Association mapping reveals novel stem rust resistance loci in durum wheat at the seedling stage

Plant Genome

Volumn 7, Issue 1, 2014, Pages

  Letta, Tesfaye ^a,e   Olivera, Pablo ^b   Maccaferri, Marco ^a   Jin, Yue ^b   Ammar, Karim ^c   Badebo, Ayele ^d   Salvi, Silvio ^a   Noli, Enrico ^a   Crossa, Jose ^c   Tuberosa, Roberto ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b USDA Agricultural Research Service Cereal Disease Laboratory   (United States)

^c INTERNATIONAL MAIZE AND WHEAT IMPROVEMENT CENTER CIMMYT   (Mexico)

^d DEBRE ZEIT AGRICULTURAL RESEARCH CENTER   (Ethiopia)

^e Sinana Agricultural Research Center   (Ethiopia)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84897412108     PISSN: None     EISSN: 19403372     Source Type: Journal    
DOI: 10.3835/plantgenome2013.08.0026     Document Type: Article

References (68)

1. Adhikari, T. B., S. Gurung, J. M. Hansen, E. W. Jackson, and J. M. Bonman. 2012. Association mapping of quantitative trait loci in spring wheat landraces conferring resistance to bacterial leaf streak and spot blotch. Plant Gen. 5: 1-16. doi: 10. 3835/plantgenome2011. 12. 0032.
2. Admassu, B., and E. Fekadu. 2005. Physiologic races and virulence diversity of Puccinia graminis. f. sp. tritici. on wheat in Ethiopia. Phytopathol. Mediterr. 44: 313-318.
3. Admassu, B., V. Lind, W. Friedt, and F. Ordon. 2009. Virulence analysis of Puccinia graminis. f. sp. tritici. populations in Ethiopia with special consideration of Ug99. Plant Pathol. 58: 362-369. doi: 10. 1111/j. 1365-3059. 2008. 01976. x.
4. Admassu, B., D. Perovic, W. Friedt, and F. Ordon. 2011. Genetic mapping of the stem rust (Puccinia graminis. f. sp. tritici. Eriks. & E. Henn) resistance gene Sr13. in wheat (Triticum aestivum. L.). Theor. Appl. Genet. 122: 643-648. doi: 10. 1007/s00122-010-1433-3.
5. Bansal, U. K., E. Bossolini, H. Miah, B. Keller, R. F. Park, and H. S. Bariana. 2008. Genetic mapping of seedling and adult plant stem rust resistance in two European winter wheat cultivars. Euphytica 164: 821-828. doi: 10. 1007/s10681-008-9736-z.
6. Bhavani, S., R. P. Singh, O. Argillier, J. Huerta-Espino, S. Singh, P. Njau, S. Brun, S. Lacam, and N. Desmouceaux. 2011. Mapping durable adult plant stem rust resistance to the race Ug99 group in six CIMMYT wheats. In: R. A. McIntosh, editor, BGRI 2011 Technical Workshop. Borlaug Global Rust Initiative, St. Paul, MN. p. 43-53.
7. Breseghello, F., and M. E. Sorrells. 2006. Association mapping of kernel size and milling quality in wheat (Triticum aestivum. L.) cultivars. Genetics 172: 1165-1177. doi: 10. 1534/genetics. 105. 044586.
8. Crossa, J., J. Burgueño, S. Dreisigacker, M. Vargas, S. A. Herrera-Foessel, M. Lillemo, R. P. Singh, R. Trethowan, M. Warburton, J. Franco, M. Reynolds, J. H. Crouch, and R. Ortiz. 2007. Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure. Genetics 177: 1889-1913.
9. Dubcovsky, J., F. Ordon, D. Perovic, B. Admassu, W. Friedt, Z. Abate, W. Zhang, and S. Chao. 2011. Conflicting mapping results for stem rust resistance gene Sr13. Theor. Appl. Genet. 122: 659. doi: 10. 1007/s00122-010-1495-2.
