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 chinensis is a solitary leaf-rolling weevil feeding on Japanese knotweed (Fallopia japonica). This pest has evolved a special proto-farming bipartite mutualism with the fungus Penicillium herquei, which provide nutrition and defensive protection for the E. chinensis larvae. Here, the genome of P. herquei was sequenced, and the structure and specific gene categories in the P. herquei genome were then comprehensively compared with the other two well-studied Penicillium species (P. decumbens and P. chrysogenum). The assembled P. herquei genome 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 the P. herquei genome. Comparative genomics demonstrate that the three Penicillium species show similar metabolic and enzymatic potential, however, P. herquei has 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 of P. herquei in E. chinensis mutualistic system. Large metabolic potential shared by Penicillium species at the genus level may explain why some Penicillium species are recruited by the Euops weevils as crop fungi.

Genomic Signatures of Domestication in a Fungus Obligately Farmed by Leafcutter Ants

“…This functional polyploidy combined with limited accuracy of existing genomes have precluded studies of changes in genome synteny as well as structural variation within haplotypes. For instance, the short-read L. gongylophorus genome of Aylward et al (2013) isolated from a Panamanian colony of Atta cephalotes provides the most current and best cited for genome for this fungal species (Floudas et al, 2015; Dentinger et al, 2016; Nygaard et al, 2016; Guo et al, 2023; Martiarena et al, 2023). While the Aylward et al (2013) genome was the state of the art at the time of its publication, it provides an incomplete and fragmented assembly that cannot delimit key features of genomic change.…”