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.

  • Article
  • Published:

NaKR1 regulates long-distance movement of FLOWERING LOCUS T in Arabidopsis

Nature Plants volume 2, Article number: 16075 (2016) Cite this article

Subjects

Abstract

Flowering plants perceive photoperiodic signals in leaves to generate mobile stimuli required for the induction of flower formation at shoot apices. Although FLOWERING LOCUS T (FT) has been identified as part of the mobile floral stimuli in Arabidopsis thaliana, the mechanisms underlying long-distance movement of FT from leaves to shoot apices remain largely unclear. Here we show that a heavy-metal-associated (HMA) domain-containing protein, SODIUM POTASSIUM ROOT DEFECTIVE 1 (NaKR1), is activated by CONSTANS (CO) under long-day conditions and regulates long-distance movement of FT in Arabidopsis. Loss of function of NaKR1 compromises FT transport to shoot apices through sieve elements, causing late flowering under long-day conditions. NaKR1 and FT share similar expression patterns and subcellular localization, and interact with each other in vivo. Grafting experiments demonstrate that NaKR1 promotes flowering through mediating FT translocation from leaves to shoot apices. Thus, photoperiodic control of floral induction requires NaKR1-mediated long-distance delivery of florigenic signals.

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: NaKR1 promotes flowering under long-day conditions.
Figure 2: NaKR1 is expressed and functional in leaf vascular tissues.
Figure 3: NaKR1 is localized in the phloem.
Figure 4: NaKR1 interacts with FT.
Figure 5: NaKR1 affects FT transport.
Figure 6: NaKR1 is required for the long-distance movement of FT.

Similar content being viewed by others

References

  1. Knott, J. E. Effect of localized photoperiod on spinach. Proc. Am. Soc. Hortic. Sci. 31, 152–154 (1934).

    Google Scholar 

  2. Chailakhyan, M. K. New facts in support of the hormonal theory of plant development. Compt. Rend. Acad. Sci. URSS 13, 79–83 (1936).

    Google Scholar 

  3. Corbesier, L. et al. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030–1033 (2007).

    Article  CAS  Google Scholar 

  4. Jaeger, K. E. & Wigge, P. A. FT protein acts as a long-range signal in Arabidopsis. Curr. Biol. 17, 1050–1054 (2007).

    Article  CAS  Google Scholar 

  5. Mathieu, J., Warthmann, N., Küttner, F. & Schmid, M. Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr. Biol. 17, 1055–1060 (2007).

    Article  CAS  Google Scholar 

  6. Tamaki, S., Matsuo, S., Wong, H. L., Yokoi, S. & Shimamoto, K. Hd3a protein is a mobile flowering signal in rice. Science 316, 1033–1036 (2007).

    Article  CAS  Google Scholar 

  7. Lin, M.-K. et al. FLOWERING LOCUS T protein may act as the long distance florigenic signal in the cucurbits. Plant Cell 19, 1488–1506 (2007).

    Article  CAS  Google Scholar 

  8. Lifschitz, E. et al. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl Acad. Sci. USA 103, 6398–6403 (2006).

    Article  CAS  Google Scholar 

  9. Wigge, P. A. et al. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309, 1056–1059 (2005).

    Article  CAS  Google Scholar 

  10. Suarez-Lopez, P. et al. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410, 1116–1120 (2001).

    Article  CAS  Google Scholar 

  11. An, H. et al. CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131, 3615–3626 (2004).

    Article  CAS  Google Scholar 

  12. Samach, A. et al. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613–1616 (2000).

    Article  CAS  Google Scholar 

  13. Takada, S. & Goto, K. TERMINAL FLOWER2, an Arabidopsis homolog of HETEROCHROMATIN PROTEIN1, counteracts the activation of FLOWERING LOCUS T by CONSTANS in the vascular tissues of leaves to regulate flowering time. Plant Cell 15, 2856–2865 (2003).

    Article  CAS  Google Scholar 

  14. Liu, L. et al. FTIP1 is an essential regulator required for florigen transport. PLoS Biol. 10, e1001313 (2012).

    Article  CAS  Google Scholar 

  15. Abe, M. et al. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309, 1052–1056 (2005).

    Article  CAS  Google Scholar 

  16. Kardailsky, I. et al. Activation tagging of the floral inducer FT. Science 286, 1962–1965 (1999).

    Article  CAS  Google Scholar 

  17. Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M. & Araki, T. A pair of related genes with antagonistic roles in mediating flowering signals. Science 286, 1960–1962 (1999).

    Article  CAS  Google Scholar 

  18. Tehseen, M., Cairns, N., Sherson, S. & Cobbett, C. S. Metallochaperone-like genes in Arabidopsis thaliana. Metallomics 2, 556–564 (2010).

    Article  CAS  Google Scholar 

  19. de Abreu-Neto, J. B., Turchetto-Zolet, A. C., de Oliveira, L. F. V., Bodanese Zanettini, M. H. & Margis-Pinheiro, M. Heavy metal-associated isoprenylated plant protein (HIPP): characterization of a family of proteins exclusive to plants. FEBS J. 280, 1604–1616 (2013).

    Article  Google Scholar 

  20. Tian, H. et al. Arabidopsis NPCC6/NaKR1 is a phloem mobile metal binding protein necessary for phloem function and root meristem maintenance. Plant Cell 22, 3963–3979 (2010).

    Article  CAS  Google Scholar 

  21. Suzuki, N., Yamaguchi, Y., Koizumi, N. & Sano, H. Functional characterization of a heavy metal binding protein CdI19 from Arabidopsis. Plant J. 32, 165–173 (2002).

