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

UNLABELLED: Leaf mold caused by the ascomycete fungus Cladosporium fulvum is a devastating disease of tomato plants. The mycoparasitic fungus Hansfordia pulvinata is an effective biocontrol agent that parasitizes C. fulvum hyphae on leaves and secretes 13-deoxyphomenone, an eremophilane-type sesquiterpene, which was also identified as a sporulation-inducing factor in Aspergillus oryzae. Here, we identified deoxyphomenone biosynthesis (DPH) gene clusters conserved in both H. pulvinata and Aspergillus section Flavi, including A. oryzae and A. flavus. Functional disruption of DPH1 orthologous genes encoding sesquiterpene cyclase in H. pulvinata, A. oryzae, and its close relative A. flavus revealed that deoxyphomenone in H. pulvinata had exogenic antifungal activity against C. fulvum and controlled endogenic sporulation in Aspergillus species. Complete DPH clusters, highly similar to those in H. pulvinata, were exclusive to Aspergillus section Flavi, while species in other Aspergillus sections contained fragmented DPH clusters. A comparative genomics analysis revealed that these DPH gene clusters share a common origin and are horizontally transferred from an ancestor of Aspergillus to H. pulvinata. Our results suggest that after horizontal transfer, H. pulvinata maintained the DPH cluster as the inhibitory effect of deoxyphomenone on spore germination and mycelial growth contributed to its mycoparasitism on the host fungus C. fulvum.

IMPORTANCE: Tomato leaf mold disease caused by C. fulvum poses a significant economic threat to tomato production globally. Breeders have developed tomato cultivars with Cf resistance genes. C. fulvum 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 H. pulvinata is crucial as an effective agent against C. fulvum. Clarifying the mechanism of mycoparasitism is significant, as it enhances its application as a biocontrol agent against plant pathogens. This study revealed how H. pulvinata produces deoxyphomenone, an antifungal compound, through horizontal gene transfer from Aspergillus 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.