Abstract
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The shortening of Aegilops speltoides segment did not facilitate recombination between stem rust resistance genes Sr36 and Sr39 . Robustness of marker rwgs28 for marker-assisted selection of Sr39 was demonstrated.
Abstract
Stem rust resistance genes Sr39 and Sr36 were transferred from Aegilops speltoides and Triticum timopheevii, respectively, to chromosome 2B of wheat. Genetic stocks RL6082 and RWG1 carrying Sr39 on a large and a shortened Ae. speltoides segments, respectively, and the Sr36-carrying Australian wheat cultivar Cook were used in this study. This investigation was planned to determine the genetic relationship between these genes. Stem rust tests on F3 populations derived from RL6082/Cook and RWG1/Cook crosses showed tight repulsion linkage between Sr39 and Sr36. The genomic in situ hybridization analysis of heterozygous F3 family from the RWG1/Cook population showed that the translocated segments do not overlap. Meiotic analysis on the F1 plant from RWG1/Cook showed two univalents at the metaphase and anaphase stages in a majority of the cells indicating absence of pairing. Since meiotic pairing has been reported to initiate at the telomere, pairing and recombination may be inhibited due to very little wheat chromatin in the distal end of the chromosome arm 2BS in RWG1. The Sr39-carrying large Ae. speltoides segment transmitted preferentially in the RL6082/Cook F3 population, whereas the Sr36-carrying T. timopheevii segment over-transmitted in the RWG1/Cook cross. Genotyping with the co-dominant Sr39- and Sr36-linked markers rwgs28 and stm773-2, respectively, matched the phenotypic classification of F3 families. The RWG1 allele amplified by rwgs28 was diagnostic for the shortened Ae. speltoides segment and alternate alleles were amplified in 29 Australian cultivars. Marker rwgs28 will be useful in marker-assisted pyramiding of Sr39 with other genes.
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References
Bansal UK, Kazi AG, Singh B, Hare RA, Bariana HS (2014a) Mapping of durable stripe rust resistance in a durum wheat cultivar Wollaroi. Mol Breed 33:51–59
Bansal UK, Wicker T, Keller B, Hayden M, Bariana HS (2014b) Molecular mapping of an adult plant stem rust resistance gene Sr56 in winter wheat cultivar Arina. Theor Appl Genet 127:1441–1448
Bariana HS, Hayden MJ, Ahmed NU, Bell JA, Sharp PJ, McIntosh RA (2001) Mapping of durable adult plant and seedling resistances to stripe rust and stem rust diseases in wheat. Aust J Agric Res 52:1247–1255
Bariana HS, Brown GN, Bansal UK, Miah H, Standen GE, Lu M (2007) Breeding triple rust resistant wheat cultivars for Australia using conventional and marker-assisted selection technologies. Aust J Agric Res 58:576–587
Bernardo AN, Bowden RL, Rouse MN, Newcomb MS, Marshall DS, Bai G (2013) Validation of molecular markers for new stem rust resistance genes in U.S. hard winter wheat. Crop Sci 53:755–764
Brown-Guedira GL, Badaeva ED, Gill BS, Cox TS (1998) Chromosome substitutions of Triticum timopheevii in common wheat and some observations on the evolution of polyploid wheat species. Theor Appl Genet 93:1291–1298
Devos KM, Millan T, Gale MD (1993) Comparative RFLP maps of the homoeologous group-2 chromosomes of wheat, rye and barley. Theor Appl Genet 85:784–792
Dundas IS, Anugrahwati DR, Verlin DC, Park RF, Bariana HS, Mago R, Islam AKMR (2007) New sources of rust resistance from alien species: meliorating linked defects and discovery. Aust J Agric Res 58:545–549
Flemmig EL (2012) Molecular markers to deploy and characterize stem rust resistance in wheat. PhD Thesis, North Carolina State University, USA. http://repository.lib.ncsu.edu/ir/bitstream/1840.16/8947/1/etd.pdf. Accessed 25 Feb 2016
