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Theoretical and Applied Genetics

, Volume 126, Issue 3, pp 663–672 | Cite as

Recent emergence of the wheat Lr34 multi-pathogen resistance: insights from haplotype analysis in wheat, rice, sorghum and Aegilops tauschii

  • Simon G. Krattinger
  • David R. Jordan
  • Emma S. Mace
  • Chitra Raghavan
  • Ming-Cheng Luo
  • Beat Keller
  • Evans S. Lagudah
Original Paper

Abstract

Spontaneous sequence changes and the selection of beneficial mutations are driving forces of gene diversification and key factors of evolution. In highly dynamic co-evolutionary processes such as plant-pathogen interactions, the plant’s ability to rapidly adapt to newly emerging pathogens is paramount. The hexaploid wheat gene Lr34, which encodes an ATP-binding cassette (ABC) transporter, confers durable field resistance against four fungal diseases. Despite its extensive use in breeding and agriculture, no increase in virulence towards Lr34 has been described over the last century. The wheat genepool contains two predominant Lr34 alleles of which only one confers disease resistance. The two alleles, located on chromosome 7DS, differ by only two exon-polymorphisms. Putatively functional homoeologs and orthologs of Lr34 are found on the B-genome of wheat and in rice and sorghum, but not in maize, barley and Brachypodium. In this study we present a detailed haplotype analysis of homoeologous and orthologous Lr34 genes in genetically and geographically diverse selections of wheat, rice and sorghum accessions. We found that the resistant Lr34 haplotype is unique to the wheat D-genome and is not found in the B-genome of wheat or in rice and sorghum. Furthermore, we only found the susceptible Lr34 allele in a set of 252 Ae. tauschii genotypes, the progenitor of the wheat D-genome. These data provide compelling evidence that the Lr34 multi-pathogen resistance is the result of recent gene diversification occurring after the formation of hexaploid wheat about 8,000 years ago.

Keywords

Sorghum Powdery Mildew Leaf Rust Hexaploid Wheat Stripe Rust 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We are indebted to the skilled technical support provided by Libby Viccars and Sutha Chandramohan. We thank Dr. Sally Norton from the Australian Tropical Grains Germplasm Centre for providing seeds of Sorghum propinquum and Dr. Joanna Risk from CSIRO Plant Industry, Canberra, for critically reviewing the manuscript. This work was supported by the Grains Research and Development Corporation grant #CSP000063, Australia, an Advanced Investigator grant of the European Research Council (ERC-2009- AdG 249996, Durableresistance), the Swiss National Science Foundation grant 3100A-127061 and a Marie Curie International Outgoing Fellowship within the 7th European Community Framework Programme (PIOF-GA-2009-252731, Dures).

Supplementary material

122_2012_2009_MOESM1_ESM.xls (85 kb)
Supplementary material 1 (XLS 85 kb)

