Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

A new 2DS·2RL Robertsonian translocation transfers stem rust resistance gene Sr59 into wheat

Abstract

Key message

A new stem rust resistance gene Sr59 from Secale cereale was introgressed into wheat as a 2DS·2RL Robertsonian translocation.

Abstract

Emerging new races of the wheat stem rust pathogen (Puccinia graminis f. sp. tritici), from Africa threaten global wheat (Triticum aestivum L.) production. To broaden the resistance spectrum of wheat to these widely virulent African races, additional resistance genes must be identified from all possible gene pools. From the screening of a collection of wheat–rye (Secale cereale L.) chromosome substitution lines developed at the Swedish University of Agricultural Sciences, we described the line ‘SLU238’ 2R (2D) as possessing resistance to many races of P. graminis f. sp. tritici, including the widely virulent race TTKSK (isolate synonym Ug99) from Africa. The breakage-fusion mechanism of univalent chromosomes was used to produce a new Robertsonian translocation: T2DS·2RL. Molecular marker analysis and stem rust seedling assays at multiple generations confirmed that the stem rust resistance from ‘SLU238’ is present on the rye chromosome arm 2RL. Line TA5094 (#101) was derived from ‘SLU238’ and was found to be homozygous for the T2DS·2RL translocation. The stem rust resistance gene on chromosome 2RL arm was designated as Sr59. Although introgressions of rye chromosome arms into wheat have most often been facilitated by irradiation, this study highlights the utility of the breakage-fusion mechanism for rye chromatin introgression. Sr59 provides an additional asset for wheat improvement to mitigate yield losses caused by stem rust.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Bedbrook JR, Jones J, O’Dell M, Thompson RD, Flavell RB (1980) A molecular description of telomeric heterochromatin in Secale species. Cell 19:545–560

  2. Cainong JC, Zavatsky LE, Chen MS, Johnson J, Friebe B, Gill BS, Lukaszewski AJ (2010) Wheat-rye T2BS·2BL-2RL recombinants with resistance to Hessian fly. Crop Sci 50:920–925

  3. Danilova TV, Friebe B, Gill BS (2012) Single-copy gene fluorescence in situ hybridization and genome analysis: Acc-2 loci mark evolutionary chromosomal rearrangements in wheat. Chromosoma 121:597–611

  4. Devos K, Atkinson MD, Chinoy CN, Francis HA, Harcourt RL, Koebner RMD, Liu CJ, Masojć P, Xie DX, Gale MD (1993) Chromosomal rearrangements in the rye genome relative to that of wheat. Theor Appl Genet 85:673–680

  5. 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

  6. Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19:1349

  7. Evanega SD, Singh RP, Coffman R, Pumphrey MO (2014) The Borlaug Global Rust Initiative: reducing the genetic vulnerability of wheat to rust. In: Tuberosa R, Graner A, Frison E (eds) Genomics of plant genetic resources. Springer, Netherlands, pp 317–331

  8. Francki MG (2001) Identification of Bilby, a diverged centromeric Ty1-copia retrotransposon family from cereal rye (Secale cereale L.). Genome 44:266–274

  9. Friebe B, Hatchett JH, Sears RG, Gill BS (1990) Transfer of Hessian fly resistance from ‘Chaupon’ rye to hexaploid wheat via a 2BS/2RL wheat-rye chromosome translocation. Theor Appl Genet 79:385–389

  10. 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

  11. Friebe B, Zhang P, Linc G, Gill BS (2005) Robertsonian translocations in wheat arise by centric misdivision of univalents at anaphase I and rejoining of broken centromeres during interkinesis of meiosis II. Cytogenet Genome Res 109:293–297

  12. González-García M, Cuacos M, González-Sánchez M, Puertas MJ, Vega JM (2011) Painting the rye genome with genome-specific sequences. Genome 54:555–564

  13. Haseneyer G, Schmutzer T, Seidel M, Zhou R, Mascher M, Schon C-C, Taudien S, Scholz U, Stein N, Mayer K, Bauer E (2011) From RNA-seq to large-scale genotyping—genomics resources for rye (Secale cereale L.). BMC Plant Biol 11:1–13

  14. Hysing SC, Hsam SLK, Singh RP, Huerta-Espino J, Boyd LA, Koebner R, Cambron KS, Johnson JW, Bland DE, Liljeroth E, Merker A (2007) Agronomic performance and multiple disease resistance in T2BS.2RL wheat-rye translocation lines. Crop Sci 47:254–260

