Genetic and wind field analysis of wheat leaf rust (Puccinia triticina) dispersal: From winter sources in Gansu and Shaanxi to summer epidemics in China

Hongfu Li^1,2Na Zhao^1,2Qinqin Zhang^1,2Liang Huang^1,2Hao Zhang^1,2Li Gao^1,2Wanquan Chen¹Tai-Guo Liu^1,2,3*

• ¹State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection (CAAS), Beijing, Beijing Municipality, China
• ²National Agricultural Experimental Station for Plant Protection, Gangu, Ministry of Agriculture and Rural Affairs, Gansu, China
• ³Control of Biological Hazard Factors (Plant Origin) for Agri-product Quality and Safety, Ministry of Agriculture and Rural Affairs, Beijing, China

Wheat leaf rust caused by Puccinia triticina (Pt) is one of the most serious diseases affecting wheat worldwide. Given that China is the world's largest wheat-producing country, there is a lack of comprehensive understanding regarding the temporal and spatial dynamics of wheat leaf rust epidemics. This study investigated the population structure of Pt across different wheat leaf rust epidemic seasons in Gansu and Shaanxi provinces. Samples were collected in 2020 winter from Gansu and Shaanxi, and during 2021 spring and summer from eight additional provinces: Shandong, Henan, Gansu, Shaanxi, Hubei, Yunnan, Guizhou, and Xinjiang. Population genetics analysis was conducted using 12 pairs of SSR markers. The results indicated that the genetic diversity of the samples was highest in Shandong (SD), Shaanxi in 2020 winter (SN_20w), and Shaanxi in 2021 summer (SN_21s), while Xinjiang (XJ) exhibited the lowest genetic diversity. Population structure analysis revealed six distinct genetic backgrounds across the 10 populations, with SN_20w and XJ showing greater genetic distances compared to other populations. There was less genetic differentiation and strong gene flow between pairwise populations of Henan (HA) and SN_21s, SD and Gansu in winter 2020 (GS_20w), Gansu in summer 2021 (GS_21s) and Hubei (HB), and GS_20w and HB, with 6 shared multi-locus genotypes detected among 4 pairwise populations. Integrating population genetic analysis, horizontal wind field analysis, topographic analysis, and the sampling timeline, this study concluded that the winter populations of Pt in the Guanzhong region experienced dominance shifts, with limited impact on the wheat leaf rust epidemic of 2021. In the 2021 epidemic season, two pathways of pathogen dispersal were proposed: (1) According Guanzhong basin to Henan province. (2) Through Hanshui River Valley to Hubei province. These findings provide valuable insights into the spatial dynamics of wheat leaf rust and inform targeted prevention and control strategies.