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 population 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 reproduction, 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.

Classical approaches to plant disease diagnosis assume a single pathogen/single disease paradigm. Here, we revisit the presumed role of Fusarium oxysporum as the causal agent of wilting and yellowing of chickpea plants on smallholder farms in Ethiopia. Contrary to expectations, detection of Fusarium DNA using conserved PCR primers failed to associate the pathogen with symptomatic plants. Instead, culture-independent sequencing of microbial communities nominated unexpected pathogens and revealed patchiness in the assembly of common microbial consortia. Surprisingly, tests of differential enrichment identified Phytophthora as the most common disease-associated taxon. More generally, across all field sites, multilevel pattern analysis identified indicator taxa whose patterns of co-occurrence demarcate discrete microbial communities and are consistent with a range of specific interactions, including mutualism and antagonism. Taken together, these data indicate that soilborne chickpea disease in Ethiopia has heterogeneous origins and that despite decades of emphasis and disease resistance breeding, the role of Fusarium as the frequent agent of chickpea disease in Ethiopia remains enigmatic.