Abstract

Head smut is a systemic disease in maize caused by the soil-borne fungus Sporisorium reilianum that poses a grave threat to maize production worldwide. A major head smut quantitative resistance locus, qHSR1, has been detected on maize chromosome bin2.09. Here we report the map-based cloning of qHSR1 and the molecular mechanism of qHSR1-mediated resistance. Sequential fine mapping and transgenic complementation demonstrated that ZmWAK is the gene within qHSR1 conferring quantitative resistance to maize head smut. ZmWAK spans the plasma membrane, potentially serving as a receptor-like kinase to perceive and transduce extracellular signals. ZmWAK was highly expressed in the mesocotyl of seedlings where it arrested biotrophic growth of the endophytic S. reilianum. Impaired expression in the mesocotyl compromised ZmWAK-mediated resistance. Deletion of the ZmWAK locus appears to have occurred after domestication and spread among maize germplasm, and the ZmWAK kinase domain underwent functional constraints during maize evolution.

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Acknowledgements

We thank J. Schirawski (RWTH Aachen University) for providing the mating-compatible S. reilianum isolates SRZ1 and SRZ2 and X. Yang (China Agricultural University) for providing the DNA for 522 maize inbred lines and 184 teosinte accessions. We also thank N. Dengler for her help in the identification of microscopy structures. This work was supported by the National High-Tech Research and Development Program of China (grant numbers 2012AA10A306 and 2012AA101104).

Author information

Author notes

    • Weiliang Zuo
    • , Qing Chao
    •  & Nan Zhang

    These authors contributed equally to this work.

Affiliations

  1. National Maize Improvement Centre of China, China Agricultural University, Beijing, People's Republic of China.

    • Weiliang Zuo
    • , Qing Chao
    • , Nan Zhang
    • , Jianrong Ye
    • , Boqi Zhang
    • , Jing Zhao
    • , Xianrong Zhao
    • , Yongsheng Chen
    • , Jinsheng Lai
    •  & Mingliang Xu
  2. Maize Research Institute, Jilin Academy of Agricultural Sciences, Gongzhuling, People's Republic of China.

    • Guoqing Tan
    •  & Yuexian Xing
  3. DuPont Agricultural Biotechnology, Wilmington, Delaware, USA.

    • Bailin Li
    •  & Kevin A Fengler
  4. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, People's Republic of China.

    • Haijun Liu
    •  & Jianbing Yan

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Contributions

W.Z. contributed the functional analysis of ZmWAK and preparation of the manuscript. N.Z. contributed the construction and transformation of the chimeric receptor. Q.C., J.Z., X.Z. and Y.C. contributed the fine mapping of qHSR1. B.Z. contributed the sequencing of the ZmWAK alleles. J. Ye contributed the microscopy of S. reiliamun. H.L. and J. Yan contributed the evolutionary analysis. Y.X. and G.T. contributed the field inoculation of head smut. B.L. and K.A.F. contributed the sequencing of the Mo17 and HZ4 BAC clones. J.L. contributed maize transformation. M.X. led the project and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Mingliang Xu.

Integrated supplementary information

Supplementary information

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  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–9.

Excel files

  1. 1.

    Supplementary Table 1

    Primers used in fine mapping and studies of molecular mechanism.

  2. 2.

    Supplementary Table 2

    ZmWAK information in 522 maize lines and 184 teosintes.

  3. 3.

    Supplementary Table 3

    Pedigree of ten inbred lines with HZ4 background.

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DOI

https://doi.org/10.1038/ng.3170

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