Please wait a minute...
Journal of Integrative Agriculture  2018, Vol. 17 Issue (08): 1779-1789    DOI: 10.1016/S2095-3119(18)61923-9
Special Issue: 植物抗病遗传合辑Plant Disease-resistance Genetics
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
Population genetic structure of Chinese Puccinia triticina races based on multi-locus sequences
LIU Tai-guo*, GE Run-jing*, MA Yu-tong, LIU Bo, GAO Li, CHEN Wan-quan
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  Received  10 October, 2017    Accepted  9 February, 2018

Puccinia triticina, the causal agent of wheat leaf rust, is one of the most devastating rust fungi attacking wheat worldwide.  Seventy-six isolates of the wheat leaf rust pathogen from Yunnan, Sichuan, Gansu and Henan provinces, China, were tested on wheat leaf rust differentials and the population structure was analyzed using four presumably neutral partial sequence markers such as elongation factor-1α (EF-1α), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), β-tubulin (TUB) and the second largest RNA polymerase subunit (RPB2).  The phenotypic diversity of Yunnan and Sichuan populations was higher than that of Gansu and Henan populations.  The four populations were separated into two clusters based on the pathogenic data.  A total of 12 single nucleotide polymorphisms (SNPs) and 32 haplotypes were identified among the four sequences.  The 32 haplotypes were divided into two clusters in a neighbor-joining tree.  Bayesian analyses also identified two clusters.  Pairwise Fst between populations in different regions were significantly different (P<0.05).  Analysis of molecular variance (AMOVA) indicated that 68% of the total genetic variation was within populations. 
Keywords:  population structure        polymorphism        virulence        wheat leaf rust        Puccinia triticina  
Received: 10 October 2017   Accepted:
Fund: The financial supports by the National Natural Science Foundation of China (31671967), the National Key Research and Development Program from the Ministry of Science and Technology, China (2016YFD0300705), the National GMO New Variety Breeding Project, China (2014ZX0801101B) and the earmarked fund for China Agriculture Research System (CARS-3) were gratefully acknowledged.
Corresponding Authors:  Correspondence LIU Tai-guo, Tel: +86-10-62815618, Fax: +86-10-62815909, E-mail:; CHEN Wan-quan, E-mail:   
About author:  * These authors contributed equally to this study.

Cite this article: 

LIU Tai-guo, GE Run-jing, MA Yu-tong, LIU Bo, GAO Li, CHEN Wan-quan. 2018. Population genetic structure of Chinese Puccinia triticina races based on multi-locus sequences. Journal of Integrative Agriculture, 17(08): 1779-1789.

Adams M, Raadik T A, Burridge C P, Georges A. 2014. Global biodiversity assessment and hyper-cryptic species complexes: More than one species of elephant in the room? Systematic Biology, 63, 518–533.
Allendorf F W. 1983. Isolation, gene flow, and genetic differentiation among populations. In: Schonewald-Cox C M, Chambe M, MacBryde B, Thomas W L, eds., Genetics and Conservation: A Reference for Managing Wild Animal and Plant Populations. Benjamin Cummings Publishing, Menlo Park. pp. 51– 65.
Althoff D M, Pellmyr O. 2002. Examining genetic structure in a bogus yucca moth: A sequential approach to phylogeography. Evolution, 56, 1632–1643.
Bakhshi M, Arzanlou M, Babai-Ahari A, Groenewald J Z, Crous P W. 2014. Multi-gene analysis of Pseudocercospora spp. from Iran. Phytotaxa, 184, 245–264.
Bouftass F, Labhilili M, Ezzahiri B, Ziouti A. 2010. Molecular polymorphism of the wheat leaf rust fungus in Morocco using amplified fragment length polymorphism. Journal of Phytopathology, 158, 111–116.
Chen W Q, Duan X Y. 2014. The hot spots in cereal rusts and powdery mildew research. Journal of Integrative Agriculture, 13, 229–232.
Chen X, Line R F, Leung H. 1993. Relationship between virulence variation and DNA polymorphism in Puccinia striiformis. Phytopathology, 83, 1489–1497.