10. Eversmeyer, M. G., and C. L. Kramer. 2000. Epidemiology of wheat leaf and stem rust in the central Great Plains of the USA. Annu. Rev. Phytopathol. 38: 491-513. doi: 10. 1146/annurev. phyto. 38. 1. 491.
11. SeedQuest, 2008. Wheat killer detected in Iran-Dangerous fungus on the move from East Africa to the Middle East. SeedQuest News. http://www. seedquest. com/News/releases/2008/march/21996. htm (verified 16 Dec. 2013).
12. Flint-Garcia, S. A., J. M. Thornsberry, and E. S. Buckler. 2003. Structure of linkage disequilibrium in plants. Annu. Rev. Plant Biol. 54: 357-374. doi: 10. 1146/annurev. arplant. 54. 031902. 134907.
13. Gupta, P. K., S. Rustgi, and P. L. Kulwal. 2005. Linkage disequilibrium and association studies in higher plants: Present status and future prospects. Plant Mol. Biol. 57: 461-485. doi: 10. 1007/s11103-005-0257-z.
14. Haile, J. K., K. Hammer, A. Badebo, R. P. Singh, and M. Röder. 2013. Haplotype analysis of molecular markers linked to stem rust resistance genes in Ethiopian improved durum wheat varieties and tetraploid wheat landraces. Genet. Resour. Crop Evol. 60: 853-864. doi: 10. 1007/s10722-012-9880-0.
15. Haile, J. K., M. M. Nachit, K. Hammer, A. Badebo, and M. S. Roder. 2012. QTL mapping of resistance to race Ug99 of Puccinia graminis. f. sp. tritici. in durum wheat (Triticum durum. Desf.). Mol. Breed. 30: 1479-1493. doi: 10. 1007/s11032-012-9734-7.
16. Hall, D., C. Tegstrom, and P. K. Ingvarsson. 2010. Using association mapping to dissect the genetic basis of complex traits in plants. Brief Funct. Genom. 9: 157-165. doi: 10. 1093/bfgp/elp048.
17. Heffner, E. L., M. E. Sorrells, and J. Jannink. 2009. Genomic selection for crop improvement. Crop Sci. 49: 1-12. doi: 10. 2135/cropsci2008. 08. 0512.
18. Hiebert, C. W., T. G. Fetch, and T. Zegeye. 2010. Genetics and mapping of stem rust resistance to Ug99 in the wheat cultivar Webster. Theor. Appl. Genet. 121: 65-69. doi: 10. 1007/s00122-010-1291-z.
19. Ingala, L., M. Lopez, M. Darino, M. F. Pergolesi, M. J. Diequez, and F. Sacco. 2012. Genetic analysis of leaf rust resistance genes and associated markers in the durable resistant wheat cultivar Sinvalocho MA. Theor. Appl. Genet. 124: 1305-1314. doi: 10. 1007/s00122-012-1788-8.
20. Jin, Y., R. P. Singh, R. W. Ward, R. Wanyera, M. Kinyua, P. Njau, and Z. A. Pretorius. 2007. Characterization of seedling infection types and adult plant infection responses of monogenic Sr. gene lines to race TTKS of Puccinia graminis. f. sp. tritici. Plant Dis. 91: 1096-1099. doi: 10. 1094/PDIS-91-9-1096.
21. Jin, Y., L. J. Szabo, Z. A. Pretorius, R. P. Singh, R. Ward, and T. J. R. Fetch. 2008. Detection of virulence to resistance gene Sr24. within race TTKS of Puccinia graminis. f. sp. tritici. Plant Dis. 92: 923-926. doi: 10. 1094/PDIS-92-6-0923.
22. Klindworth, D. L., J. D. Miller, Y. Jin, and S. S. Xu. 2007. Chromosomal locations of genes for stem rust resistance in monogenic lines derived from tetraploid wheat accession ST464. Crop Sci. 47: 1441-1450. doi: 10. 2135/cropsci2006. 05. 0345.
