Determination of heterozygosity for avirulence/virulence loci through sexual hybridization of Puccinia striiformis f. sp. tritici

Abstract

Wheat stripe rust caused by Puccinia striiformis f. sp. tritici is one of the most devastating diseases of wheat worldwide and resistant cultivars are vital for its management. Therefore, investigating the heterozygosity of the pathogen is important because of rapid virulence changes in isolates heterozygous for avirulence/virulence. An isolate of P. striiformis f. sp. tritici was selfed on Berberis shensiana to determine the heterozygosity for avirulence/virulence loci. One hundred and twenty progeny isolates obtained from this selfing were phenotyped using 25 lines of wheat containing Yr genes and genotyped with 96 simple sequencing repeat markers, with 51 pathotypes and 55 multi-locus genotypes being identified. All of these were avirulent on lines with Yr5, Yr10, Yr15, Yr24 and Yr26 and virulent on lines with Yr17, Yr25 and YrA, indicating that the parental isolate was homozygously avirulent or homozygously virulent for these loci. Segregation was found for wheat lines with Yr1, Yr2, Yr4, Yr6, Yr7, Yr8, Yr9, Yr27, Yr28, Yr32, Yr43, Yr44, YrExp2, YrSp, YrTr1, YrTye and YrV23. The 17 cultivars to which the Pst was identified as heterozygous with respect to virulence/avirulence should not be given priority in breeding programs to obtain new resistant cultivars.

Keywords

Puccinia striiformis f. sp. tritici / selfing / heterozygosity / virulence inheritance

References

[1] Zheng W M, Huang L L, Huang J Q, Wang X J, Chen X M, Zhao J, Guo J, Zhuang H, Qiu C Z, Liu J, Liu H Q, Huang X L, Pei G L, Zhan G M, Tang C L, Cheng Y L, Liu M J, Zhang J S, Zhao Z T, Zhang S J, Han Q M, Han D J, Zhang H C, Zhao J, Gao X N, Wang J F, Ni P X, Dong W, Yang L F, Yang H M, Xu J R, Zhang G Y, Kang Z S. High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus. Nature Communications, 2013, 4: 2673

[2] Chen X M. Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Canadian Journal of Plant Pathology, 2005, 27(3): 314–337

[3] Gassner G, Straib W. The determination of biological races of wheat yellow rust (Puccinia glumarum f. sp. tritici (Schmidt) Erikss.u. Henn.). Working from the Imperial Biological Institute for land and Forestry, Berlin, 1932, 20: 141–163 (in German)

[4] Goddard M V. Cytological studies of Puccinia striiformis (yellow rust of wheat). Transactions of the British Mycological Society, 1976, 66(3): 433–437

[5] Little R, Manners J G. Production of new physiological races in Puccinia striiformis (yellow rust) by heterokaryosis. Nature, 1967, 213(5074): 422

[6] Park R F, Wellings C R. Somatic hybridization in the Uredinales. Annual Review of Phytopathology, 2012, 50(1): 219–239

[7] 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. Virulence variations of Puccinia striiformis f. sp. tritici isolates collected from Berberis spp. in China. Plant Disease, 2016, 100(1): 131–138

[8] Flor H H. Current status of the gene-for-gene concept. Annual Review of Phytopathology, 1971, 9(1): 275–296

[9] Statler G D. Inheritance of pathogenicity of culture 70–1, Race 1, of Puccinia recondita tritici. Phytopathology, 1979, 69(6): 661–663

[10] Cheng P, Chen X M. Virulence and molecular analyses support asexual reproduction of Puccinia striiformis f. sp. tritici in the U.S. Pacific Northwest. Phytopathology, 2014, 104(11): 1208–1220

[11] Liu B, Chen X M, Kang Z S. Gene sequences reveal heterokaryotic variations and evolutionary mechanisms in Puccinia striiformis, the Stripe Rust pathogen. Open Journal of Genomics, 2012, 1(1): 1

[12] Tian Y, Zhan G M, Chen X M, Tungruentragoon A, Lu X, Zhao J, Huang L L, Kang Z S. Virulence and simple sequence repeat marker segregation in a Puccinia striiformis f. sp. tritici population produced by selfing a Chinese isolate on Berberis shensiana. Phytopathology, 2016, 106(2): 185–191

[13] Zhao J, Wang M N, Chen X M, Kang Z S. Role of alternate hosts in epidemiology and pathogen variation of cereal rusts. Annual Review of Phytopathology, 2016, 54(1): 207–228

