陕西中部小麦条锈菌传播规律及其菌源
的分子证据

doi:10.1016/j.jia.2023.10.026

摘要/Abstract

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.

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

. 陕西中部小麦条锈菌传播规律及其菌源的分子证据[J]. Journal of Integrative Agriculture, DOI: 10.1016/j.jia.2023.10.026.

LIU Wei, HUANG Xue-ling, JU Meng, SUN Mu-di, DU Zhi-min, KANG Zhen-sheng, ZHAO Jie. 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[J]. Journal of Integrative Agriculture, DOI: 10.1016/j.jia.2023.10.026.

参考文献

Agapow P M, Burt A. 2001. Indices of multilocus linkage disequilibrium. Molecular Ecology, Notes, 1, 101-102.

Ali S, Gautier A, Leconte M, Enjalbert J, de Vallavieille-Pope C. 2011. A rapid genotyping method for an obligate fungal pathogen, Puccinia striiformis f. sp. tritici, based on DNA extraction from infected leaf and Multiplex PCR genotyping. BMC Research Notes, 4, 240.

Ali S, Gladieux P, Leconte M, Gautier A, Justesen A F, Hovmøller M S, Enjalbert J, de Vallavieille-Pope C. 2014. Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f. sp. tritici. PLoS Pathogens, 10, e1003903.

Arnaud-Haond S, Belkhir K. 2007. GenClone: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Molecular Ecology, Notes, 7, 15-17.

Awais M, Ali S, Ju M, Liu W, Zhang G S, Zhang Z D, Li Z J, Ma X Y, Wang L, Du Z M, Tian X X, Zeng Q D, Kang Z S, Zhao J. 2022. Countrywide inter-epidemic region migration pattern suggests the role of southwestern population in wheat stripe rust epidemics in China. Environmental Microbiology, 24, 4684-4701.

Bai Q, Wan A, Wang M, See D R, Chen X M. 2021. Molecular characterization of wheat stripe rust pathogen (Puccinia striiformis f. sp. tritici) collections from nine countries. International Journal of Molecular Sciences, 22, 9457.

Boshoff W H P, Pretorius Z A, van Niekerk B D. 2002. Establishment, distribution, and pathogenicity of Puccinia striiformis f. sp. tritici in South Africa. Plant Disease, 86, 485-492.

Brown A H D, Feldman M W, Nevo E. 1980. Multilocus structure of natural populations of Hordeum spontaneum. Genetics, 96, 523-536.

Chen W, Wellings C, Chen X, Kang Z, Liu T. 2014. Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici. Molecular Plant Pathology, 15, 433-446.

Chen, X. M. 2005. Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Canadian Journal of Plant Pathology, 27, 314-337.

Craigie J H. 1945. Epidemiology of stem rust in Western Canada. The Journal of Agricultural Science, 25, 285-401.

Enjalbert J, Duan X, Leconte M, Hovmøller M S, de Vallavieille-Pope C. 2005. Genetic evidence of local adaptation of wheat yellow rust (Puccinia striiformis f. sp. tritici) within France. Molecular Ecology. 14, 2065-2073.

Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620.

Gassner G, Straib W. 1933. Über Mutatinen in einer biologischen Rasse von Puccinia glumarum tritici (Schmidt) Erikss. und Henn. Zeitschrift für Inductive Abstammungs-und Vererbungslehre. Lehre, 63, 155-180.

Guo H P, Wei H X, Feng X J, Wen Y D, Shi J N, Zhang J G. 2021. Occurrence and epidemic characteristic of wheat stripe rust for year of 2020 in Shaanxi and its causes and analysis. Shaanxi J. The Journal of Agricultural Science, 67, 89-90, 104. (in Chinese)

HovmØller M S, Justesen A F, Brown J K M. 2002. Clonality and long-distance migration of Puccinia striiformis f. sp. tritici in north-west Europe. Plant Pathology, 51, 24-32.

Huang C, Jiang Y, Ji G, Zhang G, Li H, Li Y. 2018. Spatiotemporal dynamics of wheat stripe rust epidemics at regional level in China in 2017. Journal of Plant Protection Research, 45, 20-26. (in Chinese)

Hu X P, Cao S Q, Cornelius A, Xu X M. 2020. Predicting overwintering of wheat stripe rust in central and northwestern China. Plant Disease, 104, 44-51.

Jakobsson M, Rosenberg N A. 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801-1806.

Jia Q Z, Cao S Q, Wang X M, Huang J, Sun Z Y, Zhang B, Luo H S, Li Q Q. 2021. Monitoring the variation of physiological races of Puccinia striiformis f. sp. tritici in Gansu Province during 2017-2018. Plant Protection, 47, 214-218. (in Chinese)

Jiang B B, Wang C C, Guo C W, Lv X, Gong W F, Chang J, He H P, Feng J, Chen X M, Ma Z H. 2022. Genetic relationships of Puccinia striiformis f. sp. tritici in Southwestern and Northwestern China. Microbiology Spectrum, 10, e0153022.