23. Kollers, S., B. Rodemann, J. Ling, V. Korzun, E. Ebmeyer, O. Argillier, M. Hinze, J. Plieske, D. Kulosa, M. W. Ganal, and M. S. Röder. 2013. Whole Genome Association Mapping of Fusarium Head Blight Resistance in European Winter Wheat (Triticum aestivum. L.). PLoS ONE 8(2): e57500. doi: 10. 1371/journal. pone. 0057500.
24. Letta, T., M. Maccaferri, K. Ammar, A. Badebo, A. Ricci, J. Crossa, and R. Tuberosa. 2013. Searching for novel sources of field resistance to Ug99 and Ethiopian stem rust races in durum wheat via association mapping. Theor. Appl. Genet. 126: 1237-1256. doi: 10. 1007/s00122-013-2050-8.
25. Liu, S., L. X. Yu, R. P. Singh, Y. Jin, M. E. Sorrells, and J. A. Anderson. 2010. Diagnostic and co-dominant PCR markers for wheat stem rust resistance genes Sr25. and Sr26. Theor. Appl. Genet. 120: 691-697. doi: 10. 1007/s00122-009-1186-z.
26. Maccaferri, M., M. C. Sanguineti, L. F. G. del Moral, A. Demontis, A. El.-Ahmed, F. Maalouf, H. Machlab, V. Martos, M. Moragues, J. Motawaj, M. Nachit, N. Nserallah, H. Ouabbou, C. Royo, A. Slama, and R. Tuberosa. 2011. Association mapping in durum wheat grown across a broad range of water regimes and yield potential. J. Exp. Bot. 62: 409-438. doi: 10. 1093/jxb/erq287.
27. Maccaferri, M., M. C. Sanguineti, S. Corneti, J. L. A. Ortega, M. Ben Salem, J. Bort, E. De Ambrogio, L. F. G. del Moral, A. Demontis, A. El-Ahmed, F. Maalouf, H. Machlab, V. Martos, M. Moragues, J. Motawaj, M. Nachit, N. Nserallah, H. Ouabbou, C. Royo, A. Slama, and R. Tuberosa. 2008. Quantitative trait loci for grain yield and adaptation of durum wheat (Triticum durum. Desf.) across a wide range of water availability. Genetics 178: 489-511. doi: 10. 1534/genetics. 107. 077297.
28. Maccaferri, M., M. C. Sanguineti, P. Mantovani, A. Demontis, A. Massi, K. Ammar, J. Kolmer, J. Czembor, S. Ezrati, and R. Tuberosa. 2010. Association mapping of leaf rust response in durum wheat. Mol. Breed. 26: 189-228. doi: 10. 1007/s11032-009-9353-0.
29. Maccaferri, M., M. C. Sanguineti, V. Natoli, J. L. A. Ortega, M. Ben Salem, J. Bort, C. Chenenaoui, E. De Ambrogio, L. G. del Moral, A. De Montis, A. El-Ahmed, F. Maalouf, H. Machlab, M. Moragues, J. Motawaj, M. Nachit, N. Nserallah, H. Ouabbou, C. Royo, and R. Tuberosa. 2006. A panel of elite accessions of durum wheat (Triticum durum. Desf.) suitable for association mapping studies. Plant Gen. Res. 4: 79-85. doi: 10. 1079/PGR2006117.
30. Maccaferri, M., M. C. Sanguineti, E. Noli, and R. Tuberosa. 2005. Population structure and long-range linkage disequilibrium in a durum wheat elite collection. Mol. Breed. 15: 271-289. doi: 10. 1007/s11032-004-7012-z.
31. Maccaferri, M., M. C. Sanguineti, C. Xie, J. S. Smith, and R. Tuberosa. 2007. Relationships among durum wheat accessions. II. A comparison of molecular and pedigree information. Genome 50: 385-399. doi: 10. 1139/G07-017.