References

  1. Bai YL, Pavan S, Zheng Z, Zappel NF, Reinstadler A, Lotti C, De Giovanni C, Ricciardi L, Lindhout P, Visser R, Theres K, Panstruga R (2008) Naturally occurring broad-spectrum powdery mildew resistance in a central American tomato accession is caused by loss of Mlo function. Mol Plant Microbe in 21:30–39CrossRefGoogle Scholar
  2. Bessire M, Borel S, Fabre G, Carraca L, Efremova N, Yephremov A, Cao Y, Jetter R, Jacquat AC, Metraux JP, Nawrath C (2011) A member of the pleiotropic drug resistance family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis. Plant Cell 23:1958–1970PubMedCrossRefGoogle Scholar
  3. Borghi B (2001) Italian wheat pool. In: Bonjean AP, Angus WJ (eds) The world wheat book: a history of wheat breeding. Intercept, London, pp 289–309Google Scholar
  4. Brunner S, Hurni S, Streckeisen P, Mayr G, Albrecht M, Yahiaoui N, Keller B (2010) Intragenic allele pyramiding combines different specificities of wheat Pm3 resistance alleles. Plant J 64:433–445PubMedCrossRefGoogle Scholar
  5. Camargo CEDO, Ferreira Filho AWP (2001) Sao Paulo State, Brazil Wheat Pool. In: Bonjean AP, Angus WJ (eds) The world wheat book: a history of wheat breeding. Intercept, London, pp 549–577Google Scholar
  6. Chen G, Komatsuda T, Ma JF, Nawrath C, Pourkheirandish M, Tagiri A, Hu YG, Sameri M, Li X, Zhao X, Liu Y, Li C, Ma X, Wang A, Nair S, Wang N, Miyao A, Sakuma S, Yamaji N, Zheng X, Nevo E (2011) An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proc Natl Acad Sci USA 108:12354–12359PubMedCrossRefGoogle Scholar
  7. Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J, Westphal L, Vogel J, Lipka V, Kemmerling B, Schulze-Lefert P, Somerville SC, Panstruga R (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet 38:716–720PubMedCrossRefGoogle Scholar
  8. Dakouri A, McCallum BD, Walichnowski AZ, Cloutier S (2010) Fine-mapping of the leaf rust Lr34 locus in Triticum aestivum (L.) and characterization of large germplasm collections support the ABC transporter as essential for gene function. Theor Appl Genet 121:373–384PubMedCrossRefGoogle Scholar
  9. Dillon SL, Lawrence PK, Henry RJ, Ross L, Price HJ, Johnston JS (2004) Sorghum laxiflorum and S. macrospermum, the Australian native species most closely related to the cultivated S. bicolor based on ITS1 and ndhF sequence analysis of 25 Sorghum species. Plant Syst Evol 249:233–246CrossRefGoogle Scholar
  10. Feldman M (2001) Origin of cultivated wheat. In: Bonjean AP, Angus WJ (eds) The world wheat book: a history of wheat breeding. Intercept, London, pp 3–56Google Scholar
  11. Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631–1638PubMedCrossRefGoogle Scholar
  12. Honjo Y, Hrycyna CA, Yan QW, Medina-Perez WY, Robey RW, van de Laar A, Litman T, Dean M, Bates SE (2001) Acquired mutations in the MXR/BCRP/ABCP gene alter substrate specificity in MXR/BCRP/ABCP-overexpressing cells. Cancer Res 61:6635–6639PubMedGoogle Scholar
  13. Humphry M, Reinstadler A, Ivanov S, Bisseling T, Panstruga R (2011) Durable broad-spectrum powdery mildew resistance in pea er1 plants is conferred by natural loss-of-function mutations in PsMLO1. Mol Plant Pathol 12:866–878PubMedCrossRefGoogle Scholar
  14. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  15. Ito H, Gray WM (2006) A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiol 142:63–74PubMedCrossRefGoogle Scholar
  16. Kolmer JA (2005) Tracking wheat rust on a continental scale. Curr Opin Plant Biol 8:441–449PubMedCrossRefGoogle Scholar
  17. Kolmer JA, Long DL, Kosman E, Hughes ME (2003) Physiologic specialization of Puccinia triticina on wheat in the United States in 2001. Plant Dis 87:859–866CrossRefGoogle Scholar
  18. 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/Yr18 rust resistance region in wheat germplasm. Crop Sci 48:1841–1852CrossRefGoogle Scholar
  19. 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 323:1360–1363PubMedCrossRefGoogle Scholar
  20. Krattinger SG, Lagudah ES, Wicker T, Risk JM, Ashton AR, Selter LL, Matsumoto T, Keller B (2011) Lr34 multi-pathogen resistance ABC transporter: molecular analysis of homoeologous and orthologous genes in hexaploid wheat and other grass species. Plant J 65:392–403PubMedCrossRefGoogle Scholar