Friebe B, Jiang J, Raupp WJ, McIntosh RA, Gill BS (1996) Characterization of wheat-alien translocations conferring resistance to diseases and pests: current status. Euphytica 91:59–87
Jin Y, Singh RP, Ward RW, Wanyera R, Kinyua M, Njau P, Fetch T Jr, Pretorius ZA, Yahyaoui A (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
Jin Y, Szabo LJ, Rouse MN, Fetch T Jr, Pretorius ZA, Wanyera R, Njau P (2009) Detection of virulence to resistance gene Sr36 within the TTKS race lineage of Puccinia graminis f. sp. tritici. Plant Dis 93:367–370
Joshi LM, Palmer LT (1973) Epidemiology of stem, leaf and stripe rusts of wheat in northern India. Plant Dis Reptr 57:8–12
Kerber ER, Dyck PL (1990) Transfer to hexaploid wheat of linked genes for adult-plant leaf rust and seedling stem rust resistance from an amphiploid of Aegilops speltoides x Triticum monococcum. Genome 33:530–537
Klindworth DL, Niu Z, Chao S, Friesen TL, Jin Y, Faris JD, Cai X, Xu SS (2012) Introgression and characterization of a goatgrass gene for a high level of resistance to Ug99 stem rust in tetraploid wheat. G3 2:665–673
Leonard KJ (2001) Stem rust-future enemy? In stem rust of wheat: from ancient enemy to modern foe. In: Peterson PD (ed). APS Press, St. Paul, pp 119–146
Leonard KJ, Szabo LJ (2005) Pathogen profile: stem rust of small grains and grasses caused by Puccinia graminis. Mol Plant Pathol 6:99–111
Liu W, Rouse M, Friebe B, Jin Y, Gill B, Pumphrey MO (2011) Discovery and molecular mapping of a new gene conferring resistance to stem rust, Sr53, derived from Aegilops geniculata and characterization of spontaneous translocation stocks with reduced alien chromatin. Chromosome Res 19:669–682
Lopez-Vera EE, Nelson S, Singh RP, Basnet BR, Haley SD, Bhavani S, Huerta-Espino J, Xoconostle-Cazares BG, Ruiz-Medrano R, Rouse MN, Singh S (2014) Resistance to stem rust Ug99 in six bread wheat cultivars maps to chromosome 6DS. Theor Appl Genet 127:231–239
Mago R, Zhang P, Bariana HS, Verlin DC, Bansal UK, Ellis JG, Dundas IS (2009) Development of wheat lines carrying stem rust resistance gene Sr39 with reduced Aegilops speltoides chromatin and simple PCR markers for marker-assisted selection. Theor Appl Genet 119:1441–1450
McIntosh RA, Arts CJ (1996) Genetic linkage of the Yr1 and Pm4 genes for stripe rust and powdery mildew resistance in wheat. Euphytica 89:401–403
McIntosh RA, Luig NH (1973) Recombination between genes for reaction to P. graminis at or near the Sr9 locus. In ‘Proc 4th Int Wheat Genetics Symp. In: Sears ER, Sears LMS (eds). Agricultural Experiment Station, University of Missouri, Missouri, pp 425–432
McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: an atlas of resistance genes. CSIRO Publications, Victoria
McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers J, Morris C, Appels R, Xia XC (2013) Catalogue of Gene Symbols for Wheat. 12th International Wheat Genetics Symposium, 8–13 September 2013, Yokohama, Japan
Nagarajan S, Joshi LM (1975) An historical account of wheat rust epidemics in India and their significance. Cereal Rust Bull 3:29–33
Niu Z, Klindworth DL, Friesen TL, Chao S, Jin Y, Cai X, Xu SS (2011) Targeted introgression of a wheat stem rust resistance gene by DNA marker-assisted chromosome engineering. Genetics 187:1011–1021
Olivera PD, Badebo A, Xu SS, Klindworth DL, Jin Y (2012) Resistance to race TTKSK of Puccinia graminis f. sp. tritici in Emmer Wheat. Crop Sci 52:2234–2242
Paillard S, Schnurbusch T, Winzeler M, Messmer M, Sourdille P, Abderhalden O, Keller B, Schachermayr G (2003) An integrative genetic linkage map of winter wheat (Triticum aestivum L.). Theor Appl Genet 107:1235–1242