Dadrezaie S T, Lababidi S, Nazari K, Goltapeh E M, Afshari F, Alo F, Shams-Bakhsh M, Safaie N. 2013. Molecular genetic diversity in Iranian populations of Puccinia triticina, the causal agent of wheat leaf rust. American Journal of Plant Sciences, 4, 1375–1386.
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.
Excoffier L, Laval G, Schneider S. 2005. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47.
Excoffier L, Smouse P E, Quattro J M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.
Falush D, Stephens M, Pritchard J K. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567–1587.
Fu Y X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915–925.
Fu Y X, Li W H. 1993. Statistical tests of neutrality of mutations. Genetics, 133, 693–709.
Hall T A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
He Z H, Rajaram S, Xin Z Y, Huang G Z. 2001. A History of Wheat Breeding in China. CIMMYT, Mexico.
Huang C H, Lee F L, Tai C J. 2009. The β-tubulin gene as a molecular phylogenetic marker for classification and discrimination of the Saccharomyces sensu stricto complex. Antonie Van Leeuwenhoek, 95, 135–142.
Huerta-Espino J, Singh R, Germán S, Mccallum B, Park R, Chen W, Bhardwaj S, Goyeau H. 2011. Global status of wheat leaf rust caused by Puccinia triticina. Euphytica, 179, 143–160.
Johnson A D. 2009. Single-nucleotide polymorphism bioinformatics a comprehensive review of resources. Circulation-Cardiovascular Genetics, 2, 530–536.
Kolmer J. 1996. Genetics of resistance to wheat leaf rust. Annual Review of Phytopathology, 34, 435–455.
Kolmer J. 2013. Leaf rust of wheat: Pathogen biology, variation and host resistance. Forests, 4, 70–84.
Kolmer J, Liu J, Sies M. 1995. Virulence and molecular polymorphism in Puccinia recondita f. sp. tritici in Canada. Phytopathology, 85, 276–285.
Kolmer J A. 2005. Tracking wheat rust on a continental scale. Current Opinion in Plant Biology, 8, 441–449.
Kolmer J A, Ordoñez M E. 2007. Genetic differentiation of Puccinia triticina populations in Central Asia and the Caucasus. Phytopathology, 97, 1141–1149.
Kruskal J B. 1956. On the shortest spanning subtree of a graph and the traveling salesman problem. Proceedings of the American Mathematical Society, 7, 48–50.
Li Z, Xia X, He Z, Li X, Zhang L, Wang H, Meng Q, Yang W, Li G, Liu D. 2010. Seedling and slow rusting resistance to leaf rust in Chinese wheat cultivars. Plant Disease, 94, 45–53.
Librado P, Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.
Linde C C, Liles J A, Thrall P H. 2010. Expansion of genetic diversity in randomly mating founder populations of Alternaria brassicicola Infecting Cakile maritima in Australia. Applied and Environmental Microbiology, 76, 1946–1954.
Liu M, Rodrigue N, Kolmer J. 2014. Population divergence in the wheat leaf rust fungus Puccinia triticina is correlated with wheat evolution. Heredity, 112, 443–453.
Liu M, Szabo L J, Hambleton S, Anikster Y, Kolmer J A. 2013. Molecular phylogenetic relationships of the brown leaf rust fungi on wheat, rye, and other grasses. Plant Disease, 97, 1408–1417.
Liu T G, Chen W Q. 2012. Race and virulence dynamics of Puccinia triticina in China during 2000–2006. Plant Disease, 96, 1601–1607.
Long D, Kolmer J. 1989. A North American system of nomenclature for Puccinia recondita f. sp. tritici. Phytopathology, 79, 525–529.
Mcdonald B A, Linde C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349–379.
Morgado L, Noordeloos M, Lamoureux Y, Geml J. 2013. Multi-gene phylogenetic analyses reveal species limits, phylogeographic patterns, and evolutionary histories of key morphological traits in Entoloma (Agaricales, Basidiomycota). Persoonia, 31, 159–178.
O’donnell K, Rooney A P, Proctor R H, Brown D W, Mccormick S P, Ward T J, Frandsen R J N, Lysoe E, Rehner S A, Aoki T, Robert V A R G, Crous P W, Groenewald J Z, Kang S, Geiser D M. 2013. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genetics and Biology, 52, 20–31.
