Skip to main content
Log in

Lr67/Yr46 confers adult plant resistance to stem rust and powdery mildew in wheat

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

Abstract

Key message

We demonstrate that Lr67/Yr46 has pleiotropic effect on stem rust and powdery mildew resistance and is associated with leaf tip necrosis. Genes are designated as Sr55, Pm46 and Ltn3 , respectively.

Abstract

Wheat (Triticum aestivum) accession RL6077, known to carry the pleiotropic slow rusting leaf and yellow rust resistance genes Lr67/Yr46 in Thatcher background, displayed significantly lower stem rust (P. graminis tritici; Pgt) and powdery mildew (Blumeria graminis tritici; Bgt) severities in Kenya and in Norway, respectively, compared to its recurrent parent Thatcher. We investigated the resistance of RL6077 to stem rust and powdery mildew using Avocet × RL6077 F6 recombinant inbred lines (RILs) derived from two photoperiod-insensitive F3 families segregating for Lr67/Yr46. Greenhouse seedling tests were conducted with Mexican Pgt race RTR. Field evaluations were conducted under artificially initiated stem rust epidemics with Pgt races RTR and TTKST (Ug99 + Sr24) at Ciudad Obregon (Mexico) and Njoro (Kenya) during 2010–2011; and under natural powdery mildew epiphytotic in Norway at Ås and Hamar during 2011 and 2012. In Mexico, a mean reduction of 41 % on stem rust severity was obtained for RILs carrying Lr67/Yr46, compared to RILs that lacked the gene, whereas in Kenya the difference was smaller (16 %) but significant. In Norway, leaf tip necrosis was associated with Lr67/Yr46 and RILs carrying Lr67/Yr46 showed a 20 % reduction in mean powdery mildew severity at both sites across the 2 years of evaluation. Our study demonstrates that Lr67/Yr46 confers partial resistance to stem rust and powdery mildew and is associated with leaf tip necrosis. The corresponding pleiotropic, or tightly linked, genes, designated as Sr55, Pm46, and Ltn3, can be utilized to provide broad-spectrum durable disease resistance in wheat.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Brennan PS (1975) General resistance in wheat (Triticum aestivum L.) to wheat stem rust (Puccinia graminis Pers. f. sp. tritici Erik. and Henn.). Ph.D. thesis. University of Saskatchewan, Saskatoon

  • CIMMYT (2005) Laboratory protocols: CIMMYT applied molecular genetics laboratory, 3rd edn. CIMMYT, Mexico

  • Clarkson JDS (2000) Virulence survey report for wheat powdery mildew in Europe, 1996–1998. Cereal rust and powdery mildew bulletin http://www.crpmb.org/2000/1204clarkson/

  • Dubin HJ, Brennan JP (2009) Combating stem and leaf rust of wheat-historical perspective, impacts, and lessons learned. Millions fed: proven successes in agricultural development, IFPRI, Washington D.C., IFPRI Discussion paper 00910. http://www.ifpri.org/sites/default/files/publications/ifpridp00910.pdf

  • Dyck PL, Samborski DJ (1979) Adult plant resistance in PI250413, an introduction of common wheat. Can J Plant Sci 59:329–332

    Article  Google Scholar 

  • Dyck PL, Kerber ER, Aung T (1994) An interchromosomal reciprocal translocation in wheat involving leaf rust resistance gene Lr34. Genome 37:556–559

    Article  PubMed  CAS  Google Scholar 

  • Gavin Vanegas C, Garvin DF, Kolmer JA (2007) Genetics of stem rust resistance in the spring wheat cultivar Thatcher and the enhancement of stem rust resistance by Lr34. Euphytica 159:391–401

    Article  CAS  Google Scholar 

  • Hale IL, Mamuya I, Singh D (2013) Sr31-virulent races (TTKSK, TTKST, and TTTSK) of the wheat stem rust pathogen Puccinia graminis f. sp. tritici are present in Tanzania. Plant Dis 97:557