  15. International Wheat Genome Sequencing Consortium (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:286–291

  16. Jin Y, Szabo LJ, Pretorius ZA, Singh RP, Ward R, Fetch T (2008) Detection of virulence to resistance gene Sr24 within race TTKS of Puccinia graminis f. sp. tritici. Plant Dis 92:923–926

  17. Jin Y, Szabo LJ, Rouse MN, Fetch T, 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

  18. Johansson E, Malik AH, Hussain A, Rasheed F, Newson WR, Plivelic T, Hedenqvist MS, Gällstedt M, Kuktaite R (2013) Wheat gluten polymer structures: The impact of genotype, environment, and processing on their functionality in various applications. Cereal Chem J 90:367–376

  19. Kato A, Albert PS, Vega JM, Birchler JA (2006) Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotech Histochem 81:71–78

  20. Khlestkina E, Than M, Pestsova E, Röder M, Malyshev S, Korzun V, Börner A (2004) Mapping of 99 new microsatellite-derived loci in rye (Secale cereale L.) including 39 expressed sequence tags. Theor Appl Genet 109:725–732

  21. 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 Genes Genomes Genetics 2:665–673

  22. Kole C (2011) Wild crop relatives: Genomic and breeding resources. Springer-Verlag, Berlin Heidelberg

  23. Lapitan NLV, Sears RG, Rayburn AL, Gill BS (1986) Wheat-rye translocations: detection of chromosome breakpoints by in situ hybridization with a biotin-labeled DNA probe. J Hered 77:415–419

  24. Lei M-P, Li G-R, Zhou L, Li C-H, Liu C, Yang Z-J (2013) Identification of wheat-Secale africanum chromosome 2Rafr introgression lines with novel disease resistance and agronomic characteristics. Euphytica 194:197–205

  25. Li J, Takashi RE, Mika S, Goro I, Toshiki N, Shuhei N (2013) Homoeologous relationship of rye chromosome arms as detected with wheat PLUG markers. Chromosoma 122:555–564

  26. Liu S, Yu L-X, Singh R, Jin Y, Sorrells M, Anderson J (2010) Diagnostic and co-dominant PCR markers for wheat stem rust resistance genes Sr25 and Sr26. Theor Appl Genet 120:691–697

  27. Liu W, Jin Y, Rouse M, Friebe B, Gill B, Pumphrey M (2011a) Development and characterization of wheat-Ae. searsii Robertsonian translocations and a recombinant chromosome conferring resistance to stem rust. Theor Appl Genet 122:1537–1545

  28. Liu W, Rouse M, Friebe B, Jin Y, Gill B, Pumphrey M (2011b) 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

  29. Liu W, Danilova T, Rouse M, Bowden R, Friebe B, Gill B, Pumphrey M (2013) Development and characterization of a compensating wheat-Thinopyrum intermedium Robertsonian translocation with Sr44 resistance to stem rust (Ug99). Theor Appl Genet 126:1167–1177

  30. Lukaszewski AJ (2000) Manipulation of the 1RS.1BL translocation in wheat by induced homoeologous recombination. Crop Sci 40:216–225

  31. Mago R, Spielmeyer W, Lawrence G, Lagudah E, Ellis J, Pryor A (2002) Identification and mapping of molecular markers linked to rust resistance genes located on chromosome 1RS of rye using wheat-rye translocation lines. Theor Appl Genet 104:1317–1324

  32. Mago R, Spielmeyer W, Lawrence GJ, Ellis JG, Pryor AJ (2004) Resistance genes for rye stem rust (SrR) and barley powdery mildew (Mla) are located in syntenic regions on short arm of chromosome. Genome 47:112–121

  33. Mago R, Bariana HS, Dundas IS, Spielmeyer W, Lawrence GJ, Pryor AJ, Ellis JG (2005a) 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

  34. Mago R, Miah H, Lawrence GJ, Wellings CR, Spielmeyer W, Bariana HS, McIntosh RA, Pryor AJ, Ellis JG (2005b) High-resolution mapping and mutation analysis separate the rust resistance genes Sr31, Lr26 and Yr9 on the short arm of rye chromosome 1. Theor Appl Genet 112:41–50