Ordoñez M, German S, Kolmer J. 2010. Genetic differentiation within the Puccinia triticina population in South America and comparison with the North American population suggests common ancestry and intercontinental migration. Phytopathology, 100, 376–383.
Ordoñez M, Kolmer J. 2007. Simple sequence repeat diversity of a worldwide collection of Puccinia triticina from durum wheat. Phytopathology, 97, 574–583.
Ordoñez M, Kolmer J. 2009. Differentiation of molecular genotypes and virulence phenotypes of Puccinia triticina from common wheat in North America. Phytopathology, 99, 750–758.
Parks R, Carbone I, Murphy J P, Cowger C. 2009. Population genetic analysis of an eastern US wheat powdery mildew population reveals geographic subdivision and recent common ancestry with UK and Israeli populations. Phytopathology, 99, 840–849.
Prim R C. 1957. Shortest connection networks and some generalizations. The Bell System Technical Journal, 36, 1389–1401.
Pritchard J K, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.
Rosenberg N A. 2004. DISTRUCT: A program for the graphical display of population structure. Molecular Ecology Notes, 4, 137–138.
Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.
Taerum S J, Duong T A, De Beer Z W, Gillette N, Sun J H, Owen D R, Wingfield M J. 2013. Large shift in symbiont assemblage in the invasive red turpentine beetle. PLoS ONE, 8, e78126.
Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.
Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.
Teacher A, Griffiths D. 2011. HapStar: Automated haplotype network layout and visualization. Molecular Ecology Resources, 11, 151–153.
Thrall P H, Burdon J J. 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science, 299, 1735–1737.
Woudenberg J H C, Truter M, Groenewald J Z, Crous P W. 2014. Large-spored Alternaria pathogens in section Porri disentangled. Studies in Mycology, 79, 1–47.
Van De Wouw A P, Cozijnsen A J, Hane J K, Brunner P C, Mcdonald B A, Oliver R P, Howlett B J. 2010. Evolution of linked avirulence effectors in leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathogens, 6, e1001180.
Wright S. 1949. The genetical structure of populations. Annals of Eugenics, 15, 323–354.
Zhang Y, Li S Z, Wu Z L, Yang W X, Yu Y X, Xia X C, He Z H. 2011. Contribution of CIMMYT wheat germplasm to genetic improvement of grain yield in spring wheat of Sichuan, Yunnan, Gansu, and Xinjiang provinces. Acta Agronomica Sinica, 37, 1752–1762. (in Chinese)
Zou Y C, Yang W Y, Zhu H Z, Yang E N, Pu Z J, Wu L, Tang Y L, Huang G, Li Y J, He Z H, Singh R, Rajaram S. 2007. Utilization of CIMMYT germplasm and breeding technologies in wheat improvement in Sichuan, China. Southwest China Journal of Agricultural Sciences, 20, 183–190. (in Chinese)
[1] WANG Deng-feng, YANG Xue-yun, WEI Yu-rong, LI Jian-jun, BOLATI Hongduzi, MENG Xiao-xiao, TUERXUN Gunuer, NUERDAN Nuerbaiheti, WU Jian-yong. Genome characterization of the Caprine arthritis-encephalitis virus in China: A retrospective genomic analysis of the earliest Chinese isolates[J]. >Journal of Integrative Agriculture, 2023, 22(3): 872-880.
[2] GUO Yi, GONG Ying, HE Yong-meng, YANG Bai-gao, ZHANG Wei-yi, CHEN Bo-er, HUANG Yong-fu, ZHAO Yong-ju, ZHANG Dan-ping, MA Yue-hui, CHU Ming-xing, E Guang-xin. Investigation of Mitochondrial DNA genetic diversity and phylogeny of goats worldwide[J]. >Journal of Integrative Agriculture, 2022, 21(6): 1830-1837.
[3] SHI Dong-ya, REN Wei-chao, WANG Jin, ZHANG Jie, Jane Ifunanya MBADIANYA, MAO Xue-wei, CHEN Chang-jun. The transcription factor FgNsf1 regulates fungal development, virulence and stress responses in Fusarium graminearum[J]. >Journal of Integrative Agriculture, 2021, 20(8): 2156-2169.