    Article  Google Scholar 

  • Herrera-Foessel SA, Lagudah ES, Huerta-Espino J, Hayden MJ, Bariana HS, Singh D, Singh RP (2011) New slow-rusting leaf rust and stripe rust resistance genes Lr67 and Yr46 in wheat are pleiotropic or closely linked. Theor Appl Genet 122:239–249

    Article  PubMed  Google Scholar 

  • Hiebert CW, Thomas JB, McCallum BD, Humphreys GD, DePauw RM, Hayden MJ, Mago R, Schnipenkoetter W, Hayden M (2010) An introgression on wheat chromosome 4DL in RL6077 (Thatcher*6/PI 250413) confers adult plant resistance to stripe rust and leaf rust (Lr67). Theor Appl Genet 121:1083–1091

    Article  PubMed  Google Scholar 

  • Hsam SLK, Zeller FJ (2002) Breeding for powdery mildew resistance in common wheat (Triticum aestivum L.). In: Belanger RR, Bushnell WR, Dik AJ, Carver TL (eds) The powdery mildews: a comprehensive treatise. APS Press, St. Paul, pp 219–238

    Google Scholar 

  • Johnson JW, Baenziger PS, Yamazaki WT, Smith TR (1979) Effects of powdery mildew on yield and quality of isogenic lines of “Chancellor” wheat. Crop Sci 19:349–352

    Article  Google Scholar 

  • Kolmer JA, Dyck PL, Roelfs AP (1991) An appraisal of stem and leaf rust resistance in North American hard red spring wheats and the probability of multiple mutations to virulence of populations of cereal rust fungi. Phytopathology 81:237–239

    Google Scholar 

  • Kolmer JA, Singh RP, Garvin DF, Viccars L, William HM, Huerta-Espino J, Ogbonnaya FC, Raman H, Orford S, Bariana HS, Lagudah ES (2008) Analysis of the Lr34/Yr28 rust resistance region in wheat germplasm. Crop Sci 48:1841–1852

    Article  CAS  Google Scholar 

  • Kolmer JA, Garvin DF, Jin Y (2011) Expression of a Thatcher wheat adult plant stem rust resistance QTL on chromosome arm 2BL is enhanced by Lr34. Crop Sci 51:526

    Article  Google Scholar 

  • Kota R, Spielmeyer W, McIntosh RA, Lagudah ES (2006) Fine genetic mapping fails to dissociate durable stem rust resistance gene Sr2 from pseudo-black chaff in common wheat (Triticum aestivum L.). Theor Appl Genet 112:492–499

    Article  PubMed  CAS  Google Scholar 

  • Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science (New York, NY) 323:1360–1363

    Article  CAS  Google Scholar 

  • Lagudah ES (2011) Molecular genetics of race non-specific rust resistance in wheat. Euphytica 179:81–91

    Article  Google Scholar 

  • Lagudah ES, Krattinger SG, Herrera-Foessel S, Singh RP, Huerta-Espino J, Spielmeyer W, Brow-Guedira G, Selter LL, Keller B (2009) Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor Appl Genet 119:889–898

    Article  PubMed  CAS  Google Scholar 

  • Lan CX, Herrera-Foessel SA, Singh RP, Basnet BR, Huerta-Espino J, Lagudah ES, Calvo-Salazar V (2013) Genetic analysis of resistance to leaf rust and stripe rust in Indian wheat cv. Sujata and NP876. In: Proceedings of Borlaug Global Rust Initiative, 2013 Technical Workshop, 19–22 August, New Delhi, India, p 10

  • Lillemo M, Asalf B, Singh RP, Huerta-Espino J, Chen XM, He XH, Bjornstad Å (2008) The adult plant rust resistance loci Lr34/Yr18 and Lr46/Yr29 are important determinants of partial resistance to powdery mildew in bread wheat line Saar. Theor Appl Genet 116:1155–1166

    Article  PubMed  CAS  Google Scholar 

  • Lillemo M, Singh RP, Van Ginkel M (2010) Identification of stable resistance to powdery mildew in wheat based on parametric and nonparametric methods. Crop Sci 50:478

    Article  Google Scholar 

  • Lillemo M, Joshi AK, Prasad R, Chand R, Singh RP (2013) QTL for spot blotch resistance in bread wheat line Saar co-locate to the biotrophic disease resistance loci Lr34 and Lr46. Theor Appl Genet 126:711–719

