Hiding in plain sight: Genome-wide recombination and a dynamic accessory genome drive diversity in Fusarium oxysporum f.sp. ciceris

Understanding the origins of variation in agricultural pathogens is of fundamental interest and practical importance, especially for diseases that threaten food security. Fusarium oxysporum is among the most important of soil -borne pathogens, with a global distribution and an extensive host range. The pathogen is considered to be asexual, with horizontal transfer of chromosomes providing an analog of assortment by meiotic recombination. Here, we challenge those assumptions based on the results of popula-tion genomic analyses, describing the pathogen's diversity and inferring its origins and functional consequences in the context of a single, long-standing agricultural system. We identify simultaneously low nucleotide distance among strains, and unexpectedly high levels of genetic and genomic variability. We determine that these features arise from a combination of genome- scale recombination, best explained by widespread sexual repro-duction, and presence-absence variation consistent with chromosomal rearrangement. Pangenome analyses document an accessory genome more than twice the size of the core genome, with contrasting evolutionary dynamics. The core genome is stable, with low diversity and high genetic differentiation across geographic space, while the accessory genome is paradoxically more diverse and unstable but with lower genetic differentiation and hallmarks of contemporary gene flow at local scales. We suggest a model in which episodic sexual reproduction generates haplotypes that are selected and then maintained through clone -like dynamics, followed by contemporary genomic rearrangements that reassort the accessory genome among sympatric strains. Taken together, these processes contribute unique genome content, including reassortment of virulence determinants that may explain observed variation in pathogenic potential.SignificanceFusarium oxysporum is among the most damaging of agricultural pathogens, capable of inflicting immense loss in a variety of crop species. Prevailing thought is that the organism is an exclusively asexual taxon, a notion that colors how one approaches disease control. Here, we reveal the genomic imprint of an active sexual cycle in fungal populations on chickpea. We propose that meiotic recombination generates haplotype diversity that is maintained by clonal dynamics, including restricted recombination within groups. Interestingly, these near-clonal groups derive further variation through geographically structured variation in a large accessory genome. These observations have implications for disease management and forecasting of pathogenic forms, not only in chickpea, but in all crop species impacted by the globally distributed F. oxysporum pathogen.