Association Analysis of SP-SNPs and Avirulence Genes in <i>Puccinia striiformis</i> f. sp. <i>tritici</i>, the Wheat Stripe Rust Pathogen — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Association Analysis of SP-SNPs and Avirulence Genes in <i>Puccinia striiformis</i> f. sp. <i>tritici</i>, the Wheat Stripe Rust Pathogen
Department of Plant Pathology, Washington State University, Pullman, USA
,
Department of Plant Pathology, Washington State University, Pullman, USA
,
Department of Plant Pathology, Washington State University, Pullman, USA
,
Department of Plant Pathology, Washington State University, Pullman, USA
,
United States Department of Agriculture, Agricultural Research Service, Wheat Health, Genetics, and Quality Research Unit, Pullman, USA
,
United States Department of Agriculture, Agricultural Research Service, Wheat Health, Genetics, and Quality Research Unit, Pullman, USA
1 Department of Plant Pathology, Washington State University, Pullman, USA
2 Department of Plant Pathology, Washington State University, Pullman, USA
3 Department of Plant Pathology, Washington State University, Pullman, USA
4 Department of Plant Pathology, Washington State University, Pullman, USA
5 United States Department of Agriculture, Agricultural Research Service, Wheat Health, Genetics, and Quality Research Unit, Pullman, USA
6 United States Department of Agriculture, Agricultural Research Service, Wheat Health, Genetics, and Quality Research Unit, Pullman, USA
Puccinia striiformis f. sp. tritici ( Pst ) is one of the pathogenic fungi on wheat, caused stripe rust that is a great threat for wheat production all over the world. Intensive efforts have been made to study genetics of wheat resistance to this disease, but few on avirulence of the pathogen due mainly to the nature of obligate biotrophism and the lack of systems for studying its genetics and molecular manipulations. To overcome these limitations, a natural Pst population comprising 352 isolates representative of a diverse virulence spectrum was genotyped using 97 secreted protein-single nucleotide polymorphism (SP-SNP) markers to identify candidate avirulence genes using association analysis. Among avirulence genes corresponding to 19 resistance genes, significantly associated SP-SNP markers were detected for avirulence genes AvYr1, AvYr2, AvYr6, AvYr7, AvYr8, AvYr44, AvYrExp2, AvYrSP , and AvYrTye . These results indicate that association analysis can be used to identify markers for avirulence genes. This study has laid the foundation for developing more SP-SNPs for mapping avirulence genes using segregating populations that can be generated through sexual reproduction on alternate hosts of the pathogen.
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. http://dx.doi.org/10.1080/07060660509507230
Wellings, C.R. (2011) Global Status of Stripe Rust: A Review of Historical and Current Threats. Euphytica, 179, 129-141. http://dx.doi.org/10.1007/s10681-011-0360-y
Line, R.F. (2002) Stripe Rust of Wheat and Barley in North America: A Retrospective Historical Review. Annual Review of Phytopathology, 40, 75-118. http://dx.doi.org/10.1146/annurev.phyto.40.020102.111645
Chen, X.M. (2014) Integration of Cultivar Resistance and Fungicide Application for Control of Wheat Stripe Rust. Canadian Journal of Plant Pathology, 36, 311-326. http://dx.doi.org/10.1080/07060661.2014.924560
Flor, H.H. (1971) Current Status of the Gene-for-Gene Concept. Annual Review of Phytopathology, 9, 275-296. http://dx.doi.org/10.1146/annurev.py.09.090171.001423
Laugé, R. and De Wit, J.G.M. (1998) Fungal Avirulence Genes: Structure and Possible Functions. Fungal Genetics and Biology, 24, 285-297. http://dx.doi.org/10.1006/fgbi.1998.1076
Kamoun, S. (2007) Groovy Times: Filamentous Pathogen Effectors Revealed. Current Opinion in Plant Biology, 10, 358-365. http://dx.doi.org/10.1016/j.pbi.2007.04.017
