Molecular Evidence of the West-to-East Dispersal of Puccinia striiformis f. sp. tritici in Central Shaanxi and the Migration of the Inoculum from Gansu

doi:10.1016/j.jia.2023.10.026

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Molecular Evidence of the West-to-East Dispersal of Puccinia striiformis f. sp. tritici in Central Shaanxi and the Migration of the Inoculum from Gansu

LIU Wei^1*, HUANG Xue-ling^2*, JU Meng¹, SUN Mu-di¹, DU Zhi-min¹, KANG Zhen-sheng^1#, ZHAO Jie^1#

¹State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University, Yangling 712100, P. R. China

²State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A＆F University, Yangling 712100, P. R. China

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摘要

小麦条锈菌，即条形柄锈菌小麦转化型（Puccinia striiformis West. f. sp. tritici Erikss. & Henn.），是危害小麦及部分禾本科作物的重要真菌。小麦条锈菌的夏孢子可以依靠气流远距离传播，使病原菌可以跨区传播扩散。早期研究通过小麦条锈病的田间发生时序，推测小麦条锈菌可能在陕西关中地区由西向东传播，且陕西关中地区菌源可能来自邻近省份甘肃省，但是一直没有直接证据证实这一推测。

本研究于2019-2020年和2020-2021年冬小麦种植季节在陕西关中地区（宝鸡、咸阳、西安、渭南）和甘肃省陇南、天水、平凉、庆阳四个地区共采集321株小麦条锈菌样品，使用23对KASP-SNP引物对获得的条锈菌样品进行基因分型。联合多种群体遗传方法分析了亚群体之间的关系，从DNA水平明确了2019年 ~ 2021年陕西省内关中地区小麦条锈菌的传播路径，以及小麦条锈菌自甘肃省向陕西省传播的主要路径，取得主要结果如下：

1. 证实陕西关中与甘肃条锈菌的迁移方向主要是从甘肃传向陕西关中地区，但两地间的条锈菌群体也存在一定程度的基因交流。

2. 表明陕西省关中地区条锈菌的迁移方向是由西(宝鸡)向东(渭南)扩散。陕西关中地区的四个亚群体（宝鸡、咸阳、西安、渭南）之间基因交流频繁（5.559 ≤ Nm ≤ 29.148），遗传分化程度低（0.009 ≤ Fst ≤ 0.043）。

3. 表明2019年至2021年陕西关中地区小麦条锈菌的菌源来源主要来自甘肃省陇南天水地区，平凉和庆阳地区作为次要菌源提供地。迁移网络图与风场分析支持病原菌传播路径。

4. 连锁不平衡分析表明陕西省宝鸡、咸阳地区和甘肃省陇南、天水、平凉、庆阳地区均存在较强的遗传重组信号，可能导致当地小麦条锈菌群体的遗传多样性水平升高。

综上所述，甘肃省天水和陇南地区是陕西关中地区的小麦条锈菌菌源地，为其条锈病发生提供菌源，陕西省关中地区小麦条锈菌自西向东的传播路线，即宝鸡→咸阳→西安→渭南。这一研究为陕西关中地区小麦条锈菌传播路径提供了直接分子证据，进而为阻断条锈菌在甘肃和陕西之间的传播，以及为中国小麦条锈病发生与防控提供了重要的理论依据。

Abstract

Wheat stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), is an airborne disease. In China, it frequently develops initially in central Shaanxi and southwestern Gansu, and from there, inoculum spreads to the eastern wheat production regions. Field investigations have suggested that Pst could spread from the west to the east within central Shaanxi and that Gansu could serve as the inoculum source for central Shaanxi, but there is no direct evidence for this hypothetical dispersal route. In the current study, 321 Pst isolates collected from central Shaanxi and Gansu in the 2019-2020 and 2020-2021 winter wheat cropping seasons were genotyped using 23 pairs of KASP-SNP markers. The dispersion among subpopulations was analyzed using several approaches, and overall, the populations were found to exhibit high levels of genetic diversity. There was little genetic divergence (0.05 > F_st> 0) within central Shaanxi. However, significant gene flow (Nm > 4) driven by wind-oriented dispersal from west (Baoji) to east (Weinan) occurred. There was also gene flow among the 4 Gansu subpopulations of Tianshui, Longnan, Pingliang, and Qingyang. Migration of the pathogen occurred between central Shaanxi and Gansu. Migration from Gansu to central Shaanxi was major compared with that from central Shaanxi to Gansu that was minor. Genetic variation occurred among isolates, instead of among subpopulations and within isolates. Linkage disequilibrium revealed that there was strong genetic recombination in the subpopulations from Gansu and central Shaanxi. Therefore, the present study provides molecular evidence that Pst spread from west to east in central Shaanxi and showed that Gansu (especially Longnan and Tianshui) was one of the major origins of the pathogen inoculum of wheat stripe rust in central Shaanxi. The results revealed the west-to-east transmission route of wheat stripe rust in central Shaanxi, being used to guide integrated management of the disease.

Keywords: wheat stripe rust Puccinia striiformis f. sp. tritici SNP genotyping, genetic recombination migration inoculum sources

Online: 23 October 2023

Fund: This work was supported by National Key R&D Program of China (2021YFD1401000), the National Natural Science Foundation of China (32072358, and 32272507), and the Natural Science Basic Research Plan in Shaanxi Province of China (2020JZ-15).

About author: # Correspondence ZHAO Jie, Tel/Fax: +86-29-87082726, E-mail: jiezhao@nwsuaf.edu.cn; KANG Zhen-sheng, Tel/Fax: +86-29-87080061, e-mail: kangzs@nwsuaf.edu.cn * These authors contributed equally to this work as co-first author.

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LIU Wei, HUANG Xue-ling, JU Meng, SUN Mu-di, DU Zhi-min, KANG Zhen-sheng, ZHAO Jie. 2023. Molecular Evidence of the West-to-East Dispersal of Puccinia striiformis f. sp. tritici in Central Shaanxi and the Migration of the Inoculum from Gansu. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2023.10.026

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