    Article  CAS  Google Scholar 

  22. Gao, W., Xiao, S., Li, H.-Y., Tsao, S.-W. & Chye, M.-L. Arabidopsis thaliana acyl-CoA-binding protein ACBP2 interacts with heavy-metal-binding farnesylated protein AtFP6. New Phytol. 181, 89–102 (2009).

    Article  CAS  Google Scholar 

  23. Barth, O., Vogt, S., Uhlemann, R., Zschiesche, W. & Humbeck, K. Stress induced and nuclear localized HIPP26 from Arabidopsis thaliana interacts via its heavy metal associated domain with the drought stress related zinc finger transcription factor ATHB29. Plant Mol. Biol. 69, 213–226 (2009).

    Article  CAS  Google Scholar 

  24. Zhang, C., Barthelson, R. A., Lambert, G. M. & Galbraith, D. W. Global characterization of cell-specific gene expression through fluorescence-activated sorting of nuclei. Plant Physiol. 147, 30–40 (2008).

    Article  CAS  Google Scholar 

  25. Brady, S. M. et al. A high-resolution root spatiotemporal map reveals do expression patterns. Science 318, 801–806 (2007).

    Article  CAS  Google Scholar 

  26. Deeken, R. et al. Identification of Arabidopsis thaliana phloem RNAs provides a search criterion for phloem-based transcripts hidden in complex datasets of microarray experiments. Plant J. 55, 746–759 (2008).

    Article  CAS  Google Scholar 

  27. Schwab, R., Ossowski, S., Riester, M., Warthmann, N. & Weigel, D. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18, 1121–1133 (2006).

    Article  CAS  Google Scholar 

  28. Hou, X. et al. Nuclear factor Y-mediated H3K27me3 demethylation of the SOC1 locus orchestrates flowering responses of Arabidopsis. Nature Commun. 5, 4601 (2014).

    Article  CAS  Google Scholar 

  29. Tiwari, S. B. et al. The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol. 187, 57–66 (2010).

    Article  CAS  Google Scholar 

  30. Imlau, A., Truernit, E. & Sauer, N. Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11, 309–322 (1999).

    Article  CAS  Google Scholar 

  31. Nelson, B. K., Cai, X. & Nebenführ, A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126–1136 (2007).

    Article  CAS  Google Scholar 

  32. Yamaguchi, A., Kobayashi, Y., Goto, K., Abe, M. & Araki, T. TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol. 46, 1175–1189 (2005).

    Article  CAS  Google Scholar 

  33. Yoo, S. J., Hong, S. M., Jung, H. S. & Ahn, J. H. The cotyledons produce sufficient FT protein to induce flowering: evidence from cotyledon micrografting in Arabidopsis. Plant Cell Physiol. 54, 119–128 (2013).

    Article  CAS  Google Scholar 

  34. Notaguchi, M. et al. Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering. Plant Cell Physiol. 49, 1645–1658 (2008).

    Article  CAS  Google Scholar 

  35. Bernier, G., Havelange, A., Houssa, C., Petitjean, A. & Lejeune, P. Physiological signals that induce flowering. Plant Cell 5, 1147–1155 (1993).

    Article  CAS  Google Scholar 

  36. Wahl, V. et al. Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339, 704–707 (2013).

    Article  CAS  Google Scholar 

  37. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

    Article  CAS  Google Scholar 

  38. Liu, C. et al. Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development 134, 1901–1910 (2007).

    Article  CAS  Google Scholar 

  39. Chen, L., Wang, F., Wang, X. & Liu, Y.-G. Robust one-tube Ω-PCR strategy accelerates precise sequence modification of plasmids for functional genomics. Plant Cell Physiol. 54, 634–642 (2013).

    Article  CAS  Google Scholar 

  40. Li, D. et al. A repressor complex governs the integration of flowering signals in Arabidopsis. Dev. Cell 15, 110–120 (2008).

    Article  CAS  Google Scholar 

  41. Yu, H., Yang, S. H. & Goh, C. J. DOH1, a class 1 knox gene, is required for maintenance of the basic plant architecture and floral transition in orchid. Plant Cell 12, 2143–2159 (2000).

    Article  CAS  Google Scholar 

  42. Sparkes, I. A., Runions, J., Kearns, A. & Hawes, C. Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nature Protoc. 1, 2019–2025 (2006).

    Article  CAS  Google Scholar 

  43. Wilson, S. M. & Bacic, A. Preparation of plant cells for transmission electron microscopy to optimize immunogold labeling of carbohydrate and protein epitopes. Nature Protoc. 7, 1716–1727 (2012).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. M. Ward for providing nakr1-1 seeds. This work was supported by Academic Research Funds (MOE2011-T2-2-008) from the Ministry of Education, Singapore, the Singapore National Research Foundation Investigatorship Programme (NRF-NRFI2016-02) and intramural research support from National University of Singapore and Temasek Life Sciences Laboratory.

Author information

Authors and Affiliations

  1. Department of Biological Sciences and Temasek Life Sciences Laboratory, National University of Singapore, Singapore, 117543, Singapore

    Yang Zhu, Lu Liu, Lisha Shen & Hao Yu

Authors
  1. Yang Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lisha Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hao Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Y.Z. and H.Y. conceived and designed the study. Y.Z., L.L. and L.S. performed the experiments. Y.Z., L.S. and H.Y. analysed data and wrote the paper.

Corresponding author

Correspondence to Hao Yu.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figs 1-12, Supplementary Table 1, and Supplementary Materials and Methods. (PDF 3220 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, Y., Liu, L., Shen, L. et al. NaKR1 regulates long-distance movement of FLOWERING LOCUS T in Arabidopsis. Nature Plants 2, 16075 (2016). https://doi.org/10.1038/nplants.2016.75

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2016.75

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