  35. Mago R, Verlin D, Zhang P, Bansal U, Bariana H, Jin Y, Ellis J, Hoxha S, Dundas I (2013) Development of wheat–Aegilops speltoides recombinants and simple PCR-based markers for Sr32 and a new stem rust resistance gene on the 2S#1 chromosome. Theor Appl Genet 126:2943–2955

  36. Mago R, Zhang P, Vautrin S, Šimková H, Bansal U, Luo M-C, Rouse M, Karaoglu H, Periyannan S, Kolmer J, Jin Y, Ayliffe MA, Bariana H, Park RF, McIntosh R, Doležel J, Bergès H, Spielmeyer W, Lagudah ES, Ellis JG, Dodds PN (2015) The wheat Sr50 gene reveals rich diversity at a cereal disease resistance locus. Nat Plants 1:15186

  37. Marais GF, Marais AS (1994) The derivation of compensating translocations involving homoeologous group 3 chromosomes of wheat and rye. Euphytica 79:75–80

  38. Martis MM, Zhou R, Haseneyer G, Schmutzer T, Vrána J, Kubaláková M, König S, Kugler KG, Scholz U, Hackauf B, Korzun V, Schön C-C, Doležel J, Bauer E, Mayer KFX, Stein N (2013) Reticulate evolution of the rye genome. Plant Cell 25:3685–3698

  39. McIntosh RA, Friebe B, Jiang J, The D, Gill BS (1995) Cytogenetical studies in wheat XVI. Chromosome location of a new gene for resistance to leaf rust in a Japanese wheat-rye translocation line. Euphytica 82:141–147

  40. Merker A (1984) The rye genome in wheat breeding. Hereditas 100:183–191

  41. Mujeeb-Kazi A, Kazi AG, Dundas I, Rasheed A, Ogbonnaya F, Kishii M, Bonnett D, Wang RRC, Xu S, Chen P, Mahmood T, Bux H, Farrakh S (2013) Genetic diversity for wheat improvement as a conduit to food security. In: Donald LS (ed) Advances in agronomy. Academic Press, Burlington, pp 179–257

  42. 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

  43. Niu Z, Klindworth DL, Yu G, Friesen TL, Chao S, Jin Y, Cai X, Ohm JB, Rasmussen JB, Xu S (2014) Development and characterization of wheat lines carrying stem rust resistance gene Sr43 derived from Thinopyrum ponticum. Theor Appl Genet 127:969–980

  44. Olivera PD, Jin Y, Rouse M, Badebo A, Fetch T, Singh RP, Yahyaoui A (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

  45. Olivera PD, Pretorius ZA, Badebo A, Jin Y (2013) Identification of resistance to races of Puccinia graminis f. sp. tritici with broad virulence in Triticale (×Triticosecale). Plant Dis 97:479–484

  46. Olivera P, Newcomb M, Szabo LJ, Rouse M, Johnson J, Gale S, Luster DG, Hodson D, Cox JA, Burgin L, Hort M, Gilligan CA, Patpour M, Justesen AF, Hovmøller MS, Woldeab G, Hailu E, Hundie B, Tadesse K, Pumphrey M, Singh RP, Jin Y (2015) Phenotypic and genotypic characterization of race TKTTF of Puccinia graminis f. sp. tritici that caused a wheat stem rust epidemic in southern Ethiopia in 2013–14. Phytopathology 105:917–928

  47. Patpour M, Hovmoller M, Shahin A, Newcomb M, Olivera Firpo PD, Jin Y, Luster DG, Hodson D, Nazari K, Azab M (2015a) First report of the Ug99 race group of wheat stem rust, Puccinia graminis f. sp. tritici, in Egypt in 2014. Plant Dis 92:923

  48. Patpour M, Hovmøller MS, Justesen AF, Newcomb M, Olivera P, Jin Y, Szabo LJ, Hodson D, Shahin AA, Wanyera R, Habarurema I, Wobibi S (2015b) Emergence of virulence to SrTmp in the Ug99 race group of wheat stem rust, Puccinia graminis f. sp. tritici, in Africa. Plant Dis 100:522

  49. 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

  50. 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

  51. Rahmatov M, Rouse MN, Steffenson B, Andersson S, Wanyera R, Pretorius ZA, Houben A, Nazari K, Bhavani S, Johansson E (2016) Sources of stem rust resistance in wheat-alien introgression lines. Plant Dis. doi:10.1094/PDIS-12-15-1448-RE

