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Mycoparasitism is considered a major contributor to fungus-fungus antagonism. The necrotrophs, primarily Trichoderma species, have a wider host range and less-specific mode of action, and perhaps for this reason more field and greenhouse trials have made use of these. Trichoderma species are focused in this chapter, because they have been the focus of the most work at the molecular and cellular levels. The interaction of Trichoderma with soilborne pathogenic fungi is an excellent example of necrotrophic mycoparasitism. Drastic reduction of intracellular cyclic AMP (cAMP) by knockout of adenylate cyclase leads to slow growth and loss of mycoparasitism in T. virens. In T. atroviride, mutants in the ortholog of the same mitogen-activated protein kinase (MAPK) gene, tmk1, showed increased coiling but reduced mycoparasitism in confrontation assays. A potentiation in the gene expression enables Trichoderma-treated plants to be more resistant to subsequent pathogen infection. Chytrids parasitizing vesicular arbuscular mycorrhizae were found in the fossil record of the Rhynie Chert, dating to more than 400 million years ago. There are theories that mycorrhizae themselves might have evolved from biotrophic fungal parasites of plants. Major features such as detection of the host, signal transduction, altered transcriptional patterns, and secretion of enzymes are likely to be shared, and this has provided working hypotheses to guide studies of mycoparasitism. Molecular mechanisms and genes manipulated to optimize biocontrol will be different for each type of interaction and for each niche within the complex web of fungus-fungus and fungus-root interactions.
Basic mechanisms of antagonistic fungus-fungus interactions. (A) Antibiosis: culture filtrate from Trichoderma inhibits germination of Botrytis conidia. Shown are culture filtrates from Trichoderma grown on 2% glucose (left) and on 0.5% colloidal chitin (right). Growth of Trichoderma on chitin induces production of soluble antagonistic factors, which could be enzymes or small metabolites. (Reprinted from Viterbo et al., 2001 , with permission of Blackwell Publishing Ltd.) (B) Necrotrophic mycoparasitic interactions: coiling of the mycoparasite around the host, shown here, is followed by destruction of the host. Upper panel, Trichoderma asperellum on R. solani (from Harman et al., 2004 ); lower panel, P. oligandrum hyphae interacting with F. oxysporum f. sp. radicislycopersici. (Reprinted with permission from Benhamou et al., 1997. ) (C) Parasitism of sclerotia: an important interaction for biocontrol of soilborne disease. Upper four panels, SEM images (reprinted from Mukherjee et al., 1995b, with permission of Blackwell Publishing Ltd.). Lower two panels, fluorescence of GFP-expressing Trichoderma mycelia; fluorescent mycelia are indicated by arrows (reprinted from Sarrocco et al., 2006 , with permission from Elsevier). (D) A biotrophic interaction: the parasite forms haustoria within the host cells, as in biotrophic fungus-plant interactions ( Van Den Boogert and Deacon, 1994 ). Image reprinted from Deacon (2005 ) (Fig. 12-1), courtesy of Jim Deacon, The University of Edinburgh.
Interactions with plant roots. (A) Left, interaction between T. asperellum (hypha indicated in SEM image by the arrow) and cucumber root. (Reprinted with permission from Yedidia et al., 2000 .) Right, interaction between tomato root and T. harzianum expressing GFP (fluorescent hyphae indicated by arrow). (Reprinted with permission from Chacon et al., 2007 .) (B) Consequence of Trichoderma-root interactions: induction of systemic resistance in the plant. Bioassay for induced resistance in maize seedlings against Colletotrichum graminicola. Left, symptoms on leaves of maize seedlings grown from untreated (NT) seeds, or seed treated with knockout strains (KO25 and KO46), wild-type strain (WT), or overexpression strains (OE38 and OE39) of T. virens. Lesions (indicated, for example, by black arrows in left-most leaf photo) appear dark in this grayscale image; see Djonovic et al. (2007 ) for original color image from which this figure was reprinted with permission. The gene disrupted or overexpressed in these T. virens strains encodes the secreted elicitor protein Sm1. Right, quantitative analysis of lesion size for the experiment shown in the left panel; different letters indicate significant differences ( Djonovic et al., 2007 ).
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