[14] Newton M, Johnson T, Brown A M. A preliminary study on the hybridization of physiological forms of Puccinia graminis tritici. Scientia Agrícola, 1930, 10(11): 721–731

[15] Waterhouse W L. A preliminary account of the origin of two new Australian physiological forms of Puccinia graminis tritici. Proceedings of the Linnean Society of New South Wales, 1929, 54: 96–106

[16] Jin Y, Szabo L J, Carson M. Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology, 2010, 100(5): 432–435

[17] Wang M N, Chen X M. First report of Oregon grape (Mahonia aquifolium) as an alternate host for the wheat stripe rust pathogen (Puccinia striiformis f. sp. tritici) under artificial inoculation. Plant Disease, 2013, 97(6): 839

[18] Statler G D. Inheritance of virulence of culture 73–47 Puccinia recondita. Phytopathology, 1977, 67(7): 906–908

[19] Statler G D. Inheritance of pathogenicity of progeny from an F₁ culture of Melampsora lini. Journal of Phytopathology, 1990, 128(3): 184–190

[20] Statler G D. Inheritance of virulence of Puccinia triticina culture X47, the F1 of the cross 71–112 x 70–1. Canadian Journal of Plant Pathology, 2000, 22(3): 276–279

[21] Wang M N, Wan A M, Chen X M. Genetic characterization of virulence/avirulence genes of Puccinia striiformis f. sp. tritici. Phytopathology, 2012, 102(S4): 132

[22] Rodriguez-Algaba J, Walter S, Sørensen C K, Hovmøller M S, Justesen A F. Sexual structures and recombination of the wheat rust fungus Puccinia striiformis on Berberis vulgaris. Fungal Genetics and Biology, 2014, 70: 77–85

[23] Flor H H. Tests for allelism of rust-resistance genes in flax. Crop Science, 1965, 5(5): 415–418

[24] Wellings C R. Puccinia striiformis in Australia: a review of the incursion, evolution, and adaptation of stripe rust in the period 1979–2006. Crop & Pasture Science, 2007, 58(6): 567–575

[25] McDowell J M, Woffenden B J. Plant disease resistance genes: recent insights and potential applications. Trends in Biotechnology, 2003, 21(4): 178–183

[26] Yoshida K, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H, Yoshida K, Tosa Y, Chuma I, Takano Y, Win J, Kamoun S, Terauchi R. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell, 2009, 21(5): 1573–1591

[27] 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. 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, 2013, 103(9): 927–934

[28] Zhan G M, Chen X M, Kang Z S, Huang L L, Wang M N, Wan A M, Cheng P, Cao S Q, Jin S L. Virulence and molecular comparison of Puccinia striiformis f. sp. tritici populations in China and the United States. Fungal Biology, 2012, 116(6): 643–653

[29] Line R F, Qayoum A. Virulence, aggressiveness, evolution and distribution of races of Puccinia striiformis (the cause of stripe rust of wheat) in North America, 1968–87. USDA Technical Bulletin, 1788, 1992: 61

[30] Kosman E, Leonard K J. Conceptual analysis of methods applied to assessment of diversity within and distance between populations with asexual or mixed mode of reproduction. New Phytologist, 2007, 174(3): 683–696

[31] Aljanabi S M, Martinez I. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 1997, 25(22): 4692–4693

[32] Enjalbert J, Duan X, Giraud T, Vautrin D, De Vallavieille-Pope C, Solignac M. Isolation of twelve microsatellite loci, using an enrichment protocol, in the phytopathogenic fungus Puccinia striiformis f. sp. tritici. Molecular Ecology Notes, 2002, 2(4): 563–565

[33] Bahri B, Leconte M, de Vallavieille-Pope C, Enjalbert J. Isolation of ten microsatellite loci in an EST library of the phytopathogenic fungus Puccinia striiformis f. sp. tritici. Conservation Genetics, 2009, 10(5): 1425–1428

[34] Chen C Q, Zheng W M, Buchenauer H, Huang L L, Lu N H, Kang Z S. Isolation of microsatellite loci from expressed sequence tags library of Puccinia striiformis f. sp. tritici. Molecular Ecology Resources, 2009, 9(1): 236–238

[35] Cheng P, Chen X M, Xu L S, See D R. Development and characterization of expressed sequence tag-derived microsatellite markers for the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. Molecular Ecology Resources, 2012, 12(4): 779–781

