Skip to main content
SpringerLink
Log in

Mapping and characterization of two stem rust resistance genes derived from cultivated emmer wheat accession PI 193883

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Key message

Two stem rust resistance genes identified on chromosome arms 2BL and 6AL of the cultivated emmer wheat accession PI 193883 can be used for protecting modern varieties against Ug99 strains.

Abstract

The wheat research community consistently strives to identify new genes that confer resistance to stem rust caused by the fungal pathogen Puccinia graminis f. sp. tritici Eriks & E. Henn (Pgt). In the current study, our objective was to identify and genetically characterize the stem rust resistance derived from the cultivated emmer accession PI 193883. A recombinant inbred line population developed from a cross between the susceptible durum wheat line Rusty and PI 193883 was genotyped and evaluated for reaction to Pgt races TTKSK, TRTTF, and TMLKC. Two QTLs conferring resistance were identified on chromosome arms 2BL (QSr.fcu-2B) and 6AL (QSr.fcu-6A). The stem rust resistance gene (Sr883-2B) underlying QSr.fcu-2B was recessive, and based on its physical location it is located proximal to the Sr9 region. QSr.fcu-6A was located in the Sr13 region, but PI 193883 is known to carry the susceptible haplotype S4 for Sr13, indicating that the gene underlying QSr.fcu-6A (Sr883-6A) is likely a new allele of Sr13 or a gene residing close to Sr13. Three IWGSC scaffold-based simple sequence repeat (SSR) and two SNP-based semi-thermal asymmetric reverse PCR (STARP) markers were developed for the Sr883-2B region, and one STARP marker was developed for Sr883-6A. Sr883-2B was epistatic to Sr883-6A for reaction to TTKSK and TRTTF, and the two genes had additive effects for TMLKC. These two genes and the markers developed in this research provide additional resources and tools for the improvement in stem rust resistance in durum and common wheat breeding programs.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aoun M, Kolmer JA, Rouse MN, Elias EM, Breiland M, Bulbula WD, Chao S, Acevedo M (2019) Mapping of novel leaf rust and stem rust resistance genes in the Portuguese durum wheat landrace PI 192051. Genes Genom Genet 9:2535–2547

    Google Scholar 

  • Briggs J, Chen SS, Zhang WJ, Nelson S, Dubcovsky J, Rouse MN (2015) Mapping of SrTm4, a recessive stem rust resistance gene from diploid wheat effective to Ug99. Phytopathology 105:1347–1354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fetch T, Zegeye T, Park RF, Hodson D, Wanyera R (2016) Detection of wheat stem rust races TTHSK and PTKTK in the Ug99 race group in Kenya in 2014. Plant Dis 100:1495

    Article  Google Scholar 

  • Jin Y (2005) Races of Puccinia graminis identified in the United States during 2003. Plant Dis 89:1125–1127

    Article  CAS  PubMed  Google Scholar 

  • Jin Y, Singh RP (2006) Resistance in U.S. wheat to recent eastern African isolates of Puccinia graminis f. sp. tritici with virulence to resistance gene Sr31. Plant Dis 90:476–480

    Article  CAS  PubMed  Google Scholar 

  • Jin Y, Szabo LJ, Rouse MN, Fetch T Jr, Pretorius ZA, Wanyera R, Njau P (2009) Detection of virulence to resistance gene Sr36 within race TTKS lineage of Puccinia graminis f. sp. tritici. Plant Dis 93:367–370

    Article  CAS  PubMed  Google Scholar 

  • Joehanes R, Nelson JC (2008) QGene 4.0, an extensible Java QTL-analysis platform. Bioinformatics 24:2788–2789

    Article  CAS  PubMed  Google Scholar 

  • Klindworth DL, Miller JD, Xu SS (2006) Registration of Rusty durum wheat. Crop Sci 46:1012–1013

    Article  Google Scholar 

  • 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. Genes Genomes Genet 2:665–673

    CAS  Google Scholar 

  • Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Long YM, Chao WS, Ma GJ, Xu SS, Qi LL (2017) An innovative SNP genotyping method adapting to multiple platforms and throughputs. Theor Appl Genet 130:597–607

    Article  CAS  PubMed  Google Scholar 

  • Lorieux M (2012) MapDisto: fast and efficient computation of genetic linkage maps. Mol Breeding 30:1231–1235

    Article  CAS  Google Scholar 

  • Martins WS, Soares Lucas DC, de Souza Neves KF, Bertioli DJ (2009) WebSat: a web software for microsatellite marker development. Bioinformation 3:282–283

    Article  PubMed  PubMed Central  Google Scholar 

  • McIntosh RA, Welling CR, Park RF (1995) Wheat rusts: an atlas of resistance genes. CSIRO Australia, Sydney

