Revealing inheritance of a Xinjiang isolate BGTB-1 of Puccinia striiformis f. sp. tritici and the shift of pathogenicity from avirulence to virulence at heterozygous AvrYr5 locus

doi:10.1016/j.jia.2024.04.023

Journal of Integrative Agriculture

2026, Vol. 25

Issue (2): 744-755 DOI: 10.1016/j.jia.2024.04.023

Plant Protection

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Revealing inheritance of a Xinjiang isolate BGTB-1 of Puccinia striiformis f. sp. tritici and the shift of pathogenicity from avirulence to virulence at heterozygous AvrYr5 locus

Lin Wang, Fei Liu, Yumeng Bian, Mudi Sun, Zhensheng Kang^#, JieZhao^#

State Key Laboratory of Crop Stress Resistance and High-Efficiency Production, College of Plant Protection, Northwest A&F University, Yangling 712100, China

Highlights
● Revealing complex genetic characteristic and high genetic variation of Puccinia striiformis f. sp. tritici in relatively isolated stripe rust in Xinjiang by a selfed population of a representative isolate.
● Direct evidence showing the discovery of virulent sexual progenies originated from the avirulent parental isolate at Yr5 locus via sexual reproduction under the background of the current absence of Yr5-virulent isolates in Xinjiang.
● Sexual reproduction accounts for the origin of new strains and evolution of P. striiformis f. sp. tritici in Xinjiang.

Abstract
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摘要

新疆是中国相对独立的小麦条锈病流行区，新疆的条锈菌群体与其它内陆流行区的条锈菌群体存在巨大的遗传差异。新疆的小麦条锈菌小种通常进化慢于内陆群体。近年来，一些发现新小种，因此，深入了解新疆条锈菌群体毒性进化是十分必要的。本研究通过对新疆小麦条锈菌菌系BGTB-1在转主寄主堆花小檗（Berberis aggregata）进行有性生殖获得65个自交后代群体，在25个Yr单基因系进行表型鉴定，利用19个KASP-SNP引物进行基因型测定。结果表明65个自交后代产生了56个不同毒性表型（virulence patterns, VPs）, 没有一个后代的毒性与亲本菌系是相同的，表现出100%的毒性变异率。与亲本菌系相比，39（60.0%）个自交后代表现毒性增强，18个（27.7%）显示毒性降低。所有的后代在Yr10, Yr15, Yr32和YrTr1 四个抗病位点表现无毒性，在其余21个Yr抗病位点表现无毒性/有毒性分离。Yr5, Yr7和 Yr76（A:V≈3:1）位点的无毒性由一个显性基因控制，Yr6, Yr25和Yr44 （A:V≈1:3）位点的无毒性由一个隐性基因控制。所有后代在其余的15个位点包括Yr1, Yr2, Yr3, Yr4, Yr8, Yr9, Yr17, Yr26 (=Yr24), Yr28, Yr29, Yr43, YrSp, Yr27, YrA和YrExp2表现出不同的无毒性/毒性分离比，推断由现从个基因通过不同的作用方式控制其无毒性，表明亲本菌系复杂的遗传规律。分子标记检测表明所有的65个后代表现出不同的基因型，基于此构建了一个遗传距离为441.0 cM的连锁遗传图谱。有趣的是，本研究发现虽然亲本菌系对Yr5无毒性，但是后代中有17个对基因表现有毒性，表现出在该抗病位点从无毒到有毒性的致病性变化，这是首次报道对Yr5无毒的亲本菌系通过有性生殖产生对该位点有毒性的后代。本研究为深入了解新疆小麦条锈菌的遗传特征、有性生殖与毒性变异提供了科学依据，也为理解该地区条锈菌的毒性进化与阐释条锈菌新疆群体与内陆群体的遗传差异提供了理论基础。此外，需进一步研究明确自然条件下新疆有性生殖发生在新小种产生中的作用，以及对群体遗传多样性的影响。

Abstract

In China, Xinjiang is a relatively independent epidemic region of wheat stripe rust, caused by Puccinia striiformis f. sp. tritici, due to great population genetic divergence of Xinjiang with other inland epidemic regions. In this region, race evolution was usually slower than inland populations. However, many new races have recently been found, and therefore, it is necessary for more understanding of the virulence evolution of the Xinjiang population. So, in this study, a 65 sexual progenies, derived from a Xinjiang single-urediospore isolate BGTB-1 of P. striiformis f. sp. tritici by selfing on alternate host barberry (Berberis aggregata). It was phenotyped on the 25 single Yr lines, and genotyped by 19 kompetitive allele-specific PCR-single nucleotide polymorphism (KASP-SNP) markers. As a result, the 65 progenies were identified as 56 various virulence patterns (VPs), and neither of which was identical to the parental isolate, showed 100% virulence variation. Compared with the parental isolate, of all progenies, 39 (60.0%) had increased virulence, and 18 (27.7%) had decreased virulence. All progenies exhibited avirulence to Yr10, Yr15, Yr32, and YrTr1 loci, and avirulence and virulence segregation at the remaining 21 Yr resistance loci. The results showed avirulence to Yr5, Yr7, and Yr76 (A:V≈3:1) loci is controlled by a single dominant gene, and that to Yr6, Yr25, and Yr44 (A:V≈1:3) loci by a single recessive gene. However, avirulence to the remaining 15 resistant loci including Yr1, Yr2, Yr3, Yr4, Yr8, Yr9, Yr17, Yr26 (=Yr24), Yr28, Yr29, Yr43, YrSP, Yr27, YrA, and YrExp2, with various avirulence and virulence segregation ratios, is controlled by two genes with different gene effects, indicating complex genetic traits of the parental isolate. Totally, 65 dissimilar genotypes detected among progenies using overall molecular markers, by which a linkage map was constructed, with a genetic distance of 441.0 cM. Interestingly, although the parental isolate was avirulent to Yr5, but 17 progenies showed virulence, showing the change of pathogenicity from avirulence to virulence at this resistance locus. It was for the first time to report that progenies with virulence to Yr5 produced sexually from avirulent parental isolate at this resistance locus. To our knowledge, this study offers an insight into inheritance, sexual reproduction and virulence variation of P. striiformis f. sp. tritici in Xinjiang, facilitating us to understand evolution of the rust pathogen in this region and accounting for Xinjiang population distinguished form other inland populations. Additionally, it is necessary to further confirm the roles of sexual reproduction in the emergence of new races and affecting population genetic diversity of P. striiformis f. sp. tritici under natural conditions in Xinjiang.

Keywords: wheat yellow rust Puccinia striiformis f. sp tritici sexual reproduction virulence variation new race SNP Yr5 Xinjiang

Received: 06 January 2024 Accepted: 13 March 2024 Online: 13 April 2024

Fund: This work was financially supported by Xinjiang Major Science and Technology Projects, China (2023A02009).

About author: Lin Wang, E-mail: 1183660283@qq.com; #Correspondence Jie Zhao, E-mail: jiezhao@nwafu.edu.cn; Zhensheng Kang, E-mail: kangzs@nwafu.edu.cn

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