[4] LIU Na, CHENG Fang-yun, GUO Xin, ZHONG Yuan. Development and application of microsatellite markers within transcription factors in flare tree peony (Paeonia rockii) based on next-generation and single-molecule long-read RNA-seq[J]. >Journal of Integrative Agriculture, 2021, 20(7): 1832-1848.
[5] TIAN Li, HUANG Cai-min, ZHANG Dan-dan, LI Ran, CHEN Jie-yin, SUN Wei-xia, QIU Nian-wei, DAI Xiao-feng. Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliae[J]. >Journal of Integrative Agriculture, 2021, 20(7): 1858-1870.
[6] DIAO Shu-qi, XU Zhi-ting, YE Shao-pan, HUANG Shu-wen, TENG Jin-yan, YUAN Xiao-long, CHEN Zan-mou, ZHANG Hao, LI Jia-qi, ZHANG Zhe. Exploring the genetic features and signatures of selection in South China indigenous pigs[J]. >Journal of Integrative Agriculture, 2021, 20(5): 1359-1371.
[7] ZHANG Jia-lei, GENG Yun, GUO Feng, LI Xin-guo, WAN Shu-bo. Research progress on the mechanism of improving peanut yield by single-seed precision sowing[J]. >Journal of Integrative Agriculture, 2020, 19(8): 1919-1927.
[8] Bongekile NGOBESE, Oliver Tendayi ZISHIRI, Mohamed Ezzat EL ZOWALATY. Molecular detection of virulence genes in Campylobacter species isolated from livestock production systems in South Africa[J]. >Journal of Integrative Agriculture, 2020, 19(6): 1656-1670.
[9] CHEN Bin, TIAN Yan-li, ZHAO Yu-qiang, WANG Yuan-jie, CHUAN Jia-cheng, LI Xiang, HU Bai-shi. Genomic characteristics of Dickeya fangzhongdai isolates from pear and the function of type IV pili in the chromosome[J]. >Journal of Integrative Agriculture, 2020, 19(4): 906-920.
[10] QIN Jia-xing, LI Bao-hua, ZHOU Shan-yue. A novel glycoside hydrolase 74 xyloglucanase CvGH74A is a virulence factor in Coniella vitis[J]. >Journal of Integrative Agriculture, 2020, 19(11): 2725-2735.
[11] YUAN Long-yu, HAO Yuan-hao, CHEN Qiao-kui, PANG Rui, ZHANG Wen-qing. Pancreatic triglyceride lipase is involved in the virulence of the brown planthopper to rice plants[J]. >Journal of Integrative Agriculture, 2020, 19(11): 2758-2766.
[12] ZHANG Hang, YANG Feng, LI Xin-pu, LUO Jin-yin, WANG Ling, ZHOU Yu-long, YAN Yong, WANG Xu-rong, LI Hong-sheng. Detection of antimicrobial resistance and virulence-related genes in Streptococcus uberis and Streptococcus parauberis isolated from clinical bovine mastitis cases in northwestern China[J]. >Journal of Integrative Agriculture, 2020, 19(11): 2784-2791.
[13] WANG Qian-nan, HUANG Pan-pan, ZHOU Shan-yue. Functional characterization of the catalytic and bromodomain of FgGCN5 in development, DON production and virulence of Fusarium graminearum[J]. >Journal of Integrative Agriculture, 2020, 19(10): 2477-2487.
[14] ZHANG Pei-pei, Takele Weldu Gebrewahid, ZHOU Yue, LI Qing-luo, LI Zai-feng, LIU Da-qun. Seedling and adult plant resistance to leaf rust in 46 Chinese bread wheat landraces and 39 wheat lines with known Lr genes[J]. >Journal of Integrative Agriculture, 2019, 18(5): 1014-1023.
[15] SONG Xiao-xia, ZHAO Yan, SONG Chun-yan, LI Chuan-hua, CHEN Ming-jie, HUANG Jian-chun, TAN Qi. Intergenic spacer 1 (IGS1) polymorphism map: A marker for the initial classification of cultivated Lentinula edodes strains in China[J]. >Journal of Integrative Agriculture, 2018, 17(11): 2458-2466.
No Suggested Reading articles found!