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Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition

Nature Plants volume 3, Article number: 17029 (2017) Cite this article

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Abstract

Plants uptake nitrogen (N) from the soil mainly in the form of nitrate. However, nitrate is often distributed heterogeneously in natural soil. Plants, therefore, have a systemic long-distance signalling mechanism by which N starvation on one side of the root leads to a compensatory N uptake on the other N-rich side1,2. This systemic N acquisition response is triggered by a root-to-shoot mobile peptide hormone, C-TERMINALLY ENCODED PEPTIDE (CEP), originating from the N-starved roots3,4, but the molecular nature of the descending shoot-to-root signal remains elusive. Here, we show that phloem-specific polypeptides that are induced in leaves upon perception of root-derived CEP act as descending long-distance mobile signals translocated to each root. These shoot-derived polypeptides, which we named CEP DOWNSTREAM 1 (CEPD1) and CEPD2, upregulate the expression of the nitrate transporter gene NRT2.1 in roots specifically when nitrate is present in the rhizosphere. Arabidopsis plants deficient in this pathway show impaired systemic N acquisition response accompanied with N-deficiency symptoms. These fundamental mechanistic insights should provide a conceptual framework for understanding systemic nutrient acquisition responses in plants.

Plants have evolved sophisticated strategies allowing them to modulate the efficiency of root nitrate acquisition in response to fluctuating external nitrate availability. One striking example of such a nitrate acquisition system is when local nitrogen (N)-starvation on one side of the root system leads to an upregulation of nitrate uptake in the other part of the root system1,2. This compensatory nitrate acquisition response is called systemic N-demand signalling.

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Figure 1: Identification and characterization of At1g06830 (CEPD1) and At2g47880 (CEPD2) polypeptides.
Figure 2: CEPD1 and CEPD2 are required for systemic N acquisition.
Figure 3: CEPD1 and CEPD2 are shoot-to-root mobile signals.
Figure 4: Distribution and action of CEPD1 and CEPD2 under split-root conditions.

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Acknowledgements

We thank Y. Sugisawa (The University of Tokyo) for the microarray analysis. This research was supported by a Grant-in-Aid for Scientific Research (S) (number 25221105) and a Grant-in-Aid for Scientific Research on Innovative Areas (number 15H05957) from the Japan Society for Promotion of Science.

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  1. Yuri Ohkubo and Mina Tanaka: These authors contributed equally to this work.

Authors and Affiliations

  1. Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa, 464-8602, Nagoya, Japan

    Yuri Ohkubo, Mina Tanaka, Ryo Tabata, Mari Ogawa-Ohnishi & Yoshikatsu Matsubayashi

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  1. Yuri Ohkubo
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  2. Mina Tanaka
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Contributions

Y.M. conceived this project and designed the experiments with input from Y.O., M.T., R.T. and M.O.-O. All authors performed the experiments and interpreted the results. Y.M. wrote the manuscript with input from Y.O.

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Correspondence to Yoshikatsu Matsubayashi.

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The authors declare no competing financial interests.

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Supplementary Figures 1–7 and Supplementary Tables 1 and 2. (PDF 2207 kb)

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Ohkubo, Y., Tanaka, M., Tabata, R. et al. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nature Plants 3, 17029 (2017). https://doi.org/10.1038/nplants.2017.29

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