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Haplotype diversity and evolutionary history of the Lr34 locus of wheat

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Abstract

Leaf rust caused by Puccinia triticina is a major disease of wheat, and genetic resistance remains the best strategy for managing it. The resistance gene Lr34 has been key in the genetic management of wheat leaf rust worldwide. However, little is known about the geo-genetic diversity, history and origin of this unique gene. This study was conducted to provide a comprehensive analysis of the genetic diversity at the Lr34 locus of a world wheat germplasm collection. A total of 52 alleles were detected for the 10 Lr34 markers. On the basis of the Lr34-specific markers, the world collection was divided into five major haplotypes (H), of which H1 was consistently associated with the resistance phenotype Lr34+. Phenotypic data confirmed the susceptible phenotypes of H2, H3 and H4 and the susceptible or intermediate phenotype of H5. SNP12 (C/T) was the only mutation differentiating the resistant haplotype from the susceptible ones. Combined analysis of the 10 markers resulted in dividing the major haplotypes into 118 different sub-haplotypes. Structure and clustering analyses grouped them into two main clusters and seven sub-clusters. Variance between the main clusters represented the largest proportion of the total variation. H2, the only haplotype found in Aegilops tauschii, is the ancestral haplotype and H1 (Lr34+) likely arose after the advent of hexaploid wheat. Analysis of geographical distribution showed that H1 was more frequent in the Asian germplasm while H2 dominated the European germplasm. Lr34, a gain-of-function mutation, is hypothesized to have originated in Asia.

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Acknowledgments

The authors are grateful to Elsa Reimer and Andrzej Walichnowski for technical support, Braulio Soto-Cerda for help with the Structure analysis and Michael Shillinglaw for figure preparation. AD was supported by Monsanto’s Beachell-Borlaug International Scholarship Program (MBBISP).

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Correspondence to Sylvie Cloutier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

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Online Resource 1 – Table S1 Description of germplasm including accession number, name, country of origin and genotypic data for 10 Lr34 locus markers (PDF 534 kb)

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Online Resource 2 – Table S2 Genotypes of the 112 accessions of Aegilops tauschii as defined by the four genic markers identified to date (PDF 166 kb)

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Online Resource 3 – Fig. S1 A schematic diagram of the Lr34 locus illustrating the locations of the ten molecular markers. Genetic distances are in cM and physical distance is in Kb (PDF 192 kb)

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Online Resource 4 – Table S3 Genotypes and phenotypes (MRS) of hexaploid wheat accessions Thatcher-Lr34, Thatcher, Odess Kaja 13 and Koktunkulskaja 332 (PDF 18 kb)

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Online Resource 5 – Table S4 Allele sizes and frequencies for 10 Lr34 locus specific markers assessed in a world collection of 310 wheat accessions (PDF 58 kb)

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Online Resource 6 – Table S5 Extent of the genetic diversity at the Lr34 locus as described by 10 molecular markers assayed on 310 accessions of a wheat germplasm collection (PDF 14 kb)

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Online Resource 7 – Fig. S2 Population structure analysis of the 310 accessions based on the 10 markers assessed at the Lr34 locus. A. Model-based Bayesian clustering performed using STRUCTURE for K = 2 groups. Each of the 310 accessions is represented by a column broken into red and green segments with length proportional to each of the K inferred ancestral groups (Lr34+ and Lr34-) shown underneath. B. Estimation of the number of sub-populations based on the Evanno criterion. Ad-hoc statistic ∆K (Evanno et al. 2005) for K values of 1 to 10 (PDF 137 kb)

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Online Resource 8 – Table S6 Analysis of molecular variance (AMOVA) of the 310 accessions of the world collection of wheat based on the Lr34 markers (PDF 13 kb)

Online Resource 9 – Table S7 Sub-clusters pairwise Fst differences (PDF 14 kb)

Online Resource 10 – Table S8 LD and r2 values for the ten markers at the Lr34 locus for the entire WC (PDF 21 kb)

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Online Resource 11 – Table S9 LD and r2 values for the ten markers at the Lr34 locus for the Lr34+ sub-haplotypes (PDF 20 kb)

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Online Resource 12 – Table S10 LD and r2 values for the ten markers at the Lr34 locus for the Lr34- sub-haplotypes (PDF 20 kb)

Online Resource 13 – Table S11 Geographical distribution of Lr34 haplotypes (PDF 17 kb)

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Dakouri, A., McCallum, B.D. & Cloutier, S. Haplotype diversity and evolutionary history of the Lr34 locus of wheat. Mol Breeding 33, 639–655 (2014). https://doi.org/10.1007/s11032-013-9981-2

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