[36] Luo H Y, Wang X J, Zhan G M, Wei G R, Zhou X L, Zhao J, Huang L L, Kang Z S. Genome-wide analysis of simple sequence repeats and efficient development of polymorphic SSR markers based on whole genome re-sequencing of multiple isolates of the Wheat Stripe Rust fungus. PLoS One, 2015, 10(6): e0130362

[36a] Bailey J, Karaoglu H, Weling S C R, Park R F. Isolation and characterisation of 25 genome-derived simple sequence repeat markers for Puccinia striiformis f. sp. tritici. Molecular Ecology Resources, 2013, 13(4): 760–762

[36b] Zhan G M, Wang F P, Luo H Y, Jiang S C, Zheng W M, Huang L L, Kang Z S. Screening for simple sequence repeat markers in Puccinia striiformis tritici based on genomic sequence. Journal of Zhejiang University-SCIENCE B, 2015, 16(8): 727–732

[37] Holland M M, Parson W. GeneMarker HID: A reliable software tool for the analysis of forensic STR data. Journal of Forensic Sciences, 2011, 56(1): 29–35

[38] Rohlf F. NTSYS-pc N T. Multivariate analysis system, Version 2.10 e.New York: Applied Biostatistics Incorprated, 2000

[39] Zhang L Y, Wang S Q, Li H H, Deng Q M, Zheng A P, Li S C, Li P, Li Z L, Wang J K. Effects of missing marker and segeregating distortion on QTL mapping in F₂ populations. Theoretical and Applied Genetics, 2010, 121(6): 1071–1082

[41] Bourras S, McNally K E, Ben-David R, Parlange F, Roffler S, Praz C R, Oberhaensli S, Menardo F, Stirmweis D, Frenkel Z, Schaefer L K, Flückiger S, Treier G, Herren G, Korol A B, Wicker T, Keller B. Multiple avirulence loci and allele-specific effector recognition control the Pm3 race-specific resistance of wheat to powdery mildew. Plant Cell, 2015, 27(10): 2991–3012

[42] Zambino P J, Kubelik A R, Szabo L J. Gene action and linkage of avirulence genes to DNA markers in the rust fungus Puccinia graminis. Phytopathology, 2000, 90(8): 819–826

[43] Samborski D J, Dyck P L. Inheritance of virulence in Puccinia recondita on six backcross lines of wheat with single genes for resistance to leaf rust. Canadian Journal of Botany, 1976, 54(14): 1666–1671

[44] Lawrence G J. Melampsora lini, rust of flax and linseed. Advances in Plant Pathology, 1988, 6: 313–331

[45] Wan A M, Chen X M. Virulence characterization of Puccinia striiformis f. sp. tritici using a new set of Yr single-gene line differentials in the United States in 2010. Plant Disease, 2014, 98(11): 1534–1542

[46] Liu T G, Peng Y L, Chen W Q, Zhang Z Y. First detection of virulence in Puccinia striiformis f. sp. tritici in China to resistance genes Yr24 (= Yr26) present in wheat cultivar Chuanmai 42. Plant Disease, 2010, 94(9): 1163

[47] Sharma-Poudyal D, Chen X, Wan A, Zhan G, Kang Z, Cao S, Jin S, Morgounov A, Akin B, Mert Z, Shah S J A, Bux H, Ashraf M, Sharma R C, Madariaga R, Puri K D, Wellings C, Xi K, Wanyera R, Manninger K, Ganzález M I, Koyda M, Sanin S, Patzek L J. Virulence characterization of international collections of the wheat stripe rust pathogen, Puccinia striiformis f. sp. tritici. Plant Disease, 2013, 97(3): 379–386

[48] Chen X M. High-temperature adult-plant resistance, key for sustainable control of stripe rust. American Journal of Plant Sciences, 2013, 4(3): 608–627

Supplementary materials

The online version of this article at http://dx.doi.org/10.15302/J-FASE-2016114 contains supplementary materials (Tables S1–S4).

Acknowledgements

This work was supported by the National Key Basic Research Program of China (2013CB127700), the National Natural Science Foundation of China (31271986, 31371882), Modern Agro-industry Technology Research System in China (CARS-3-1-11), and the 111 Project of the Ministry of Education of China (B07049).

Compliance with ethics guidelines

Yuan Tian, Gangming Zhan, Xia Lu, Jie Zhao, Lili Huang, and Zhensheng Kang declare that they have no conflict of interest or financial conflicts to disclose.

This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2016. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)