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

Zhiwei Song; Jinshui Zheng; Yancun Zhao; Jiakang Yin; Dehong Zheng; Huifeng Hu; Hongxia Liu; Ming Sun; Lifang Ruan; Fengquan Liu

doi:10.3389/fcimb.2023.1183416

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

Front Cell Infect Microbiol. 2023 May 26:13:1183416. doi: 10.3389/fcimb.2023.1183416. eCollection 2023.

Authors

Zhiwei Song¹, Jinshui Zheng^{2

3}, Yancun Zhao¹, Jiakang Yin^{2

3}, Dehong Zheng^{2

3}, Huifeng Hu^{2

3}, Hongxia Liu⁴, Ming Sun^{2

3}, Lifang Ruan^{2

3}, Fengquan Liu¹

Affiliations

¹ Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, China.
² State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China.
³ Hubei Key Laboratory of Agricultural Bioinformatics, Huazhong Agricultural University, Wuhan, China.
⁴ Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Nanjing, China.

Abstract

The Xanthomonas oryzae pv. oryzae (Xoo) is a bacterial pathogen causing bacterial blight disease in rice, resulting in significant yield reductions of up to 50% in rice production. Despite its serious threat to food production globally, knowledge of its population structure and virulence evolution is relatively limited. In this study, we employed whole-genome sequencing to explore the diversity and evolution of Xoo in the main rice-growing areas of China over the past 30 years. Using phylogenomic analysis, we revealed six lineages. CX-1 and CX-2 primarily contained Xoo isolates from South China, while CX-3 represented Xoo isolates from North China. Xoo isolates belonging to CX-5 and CX-6 were the most prevalent across all studied areas, persisting as dominant lineages for several decades. Recent sporadic disease outbreaks were primarily caused by Xoo isolates derived from the two major lineages, CX-5 and CX-6, although Xoo isolates from other lineages also contributed to these outbreaks. The lineage and sub-lineage distributions of Xoo isolates were strongly correlated with their geographical origin, which was found to be mainly determined by the planting of the two major rice subspecies, indica and japonica. Moreover, large-scale virulence testing was conducted to evaluate the diversity of pathogenicity for Xoo. We found rapid virulence evolution against rice, and its determinant factors included the genetic background of Xoo, rice resistance genes, and planting environment of rice. This study provides an excellent model for understanding the evolution and dynamics of plant pathogens in the context of their interactions with their hosts, which are shaped by a combination of geographical conditions and farming practices. The findings of this study may have important implications for the development of effective strategies for disease management and crop protection in rice production systems.

Keywords: Xanthomonas oryzae pv. oryzae; genomic epidemiology; large-scale virulence test; plant pathogen; rapid virulence dynamics.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Agriculture
China
Disease Management
Metagenomics
Oryza*

Grants and funding

This work was supported by National Key Research and Development Program of China (2017YFD0201100), National Natural Science Foundation of China (NSFC) (32072379, 31770003, 31571974 and 31801697), Fundamental Research Funds for the Central University (2662018JC015 and 2662016QD039), Science and Technology Department of Hubei Province (2017CFB438) and Special Fund for Agro-scientific Research in the Public Interest (201303015).