    Article  PubMed  CAS  Google Scholar 

  • Mago R, Bariana HS, Dundas IS, Spielmeyer W, Lawrence GJ, Pryor AJ, Ellis JG (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

    Article  PubMed  CAS  Google Scholar 

  • Mago R, Tabe L, McIntosh RA, Pretorius Z, Kota R, Paux E, Wicker T, Breen J, Lagudah ES, Ellis JG, Spielmeyer W (2011) A multiple resistance locus on chromosome arm 3BS in wheat confers resistance to stem rust (Sr2), leaf rust (Lr27) and powdery mildew. Theor Appl Genet 123:615–623

    Article  PubMed  CAS  Google Scholar 

  • McDonald BA, Linde C (2002) The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica 124:163–180

    Article  CAS  Google Scholar 

  • McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers J, Morris C, Somers DJ, Appels R, Devos KM (2012) Catalogue of gene symbols for wheat, 2012 (Supplement). http://www.wheat.pw.usda.gov/GG2/pubs.shtml

  • Nazareno NRX, Roelfs AP (1981) Adult plant resistance of Thatcher wheat to stem rust. Phytopathology 71:181–185

    Article  Google Scholar 

  • Njau PN, Bhavani S, Huerta-Espino J, Keller B, Singh RP (2013) Identification of QTL associated with durable adult plant resistance to stem rust race Ug99 in wheat cultivar “Pavon 76”. Euphytica 190:33–44

    Article  Google Scholar 

  • Parlevliet JE (1985) Resistance of the non-race-specific type. In: Roelfs AP, Bushnell WR (eds) The cereal rusts, vol. II, Diseases, distribution, epidemiology, and control. Academic Press, Inc., ORL, FL, pp 501–525

  • Peterson R, Campbell A, Hannah A (1948) A diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Can J Res 26:496–500

    Article  Google Scholar 

  • Rajaram S, Singh RP, Torres E (1988) Current CIMMYT approaches in breeding wheat for rust resistance. In: Simmonds NW, Rajaram S (eds) Breeding strategies for resistance to the rusts of wheat. CIMMYT, Mexico, pp 101–118

    Google Scholar 

  • Risk JM, Selter LL, Krattinger SG, Viccars LA, Richardson TM, Buesing G, Herren G, Lagudah ES, Keller B (2012) Functional variability of the Lr34 durable resistance gene in transgenic wheat. Plant Biotechnol J 10:477–487

    Article  PubMed  CAS  Google Scholar 

  • Roelfs A, Singh R, Saari E (1992) Rust diseases of wheat: concepts and methods of disease management. CIMMYT, Mexico

    Google Scholar 

  • Rosewarne GM, Singh RP, Huerta-Espino J, William HM, Bouchet S, Cloutier S, McFadden H, Lagudah ES (2006) Leaf tip necrosis, molecular markers and beta1-proteasome subunits associated with the slow rusting resistance genes Lr46/Yr29. Theor Appl Genet 112:500–508

    Article  PubMed  CAS  Google Scholar 

  • Rosewarne GM, Singh RP, Huerta-Espino J, Herrera-Foessel SA, Forrest KL, Hayden MJ, Rebetzke GJ (2012) Analysis of leaf and stripe rust severities reveals pathotype changes and multiple minor QTLs associated with resistance in an Avocet × Pastor wheat population. Theor Appl Genet 124:1–12

    Article  CAS  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  Google Scholar 

  • Saari E, Prescott J (1985) World distribution in relation to economic losses. In: Roelfs AP, Bushnell WR (eds) The cereal rusts Volume II Diseases, distribution, epidemiology, and control. Academic Press, Inc., pp 259–98

  • SAS Institute Inc (1999) SAS/STAT User’s Guide. SAS Institute Inc, Cary

    Google Scholar 

  • Singh RP (1991) Pathogenic variations of Puccinia recondita f.sp. tritici and P. graminis f.sp. tritici in wheat growing areas of Mexico during 1988 and 1989. Plant Dis 75:790–794

