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BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust

Nature Plants volume 4, pages 662–668 (2018)Cite this article

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Abstract

Crop diseases reduce wheat yields by ~25% globally and thus pose a major threat to global food security1. Genetic resistance can reduce crop losses in the field and can be selected through the use of molecular markers. However, genetic resistance often breaks down following changes in pathogen virulence, as experienced with the wheat yellow (stripe) rust fungus Puccinia striiformis f. sp. tritici (Pst)2. This highlights the need to (1) identify genes that, alone or in combination, provide broad-spectrum resistance, and (2) increase our understanding of the underlying molecular modes of action. Here we report the isolation and characterization of three major yellow rust resistance genes (Yr7, Yr5 and YrSP) from hexaploid wheat (Triticum aestivum), each having a distinct recognition specificity. We show that Yr5, which remains effective to a broad range of Pst isolates worldwide, is closely related yet distinct from Yr7, whereas YrSP is a truncated version of Yr5 with 99.8% sequence identity. All three Yr genes belong to a complex resistance gene cluster on chromosome 2B encoding nucleotide-binding and leucine-rich repeat proteins (NLRs) with a non-canonical N-terminal zinc-finger BED domain3 that is distinct from those found in non-NLR wheat proteins. We developed diagnostic markers to accelerate haplotype analysis and for marker-assisted selection to expedite the stacking of the non-allelic Yr genes. Our results provide evidence that the BED-NLR gene architecture can provide effective field-based resistance to important fungal diseases such as wheat yellow rust.

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Fig. 1: Yr5 and YrSP are closely related sequences and distinct from Yr7.
Fig. 2: Yr7 and Yr5/YrSP encode integrated BED-domain immune receptor genes
Fig. 3: BED domains from BED-NLRs and non-NLR proteins are distinct

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Acknowledgements

This work was supported by the UK Biotechnology and Biological Sciences Research Council Designing Future Wheat programme BB/P016855/1 and the Grains Research and Development Corporation, Australia. C.M. was funded by a PhD studentship from Group Limagrain and J.Z. is funded by PhD scholarships from the National Science Foundation (NSF) and the Monsanto Beachell-Borlaug International Scholars Programs (MBBISP). We thank the International Wheat Genome Sequencing Consortium for allowing pre-publication access to the RefSeq v1.0 assembly and gene annotation. We thank J. Dubcovsky and X. Zhang (University of California, Davis) for providing Yr5 cultivars. We thank the John Innes Centre Horticultural Services and Limagrain Rothwell staff for management of the wheat populations. We also thank S. Specel (Limagrain; Clermont-Ferrand) and R. Goram (JIC) for their help in designing and running KASP assays, and S. Hoxha (The University of Sydney) for technical assistance. This research was supported by the NBI Computing Infrastructure for Science (CiS) group in Norwich, UK.

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  1. These authors contributed equally: C. Marchal and J. Zhang.

Authors and Affiliations

  1. John Innes Centre, Norwich Research Park, Norwich, UK

    Clemence Marchal, Burkhard Steuernagel, Nikolai M. Adamski, Brande B. H. Wulff & Cristobal Uauy

  2. University of Sydney, Plant Breeding Institute, Cobbitty, New South Wales, Australia

    Jianping Zhang, Peng Zhang & Robert McIntosh

  3. Commonwealth Scientific and Industrial Research Organization (CSIRO) Agriculture & Food, Canberra, Australian Capital Territory, Australia

    Jianping Zhang & Evans Lagudah

  4. Henan Tianmin Seed Company Limited, Lankao County, Henan Province, China

    Jianping Zhang

  5. Limagrain UK Ltd, Rothwell, Market Rasen, Lincolnshire, UK

    Paul Fenwick & Simon Berry

  6. National Institute of Agricultural Botany (NIAB), Cambridge, UK

    Lesley Boyd

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Contributions

C.M. performed the experiments to clone Yr7 and Yr5 and the subsequent analyses of their loci and BED domains, designed the gene-specific markers, analysed the genotype data in the studied panels, and designed and made the figures. J.Z. performed the experiments to clone YrSP, confirm the Yr7 and Yr5 genes in AvocetS-Yr7 and AvocetS-Yr5 mutants, and identified the full length of Yr5 and YrSP with their respective regulatory elements. C.M. and J.Z. developed the gene-specific markers. P.Z. and R.M. performed the EMS treatment, isolation, and confirmation of Yr7, Yr5 and YrSP mutants in AvocetS NILs. P.F. performed the pathology work on the Cadenza Yr7 mutants and the mapping populations. B.S. helped with the NLR -Annotator analysis and provided the bait library for target enrichment and sequencing of NLRs. N.M.A. provided DNA samples for allelic variation studies. L.B. provided Lemhi-Yr5 mutants. R.M., E.L., P.Z., B.W., S.B. and C.U. conceived, designed and supervised the research. C.M. and C.U. wrote the manuscript. J.Z., P.Z., R.M., B.W., N.M.A., L.B. and E.L. provided edits.

Corresponding author

Correspondence to Cristobal Uauy.

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Competing interests

A patent application based on this work has been filed (United Kingdom Patent Application No. 1805865.1).

Data availability

The data that support the findings of this study are presented in the supplementary information. All sequencing data have been deposited in the NCBI Short Reads Archive under accession numbers listed in Supplementary Table 14 (SRP139043). Cadenza (Yr7) and Lemhi (Yr5) mutants are available through the JIC Germplasm Resource Unit (www.seedstor.ac.uk).

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Supplementary information

Supplementary Information

Supplementary Notes and Supplementary Figures 1–10.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–13.

Supplementary File 1

Annotation of the Yr7 locus in Cadenza with exon/intron structure, positions of mutations and the position of primers for long-range PCR and nested PCRs that were carried out prior to Sanger sequencing.

Supplementary File 2

Annotation of the Yr5/YrSP locus in Lemhi-Yr5 and AvocetS-YrSP, respectively, with exon/intron structure, the position of mutations and the position of primers for long-range PCR and nested PCRs that were carried out prior to Sanger sequencing.

Supplementary File 3

Curation of the Yr7 locus in the Cadenza genome assembly based on Sanger sequencing results.

Supplementary File 4

Syntenic region across different grasses (Supplementary Table 6) and the NLR loci identified with NLR-Annotator.

Supplementary File 5

Curated sequences of BED-NLRs from chromosome 2B and Ta_2D7.

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Marchal, C., Zhang, J., Zhang, P. et al. BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust. Nature Plants 4, 662–668 (2018). https://doi.org/10.1038/s41477-018-0236-4

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