Population Genomics of Macrophomina spp. Reveals Cryptic Host Specialization and Evidence for Meiotic Recombination

Abstract

Knowledge of the factors structuring populations of pathogenic fungi is fundamental to disease management efforts and basic biology. However, this crucial information is missing for many important pathogens, including broad host range and drought-associated pathogens from the globally distributed Macrophomina genus. The objectives of this work were to evaluate the evidence for host specialization, geographic adaptation, and recombination using a global survey of Macrophomina isolates from diverse geographic, temporal, and host sources. We obtained high-quality short-read sequence data for 463 Macrophomina spp. isolates, representing four putative species, collected from 91 host plant species and soil in 23 countries. Analysis of bi-allelic, single nucleotide polymorphismsrevealed high diversity, admixture, and equal mating type ratios suggesting on-going recombination. Although most tested isolates asymptomatically colonized strawberry, only strawberry-derived isolates caused disease on this host. These isolates were all in a single lineage, suggesting the ability to cause disease on strawberry is not widespread among M. phaseolina. Significant associations were also found between isolation from soybean plants and specific population clusters, suggesting that specialization for virulence or reproduction has also occurred for soybean. Geography ? isolate genotype associations were weak, suggesting Macrophomina spp. were frequently trafficked between regions. Reference free whole genome comparisons support current boundaries among four Macrophomina species, and new molecular markers were designed to specifically identify each species. Contrary to expectations, M. phaseolina should be considered a single species with both specialist and generalist populations in which meiosis can maintain genetic diversity.