32. Mago, R., H. S. Bariana, I. S. Dundas, W. Spielmeyer, G. J. Lawrence, A. J. Pryor, and J. G. Ellis. 2005. Development of PCR markers for the selection of wheat stem rust resistance genes Sr24. and Sr26. in diverse wheat germplasm. Theor. Appl. Genet. 111: 496-504. doi: 10. 1007/s00122-005-2039-z.
33. Mago, R., G. Brown-Guedira, S. Dreisigacker, J. Breen, Y. Jin, R. Singh, R. Appels, E. S. Lagudah, J. Ellis, and W. Spielmeyer. 2010. An accurate DNA marker assay for stem rust resistance gene Sr2. in wheat. Theor. Appl. Genet. 122: 735-744. doi: 10. 1007/s00122-010-1482-7.
34. McIntosh, R. A., and G. N. Brown. 1997. Anticipatory breeding for resistance to rust diseases in wheat. Annu. Rev. Phytol. 35: 311-326. doi: 10. 1146/annurev. phyto. 35. 1. 311.
35. McIntosh, R. A., C. R. Wellings, and R. F. Park. 1995. Wheat rusts: An atlas of resistance genes. CSIRO, Canberra, ACT, Australia.
36. Niks, R. E., E. Fernández, B. Van Haperen, B. Bekele Aleye, and F. B. Martínez. 2000. Specificity of QTLs for partial and non-host resistance of barley to leaf rust fungi. Acta Phytopathol. Hun. 35: 13-21.
37. Olivera, P. D., Y. Jin, M. Rouse, A. Badebo, T. Fetch, Jr., R. P. Singh, and A. M. Yahyaoui. 2012. Races of Puccinia graminis. f. sp. tritici. with combined virulence to Sr13. and Sr9e. in a field stem rust screening nursery in Ethiopia. Plant Dis. 96: 623-628. doi: 10. 1094/PDIS-09-11-0793.
38. Pretorius, Z. A., R. P. Singh, W. W. Wagoire, and T. S. Payne. 2000. Detection of virulence to wheat stem rust resistance gene Sr31. in Puccinia graminis. f. sp. tritici. in Uganda. Plant Dis. 84: 203. doi: 10. 1094/PDIS. 2000. 84. 2. 203B.
39. Pretorius, Z. A., L. J. Szabo, W. H. P. Boshoff, L. Herselman, B. Visser. 2012. First report of a new TTKSF race of wheat stem rust (Puccinia graminis f. sp. tritici) in South Africa and Zimbabwe. Plant Dis. 96: 590. doi: 10. 1094/PDIS-12-11-1027-PDN.
40. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
41. Qi, X., G. Jiang, W. Chen, R. E. Niks, P. Stam, and P. Lindhout. 1999. Isolatespecific QTLs for partial resistance to Puccinia hordei. in barley. Theor. Appl. Genet. 99: 877-884. doi: 10. 1007/s001220051308.
42. Rohlf, F. J. 1997. NTSYS-pc v. 2. 0. Exeter Press, East Setauket, NY.
43. Roelfs, A. P., D. L. Long, and J. J. Robert. 1993. Races of Puccinia graminis. in the United States during 1990. Plant Dis. 77: 125-128. doi: 10. 1094/PD-77-0125.
44. Roelfs, A. P., and J. W. Martens. 1988. An international system of nomenclature for Puccinia graminis. f. sp. tritici. Phytopathology 78: 526-533. doi: 10. 1094/Phyto-78-526.
45. Rouse, M. N., I. C. Nava, S. Chao, J. A. Anderson, and Y. Jin. 2012. Identification of markers linked to the race Ug99 effective stem rust resistance gene Sr28. in wheat (Triticum aestivum. L.). Theor. Appl. Genet. 125: 877-885. doi: 10. 1007/s00122-012-1879-6.
