Trichoderma atroviridefrom Predator to Prey: Role of the Mitogen-Activated Protein Kinase Tmk3 in Fungal Chemical Defense against Fungivory byDrosophila melanogasterLarvae

ABSTRACTThe response to injury represents an important strategy for animals and plants to survive mechanical damage and predation. Plants respond to injury by activating a defense response that includes the production of an important variety of compounds that help them withstand predator attack and recover from mechanical injury (MI). Similarly, the filamentous fungusTrichoderma atrovirideresponds to MI by strongly modifying its transcriptional profile and producing asexual reproduction structures (conidia). Here, we analyzed whether the response to MI inT. atrovirideis related to a possible predator defense mechanism from a metabolic perspective. We found that the production of specific groups of secondary metabolites increases in response to MI but is reduced after fungivory byDrosophila melanogasterlarvae. We further show that fungivory results in repression of the expression of genes putatively involved in the regulation of secondary metabolite production inT. atroviride. Activation of secondary metabolite production appears to depend on the mitogen-activated protein kinase (MAPK) Tmk3. Interestingly,D. melanogasterlarvae preferred to feed on atmk3gene replacement mutant rather than on the wild-type strain. Consumption of the mutant strain, however, resulted in increased larval mortality.IMPORTANCEFungi, like other organisms, have natural predators, including fungivorous nematodes and arthropods that use them as an important food source. Thus, they require mechanisms to detect and respond to injury.Trichoderma atrovirideresponds to mycelial injury by rapidly regenerating its hyphae and developing asexual reproduction structures. Whether this injury response is associated with attack by fungivorous insects is unknown. Therefore, determining the possible conservation of a defense mechanism to predation inT. atrovirideand plants and elucidating the mechanisms involved in the establishment of this response is of major interest. Here, we describe the chemical response ofT. atrovirideto mechanical injury and fungivory and the role of a MAPK pathway in the regulation of this response.