Plant recognition byTrichoderma harzianumelicits upregulation of a novel secondary metabolite cluster required for colonization

Abstract

AbstractTrichoderma harzianumis a filamentous ascomycete frequently applied as biocontrol agent in agriculture. While mycoparasitism and antagonism ofTrichodermaspp. against fungal pathogens are well known, early fungal responses to the presence of a plant await broader investigation. Analyzing early stages of plant-fungus communication we show thatT. harzianumB97 chemotropically responds to a plant extract and that both plant and fungus alter secondary metabolite secretion upon recognition. We developed a strategy for omics-analysis simulating conditions of early plant recognition eliciting a chemotropic response in the fungus and found 102 genes to be differentially regulated, including nitrate and nitrite reductases. Additionally, the previously uncharacterizedPlantCommunicationAssociated (PCA) gene cluster was strongly induced upon recognition of the plant, comprises a palindromic DNA motif and was essential for plant colonization. The PCA-cluster is only present in the Harzianum clade ofTrichodermaand closely related to a homologous cluster inMetarhiziumspp. Horizontal gene transfer (HGT) was detected for PCA-cluster genes by plants, while the cluster inT. harzianumis likely under balancing or positive selection.Hence, the PCA-cluster mediates early fungus-plant chemical communication and may be responsible for the high potential ofT. harzianumand closely related species for biocontrol applications.Plain language summaryInteractions of plants with fungi – beneficial or pathogenic – are crucial for the ecological function of both partners. Yet, the chemical “language” they use and how or when they use it is still insufficiently known. We describe discovery of a novel gene cluster, which is strongly induced upon plant recognition and essential for plant-fungal interkingdom interaction in the biocontrol-agentTrichoderma harzianum.