Ju M, Liu W, Wang L, Sun M D, Kang Z S, Zhao J. 2022. Two main routes of spore migration contributing to the occurrence of wheat stripe rust in the Jiangsu and Zhejiang costal sporadic epidemiological region in 2019 based on phenotyping and genotyping analyses. Plant Disease, 106, 2948-2957.

Kamvar Z N, Tabima J F, Grünwald N J. 2014. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/ or sexual reproduction. PeerJ, 2, e281.

Kang Z S, Wang X J, Zhao J, Tang C L, Huang L L. 2015. Advances in research of pathogenicity and virulence variation of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. Scientia Agricultura Sinica, 48, 3439-3453. (in Chinese)

Li D K, Wang Z, Xie F Z. 2019. Occurrence regularity and meteorological influencing factors of wheat stripe rust in Shaanxi Province. Journal of Catastrophology, 34, 59-65. (in Chinese)

Li Q, Qin J F, Zhao Y Y, Zhao J, Huang L L, Kang Z S. 2016. Virulence analysis of sexual progeny of the wheat tripe rust pathogen recovered from wild barberry in Shaanxi and Gansu. Acta Phytopathologica Sinica, 46, 809-820. (in Chinese)

Li Z Q, Liu H W. 1956. Primary studies on the trend of occurrence and development of the stripe rust of wheat (Puccinia glumarum (Sch.) Eriks. and Henn.) in provinces Shaanxi, Gansu, and Qinghai. Journal of Northwest A&F University (Nat. Sci. Ed.), 4, 1-18. (in Chinese)

Li Z Q, Liu H W. 1957. Primary studies on the trend of occurrence and development of the stripe rust of wheat (Puccinia glumarum (Sch.) Eriks. and Henn.) in provinces Shaanxi, Gansu, and Qinghai (continued). Journal of Northwest A&F University (Nat. Sci. Ed.), 1, 33-46. (in Chinese)

Li Z Q, Zeng S M. 2002. Wheat Rust in China. China Agricultural Press. Beijing.

Liu B, Liu T G, Zhang Z Y, Jia Q Z, Wang B T, Gao L, Peng Y L, Jin S L, Chen W Q. 2017. Discovery and pathogenicity of CYR34, a new race of Puccinia striiformis f. sp. tritici in China. Acta Phytopathologica Sinica, 47, 681-687. (in Chinese)

Liu K, and Muse S V. 2005. PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics, 21, 2129-2129.

Liu T G, Peng Y L, Chen W Q, Zhang Z Y. 2010. First detection of virulence in Puccinia striiformis f. sp. tritici in China to resistance gene Yr24 (= Yr26) present in wheat cultivar Chuanmai 42. Plant Disease, 94, 1163.

Ma Z H. 2018. Researches and control of wheat stripe rust in China. Plant Protection, 5, 1-6. (in Chinese)

Meng Y, Yang C B, Jiang S C, Huang L L, Kang Z S, Zhan, G M. 2020. Development and evaluation of SNP molecular markers of wheat stripe rust based on KASP technology. Journal of Plant Protection, 47, 65-73. (in Chinese)

Nei M. 1972. Genetic distance between populations. The American Naturalist, 106, 283-292.

O’Brien L, Brown J S, Young R M, Pascoe I. 1980. Occurrence and distribution of wheat stripe rust in Victoria and susceptibility of commercial wheat cultivars. Australasian Plant Pathology, 9, 14.

Peakall R, Smouse P E. 2006. Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology, Notes, 6, 288-295.

Peakall R, and Smouse, P. E. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics, 28, 2537-2539.

Pretorius Z A, Boshoff W H P, Kema, G H J. 1997. First report of Puccinia striiformis f. sp. tritici on wheat in South Africa. Plant Disease, 81,424.

Pritchard J K, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.

Rapilly F. 1979. Yellow rust epidemiology. Annual Review of Phytopathology, 17, 59-73.

Rosenberg N A. 2004. DISTRUCT: a program for the graphical display of population structure. Molecular Ecology, 4, 137-138.

Shaanxi Provincial Station of Plant Protection (SXPSPP). 1977. Historic retrospection and current status of wheat stripe rust in Shaanxi Province. Shaanxi Journal of Agricultural Sciences, 8, 3-5. (in Chinese)

Shannon C E. 2001. A mathematical theory of communication. ACM SIGMOBILE Mobile Computing and Communications Review, 5, 3-55.

Sharma-Poudyal D, Chen X, Rupp R A. 2014. Potential oversummering and overwintering regions for the wheat stripe rust pathogen in the contiguous United States. International Journal of Biometeorology, 58, 987-997.

