The polygenic strategies of Botrytis cinerea for virulence across eight eudicot host species

Abstract

Diverse qualitative and quantitative genetic architectures can successfully influence fungal virulence and host range. To model the quantitative genetic architecture of a generalist pathogen with an extensive host range, we conducted a genome-wide association study (GWAS) of the virulence of Botrytis cinerea across eight hosts. This approach revealed 4772 candidate genes, about one-third of the Botrytis genome, contributing to virulence with small effect sizes. The candidate genes are evenly spread across the core chromosomes with no indication of bipartite genomic architecture. The GWAS-identified polymorphisms and genes show that B. cinerea relies on genetic variants across hundreds of genes for infecting diverse hosts, with most genes influencing relatively few hosts. When pathogen genes associated to multiple hosts, they typically influenced more unrelated than related host species. Comparative genomics further suggested that the GWAS-identified genes are largely syntenic with other specialist Botrytis species and not novel to B. cinerea. Overall, B. cinereas generalist behavior is derived from the sum of the genome-wide genetic variation acting within gene networks that differentially coordinate the interaction with diverse hosts.