Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

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

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

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

References

  1. Gansel, X., Munos, S., Tillard, P. & Gojon, A. Differential regulation of the NO3– and NH4+ transporter genes AtNrt2.1 and AtAmt1.1 in Arabidopsis: relation with long-distance and local controls by N status of the plant. Plant J. 26, 143–155 (2001).

    Google Scholar 

  2. Ruffel, S. et al. Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc. Natl Acad. Sci. USA 108, 18524–18529 (2011).

    Google Scholar 

  3. Tabata, R . et al. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346, 343–346 (2014).

    Google Scholar 

  4. Ohyama, K., Ogawa, M. & Matsubayashi, Y. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J. 55, 152–160 (2008).

    Google Scholar 

  5. Delay, C., Imin, N. & Djordjevic, M. A. CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants. J. Exp. Bot. 64, 5383–5394 (2013).

    Google Scholar 

  6. Roberts, I. et al. The CEP family in land plants: evolutionary analyses, expression studies, and role in Arabidopsis shoot development. J. Exp. Bot. 64, 5371–5381 (2013).

    Google Scholar 

  7. Huault, E. et al. Local and systemic regulation of plant root system architecture and symbiotic nodulation by a receptor-like kinase. PLoS Genet. 10, e1004891 (2014).

    Google Scholar 

  8. Endo, M., Shimizu, H. & Araki, T. Rapid and simple isolation of vascular, epidermal and mesophyll cells from plant leaf tissue. Nat. Protoc. 11, 1388–1395 (2016).

    Google Scholar 

  9. Ogilvie, H. A., Imin, N. & Djordjevic, M. A. Diversification of the C-TERMINALLY ENCODED PEPTIDE (CEP) gene family in angiosperms, and evolution of plant-family specific CEP genes. BMC Genomics 15, 870 (2014).

    Google Scholar 

  10. Rouhier, N., Couturier, J. & Jacquot, J. P. Genome-wide analysis of plant glutaredoxin systems. J. Exp. Bot. 57, 1685–1696 (2006).

    Google Scholar 

  11. Gutsche, N., Thurow, C., Zachgo, S. & Gatz, C. Plant-specific CC-type glutaredoxins: functions in developmental processes and stress responses. Biol. Chem. 396, 495–509 (2015).

    Google Scholar 

  12. Xing, S., Rosso, M. G. & Zachgo, S. ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana. Development 132, 1555–1565 (2005).

    Google Scholar 

  13. Xing, S. & Zachgo, S. ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. Plant J. 53, 790–801 (2008).

    Google Scholar 

  14. Patterson, K . et al. Nitrate-regulated glutaredoxins control Arabidopsis primary root growth. Plant Physiol. 170, 989–999 (2016).

    Google Scholar 

  15. Filleur, S. & Daniel-Vedele, F. Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display. Planta 207, 461–469 (1999).

    Google Scholar 

  16. Chiou, T. J. & Lin, S. I. Signaling network in sensing phosphate availability in plants. Annu. Rev. Plant Biol. 62, 185–206 (2011).

    Google Scholar 

  17. Vert, G. A., Briat, J. F. & Curie, C. Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol. 132, 796–804 (2003).

    Google Scholar 

  18. Okamoto, S., Shinohara, H., Mori, T., Matsubayashi, Y. & Kawaguchi, M. Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat. Commun. 4, 2191 (2013).

    Google Scholar 

  19. Driscoll, S. P., Prins, A., Olmos, E., Kunert, K. J. & Foyer, C. H. Specification of adaxial and abaxial stomata, epidermal structure and photosynthesis to CO2 enrichment in maize leaves. J. Exp. Bot. 57, 381–390 (2006).

    Google Scholar 

  20. Kuromori, T . et al. A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J. 37, 897–905 (2004).

    Google Scholar 

  21. Alonso, J. M. et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653–657 (2003).

  22. Turnbull, C. G., Booker, J. P. & Leyser, H. M. Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J. 32, 255–262 (2002).

    Google Scholar 

Download references

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.

Author information

Author notes

  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

Authors
  1. Yuri Ohkubo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mina Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ryo Tabata
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mari Ogawa-Ohnishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoshikatsu Matsubayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Corresponding author

Correspondence to Yoshikatsu Matsubayashi.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2017.29

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing