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A barley cultivation-associated polymorphism conveys resistance to powdery mildew

Nature volume 430, pages 887891 (19 August 2004) | Download Citation

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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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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.

Author information

Author notes

    • Pietro Piffanelli
    •  & Luke Ramsay

    These authors contributed equally to this work

    • Pietro Piffanelli

    Present address: CIRAD, Avenue Agropolis, 34398 Montpellier, Cedex 5, France

Affiliations

  1. The Sainsbury Laboratory, John Innes Centre, Colney Lane, Norwich NR4 7UH, UK

    • Pietro Piffanelli
  2. Genomics Unit, Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, UK

    • Luke Ramsay
    •  & Robbie Waugh
  3. CIRAD, Avenue Agropolis, 34398 Montpellier, Cedex 5, France

    • Abdellah Benabdelmouna
    •  & Angélique D'Hont
  4. Max-Planck-Institut für Züchtungsforschung, Department of Plant Breeding and Yield Physiology, Carl-von-Linne-Weg 10, D-50829 Köln, Germany

    • Karin Hollricher
  5. Risø National Laboratory, Plant (formerly: Agricultural) Research Department, DK-4000 Roskilde, Denmark

    • Jørgen Helms Jørgensen
  6. Max-Planck-Institut für Züchtungsforschung, Department of Plant–Microbe Interactions, Carl-von-Linné-Weg 10, D-50829 Köln, Germany

    • Paul Schulze-Lefert
    •  & Ralph Panstruga

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Competing interests

The authors declare that they have no competing financial interests.

Corresponding author

Correspondence to Paul Schulze-Lefert.

Supplementary information

PDF files

  1. 1.

    Supplementary Figure 1

    Phenotypic and molecular analysis of mlo-11 revertant progeny.

  2. 2.

    Supplementary Figure 2

    Southern blot analysis using methylation sensitive/insensitive isoschizomers.

  3. 3.

    Supplementary Figure 3

    Molecular analysis of aberrant mlo-11 transcripts.

  4. 4.

    Supplementary Figure 4

    Location of SSR and MITE markers used for haplotype analysis of barley germplasm.

  5. 5.

    Supplementary Table 1

    Number of susceptible plants obtained in selfings of various mlo barley lines.

  6. 6.

    Supplementary Table 2

    Segregation analysis of susceptible mlo-11 revertant #2.

  7. 7.

    Supplementary Table 3

    Compilation of designations of various broad-spectrum powdery mildew resistant Ethiopian barley accessions.

  8. 8.

    Supplementary Table 4

    Single cell complementation efficiency of Mlo-encoding constructs driven by various regulatory sequences.

Excel files

  1. 1.

    Supplementary Table 5

    Haplotype analysis of barley germplasm.

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DOI

https://doi.org/10.1038/nature02781

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