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NIN interacts with NLPs to mediate nitrate inhibition of nodulation in Medicago truncatula

Nature Plants volume 4, pages 942–952 (2018)Cite this article

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An Author Correction to this article was published on 16 November 2018

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Abstract

Legume plants can assimilate inorganic nitrogen and have access to fixed nitrogen through symbiotic interaction with diazotrophic bacteria called rhizobia. Symbiotic nitrogen fixation is an energy-consuming process and is strongly inhibited when sufficient levels of fixed nitrogen are available, but the molecular mechanisms governing this regulation are largely unknown. The transcription factor nodule inception (NIN) is strictly required for nodulation and belongs to a family of NIN-like proteins (NLPs), which have been implicated in the regulation of nitrogen homeostasis in Arabidopsis. Here, we show that mutation or downregulation of NLP genes prevents nitrate inhibition of infection, nodule formation and nitrogen fixation. We find that NIN and NLPs physically interact through their carboxy-terminal PB1 domains. Furthermore, we find that NLP1 is required for the expression of nitrate-responsive genes and that nitrate triggers NLP1 re-localization from the cytosol to the nucleus. Finally, we show that NLP1 can suppress NIN activation of CRE1 expression in Nicotiana benthamiana and Medicago truncatula. Our findings highlight a central role for NLPs in the suppression of nodulation by nitrate.

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Fig. 1: Nitrate-tolerant phenotype of nodulation in NLP-RNAi roots.
Fig. 2: The NLP1 mutants and overexpression plants symbiotic phenotype.
Fig. 3: NIN interacts with NLPs.
Fig. 4: NLP1 is involved in the nitrate signalling pathway and nitrate triggers the shuttling of NLP1 from the cytosol to the nucleus.
Fig. 5: NLP1 suppresses NIN activation of target gene expression.
Fig. 6: A proposed model of the role of the NIN–NLP complex in nitrate inhibition of nodulation.

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Data availability

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

Change history

  • 16 November 2018

    In the version of this Article originally published, the name of author Zhenpeng Luo was incorrectly listed as Zhenpeng Luo Luo. Additionally, nitrate in Fig. 6b was incorrectly shown as ‘NO3+’ rather than ‘NO3–’. This has now been amended.

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Acknowledgements

We thank G. Hong (Institute of Biochemistry and Cell Biology, CAS, China) for help with the ARA assays, Y. Wang (Shandong Agricultural University, China) for kindly providing the proNRP-YFP vector and J. Murray (SIPPE, China) for making constructive suggestions on the work and helpful comments on the manuscript. This work was funded by grants from the National Key R&D Program of China (2016YFA0500500 and 2016YFD0100702), the National Natural Science Foundation of China (31670242) and XDPB0400 of CAS to F.X.

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Authors and Affiliations

  1. National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China

    Jie-shun Lin, Xiaolin Li, Zhenpeng Luo & Fang Xie

  2. University of the Chinese Academy of Sciences, Beijing, China

    Jie-shun Lin & Zhenpeng Luo

  3. Noble Research Institute, LLC, Ardmore, OK, USA

    Kirankumar S. Mysore & Jiangqi Wen

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  1. Jie-shun Lin
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  2. Xiaolin Li
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Contributions

F.X. and J.-s.L. designed the research. J.-s.L. conducted most of the experiments. X.L. did the sections. Z.L. conducted the ARA assays. K.S.M. and J.W. carried out the Tnt1 insertion screening. F.X. and J.-s.L. wrote the paper.

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Correspondence to Fang Xie.

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Lin, Js., Li, X., Luo, Z. et al. NIN interacts with NLPs to mediate nitrate inhibition of nodulation in Medicago truncatula. Nature Plants 4, 942–952 (2018). https://doi.org/10.1038/s41477-018-0261-3

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