Park RF (2007) Stem rust of wheat in Australia. Aust J Agric Res 58:558–566
Pretorius ZA, Singh RP, Wagoire WW, Payne TS (2000) Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis 84:203
Qi LL, Pumphrey MO, Friebe B, Zhang P, Qian C, Bowden RL, Rouse MN, Jin Y, Gill BS (2011) A novel Robertsonian translocation event leads to transfer of a stem rust resistance gene (Sr52) effective against race Ug99 from Dasypyrum villosum into bread wheat. Theor Appl Genet 123:159–167
Rees RG (1972) Uredospore movement and observations on the epidemiology of wheat rusts in north-eastern Australia. Aust J Agric Res 23:215–223
Sai Prasad SV, Singh SK, Ambati VD, Prakasha TL, Singh JB, Dubey VG, Kantwa SR, Mishra AN (2014) Introgression of stem rust resistance gene Sr36 into durum wheat back ground using marker assisted backcross breeding. J Wheat Res 6:21–24
Singh RP, Hodson DP, Jin Y, Huerta-Espino J, Kinyua M, Wanyera R, Njau P, Ward RW (2006) Current status, likely migration and strategies to mitigate the threat to wheat production from race Ug99 (TTKS) of stem rust pathogen. CAB Rev Perspect Agric Vet Sci Nutr Nat Res 54:1–13
Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Njau P, Wanyera R, Herrera-Foessel SA, Ward RW (2008) Will stem rust destroy the world’s wheat crop? Adv Agron 98:271–309
Singh PR, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S, Njau P, Herrera-Foessel S, Singh PK, Singh S, Govindan V (2011) The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu Rev Phytopathol 49:465–481
Stakman EC, Harrar JG (1957) Principles of plant pathology. Ronald Press, New York
Tsilo TJ, Jin Y, Anderson JA (2008) Diagnostic microsatellite markers for the detection of stem rust resistance gene Sr36 in diverse genetic backgrounds of wheat. Crop Sci 48:253–261
Watson IA (1981) Wheat and its rust parasites in Australia. In wheat science-today and tomorrow. In: Evans LT, Peacock WJ (eds). Cambridge University Press, London, pp 129–147
Wu S, Pumphrey MO, Bai G (2009) Molecular mapping of stem rust-resistance gene Sr40 in wheat. Crop Sci 49:1681–1686
Xue S, Zhang Z, Lin F, Kong Z, Cao Y, Li C, Yi H, Mei M, Zhu H, Wu J, Xu H, Zhao D, Tian D, Zhang C, Ma Z (2008) A high-density intervarietal map of the wheat genome enriched with markers derived from expressed sequence tags. Theor Appl Genet 117:181–189
Zadoks JC (1963) Epidemiology of wheat rusts in Europe. FAO Plant Prot Bull 13:97–108
Zadoks JC (2008) On the political economy of plant disease epidemics: Capita selecta in historic epidemiology. Academic Publishers, Wageningen
Zaharieva M, Monneveux P, Henry M, Rivoal R, Valkoun J, Nachit MM (2001) Evaluation of a collection of wild wheat relative Aegilops geniculata Roth and identification of potential sources for useful traits. Euphytica 119:33–38
Zhang P, Friebe B, Lukaszewski AJ, Gill BS (2001) The centromere structure in Robertsonian wheat-rye translocation chromosomes indicates that centric breakage-fusion can occur at different positions within the primary constriction. Chromosoma 110:335–344
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The authors are grateful to GRDC Australia and NARO-Uganda for funding this study. We thank Dr Hanif Miah for the excellent technical support.
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Chemayek, B., Bansal, U.K., Qureshi, N. et al. Tight repulsion linkage between Sr36 and Sr39 was revealed by genetic, cytogenetic and molecular analyses. Theor Appl Genet 130, 587–595 (2017). https://doi.org/10.1007/s00122-016-2837-5
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DOI: https://doi.org/10.1007/s00122-016-2837-5