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Orthologous receptor kinases quantitatively affect the host status of barley to leaf rust fungi

Nature Plants volume 5, pages 1129–1135 (2019)Cite this article

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Abstract

Global food security depends on cereal crops with durable disease resistance. Most cereals are colonized by rust fungi, which are pathogens of major significance for global agriculture1. Cereal rusts display a high degree of host specificity and one rust species or forma specialis generally colonizes only one cereal host2. Exploiting the non-host status and transferring non-host resistance genes between cereal crop species has been proposed as a strategy for durable rust resistance breeding. The molecular determinants that define the host status to rusts, however, are largely unknown. Here, we show that orthologous genes at the Rphq2 locus for quantitative leaf rust resistance from cultivated barley3 and Rph22 from wild bulbous barley4 affect the host status to leaf rusts. Both genes encode lectin receptor-like kinases. We transformed Rphq2 and Rph22 into an experimental barley line that has been bred for susceptibility to non-adapted leaf rusts, which allowed us to quantify resistance responses against various leaf rust species. Rphq2 conferred a much stronger resistance to the leaf rust of wild bulbous barley than to the leaf rust adapted to cultivated barley, while for Rph22 the reverse was observed. We hypothesize that adapted leaf rust species mitigate perception by cognate host receptors by lowering ligand recognition. Our results provide an example of orthologous genes that connect the quantitative host with non-host resistance to cereal rusts. Such genes provide a basis to exploit non-host resistance in molecular breeding.

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Fig. 1: Rphq2 and Rph22 phenotype and mapping.
Fig. 2: Resistance mediated by Hv-LecRK and Hb-LecRK is stronger against non-adapted than against adapted leaf rust species.
Fig. 3: Molecular characterization of Hv-LecRK and Hb-LecRK proteins.

Data availability

All data are available in the main text or the Supplementary Information. GenBank accession numbers: MK512576–MK512578, MK530949, MK530950, MK569504 and MN128516–MN128521.

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Acknowledgements

We thank J. Bucher (Wageningen University & Research) for producing the time-lapse video, Y. Jiang (King Abdullah University of Science and Technology) for advising on the Rphq2/Rph22 functional analyses, and J. Rajaraman (IPK Gatersleben) for providing the plasma membrane marker plasmid. This publication is based on work supported by the King Abdullah University of Science and Technology Office of Sponsored Research under Award No. OSR-CRG2018-3768 (to Y.W. and S.G.K.), the New Zealand Institute for Plant & Food Research Limited Strategic Science Investment Fund (to P.A.J.), National Natural Science Foundation of China grant no. 31471756 (to X.Q.), and NWO-ALW (file number 849.13.002) as part of the ERA-CAPS project DURESTrit 13.006 (to Y.W.).

Author information

Author notes

  1. Sudeep Subedi

    Present address: Nepal Agricultural Research Council, Kathmandu, Nepal

Authors and Affiliations

  1. Plant Breeding, Wageningen University & Research, Wageningen, the Netherlands

    Yajun Wang, Sudeep Subedi, Harmen de Vries, Pieter Doornenbal, Anton Vels & Rients E. Niks

  2. Center for Desert Agriculture, Biological and Environmental Science & Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia

    Yajun Wang, Ikram Blilou & Simon G. Krattinger

  3. Plant Reproductive Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben, Gatersleben, Germany

    Goetz Hensel & Jochen Kumlehn

  4. The New Zealand Institute for Plant and Food Research Limited, Lincoln, New Zealand

    Paul A. Johnston

  5. Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, China

    Xiaoquan Qi

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Contributions

Y.W., X.Q., R.E.N. and S.G.K. designed research. Y.W., S.S., H.d.V., P.D. and P.A.J. performed molecular experiments. Y.W., S.S., H.d.V., P.D., A.V. and R.E.N. performed rust inoculations and phenotypic scorings. G.H. and J.K. stably transformed the barley line Golden SusPtrit. Y.W. and I.B. performed subcellular localization. Y.W., R.E.N. and S.G.K. wrote the paper. All authors have read and approved the manuscript.

Corresponding authors

Correspondence to Rients E. Niks or Simon G. Krattinger.

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Peer review information Nature Plants thanks Peter Dracatos, Kirankumar Mysore and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–12, Supplementary Tables 1 and 2, and legend for the Supplementary Video.

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Supplementary Video

Time-lapse video showing P. hordei development on barley plants expressing Rphq2 and Rph22.

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Wang, Y., Subedi, S., de Vries, H. et al. Orthologous receptor kinases quantitatively affect the host status of barley to leaf rust fungi. Nat. Plants 5, 1129–1135 (2019). https://doi.org/10.1038/s41477-019-0545-2

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