Population Genomics of Pseudocercospora griseola Reveals New Groups in the Middle American Clade and the Presence of the Endophytic Bacterium Achromobacter xylosoxidans

Angular leaf spot, caused by Pseudocercospora griseola, is an important disease of common beans. The pathogen, P. griseola, is highly variable and has co-evolved with its host. In this study, 48 isolates of P. griseola from Puerto Rico, Guatemala, Honduras, and Tanzania were sequenced via 3RADseq, resulting in the de novo assembly of 42,214 contigs. Phylogenomic, population genetic structure, and principal component analyses using 1,260 single-nucleotide polymorphisms (SNPs) divided these isolates into two populations, Andean and Middle American, and the Middle American population was further divided into three subpopulations. There were moderate to high levels of differentiation between P. griseola populations, with pairwise fixation index (FST) values ranging from 0.11 to 0.95. The Andean population was composed of isolates from Tanzania and was separated from the Middle American population (FST = 0.95). The Middle American population was separated into three subpopulations including isolates from (i) Guatemala and Honduras, (ii) Tanzania, and (iii) Puerto Rico. Pathogenicity testing of 27 isolates from Puerto Rico, using 12 common bean differential lines, identified 10 races, but these races were not associated with SNPs found in virulence genes. DNA of an endophytic bacterium (Achromobacter xylosoxidans) was found in seven mildly virulent isolates, suggesting a possible role of the bacterium in the observed virulence patterns. To understand the evolution and diversity of P. griseola, further study of the virulence genes and the interactions among the endophytic bacterium, the fungus, and the host plant is required. Such information is critical to inform breeding strategies for the development of resistant germplasm and cultivars.