Cryptic recombination and transposition drive structural variation to shape genomic plasticity and life history traits in a host generalist fungal plant pathogen

Abstract

Background:An understanding of plant pathogen evolution is important for sustainable management of crop diseases. Plant pathogen populations must maintain adequate heritable phenotypic variability to survive. Polymorphisms >= 50 bp, known as structural variants (SVs), could contribute strongly to this variability by disrupting gene activities. SV acquisition is largely driven by mobile genetic elements called transposons, though a less appreciated source of SVs is erroneous meiotic double-strand break repair. The relative impacts of transposons and recombination on SV diversity and the overall contribution of SVs to phenotypic variability is elusive, especially in host generalists.Results:We use 25 high quality genomes to create a graphical pan-genome of the globally distributed host-generalist crop pathogenSclerotinia sclerotiorum. Outcrossing and recombination rates in this self-fertile species have been debated. Using bisulfite sequencing, and short read data from 190 strains, we show thatS. sclerotiorumhas many hallmarks of eukaryotic meiosis, including recombination hot and cold spots, centromeric and genic recombination suppression, and rapid linkage disequilibrium decay. Using a new statistic that captures average pairwise structural variation, we show that recombination and transposons make distinct contributions to SV diversity. Furthermore, despite only 5 % of genes being dispensable, SVs often had a stronger impact than other variants across 14 life history traits measured in 103 distinct strains.Conclusion:Transposons and recombination make distinct contributions to SV diversity inS. sclerotiorum. Despite limited gene content diversity, SVs may strongly impact phenotypic variability. This sheds light on the genomic forces shaping adaptive flexibility in host generalists.