Population genomic analyses reveal extensive genomic regions within selective sweeps associated with adaptation and demographic history of a wheat fungal pathogen

Authors: XING, YUN - Institute Of Plant Protection - China; XIA, CHONGJING - Institute Of Plant Protection - China; HUANG, LIANG - Institute Of Plant Protection - China; ZHAO, NA - Institute Of Plant Protection - China; LI, HONGFU - Institute Of Plant Protection - China; ZHANG, XINGZHONG - Institute Of Plant Protection - China; QIU, AGE - Institute Of Plant Protection - China; TANG, WANGQIANG - Institute Of Plant Protection - China; WANG, MAINAN - Washington State University; Chen, Xianming; LIU, BO - Institute Of Plant Protection - China; ZHANG, HAO - Institute Of Plant Protection - China; GAO, LI - Institute Of Plant Protection - China; CHEN, WANQUAN - Institute Of Plant Protection - China; LIU, TAIGUO - Institute Of Plant Protection - China

Submitted to: Meeting Abstract
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/9/2023
Publication Date: N/A
Citation: N/A

Interpretive Summary: Plant pathogens can quickly evolve in response to the changing host and environment, resulting in destructive epidemics. The stripe rust fungus, causing wheat stripe rust disease worldwide, is one such pathogen. In the arms race between pathogens and hosts, changes in host populations exerted continuous selective forces on the dynamics of pathogens. However, the footprints of these selection forces and the demography of the wheat stripe rust pathogen remain poorly explored, limited our understanding of the evolutionary processes that shape the spread and evolution of pathogens. In this study, we revealed several features of worldwide stripe rust populations through population genomic analyses. There might be limited gene flow between the populations from China and other countries. A slower rate of linkage disequilibrium decay was detected comparing to other rust fungi with known sexual reproduction. Furthermore, we detected extensive hard and soft sweeps associated with the stripe rust pathogen adaptation. Genes within the selective sweeps were enriched in secreted proteins and effectors and showed functions related to pathogenicity or virulence, temperature tolerance, and fungicide resistance implying that the stripe rust populations suffered positive selection pressures from host and abiotic factors. Moreover, demographic history indicated the stripe rust pathogen populations experienced strong bottlenecks at the beginning of the wheat domestication around 10,000 years ago and during modern agriculture around 100 years ago, suggesting that the crop domestication and breeding programs could continuously contribute to the decline of pathogen effective population sizes. Our results provided insights into the evolution of the stripe rust pathogen genome and highlighted the role of modern agriculture on pathogen demography.

Technical Abstract: Plant pathogens can quickly evolve in response to the changing host and environment, resulting in destructive epidemics. The fungus Puccinia striiformis f. sp. tritici (Pst), causing wheat stripe rust disease worldwide, is one such pathogen. In the arms race between pathogens and hosts, changes in host populations exerted continuous selective forces on the dynamics of pathogens. However, the footprints of these selection forces and the demography of Pst remain poorly explored, limited our understanding of the evolutionary processes that shape the spread and evolution of pathogens. In this study, we revealed several features of worldwide Pst populations through population genomic analyses. There might be limited gene flow between Pst populations from China and other countries. A slower rate of linkage disequilibrium decay was detected comparing to rust fungi with known sexual reproduction. Furthermore, we detected extensive hard and soft sweeps associated with Pst adaptation. Genes within the selective sweeps were enriched in secreted proteins and effectors and showed functions related to pathogenicity or virulence, temperature tolerance, and fungicide resistance implying that Chinese Pst populations suffered positive selection pressures from host and abiotic factors. Moreover, demographic history indicated Pst populations experienced strong bottlenecks at the beginning of the wheat domestication around 10,000 years ago and during modern agriculture around 100 years ago, suggesting that the crop domestication and breeding programs could continuously contribute to the decline of pathogen effective population sizes. Our results provided insights into the evolution of the Pst genome and highlighted the role of modern agriculture on pathogen demography.