Slatkin M, Barton N H. 1989. A comparison of three indirect methods for estimating average levels of gene flow. Evolution, 43, 1349-1368.

Stakman E C. 1923. The wheat rust problem in the United States. Pan-Pacific Science Congress, 1, 88-96.

Wan A M, Chen X M, He Z H. 2007. Wheat stripe rust in China. Australian Journal of Agricultural Research, 58, 605-619.

Wan A M, Zhao Z H, Chen X M, He Z H, Jin S L, Jia Q Z, Yao G, Yang J X, Wang B T, Li G B, Bi Y Q, Yuan Z Y. 2004. Wheat Stripe Rust Epidemic and Virulence of Puccinia striiformis f. sp. tritici in China in 2002. Plant Disease, 88, 896-904.

Wan Q, Liang J M, Luo Y, Ma Z H. 2015. Population genetic structure of Puccinia striiformis in northwestern China. Plant Disease, 99, 1764-1774.

Wang C H, Li Y X, Wang B T, Hu X P. 2022. Genetic analysis reveals relationships among populations of Puccinia striiformis f. sp. tritici from the Longnan, Longdong and central Shaanxi regions of China. Phytopathology, 112, 278-289.

Wang J F, Lu N H, Chen C Q, Zhan G M, Huang L L, Kang Z S. 2013. Analysis of population genetic structure of Puccinia striiformis f. sp. tritici in Shaanxi Province, China. Acta Phytopathologica Sinica, 43, 294-300. (in Chinese)

Wang Z Y, Zhao J, Chen X M, Peng Y L, Ji J J, Zhao S L, Lv Y J, Huang L L, Kang Z S. 2016. Virulence variation of Puccinia striiformis f. sp. tritici collected from Berberis spp. in China. Plant Disease, 100, 131-138.

Wellings C R. 2011. Global status of stripe rust: a review of historical and current threats. Euphytica, 179, 129-141.

Wellings C R, McIntosh R A. 1990. Puccinia striiformis f. sp. tritici in Australasia: pathogenic changes during the first 10 years. Plant Pathology (Oxford), 39, 316-325.

Wellings C R, Wright D G, Keiper F, Loughman R. 2003. First detection of wheat stripe rust in Western Australia: evidence for a foreign incursion. Australasian Plant Pathology, 32, 321-322.

Xia C J, Wan A M, Wang M N, Jiwan D A, See D R, Chen X M. 2016. Secreted protein gene derived-single nucleotide polymorphisms (SP-SNPs) reveal population diversity and differentiation of Puccinia striiformis f. sp. tritici in the United States. Fungal Biology, 120, 729-744.

Xie S X, Wang K N, Chen Y L, Chen W Q. 1993. Preliminary studies on the relationship between transport of wheat stripe rust and the upper air current in China. Acta Phytopathologica Sinica. 23, 203-209. (in Chinese)

Xu X M, Ma L J, Hu X P. 2019. Overwintering of wheat stripe rust under field conditions in the northwestern regions of China. Plant Disease, 103, 638-644.

Yeh F C, Yang R C, Boyle T. 1999. POPGENE version 1.32: Microsoft windows-based freeware for population genetic analysis, a quick user guide. University of Alberta, Center for International Forestry Research, Alberta, Canada.

Zadoks J C. 1961. Yellow rust on wheat: Studies in epidemiology and physiologic specialization. Tijdschr Planteziekten, 67, 69-256.

Zeng S M, Luo Y 2006. Long-distance spread and interregional epidemics of wheat stripe rust in China. Plant Disease, 90, 980-988.

Zeng S M, Luo Y. 2008. Systems analysis of wheat stripe rust epidemics in China. European Journal of Plant Pathology, 121, 425-438.

Zhang B, Huang J, Jia Q Z, Cao S Q, Sun Z Y, Jin S L. 2015. Analysis of population genetic structure of Puccinia striiformis f. sp. tritici from central Gansu and the surrounding areas. Journal of Plant Protection, 42, 334-339. (in Chinese)

Zhao J, Wang L, Wang Z Y, Chen X M, Zhang H C, Yao J N, Zhan G M, Chen W, Huang L L, Kang Z S. 2013. Identification of eighteen Berberis species as alternate hosts of Puccinia striiformis f. sp. tritici and virulence variation in the pathogen isolates from natural infection of barberry plants in China. Phytopathology, 103, 927-934.

Zhao Y Y, Li Q, Huang L L, Kang Z S, Zhao J. 2023. Virulence phenotyping and molecular genotyping reveal high diversity within and strong gene flow between the Puccinia striiformis f. sp. tritici populations collected from barberry and wheat in Shaanxi province of China. Plant Disease, 107, 701-712.