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

Trichoderma harzianum is a filamentous ascomycete frequently applied as biocontrol agent in agriculture. While mycoparasitism and antagonism of Trichoderma spp. 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 that T. harzianum B97 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 uncharacterized P lant C ommunication A ssociated (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 of Trichoderma and closely related to a homologous cluster in Metarhizium spp. Horizontal gene transfer (HGT) was detected for PCA-cluster genes by plants, while the cluster in T. harzianum is likely under balancing or positive selection. Hence, the PCA-cluster mediates early fungus-plant chemical communication and may be responsible for the high potential of T. harzianum and closely related species for biocontrol applications. Plain language summary Interactions 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-agent Trichoderma harzianum .