Population genomics and pathotypic evaluation of the bacterial leaf blight pathogen of rice reveals rapid evolutionary dynamics of a plant pathogen

Abstract

Xanthomonas oryzae pv. oryzae (Xoo) causes bacterial blight disease, which reduces crop yield by up to 50% in rice production. Despite its substantial threat on food production worldwide, knowledge about its population structure, virulence diversity and the relationship between them is limited. We used whole-genome sequencing to explore the diversity and evolution of Xoo during the past 30 years in the main rice-planting areas of China. Six separate lineages were revealed by phylogenomic analysis, with CX-5 and CX-6 predominating in the population for decades. The recent sporadic outbreaks were respectively caused by Xoo derived from these lineages especially the two major ones. The lineage and sub-lineage distribution of isolates strongly correlated to their geographical origin, which was found to be mainly determined by the planting of the two major rice subspecies, indica and japonica. Large-scale virulence testing was conducted to evaluate the diversity of pathogenicity for Xoo. We found rapid virulence dynamics against rice, and its determinant factors including genetic background of Xoo, rice resistance genes and the planting environment of rice. Genetic background was investigated deeply by comparative genomics, which indicates that transposition events contributing the most to evolution of the Xoo genome and the rapid diversification of virulence. This study provided a good model to understand the evolution and dynamics of plant pathogens in the context of interaction with their hosts which are influenced by both geographical conditions and farming practices.