46. Rutkoski, J. E., J. Benson, Y. Jia, G. Brown-Guedira, J.-L. Jannink, and M. Sorrells. 2012. Evaluation of genomic prediction methods for Fusarium head blight resistance in wheat. Plant Gen. 5: 51-61. doi: 10. 3835/plantgenome2012. 02. 0001.
47. Rutkoski, J. E., E. L. Heffner, and M. E. Sorrells. 2011. Genomic selection for durable stem rust resistance in wheat. Euphytica 179: 161-173. doi: 10. 1007/s10681-010-0301-1.
48. Simons, K., Z. Abate, S. Chao, W. Zhang, M. Rouse, Y. Jin, E. Elias, and J. Dubcovsky. 2011. Genetic mapping of stem rust resistance gene Sr13. in tetraploid wheat (Triticum turgidum. ssp. durum. L.). Theor. Appl. Genet. 122: 649-658. doi: 10. 1007/s00122-010-1444-0.
49. Singh, R. P., D. P. Hodson, J. Huerta-Espino, Y. Jin, S. Bhavani, P. Njau, S. Herrera-Foessel, P. K. Singh, S. Singh, and V. Govindan. 2011. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu. Rev. Phytopathol. 49: 465-481. doi: 10. 1146/annurevphyto-072910-095423.
50. Singh, R. P., D. P. Hodson, Y. Jin, J. Huerta-Espino, M. G. Kinyua, R. Wanyera, P. Njau, and R. W. Ward. 2006. Current status, likely migration and strategies to mitigate the threat to wheat production from race Ug99 (TTKS) of stem rust pathogen. CAB Rev. 1(54): 1-13.
51. Singh, R. P., J. Huerta-Espino, G. Fuentes, E. Duveiller, L. Gilchrist, M. Henry, M. J. Nicol. 2005. Resistance to diseases. In: C. Royo et al., editors, Durum wheat breeding: Current approaches and future strategies. Food Product Press, Binghamton, NY. p. 291-315.
52. Singh, A., M. P. Pandey, A. K. Singh, R. E. Knox, K. Ammar, J. M. Clarke, F. R. Clarke, R. P. Singh, C. J. Pozniak, R. M. Depauw, B. D. McCallum, R. D. Cuthbert, H. S. Randhawa, and T. G. Fetch. 2013. Identification and mapping of leaf, stem and stripe rust resistance quantitative trait loci and their interactions in durum wheat. Mol. Breed. 31: 405-418. doi: 10. 1007/s11032-012-9798-4.
53. Stakman, E. C., D. M. Steward, and W. Q. Loegering. 1962. Identification of physiologic races of Puccinia graminis. var. tritici. US Dep. Agric. Agric. Res. Serv. E-617.
54. Storey, J. D., and R. Tibshirani. 2003. Statistical significance for genome wide studies. Proc. Natl. Acad. Sci. USA 100: 9440-9445. doi: 10. 1073/pnas. 1530509100.
55. Sukumaran, S., and J. Yu. 2014. Association mapping of genetic resources: Achievements and future perspectives. In: R. Tuberosa, A. Graner, and E. Frison, editors, Genomics of Plant Genetic Resources. Springer, Berlin. p. 207-235.
56. Trebbi, D., M. Maccaferri, P. de Heer, A. Sorensen, S. Giuliani, S. Salvi, M. C. Sanguineti, A. Massi, E. A. G. van der Vossen, and R. Tuberosa. 2011. High-throughput SNP discovery and genotyping in durum wheat (Triticum durum. Desf.). Theor. Appl. Genet. 123: 555-569. doi: 10. 1007/s00122-011-1607-7.
57. Tsilo, T. J., Y. Jin, and J. A. Anderson. 2007. Microsatellite markers linked to stem rust resistance allele Sr9a. in wheat. Crop Sci. 47: 2013-2020. doi: 10. 2135/cropsci2007. 02. 0087.