Catanzariti, A.M., Dodds, P.N., Lawrence, G.J., Ayliffe, M.A. and Ellis, J.G. (2006) Haustorially Expressed Secreted Proteins from Flax Rust are Highly Enriched for Avirulence Elicitors. The Plant Cell, 18, 243-256. http://dx.doi.org/10.1105/tpc.105.035980
Nirmala, J., Drader, T., Lawrence, P.K., Yin, C., Hulbert, S., Steber, C.M., Steffenson, B.J., Szabo, L.J., Wettstein, D. and Kleinhofs, A. (2011) Concerted Action of Two Avirulent Spore Effectors Activates Reaction to Puccinia graminis1 (Rpg1)-Mediated Cereal Stem Rust Resistance. Proceedings of the National Academy of Sciences, 108, 14676-14681. http://dx.doi.org/10.1073/pnas.1111771108
Chen, X.M. (2013) High Temperature Adult-Plant Resistance, Key for Sustainable Control of Stripe Rust. American Journal of Plant Sciences, 4, 608-627. http://dx.doi.org/10.4236/ajps.2013.43080
Huang, X.L., Chen, X.M., Coram, T., Wang, M.N. and Kang, Z.S. (2011) Gene Expression Profiling of Puccinia striiformis f. sp. tritici during Development Reveals a Highly Dynamic Transcriptome. Journal of Genetics and Genomics, 38, 357-371. http://www.sciencedirect.com/science/article/pii/S1673852711001275
Cantu, D., Segovia, V., MacLean, D., Bayles, R., Chen, X.M. Kamoun, S., Dubcovsky, J., Saunders, D.G. and Uauy, C. (2013) Genome Analyses of the Wheat Yellow (Stripe) Rust Pathogen Puccinia striiformis f. sp. tritici Reveal Polymorphic and Haustorial Expressed Secreted Proteins as Candidate Effectors. BMC Genomics, 14, 270. http://dx.doi.org/10.1186/1471-2164-14-270
Zhang, Y., Qu, Z., Zheng, W., Liu, B., Wang, X., Xue, X., Xu, L., Huang, L., Han, Q., Zhao, J. and Kang, Z. (2008) Stage-Specific Gene Expression During Urediniospore Germination in Puccinia striiformis f. sp. tritici. BMC Genomics, 9, 203. http://dx.doi.org/10.1186/1471-2164-9-203
Yin, C.T., Chen, X.M., Wang, X.J., Han Q.M., Kang, Z.S. and Hulbert, S. (2009) Generation and Analysis of Expression Sequence Tags from Haustoria of the Wheat Stripe Rust Fungus Puccinia striiformis f. sp. tritici. BMC Genomics, 10, 626. http://dx.doi.org/10.1186/1471-2164-10-626
Wan, A.M. and Chen, X.M. (2014) Virulence Characterization of Puccinia striiformis f. sp. tritici Using a New Set of Yr Singlegene Line Differentials in the United States in 2010. Plant Disease, 98, 1534-1542. http://dx.doi.org/10.1094/PDIS-01-14-0071-RE
Line, R.F. and Qayoum, A. (1992) Virulence, Aggressiveness, Evolution, and Distribution of Races of Puccinia striiformis (the Cause of Stripe Rust of Wheat) in North America, 1968-87. Technical Bulletin Number 1788. United States Department of Agriculture, Agricultural Research Service, Washington DC.
Chen, X.M, Line, R.F. and Leung, H. (1993) Relationship between Virulence Variation and DNA Polymorphism in Puccinia striiformis. Phytopathology, 83, 1489-1497. http://dx.doi.org/10.1094/Phyto-83-1489
Lipka, A.E., Tian, F., Wang, Q., Peiffer, J., Li, M., Bradbury, P.J., Gore, M.A., Buckler, E. and Zhang, Z. (2012) GAPIT: Genome Association and Prediction Integrated Tool. Bioinformatics, 28, 2397-2399. http://dx.doi.org/10.1093/bioinformatics/bts444
Benjamini, Y. and Hochberg, Y. (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society, 57, 289-300.
Newmark, P.A. and Boswell, R.E. (1994) The Mago Nashi Locus Encodes an Essential Product Required for Germ Plasm Assembly in Drosophila. Development, 120, 1303-1313.
Venugopal, S.C., Chanda, B., Vaillancourt, L., Kachroo, A. and Kachroo, P. (2009) The Common Metabolite Glycerol-3-Phosphate Is a Novel Regulator of Plant Defense Signaling. Plant Signaling & Behavior, 4, 746-749. http://dx.doi.org/10.4161/psb.4.8.9111
Achsel, T., Brahms, H., Kastner, B., Bachi, A., Wilm, M. and Luhrmann, R. (1999) A Doughnut-Shaped Heteromer of Human Sm-Like Proteins Binds to the 3’-End of U6 snRNA, Thereby Facilitating U4/U6 Duplex Formation in Vitro. The EMBO Journal, 18, 5789-5802. http://dx.doi.org/10.1093/emboj/18.20.5789
Thevelein, J.M. (1984) Regulation of Trehalose Mobilization in Fungi. Microbiological Reviews, 48, 42-59.
