The emergence of bacterial blight pathogen followed the dispersal pattern of rice in Asia

Abstract

Crop domestication has a significant effect on the evolutionary trajectory of plant pathogens by providing new ecological niches and abundant resources. The domestication of Asian rice (Oryza sativa) in Asia, approximately 9,000 years ago, might have shaped the genetic makeup of associated microbes into modern threats. In this study, we provide insight into the evolutionary history and dispersal pattern of the rice bacterial blight (BB) pathogen, Xanthomonas oryzae pv. oryzae (Xoo), one of the most destructive rice pathogens in the last century. The analysis of 433 Asian Xoo (AXoo) genomes identified twelve modern populations derived from three ancestral lineages (AXooL). Each population emerged with a unique genetic composition including the combination of pathogenicity factors. Bayesian reconstruction suggests that Xoo lineages emerged alongside O. sativa domestication hotspots and followed the dispersal pattern of rice across the continent. An ancient Xoo lineage (AXooL1) emerged in China and was likely dispersed with japonica rice. A second lineage (AXooL2) which could have turned up from China and spread across India, then evolved due to the domestication and spread of indica rice, and later on expanded eastward of Asia.. We also showed that recombination played a significant role in the emergence of AXooL3, which appeared more recently and might have spread with the rice trading routes. Our study aligns the evolution and dissemination of the phylogroup AXoo with the history of O. sativa, offering valuable insights for the formulation of precise disease management strategies. AUTHOR SUMMARYRice domestication was a crucial step in the development of Asian civilization. However, this process also affected the evolution of an associated pathogen, leading to its emergence as a global threat. Rice bacterial blight (BB), caused by the pathogen Xanthomonas oryzae pv. oryzae (Xoo), has been a scourge in many Asian countries. Using population genomics, we explored the diversity and evolutionary history of Xoo in Asia (AXoo). Here we show that two ancestral pathogen lineages emerged in rice domestication centers (China and India) and dispersed with rice across the continent. More recently, recombination played a crucial role in the appearance of a third lineage that spread through trading activity. This study provides the implications of the adaptation of AXoo in Oryza sativa, and might be valuable in forecasting BB outbreaks.