58. van Poecke, R., M. Maccaferri, J. Tang, H. Truong, A. Janssen, N. van Orsouw, S. Salvi, M. C. Sanguineti, R. Tuberosa, and E. A. G. van der Vossen. 2013. Sequence-based SNP genotyping in durum wheat. Plant Biotechnol. J. 11: 809-817. doi: 10. 1111/pbi. 12072.
59. You, F. M., N. X. Huo, K. R. Deal, Y. Q. Gu, M. C. Luo, P. E. McGuire, J. Dvorak, and O. D. Anderson. 2011. Annotation-based genome-wide SNP discovery in the large and complex Aegilops tauschii. genome using next-generation sequencing without a reference genome sequence. BMC Genomics 12: 59-77. doi: 10. 1186/1471-2164-12-59.
60. Yu, L.-X., Z. Abate, J. A. Anderson, U. K. Bansal, H. S. Bariana, S. Bhavani, J. Dubcovsky, E. S. Lagudah, S. X. Liu, P. K. Sambasivam, R. P. Singh, and M. E. Sorrells. 2009. Developing and optimizing markers for stem rust resistance in wheat. In. Proceedings of 2009 Technical Workshop, Borlaug Global Rust Initiative, Cd. Obregón, Sonora, Mexico. p. 117-130.
61. Yu, L.-X., S. Liu, J. A. Anderson, R. P. Singh, Y. Jin, G. Brown-Guidera, S. Bhavani, A. Morgounov, Z. He, J. Huerta-Espino, and M. E. Sorrells. 2010. Haplotype diversity of stem rust resistance loci in uncharacterized wheat lines. Mol. Breed. 26: 667-680. doi: 10. 1007/s11032-010-9403-7.
62. Yu, L.-X., A. Lorenz, J. Rutkoski, R. P. Singh, S. Bhavani, J. Huerta-Espino, and M. E. Sorrells. 2011. Association mapping and gene-gene interaction for stem rust resistance in CIMMYT spring wheat germplasm. Theor. Appl. Genet. 123: 1257-1268. doi: 10. 1007/s00122-011-1664-y.
63. Yu, L.-X., A. Morgounov, R. Wanyera, M. Keser, S. K. Singh, and M. E. Sorrells. 2012. Identification of Ug99 stem rust resistance loci in winter wheat germplasm using genome-wide association analysis. Theor. Appl. Genet. 125: 749-758. doi: 10. 1007/s00122-012-1867-x.
64. Yu, J. M., G. Pressoir, W. H. Briggs, IV, M. Yamasaki, J. F. Doebley, M. D. McMullen, B. S. Gaut, D. M. Nielsen, J. B. Holland, S. Kresovich, and E. S. Buckler. 2006. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38: 203-208. doi: 10. 1038/ng1702.
65. Zhang, D., G. Bai, C. Zhu, J. Yu, and B. F. Carver. 2010. Genetic diversity, population structure, and linkage disequilibrium in U. S. elite winter wheat. Plant Gen. 3: 117-127. doi: 10. 3835/plantgenome2010. 03. 0004.
66. Zhang, D., R. Bowden, and G. Bai. 2011. A method to linearize Stakman infection type ratings for statistical analysis. In: Proc. of the 2011 Borlaug Global Rust Initiative Technical Workshop, 17-20 June 2011, St. Paul, MN. p. 28.
67. Zhu, C., M. Gore, E. S. Buckler, and J. Yu. 2008. Status and prospects of association mapping in plants. Plant Gen. 1: 5-20. doi: 10. 3835/plantgenome2008. 02. 0089.
68. Zhu, S., K. J. Leonard, and H. F. Kaeppler. 2003. Quantitative trait loci associated with seedling resistance to isolates of Puccinia coronata. in oat. Phytopathology 93: 860-866. doi: 10. 1094/PHYTO. 2003. 93. 7. 860.