Understanding countrywide pathogen population structure and inter‐epidemic region spread is crucial for deciphering crop potential losses. Wheat stripe rust caused by Puccinia striiformis f. sp. tritici is a destructive disease that affects worldwide wheat production, widespread in China, representing largest epidemic region globally. This study aimed to understand the population structure and migration route of P. striiformis f. sp. tritici across China based on sampling from 15 provinces representing six epidemic zones, viz., over‐summering, over‐wintering, eastern, Yun‐Gui, Xinjiang and Tibet epidemic regions. High genotypic diversity was recorded in over‐summering, Tibet and over‐wintering epidemic regions. Epidemic regions partly explain population subdivision with variable divergence (FST = 0.005–0.344). Xinjiang and Tibet epidemic regions were independent epidemic zones with least sharing of genotypes. Among other epidemic zones, i.e. over‐summering, over‐wintering, eastern and Yun‐Gui epidemic zones, re‐sampling MLGs, clustering‐based structure, DAPC analyses, relative migration and low divergence (FST from 0.006 to 0.073) revealed frequent geneflow. Yun‐Gui epidemic regions, with a potential for both over‐summering and over‐wintering, could play an important role in causing epidemics in main wheat‐cultivating areas of China. High diversity, recombination signatures and inter‐epidemic region migration patterns need to be considered in host‐resistant cultivar development in China and neighbouring countries, considering risk of long‐distance migration capacity of pathogen.

Wheat stripe rust, caused by Puccinia striiformis f. sp. tritici, is a destructive disease in many countries. In China, wheat stripe rust generally occurs in northwestern and southwestern China and sporadically in the Jiangsu and Zhejiang costal epidemiological region (JZER), where an outbreak of the disease occurred in 2019. To understand the population structure and potential inoculum sources of the pathogen in this region, 171 isolates collected from 93 wheat fields of 53 counties in 10 provinces were phenotyped with two sets of wheat differentials and genotyped with 20 pairs of SNP primers. Phenotype tests indicated that identical races (CYR34, CYR33, Su11-139, and Su11-14-1) detected in Jiangsu and Zhejiang were shared with the oversummering regions (Gansu), overwintering regions (Hubei, Henan, and Shaanxi), and Yun-Gui epidemiological regions (Yunnan and Guizhou). In ZJER, races CYR32, G22-14, G22-68 were detected in Jiangsu, but not in Zhejiang, and Su11-208 was identified in Zhejiang, but not in Jiangsu. Genotypic analysis revealed remarkable gene flows amongst the Jiangsu, Yunnan, Henan, and Anhui populations, as well as those of Zhejiang, Guizhou, and Sichuan, showing that wheat stripe rust in Zhejiang and Jiangsu was from spores migrated from different routes. Major gene flows were detected between the Jiangsu and Zhejiang populations. P. striiformis f. sp. tritici from both overwintering regions (Yunnan, Sichuan, Guizhou, Henan, Hubei, and Shaanxi) and oversummering regions (Gansu) contributed to the wheat stripe rust epidemic in the JZER region in 2019.

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To understand inheritance of the TSA-6 Puccinia striiformis f. sp. tritici isolate, virulent to Yr5, that was recently detected in China, we analyzed avirulence and virulence of 120 selfed progeny lines from Berberis shensiana. The results showed that the TSA-6 isolate is virulent against the Yr5 resistance gene, and overall progeny lines were categorized into 73 virulence phenotypes (VPs), and of these, 72 VPs differed from the isolate TSA-6, and only 1 VP including 3 progeny was identical to the parental isolate. The analyses indicated that the TSA-6 isolate is homozygous for avirulence at Yr10, Yr15 and Yr26 resistance loci, and virulence at YrA resistance locus. The TSA-6 isolate is heterozygous for avirulence at the Yr2, Yr3, Yr5, Yr7 and Yr8 resistance loci, which are controlled by a dominant/recessive relationship. The Yr1, Yr6, Yr9, Yr17, Yr27, Yr25, Yr28, Yr29, Yr32, YrTr1 and YrSP resistance loci are governed by two complementary dominant/recessive genes. Avirulence against heterozygous Yr4, Yr43，Yr44, Yr76 and YrExp2 resistance loci is regulated by a dominant and recessive, or a dominant and suppressor gene pairs. Totally, 117 multi-locus genotypes (MLGs) were detected at 24 KASP-SNP marker loci among the 120 progeny. Using these marker loci, we constructed a linkage map with a genetic distance interval spanning 624.5 cM. Quantitative trait loci (QTL) corresponding to phenotypic segregation for virulence at 20 Yr resistance loci in addition to the Yr1 resistance locus were identified. These results facilitate our understanding of Pst virulence evolution, and simplify breeding of wheat cultivars with effective resistance to wheat stripe rust.