Polygenic strategies for host-specific and general virulence of Botrytis cinerea across diverse eudicot hosts

Abstract

Diverse qualitative and quantitative genetic architectures can successfully enable 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 lesion area of Botrytis cinerea across 8 hosts. This revealed that it was possible to partition the virulence, as defined by the lesion area, common across all hosts from host-specific virulence. All traits showed that a large proportion of the Botrytis genome likely contributes to fungal lesion development on leaves 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 growing on diverse hosts, with most genes influencing relatively few hosts. When pathogen genes were associated with multiple hosts, they were associated with unrelated rather than related host species. Comparative genomics further suggested that the GWAS-identified genes are largely syntenic with other specialist Botrytis species and not unique to B. cinerea. Overall, as shown in Arabidopsis thaliana, B. cinerea’s 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.