Abstract

To ensure high crop yields in a sustainable manner, a comprehensive understanding of the control of nutrient acquisition is required. In particular, the signalling networks controlling the coordinated utilization of the two most highly demanded mineral nutrients, nitrogen and phosphorus, are of utmost importance. Here, we reveal a mechanism by which nitrate activates both phosphate and nitrate utilization in rice (Oryza sativa L.). We show that the nitrate sensor NRT1.1B interacts with a phosphate signalling repressor SPX4. Nitrate perception strengthens the NRT1.1B–SPX4 interaction and promotes the ubiquitination and degradation of SPX4 by recruiting NRT1.1B interacting protein 1 (NBIP1), an E3 ubiquitin ligase. This in turn allows the key transcription factor of phosphate signalling, PHR2, to translocate to the nucleus and initiate the transcription of phosphorus utilization genes. Interestingly, the central transcription factor of nitrate signalling, NLP3, is also under the control of SPX4. Thus, nitrate-triggered degradation of SPX4 activates both phosphate- and nitrate-responsive genes, implementing the coordinated utilization of nitrogen and phosphorus.

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Data availability

The data that support the findings of this study are available from the corresponding authors upon request.

Additional information

Journal peer review information: Nature Plants thanks Dong Liu, Nicholaus von Wiren, Ying Liu, Ricardo Giehl and other anonymous reviewers for their contribution to the peer review of this work.

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Change history

  • 24 April 2019

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

  • 15 May 2019

    Owing to a technical fault, in the corrected version of the left panel of Fig. 4g, an extraneous vertical line appeared; this has now been removed.

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Acknowledgements

pCAMBIA1300–nLUC/cLUC vectors were kindly provided by J.-M. Zhou, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences. The SPX4progSPX4GUS transgenic rice was kindly provided by C. Mao, College of Life Sciences, Zhejiang University. The authors thank T. O. Jobe (University of Cologne) for proofreading the manuscript. This work was supported by grants from the Chinese Academy of Sciences (XDA08010400), the National Natural Sciences Foundation of China (31500975 and 31771348) and the China Postdoctoral Science Foundation (2017M610126). Research in the laboratory of S. Kopriva was supported by Deutsche Forschungsgemeinschaft (EXC 1028).

Author information

Author notes

  1. These authors contributed equally: Bin Hu, Zhimin Jiang, Wei Wang, Yahong Qiu.

Affiliations

  1. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

    • Bin Hu
    • , Zhimin Jiang
    • , Wei Wang
    • , Yahong Qiu
    • , Zhihua Zhang
    • , Yongqiang Liu
    • , Aifu Li
    • , Xiaokai Gao
    • , Linchuan Liu
    • , Feifei Yu
    • , Sai Kang
    • , Yiqin Wang
    • , Junpeng Xie
    • , Shouyun Cao
    • , Qi Xie
    •  & Chengcai Chu
  2. College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China

    • Yahong Qiu
    • , Zhihua Zhang
    • , Yongqiang Liu
    • , Aifu Li
    • , Junpeng Xie
    •  & Chengcai Chu
  3. Biogle Genome Editing Center, Changzhou, China

    • Yangwen Qian
  4. State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

    • Xiahe Huang
    •  & Yingchun Wang
  5. School of Agriculture, Henan University of Science and Technology, Luoyang, China

    • Lianhe Zhang
  6. Botanical Institute, Cluster of Excellence on Plant Sciences, University of Cologne, Cologne, Germany

    • Stanislav Kopriva

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Contributions

B.H., Z.J. and W.W. designed research, performed experiments, analysed the data and wrote the manuscript. Y. Qiu, Z.Z., Y.L., A.L., X.G., L.L., Y. Qian, X.H., F.Y., S. Kang, Yiq. W., J.X., S.C., L.Z., Ying. W., Q.X. and S. Kopriva conducted some of the experiments. C.C. designed research, wrote the manuscript and supervised the project.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Bin Hu or Chengcai Chu.

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https://doi.org/10.1038/s41477-019-0384-1

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