Genome analysis and genomic comparison of a fungal cultivar of the nonsocial weevil Euops chinensis reveals its plant decomposition and protective roles in fungus-farming mutualism

Abstract

Fungus-farming mutualisms are models for studying co-evolutionary among species. Compared to well-documented fungus-farming in social insects, the molecular aspects of fungus-farming mutualisms in nonsocial insects have been poorly explored.Euops chinensisis a solitary leaf-rolling weevil feeding on Japanese knotweed (Fallopia japonica). This pest has evolved a special proto-farming bipartite mutualism with the fungusPenicillium herquei, which provide nutrition and defensive protection for theE. chinensislarvae. Here, the genome ofP. herqueiwas sequenced, and the structure and specific gene categories in theP. herqueigenome were then comprehensively compared with the other two well-studiedPenicilliumspecies (P. decumbensandP. chrysogenum). The assembledP. herqueigenome had a 40.25  Mb genome size with 46.7% GC content. A diverse set of genes associating with carbohydrate-active enzymes, cellulose and hemicellulose degradation, transporter, and terpenoid biosynthesis were detected in theP. herqueigenome. Comparative genomics demonstrate that the threePenicilliumspecies show similar metabolic and enzymatic potential, however,P. herqueihas more genes associated with plant biomass degradation and defense but less genes associating with virulence pathogenicity. Our results provide molecular evidence for plant substrate breakdown and protective roles ofP. herqueiinE. chinensismutualistic system. Large metabolic potential shared byPenicilliumspecies at the genus level may explain why somePenicilliumspecies are recruited by theEuopsweevils as crop fungi.