  21. Lagudah ES (2011) Molecular genetics of race non-specific rust resistance in wheat. Euphytica 179:81–91CrossRefGoogle Scholar
  22. Lagudah ES, Clarke BC, Appels R (1989) Phylogenetic relationships of Triticum tauschii, the D-genome donor to hexaploid wheat. 4. variation and chromosomal location of 5S DNA. Genome 32:1017–1025PubMedCrossRefGoogle Scholar
  23. Lagudah ES, McFadden H, Singh RP, Huerta-Espino J, Bariana HS, Spielmeyer W (2006) Molecular genetic characterisation of the Lr34/Yr18 slow rusting resistance gene region in wheat. Theor Appl Genet 114:21–30PubMedCrossRefGoogle Scholar
  24. Lagudah ES, Krattinger SG, Herrera-Foessel S, Singh RP, Huerta-Espino J, Spielmeyer W, Brown-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 119:889–898PubMedCrossRefGoogle Scholar
  25. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948PubMedCrossRefGoogle Scholar
  26. 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 123:615–623PubMedCrossRefGoogle Scholar
  27. McCallum BD, Humphreys DG, Somers DJ, Dakouri A, Cloutier S (2012) Allelic variation for the rust resistance gene Lr34/Yr18 in Canadian wheat cultivars. Euphytica 183:261–274CrossRefGoogle Scholar
  28. McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers J, Morris C, Somers DJ, Appels R, Devos KM (2008) Catalogue of gene symbols for wheat. In: Appels R, Eastwood R, Lagudah E, Langridge P, Mackay M, McIntyre L, Sharp P (eds) Proceedings of the 11th international wheat genetics symposium. Sydney University Press, SydneyGoogle Scholar
  29. McNally KL, Childs KL, Bohnert R, Davidson RM, Zhao K, Ulat VJ, Zeller G, Clark RM, Hoen DR, Bureau TE, Stokowski R, Ballinger DG, Frazer KA, Cox DR, Padhukasahasram B, Bustamante CD, Weigel D, Mackill DJ, Bruskiewich RM, Ratsch G, Buell CR, Leung H, Leach JE (2009) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proc Natl Acad Sci USA 106:12273–12278PubMedCrossRefGoogle Scholar
  30. Park RF, Bariana HS, Wellings CR, Wallwork H (2002) Detection and occurrence of a new pathotype of Puccinia triticina with virulence for Lr24 in Australia. Aust J Agr Res 53:1069–1076CrossRefGoogle Scholar
  31. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob ur R, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556PubMedCrossRefGoogle Scholar
  32. Piffanelli P, Ramsay L, Waugh R, Benabdelmouna A, D’Hont A, Hollricher K, Jorgensen JH, Schulze-Lefert P, Panstruga R (2004) A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature 430:887–891PubMedCrossRefGoogle Scholar
  33. 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 84:203CrossRefGoogle Scholar
  34. Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375PubMedCrossRefGoogle Scholar
  35. 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 10:477–487PubMedCrossRefGoogle Scholar
  36. Salamini F, Ozkan H, Brandolini A, Schafer-Pregl R, Martin W (2002) Genetics and geography of wild cereal domestication in the Near East. Nat Rev Genet 3:429–441PubMedGoogle Scholar
  37. Sun XC, Bai GH, Carver B (2009) Molecular markers for wheat leaf rust resistance gene Lr41. Mol Breed 23:311–321CrossRefGoogle Scholar
  38. Yang WX, Yang FP, Liang D, He ZH, Shang XW, Xia XC (2008) Molecular characterization of slow-rusting genes Lr34/Yr18 in Chinese wheat cultivars. Acta Agron Sinica 34:1109–1113CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Simon G. Krattinger
    • 1
    • 2
  • David R. Jordan
    • 3
  • Emma S. Mace
    • 4
  • Chitra Raghavan
    • 5
  • Ming-Cheng Luo
    • 6
  • Beat Keller
    • 2
  • Evans S. Lagudah
    • 1
  1. 1.CSIRO Plant IndustryCanberraAustralia
  2. 2.Institute of Plant BiologyUniversity of ZurichZurichSwitzerland
  3. 3.Queensland Alliance for Agriculture and Food Innovation, Hermitage Research FacilityThe University of QueenslandWarwickAustralia
  4. 4.Department of Agriculture, Fisheries and Forestry, Hermitage Research FacilityAgri-Science QueenslandWarwickAustralia
  5. 5.Plant Breeding, Genetics, and Biotechnology DivisionInternational Rice Research InstituteMetro ManilaPhilippines
  6. 6.Department of Plant SciencesUniversity of CaliforniaDavisUSA

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