    Book  Google Scholar 

  • McVey DM, Hamilton K (1985) Stem rust resistance gene from Triumph 64 identified in four other winter wheats. Plant Dis 69:217–218

    Article  Google Scholar 

  • Newcomb M, Olivera PD, Rouse MN, Szabo LJ, Johnson J, Gale S, Luster DG, Wanyera R, Macharia G, Bhavani S, Hodson D, Patpour M, Hovmøller MS, Fetch TG Jr, Jin Y (2016) Kenyan isolates of Puccinia graminis f. sp. tritici from 2008 to 2014: virulence to SrTmp in the Ug99 race group and implications for breeding programs. Phytopathology 106:729–736

    Article  CAS  PubMed  Google Scholar 

  • Olivera Firpo PD, Newcomb M, Flath K, Sommerfeldt-Impe N, Szabo LJ, Carter M, Luster DG, Jin Y (2017) Characterization of Puccinia graminis f. sp. tritici isolates derived from an unusual wheat stem rust outbreak in Germany in 2013. Plant Pathol 66:1258–1266

    Article  Google Scholar 

  • Olivera PD, Jin Y, Rouse M, Badebo A, Fetch T Jr, Singh RP, Yahyaoui A (2012a) 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

    Article  CAS  PubMed  Google Scholar 

  • Olivera PD, Badebo A, Xu SS, Klindworth DL, Jin Y (2012b) Resistance to race TTKSK of Puccinia graminis f. sp. tritici in Emmer wheat. Crop Sci 52:2234–2242

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Olson EL, Brown-Guedira G, Marshall DS, Jin Y, Mergoum M, Lowe I, Dubcovsky J (2010) Genotyping of U.S. wheat germplasm for presence of stem rust resistance genes Sr24, Sr36 and Sr1RS Amigo. Crop Sci 50:668–675

    Article  CAS  Google Scholar 

  • Periyannan SK, Qamar ZU, Bansal UK, Bariana HS (2014) Development and validation of molecular markers linked with stem rust resistance gene Sr13 in durum wheat. Crop Pasture Sci 65:74–79

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Roelfs AP (1978) Estimated losses caused by rust in small grain cereals in the United States 1918–76. United States Department of Agriculture, Agricultural Research Service, Washington DC

    Google Scholar 

  • Roelfs AP, Martens JW (1988) An international system of nomenclature for Puccinia graminis f. sp. tritici. Phytopathology 78:526–533

    Article  Google Scholar 

  • Roelfs AP, McVey DV (1975) Races of Puccinia graminis f. sp. tritici in the U.S.A. during 1974. Plant Dis Report 59:681–685

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rouse MN, Nirmala J, Jin Y, Chao S, Fetch TG Jr, Pretorius ZA, Hiebert CW (2014) Characterization of Sr9h, a wheat stem rust resistance allele effective to Ug99. Theor Appl Genet 127:1681–1688

    Article  CAS  PubMed  Google Scholar 

  • Saari EE, Prescott JM (1985) World distribution in relation to economic losses. In: Roelfs AP, Bushnell WR (eds) The cereal rusts. Diseases, distribution, epidemiology, and control, vol 2. Academic Press, Orlando, pp 259–298

    Chapter  Google Scholar 

  • Saini J, Faris JD, Zhang Q, Rouse MN, Jin Y, Long Y, Klindworth DL, Elias EM, McClean PE, Edwards MC, Xu SS (2018) Identification, mapping, and marker development of stem rust resistance genes in durum wheat ‘Lebsock’. Mol Breed 38:77. https://doi.org/10.1007/s11032-018-0833-y

    Article  CAS  Google Scholar 

  • Sharma JS, Running KLD, Xu SS, Zhang Q, Haugrud ARP, Sharma S, McClean PE, Faris JD (2019) Genetic analysis of threshability and other spike traits in the evolution of cultivated emmer to fully domesticated durum wheat. Mol Genet Genomics 294:757–771

    Article  CAS  PubMed  Google Scholar 

  • Simons K, Abate Z, Chao S, Zhang W, Rouse M, Jin Y, Elias E, Dubcovsky J (2011) Genetic mapping of stem rust resistance gene Sr13 in tetraploid wheat (Triticum turgidum ssp. durum L.). Theor Appl Genet 122:649–658

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Spielmeyer W, Sharp PJ, Lagudah ES (2003) Identification and validation of markers linked to broad-spectrum stem rust resistance gene Sr2 in wheat (Triticum aestivum L.). Crop Sci 43:333–336

