungi 7:1050. doi:, PMID:
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178.
Wang H. Zhang R. Mao Y. Jiang W. Chen X. Shen X.. (2022 ). Effects of Trichoderma asperellum 6S-2 on apple tree growth and replanted soil microbial environment. J. Fungi 8:63. doi:, PMID:
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Xu H. Yan L. Zhang M. Chang X. Zhu D. Wei D.. (2022 ). Changes in the density and composition of rhizosphere pathogenic Fusarium and beneficial Trichoderma contributing to reduced root rot of intercropped soybean. Pathogens 11:478. doi:, PMID:
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Ye L. Zhao X. Bao E. Li J. Zou Z. Cao K. (2020 ). Bio-organic fertilizer with reduced rates of chemical fertilization improves soil fertility and enhances tomato yield and quality. Sci. Rep. 10:177. doi:, PMID:
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You J. Li G. Li C. Zhu L. Yang H. Song R.. (2022 ). Biological control and plant growth promotion by volatile organic compounds of Trichoderma koningiopsis T-51. J. Fungi 8:131. doi:, PMID:
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182.
Yuan M. Huang Y. Ge W. Jia Z. Song S. Zhang L.. (2019 ). Involvement of jasmonic acid, ethylene and salicylic acid signaling pathways behind the systemic resistance induced by Trichoderma longibrachiatum H9 in cucumber. BMC Genomics 20:144. doi:, PMID:
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183.
Zaid R. Koren R. Kligun E. Gupta R. Leibman-Markus M. Mukherjee P. K.. (2022 ). Gliotoxin, an immunosuppressive fungal metabolite, primes plant immunity: evidence from Trichoderma virens-tomato interaction. MBio 13:e0038922. doi:, PMID:
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Zhang J. Chen J. Liu Z. Guan S. Li J. Zhang C.. (2017 ). Evaluation of the combined use of Trichoderma atroviride metabolite and brassinolide in the promotion of vegetable growth and control of Botrytis cinere. J. Shanghai Jiaotong Univ. 35, 1–7
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185.
Optimization of the Fermentation Media and Parameters for the Bio-control Potential of Trichoderma longibrachiatum T6 Against Nematodes · 2020
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186.
Zhang F. Huo Y. Cobb A. B. Luo G. Zhou J. Yang G.. (2018 ). Trichoderma biofertilizer links to altered soil chemistry, altered microbial communities, and improved grassland biomass. Front. Microbiol. 9:848. doi:, PMID:
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Zhang C. Wang W. Hu Y. Peng Z. Ren S. Xue M.. (2022 ). A novel salt-tolerant strain Trichoderma atroviride HN082102.1 isolated from marine habitat alleviates salt stress and diminishes cucumber root rot caused by Fusarium oxysporum. BMC Microbiol. 22:67. doi:, PMID:
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188.
Zhang C. Wang W. Xue M. Liu Z. Zhang Q. Hou J.. (2021 ). The combination of a biocontrol agent Trichoderma asperellum SC012 and hymexazol reduces the effective fungicide dose to control Fusarium wilt in cowpea. J. Fungi 7:685. doi:, PMID:
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Zhang Y. Xiao J. Yang K. Wang Y. Tian Y. Liang Z. (2022 ). Transcriptomic and metabonomic insights into the biocontrol mechanism of Trichoderma asperellum M45a against watermelon Fusarium wilt. PLoS One 17:e0272702. doi:, PMID:
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190.
Zheng H. Qiao M. Lv Y. Du X. Zhang K. Q. Yu Z. (2021 ). New species of Trichoderma isolated as endophytes and saprobes from Southwest China. J. Fungi 7:467. doi:, PMID:
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Zhou D. Huang X. F. Guo J. Dos-Santos M. L. Vivanco. (2018 ). Trichoderma gamsii affected herbivore feeding behaviour on arabidopsis thaliana by modifying the leaf metabolome and phytohormones. Microb Biotechnol. 11, 1195–1206., PMID:
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Zhu N. Zhou J. J. Zhang S. W. Xu B. L. (2022 ). Mechanisms of Trichoderma longibrachiatum T6 fermentation against Valsa mali through inhibiting its growth and reproduction, pathogenicity and gene expression. J. Fungi 8:113. doi:, PMID:
Not in our library10.3390/jof8020113

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Physiological defensive modes to biologically induce drought tolerance in broccoli via inoculation with mycorrhiza and Trichoderma · 2025
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