  52. Riley R, Chapman V (1958) Genetic control of the cytologically diploid behaviour of hexaploid wheat. Nature 182:713–715

  53. Roberts MA, Reader SM, Dalgliesh C, Miller TE, Foote TN, Fish LJ, Snape JW, Moore G (1999) Induction and characterization of Ph1 wheat mutants. Genetics 153:1909–1918

  54. Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier M-H, Leroy P, Ganal MW (1998) A microsatellite map of wheat. Genetics 149:2007–2023

  55. Rouse MN, Wanyera R, Njau P, Jin Y (2011) Sources of resistance to stem rust race Ug99 in spring wheat germplasm. Plant Dis 95:762–766

  56. Rouse M, Nirmala J, Jin Y, Chao S, Fetch T Jr, Pretorius Z, Hiebert C (2014) Characterization of Sr9 h, a wheat stem rust resistance allele effective to Ug99. Theor Appl Genet 127:1681–1688

  57. Saal B, Wricke G (1999) Development of simple sequence repeat markers in rye (Secale cereale L.). Genome 42:964–972

  58. Schlegel RHJ (2014) Rye genetics breeding and cultivation. Taylor and Francis Group, LLC CRC Press is an imprint of Taylor and Francis Group, an Informa business

  59. Sears ER (1977) An induced mutant with homoeologous pairing in common wheat. Can J Genet Cytol 19:585–593

  60. Singh RP, 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

  61. Singh RP, Hodson DP, Jin Y, Lagudah ES, Ayliffe MA, Bhavani S, Rouse MN, Pretorius ZA, Szabo LJ, Huerta-Espino J, Basnet BR, Lan C, Hovmøller MS (2015) Emergence and spread of new races of wheat stem rust fungus: continued threat to food security and prospects of genetic control. Phytopathology 105:872–884

  62. Somers D, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114

  63. Stakman EC, Stewart DM, Loegering WQ (1962) Identification of physiologic races of Puccinia graminis var. tritici. United States Department of Agriculture, Agricultural Research Service, Beltsville, MD E-617

  64. Szabo L, Cuomo C, Park R (2014) Puccinia graminis. In: Dean RA, Lichens-Park A, Kole C (eds) Genomics of plant-associated fungi: monocot pathogens. Springer, Berlin Heidelberg, pp 177–196

  65. The TT, Gupta RB, Dyck PL, Appels R, Hohmann U, McIntosh RA (1991) Characterization of stem rust resistant derivatives of wheat cultivar Amigo. Euphytica 58:245–252

  66. Xu H, Yin D, Li L, Wang Q, Li X, Yang X, Liu W, An D (2012) Development and application of EST-based markers specific for chromosome arms of rye (Secale cereale L.). Cytogenetic and Genome Res 136:220–228

Download references

Acknowledgments

Mahbubjon Rahmatov was supported through Monsanto’s Beachell-Borlaug International Fellowship and the Swedish University of Agricultural Sciences. We also acknowledge support from the Lieberman-Okinow Endowment at the University of Minnesota (Brian Steffenson), the Durable Rust Resistance in Wheat Project administrated through Cornell University and supported by the Bill and Melinda Gates Foundation and UK Department for International Development (Matthew Rouse and Brian Steffenson); USDA-ARS Appropriated Project 5062-21220-021-00 (Matthew Rouse), and USDA-ARS National Plant Disease Recovery System (Matthew Rouse). We thank Sam Stoxen and Matthew Martin for their technical assistance, and Dr. Viktor Korzun and Dr. Marion Röder for providing the Xrems and Xgwm rye markers. Mention of trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the USDA, and does not imply its approval to the exclusion of other products and vendors that might also be suitable.

Author information

Correspondence to Mahbubjon Rahmatov.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by S S. Xu.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rahmatov, M., Rouse, M.N., Nirmala, J. et al. A new 2DS·2RL Robertsonian translocation transfers stem rust resistance gene Sr59 into wheat. Theor Appl Genet 129, 1383–1392 (2016). https://doi.org/10.1007/s00122-016-2710-6

Download citation

Keywords

  • Simple Sequence Repeat Marker
  • Stem Rust
  • Robertsonian Translocation
  • Stem Rust Resistance
  • Stem Rust Resistance Gene