Biological control involves the use of beneficial organisms, their genes, and/or products, such as metabolites, that reduce the negative effects of plant pathogens and promote positive responses by the plant. Disease suppression, as mediated by biocontrol agents, is the consequence of the interactions between the plant, pathogens, and the microbial community. Antagonists belonging to the genus Trichoderma are among the most commonly isolated soil fungi. Due to their ability to protect plants and contain pathogen populations under different soil conditions, these fungi have been widely studied and commercially marketed as biopesticides, biofertilizers and soil amendments. Trichoderma spp. also produce numerous biologically active compounds, including cell wall degrading enzymes, and secondary metabolites. Studies of the three-way relationship established with Trichoderma, the plant and the pathogen are aimed at unravelling the mechanisms involved in partner recognition and the cross-talk used to maintain the beneficial association between the fungal antagonist and the plant. Several strategies have been used to identify the molecular factors involved in this complex tripartite interaction including genomics, proteomics and, more recently, metabolomics, in order to enhance our understanding. This review presents recent advances and findings regarding the biocontrol-resulting events that take place during the Trichoderma –plant–pathogen interaction. We focus our attention on the biological aspects of this topic, highlighting the novel findings concerning the role of Trichoderma in disease suppression. A better understanding of these factors is expected to enhance not only the rapid identification of effective strains and their applications but also indicate the potentials for improvement of natural strains of Trichoderma .

Trichoderma–plant–pathogen interactions

Trichoderma is a genus of common filamentous fungi that display a remarkable range of lifestyles and interactions with other fungi, animals and plants. Because of their ability to antagonize plant-pathogenic fungi and to stimulate plant growth and defence responses, some Trichoderma strains are used for biological control of plant diseases. In this Review, we discuss recent advances in molecular ecology and genomics which indicate that the interactions of Trichoderma spp. with animals and plants may have evolved as a result of saprotrophy on fungal biomass (mycotrophy) and various forms of parasitism on other fungi (mycoparasitism), combined with broad environmental opportunism.

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Trichoderma : the genomics of opportunistic success

Antagonistic fungi, trichoderma spp.: panoply of biological control

Research on the mechanisms employed by the biocontrol agent Trichoderma virens to suppress cotton (Gossypium hirsutum) seedling disease incited by Rhizoctonia solani has shown that mycoparasitism and antibiotic production are not major contributors to successful biological control. In this study, we examined the possibility that seed treatment with T. virens stimulates defense responses, as indicated by the synthesis of terpenoids in cotton roots. We also examined the role of these terpenoid compounds in disease control. Analysis of extracts of cotton roots and hypocotyls grown from T. virens-treated seed showed that terpenoid synthesis and peroxidase activity were increased in the roots of treated plants, but not in the hypocotyls of these plants or in the untreated controls. Bioassay of the terpenoids for toxicity to R. solani showed that the pathway intermediates desoxyhemigossypol (dHG) and hemigossypol (HG) were strongly inhibitory to the pathogen, while the final product gossypol (G) was toxic only at a much higher concentration. Strains of T. virens and T. koningii were much more resistant to HG than was R. solani, and they thoroughly colonized the cotton roots. A comparison of biocontrol efficacy and induction of terpenoid synthesis in cotton roots by strains of T. virens, T. koningii, T. harzianum, and protoplast fusants indicated that there was a strong correlation (+0.89) between these two phenomena. It, therefore, appears that induction of defense response, particularly terpenoid synthesis, in cotton roots by T. virens may be an important mechanism in the biological control by this fungus of R. solani-incited cotton seedling disease.

Induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. [Erratum: 2003 Dec., v. 93, no. 12, p. 1606.]