    Article  Google Scholar 

  • Singh RP (1992) Association between gene Lr34 for leaf rust and leaf tip necrosis in wheat. Crop Sci 32:874–878

    Article  Google Scholar 

  • Singh RP, Nelson JC, Sorrells ME (2000) Mapping Yr28 and other genes for resistance to stripe rust in wheat. Crop Sci 40:1148–1155

    Article  CAS  Google Scholar 

  • Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S, Njau P, Herrera-Foessel S, Singh PK, Singh S, Govindan V (2011a) The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu Rev Phytopathol 49:465–481

    Article  PubMed  CAS  Google Scholar 

  • Singh RP, Huerta-Espino J, Bhavani S, Herrera-Foessel SA, Singh D, Singh PK, Velu G, Mason RE, Jin Y, Njau P, Crossa J (2011b) Race non-specific resistance to rust diseases in CIMMYT spring wheats. Euphytica 179:175–186

    Article  Google Scholar 

  • Singh R, Herrera-Foessel SA, Huerta-Espino J, Bariana HS, Bansal U, McCallum BD, Hiebert CW, Bhavani S, Singh S, Lan C, Lagudah ES (2012) Lr34/Yr18/Sr57/Pm38/Bdv1/Ltn1 confers slow rusting, adult plant resistance to Puccinia graminis tritici. In: 13th Cereal Rust and Powdery Mildew Conference, August 28–September 1, 2012. Friendship Hotel, Beijing. p 173

  • Singh RP, Herrera-Foessel SA, Huerta-Espino J, Lan CX, Basnet BR, Bhavani S, Lagudah ES (2013) Pleiotropic gene Lr46/Yr29/Pm39/Ltn2 confers slow rusting, adult plant resistance to wheat stem rust fungus. In: Proceedings Borlaug Global Rust Initiative, 2013 Technical Workshop, 19–22 August, New Delhi, India, p 17.1

  • Skinnes H (2002) Breakdown of race specific resistance to powdery mildew in Norwegian wheat. Powdery Mildew Bulletin 30 (http://www.crpmb.org) 2002/1201skinnes

  • Sunderwirth SD, Roelfs AP (1980) Greenhouse evaluation of the adult plant resistance of Sr2 to wheat stem rust. Phytopathology 70:634

    Article  Google Scholar 

  • William M, Singh RP, Huerta-Espino J, Ortiz Islas S, Hoisington D (2003) Molecular marker mapping of leaf rust resistance gene Lr46 and its association with stripe rust resistance gene Yr29 in wheat. Phytopathology 93:153–159

    Article  PubMed  CAS  Google Scholar 

  • Yu L-X, Lorenz A, Rutkoski J, Singh RP, Bhavani S, Huerta-Espino J, Sorrells ME (2011) Association mapping and gene–gene interaction for stem rust resistance in CIMMYT spring wheat germplasm. Theor Appl Genet 123:1257–1268

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We acknowledge the financial support by the Australian Grains Research and Development Corporation (GRDC) and Australian Cereal Rust Control Program, and appreciate the technical editing by Emma Quilligan (CIMMYT). The field testing of powdery mildew resistance in Norway was supported by a Grant from the Research Council of Norway (NFR 185046).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

The experiments comply with the current laws of the country in which they were performed.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sybil A. Herrera-Foessel.

Additional information

Communicated by J. Yan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2013_2256_MOESM1_ESM.docx

Supplementary material 1 (DOCX 225 kb) Fig. S1 Infected stems with Pgt race RTR of two RILs from the Avocet/RL6077 population, not carrying Lr67/Yr46 (left) and carrying Lr67/Yr46 (right), when evaluated at Ciudad Obregon, Mexico, in the 2010-2011 crop cycle

Rights and permissions

Reprints and permissions

About this article

Cite this article

Herrera-Foessel, S.A., Singh, R.P., Lillemo, M. et al. Lr67/Yr46 confers adult plant resistance to stem rust and powdery mildew in wheat. Theor Appl Genet 127, 781–789 (2014). https://doi.org/10.1007/s00122-013-2256-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-013-2256-9

Keywords

Navigation