Mulichak, A.M., Bonin, C.P., Reiter, W.D. and Garavito, R.M. (2002) Structure of the MUR1 GDP-Mannose 4,6-Dehydratase from Arabidopsis thaliana: Implications for Ligand Binding and Specificity. Biochemistry, 41, 15578-15589. http://dx.doi.org/10.1021/bi0266683
Klune, J.R., Dhupar, R., Cardinal, J., Billiar, T.R. and Tsung, A. (2008) HMGB1: Endogenous Danger Signaling. Molecular Medicine, 14, 476-484.
Bhasin, M., Reinherz, E.L. and Reche, P.A. (2006) Recognition and Classification of Histones Using Support Vector Machine. Journal of Computational Biology, 13, 102-112. http://dx.doi.org/10.1089/cmb.2006.13.102
Maher, B. (2008) Personal Genomes: The Case of the Missing Heritability. Nature, 456, 18-21. http://dx.doi.org/10.1038/456018a
Witte, J.S. (2010) Genome-Wide Association Studies and Beyond. Annual Review of Public Health, 31, 9-20. http://dx.doi.org/10.1146/annurev.publhealth.012809.103723
Brachi, B., Morris, G.P. and Borevitz, J.O. (2011) Genome-Wide Association Studies in Plants: The Missing Heritability Is in the Field. Genome Biology, 12, 232. http://dx.doi.org/10.1186/gb-2011-12-10-232
Wang, W.Y.S., Barratt, B.J., Clayton, D.G. and Todd, J.A. (2005) Genome-Wide Association Studies: Theoretical and Practical Concerns. Nature Review of Genetics, 6, 109-118. http://dx.doi.org/10.1038/nrg1522
Joosten, M.H.A.J., Cozijnsen, T.J. and De Wit, P.J.G.M. (1994) Host Resistance to a Fungal Tomato Pathogen Lost by a Single Base-Pair Change in an Avirulence Gene. Nature, 367, 384-386. http://dx.doi.org/10.1038/367384a0
Hirschhorn, J.N. and Daly, M.J. (2005) Genome-Wide Association Studies for Common Diseases and Complex Traits. Nature Review of Genetics, 6, 95-108. http://dx.doi.org/10.1038/nrg1521
Flint-Garcia, S.A., Thornsberry, J.M. and Buckler IV, E.S. (2003) Struc-ture of Linkage Disequilibrium in Plants. Annual Review of Plant Biology, 54, 357-374. http://dx.doi.org/10.1146/annurev.arplant.54.031902.134907
Pearson, T.A. and Manolio, T.A. (2008) How to Interpret a Genome-Wide Association Study. The Journal of the American Medical Association, 299, 1335-1344. http://dx.doi.org/10.1001/jama.299.11.1335
McMullen, M.D., Kresovich, S., Villeda, H.S., Bradbury, P., Li, H., Sun, Q., Flint-Garcia, S., Thornsberry, J., Acharya, C., Bottoms, C., Brown, P., et al. (2009) Genetic Properties of the Maize Nested Association Mapping Population. Science, 325, 737-740. http://dx.doi.org/10.1126/science.1174320
Chanock, S.J., Manolio, T., Boehnke, M., Boerwinkle, E., Hunter, D.J., Thomas, G., Hirschhorn, J.N., Abecasis, G., Altshuler, D., Bailey-Wilson, J.E., et al., NCI-NHGRI Working Group on Replication in Association Studies (2007) Replicating Genotype-Phenotype Associations. Nature, 447, 655-660. http://dx.doi.org/10.1038/447655a
Yoshida, K., Saitoh, H., Fujisawa, S., Kanzaki, H., Matsumura, H., Yoshida, K., Tosa, Y., Chuma, I., Takano, Y., Win, J., Kamoun, S. and Terauchi, R. (2009) Association Genetics Reveals Three Novel Avirulence Genes from the Rice Blast Fungal Pathogen Magnaporthe oryzae. The Plant Cell, 21, 1573-1591. http://dx.doi.org/10.1105/tpc.109.066324
Jin, Y., Szabo, L. and Carson, M. (2010) Century-Old Mystery of Puccinia striiformis Life History Solved with the Identification of Berberis spp. as an Alternate Host. Phytopathology, 100, 432-435. http://dx.doi.org/10.1094/PHYTO-100-5-0432
Wang, M.N. and Chen, X.M. (2013) 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, 97, 839. http://dx.doi.org/10.1094/PDIS-09-12-0864-PDN
Wang, M.N. and Chen, X.M. (2015) Barberry Does Not Function as an Alternate Host for Puccinia striiformis f. sp. tritici in the US Pacific Northwest Due to Teliospore Degradation and Barberry Phenology. Plant Disease, 99, 1500-1506. http://dx.doi.org/10.1094/PDIS-12-14-1280-RE