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A barley cultivation-associated polymorphism conveys resistance to powdery mildew

Abstract

Barley (Hordeum vulgare) has played a pivotal role in Old World agriculture since its domestication about 10,000 yr ago1. Barley plants carrying loss-of-function alleles (mlo) of the Mlo locus are resistant against all known isolates of the widespread powdery mildew fungus2. The sole mlo resistance allele recovered so far from a natural habitat, mlo-11, was originally retrieved from Ethiopian landraces and nowadays controls mildew resistance in the majority of cultivated European spring barley elite varieties2. Here we use haplotype analysis to show that the mlo-11 allele probably arose once after barley domestication. Resistance in mlo-11 plants is linked to a complex tandem repeat array inserted upstream of the wild-type gene. The repeat units consist of a truncated Mlo gene comprising 3.5 kilobases (kb) of 5′-regulatory sequence plus 1.1 kb of coding sequence. These generate aberrant transcripts that impair the accumulation of both Mlo wild-type transcript and protein. We exploited the meiotic instability of mlo-11 resistance and recovered susceptible revertants in which restoration of Mlo function was accompanied by excision of the repeat array. We infer cis-dependent perturbation of transcription machinery assembly by transcriptional interference in mlo-11 plants as a likely mechanism leading to disease resistance.

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Figure 1: Phenotypic and molecular characterization of barley Mlo wild-type plants, resistant mlo-11 mutants, susceptible mlo-11 revertants and their resistant siblings.
Figure 2: Schematic representation of the Mlo locus and mlo-11 repeat array organization.
Figure 3: Phylogenetic relationship of barley germplasm based on haplotype analysis at Mlo.

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Acknowledgements

We thank B. Koop, C. Casais, I. Tierney and M. Macaulay for technical assistance; I. Somssich for experimental proposals; and N. Collins and M. Koornneef for suggestions on the manuscript. This work was supported by grants from the Gatsby Charitable Foundation to P.S.-L., from the Max-Planck Society to R.P., from Génoplante to A.B., and from the Scottish Executive Environment and Rural Affairs Department and the European Commission to R.W.

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Correspondence to Paul Schulze-Lefert.

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Supplementary information

Supplementary Figure 1

Phenotypic and molecular analysis of mlo-11 revertant progeny. (PDF 990 kb)

Supplementary Figure 2

Southern blot analysis using methylation sensitive/insensitive isoschizomers. (PDF 773 kb)

Supplementary Figure 3

Molecular analysis of aberrant mlo-11 transcripts. (PDF 982 kb)

Supplementary Figure 4

Location of SSR and MITE markers used for haplotype analysis of barley germplasm. (PDF 325 kb)

Supplementary Table 1

Number of susceptible plants obtained in selfings of various mlo barley lines. (PDF 7 kb)

Supplementary Table 2

Segregation analysis of susceptible mlo-11 revertant #2. (PDF 10 kb)

Supplementary Table 3

Compilation of designations of various broad-spectrum powdery mildew resistant Ethiopian barley accessions. (PDF 5 kb)

Supplementary Table 4

Single cell complementation efficiency of Mlo-encoding constructs driven by various regulatory sequences. (PDF 8 kb)

Supplementary Table 5

Haplotype analysis of barley germplasm. (XLS 93 kb)

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Piffanelli, P., Ramsay, L., Waugh, R. et al. A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature 430, 887–891 (2004). https://doi.org/10.1038/nature02781

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  • DOI: https://doi.org/10.1038/nature02781

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