    CAS  Google Scholar 

  • Stakman EC, Stewart DM, Loegering WQ (1962) Identification of physiologic races of Puccinia graminis var. tritici. USDA ARS E-617. U.S. Gov. Print. Off., Washington

    Google Scholar 

  • Wessels E, Prins R, Boshoff WHP, Zurn JD, Acevedo M, Pretorius ZA (2019) Mapping a resistance gene to Puccinia graminis f. sp. tritici in the bread wheat cultivar ‘Matlabas’. Plant Dis. https://doi.org/10.1094/PDIS-10-18-1731-RE

    Article  PubMed  Google Scholar 

  • Williams ND, Miller JD, Klindworth DL (1992) Induced mutations of a genetic suppressor of resistance to wheat stem rust. Crop Sci 32:612–616

    Article  Google Scholar 

  • You FM, Huo N, Gu YQ, Luo M-C, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformatics 9:253. https://doi.org/10.1186/1471-2105-9-253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Bowden RL, Yu J, Carver BF, Bai G (2014) Association analysis of stem rust resistance in US winter wheat. PLoS One 9:e103747. https://doi.org/10.1371/journal.pone.0103747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Chen S, Abate Z, Nirmala J, Rouse MN, Dubcovsky JD (2017) Identification and characterization of Sr13, a tetraploid wheat gene that confers resistance to the Ug99 stem rust race group. Proc Natl Acad Sci USA 114:E9483–E9492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zurn JD, Newcomb M, Rouse MN, Jin Y, Chao S, Sthapit J, See DR, Wanyera R, Njau P, Bonman JM, Brueggeman R, Acevedo M (2014) High-density mapping of a resistance gene to Ug99 from the Iranian landrace PI 626573. Mol Breed 34:871–881

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Shiaoman Chao and Mary Osenga, at the USDA-ARS Small Grains Genotyping Lab at Fargo, ND, for assistance in genotyping the mapping population using the wheat 90 K SNP iSelect assays and Danielle Holmes for technical support in stem rust evaluations. This research was supported in part by funds to S. S. X. and M. N. R. provided through grants from the Bill & Melinda Gates Foundation and UK Department for International Development to Cornell University for the Durable Rust Resistance in Wheat (DRRW) and Delivering Genetic Gain in Wheat (DGGW) Projects. It was also funded by the US Department of Agriculture–Agriculture Research Service (USDA-ARS) Current Research Information System (CRIS) Projects Nos. 3060-21000-038-00D and 5062-21220-023-00-D.

Author information

Authors and Affiliations

  1. Department of Plant Sciences, North Dakota State University, Fargo, ND, 58108, USA

    Jyoti S. Sharma, Qijun Zhang, Yunming Long & Phillip E. McClean

  2. USDA-ARS, Cereal Disease Laboratory and Department of Plant Pathology, University of Minnesota, St. Paul, MN, 55108, USA

    Matthew N. Rouse & Yue Jin

  3. USDA-ARS, Cereal Crops Research Unit, Edward T. Schafer Agricultural Research Center, 1616 Albrecht Blvd. North, Fargo, ND, 58102-2765, USA

    Daryl L. Klindworth, Timothy L. Friesen, Steven S. Xu & Justin D. Faris

  4. Department of Plant Pathology, University of Minnesota, St. Paul, MN, 55108, USA

    Pablo D. Olivera

  5. Morden Research and Development Centre, Agriculture and Agri-Food Canada, 100, Morden, MB, R6M 1Y5, Canada

    Jyoti S. Sharma

Authors
  1. Jyoti S. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qijun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew N. Rouse
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daryl L. Klindworth
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Timothy L. Friesen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yunming Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pablo D. Olivera
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yue Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Phillip E. McClean
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Steven S. Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Justin D. Faris
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JF, SX, MR, YJ, and PO initiated the study and designed the experiment. QZ, DK, and SX developed the mapping populations. JS, DK, and TF conducted stem rust test using TMLKC and other North American races. MR, PO, and YJ conducted the stem rust tests using TTKSK and TRTTF. JS, YL, JF, and SX developed STARP and SSR markers. JS, PM, and JF conducted linkage analysis of stem rust resistance. JS and JF wrote the manuscript, and all authors contributed to the final version.

Corresponding author

Correspondence to Justin D. Faris.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical standards

The experiments were performed in compliment with the current laws of the United States of America.

Additional information

Communicated by Thomas Miedaner.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Disclaimer: Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharma, J.S., Zhang, Q., Rouse, M.N. et al. Mapping and characterization of two stem rust resistance genes derived from cultivated emmer wheat accession PI 193883. Theor Appl Genet 132, 3177–3189 (2019). https://doi.org/10.1007/s00122-019-03417-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-019-03417-x

Search

Navigation