Adaptive evolution of sesquiterpene deoxyphomenone in mycoparasitism byHansfordia pulvinataassociated with horizontal gene transfer fromAspergillusspecies

Abstract

AbstractLeaf mold caused by the ascomycete fungusCladosporium fulvumis a devastating disease of tomato plants. The mycoparasitic fungusHansfordia pulvinatais an effective biocontrol agent that parasitizesC. fulvumhyphae on leaves and secretes 13-deoxyphomenone, an eremophilane-type sesquiterpene, which was also identified as a sporulation-inducing factor inAspergillus oryzae. Here, we identified deoxyphomenone biosynthesis (DPH) gene clusters conserved in bothH. pulvinataandAspergillussectionFlaviincludingA. oryzaeandA. flavus. Functional disruption ofDPH1orthologous genes encoding sesquiterpene cyclase inH. pulvinata,A. oryzaeand its close relativeA. flavusrevealed that deoxyphomenone inH. pulvinatahad exogenic antifungal activity against the host fungusC. fulvumand controlled endogenic sporulation inAspergillusspecies. Deoxyphomenone also inhibited mycelial growth ofC. fulvumand the non-host tomato pathogenPseudocercospora fuligena. CompleteDPHclusters, highly similar to those inH. pulvinata, were exclusive toAspergillussectionFlavi, while species in otherAspergillussections contained fragmentedDPHclusters. A comparative genomics analysis revealed that theseDPHgene clusters share a common origin and are horizontally transferred across large taxonomic distances from an ancestor ofAspergillustoH. pulvinata. Our results suggest that, after horizontal transfer,H. pulvinatamaintained theDPHcluster as the inhibitory effect of deoxyphomenone on spore germination and mycelial growth contributed to its mycoparasitism on the host fungusC. fulvum.