Population genomic and evolution of Xanthomonas oryzae pv. oryzae in the Philippines

The impact of modern agriculture on the evolutionary trajectory of plant pathogens is a central question for the sustainability of our crops. The Green Revolution replaced traditional rice landraces with high-yielding varieties creating a uniform selection pressure that allow measuring that effect. In this study, we analyzed a unique historical record to assess the impact of a major resistance gene, Xa4, in the population structure of Xanthomonas oryzae pv. oryzae (Xoo) collected in the Philippine archipelago during 40 years. After deployment in the early 1960’s, emerging of virulent pathogen groups were associated with increasing adoption of rice varieties caring Xa4, which reached 80% of the total planted area. Whole genomes analysis of a representative sample suggested six major groups with distinctive signatures of selection in genes related to secretion system, cell-wall degradation, lipopolysaccharide production, and detoxification of host defense components. Association genetics also suggested that each population might evolve different mechanisms to adapt to Xa4. Interestingly, we found evidence of strong selective sweep affecting several populations in the mid-1980’s, suggesting a major bottleneck that coincides with the pick of Xa4 deployment in the archipelago. Our study highlights how modern agricultural practices facilitate the adaptations of pathogens to overcome our standard crop improvement efforts.