Adaptive evolution of sesquiterpene deoxyphomenone in mycoparasitism by associated with horizontal gene transfer from species.

UNLABELLED

Leaf mold caused by the ascomycete fungus is a devastating disease of tomato plants. The mycoparasitic fungus is an effective biocontrol agent that parasitizes hyphae on leaves and secretes 13-deoxyphomenone, an eremophilane-type sesquiterpene, which was also identified as a sporulation-inducing factor in . Here, we identified deoxyphomenone biosynthesis () gene clusters conserved in both and section , including and . Functional disruption of orthologous genes encoding sesquiterpene cyclase in , , and its close relative revealed that deoxyphomenone in had exogenic antifungal activity against and controlled endogenic sporulation in species. Complete clusters, highly similar to those in , were exclusive to section , while species in other sections contained fragmented clusters. A comparative genomics analysis revealed that these gene clusters share a common origin and are horizontally transferred from an ancestor of to . Our results suggest that after horizontal transfer, maintained the cluster as the inhibitory effect of deoxyphomenone on spore germination and mycelial growth contributed to its mycoparasitism on the host fungus .

IMPORTANCE

Tomato leaf mold disease caused by poses a significant economic threat to tomato production globally. Breeders have developed tomato cultivars with resistance genes. frequently evolves new races that overcome these genetic defenses, complicating control efforts. Additionally, the pathogen has developed resistance to chemical fungicides, prompting the need for sustainable alternatives like biocontrol agents. The mycoparasitic fungus is crucial as an effective agent against . Clarifying the mechanism of mycoparasitism is significant, as it enhances its application as a biocontrol agent against plant pathogens. This study revealed how produces deoxyphomenone, an antifungal compound, through horizontal gene transfer from species. It is hypothesized that mycoparasitism could be one of the mechanisms that facilitated horizontal gene transfer between fungi. These insights facilitate the development of eco-friendly, sustainable agricultural practices by reducing dependence on chemical fungicides and promoting natural pathogen control methods.