Recent emergence of the wheat Lr34 multi-pathogen resistance: insights from haplotype analysis in wheat, rice, sorghum and Aegilops tauschii
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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.
KeywordsSorghum Powdery Mildew Leaf Rust Hexaploid Wheat Stripe Rust
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).
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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