After 25 years of working with bacteria, actinomycetes, and fungi as biocontrol agents of cotton seedling and root diseases, I believe Trichoderma virens to be one of the most versatile and effective biocontrol agents we have studied. The species contains an arsenal of mechanisms and antimicrobial metabolites that give it a wide spectrum of activity against different pathogens (1,6,7, 22,29,30), and the capacity to control a number of diseases (4,6, 7,9,20,29,30). To a biocontrol scientist, one of the salient features of Trichoderma virens, and one of the reasons it has been so frequently studied, is that it is an aggressive mycoparasite of other fungi (7,22,23), many of which are plant pathogens. It not only parasitizes the hyphae of many fungal species, but it also can penetrate and destroy some of the resting structures, thereby reducing their inoculum potential in soil (1,7,22). Mycoparasitism in T. virens has been associated with its capacity to synthesize extracellular chitinase (2). In addition to its mycoparasitic character, T. virens is also a vigorous saprophyte that can be cultured on any one of a number of substrates and can maintain itself in the absence of the host. Concomitant with its mycoparasitic activities, T. virens also produces several potent epithiodiketopiperazine antibiotics. The antibiotic gliotoxin, (24) which is produced by “Q” strains of T. virens, has a wide spectrum of activity against bacteria, actinomycetes, and fungi. Gliotoxin has also been reported to act synergistically with chitinase in the antifungal activities of T. virens (3). The antibiotic gliovirin (16) produced by “P” strains of this fungus, although closely related to gliotoxin, has a much more restricted spectrum of activity, and it is not effective against bacteria, actinomycetes, or most fungi. It is, however, a potent inhibitor of oomycetes, such as Pythium and Phytophthora species. “Q” strains of T. virens do not produce gliovirin, and “P” strains do not produce gliotoxin (19). When either “P” or “Q” strains of T. virens are grown on substrates with high C/N ratios, they both produce the steroid-like compound viridiol. Viridiol has little or no antibiotic activity, but it is a potent phytotoxin when placed in contact with the roots of plants. With proper placement, i.e., mixed into surface soil, it can act as an effective herbicide for weeds, without harm to the crop plant that is planted at greater depth (17). It has recently been discovered that strains of T. virens produce a mixture of peptaibols, linear peptide antibiotics, but their role in biological control is as yet unknown (25). With antimicrobial mechanisms such as mycoparasitism and antibiotic production present, it would stand to reason that they play an important role in the biocontrol activities of this fungus. It was this hypothesis that guided most of our early research (1,7, 16,15,22–24,26). This, however, does not appear to be the case for cotton seedling diseases. When mutants of T. virens deficient for mycoparasitism, antibiotic production, or both were induced with UV light, they proved to be as biocontrol effective as the parent strains (8,18). In addition, T. virens strains grown on substrates that do not induce antibiotic production are just as effective as biocontrol agents of cotton seedling disease as those that are grown on substrates that do induce antibiotic production. If the mechanisms of mycoparasitism and antibiosis are not vital to biological control by T. virens, what mechanisms are? By culturing fungi from the roots of treated cotton plants taken at intervals from field plantings throughout the growing season, we discovered that T. virens could be recovered from surface-sterilized roots at any time. The fungus colonized the tap and secondary roots in the upper reaches of the soil. However, late in the season it was found mostly on the tap and primary roots (28). Because the roots were rigorously surface-sterilized, we surmised that the fungus had penetrated the roots. This hypothesis was later supported by colleagues in Israel working with T. harzianum. They demonstrated microscopically that the fungus penetrated the epidermis and grew into the outer layers of the root cortex where it induced defense responses in cucumber (27). We discovered that colonization of the cotton root by T. virens induced the synthesis of high levels of the terpenoid aldehydes hemigossypol (HG) and desoxyhemigossypol (dHG) that are intermediates in the pathway leading to synthesis of the dimer, gossypol. Bioassay of these compounds and gossypol against Rhizoctonia solani showed that both intermediates were strongly inhibitory to the pathogen, with dHG showing twice the toxicity of HG. Gossypol was only slightly inhibitory to R. solani. Bioassay of HG against T. virens and T. koningii showed that both fungi were resistant to the toxin (14). It was later learned that T. virens induced terpenoid synthesis in the cotton root by production of an 18-kDa protein that elicited both increased peroxidase activity and terpenoid concentrations in inoculated roots (5). Research has shown that there is a strong correlation between the Corresponding author: C. R. Howell; E-mail address: chowell@cpru.usda.gov

https://apsjournals.apsnet.org/doi/pdf/10.1094/PHYTO-96-0178

Understanding the Mechanisms Employed by Trichoderma virens to Effect Biological Control of Cotton Diseases.

A study of the characteristics of “P” and “Q” strains of Trichoderma virens to account for differences in biological control efficacy against cotton seedling diseases

L.S. Puckhaber

Papers

A study of the characteristics of “P” and “Q” strains of Trichoderma virens to account for differences in biological control efficacy against cotton seedling diseases