A transcription factor coordinating internode elongation and photoperiodic signals in rice

Nature Plants volume 5, pages358–362(2019)Cite this article

Subjects

Abstract

In several plant species, inflorescence formation is accompanied by stem elongation. Both processes are accelerated in rice upon perception of shortening days. Here, we show that PREMATURE INTERNODE ELONGATION 1 (PINE1), encoding a rice zinc-finger transcription factor, reduces the sensitivity of the stem to gibberellin (GA). The florigens reduce PINE1 expression to increase stem responsiveness to GA and promote flowering. These data indicate the existence of a regulatory network coordinating flowering and GA-dependent growth.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

Rent or Buy

All prices are NET prices.

Fig. 1: Identification of PINE1 and regulation of its expression by photoperiodic and florigenic signals.
Fig. 2: Mutation of PINE1 increases the sensitivity of the stem to GAs and induces stem elongation.

Data availability

The RNA-seq data that support the findings of this study have been deposited in the GEO with the series record number GSE90493.

References

  1. 1.

    Brambilla, V. & Fornara, F. J. Integr. Plant Biol. 55, 410–418 (2013).

    CAS  Article  Google Scholar 

  2. 2.

    Zhao, J. et al. New Phytol. 208, 936–948 (2015).

    CAS  Article  Google Scholar 

  3. 3.

    Taoka, K. et al. Nature 476, 332–335 (2011).

    CAS  Article  Google Scholar 

  4. 4.

    Kobayashi, K. et al. Plant Cell 24, 1848–1859 (2012).

    CAS  Article  Google Scholar 

  5. 5.

    Tamaki, S. et al. Proc. Natl Acad. Sci. USA 112, E901–E910 (2015).

    CAS  Article  Google Scholar 

  6. 6.

    Hedden, P. & Sponsel, V. J. Plant Growth Regul. 34, 740–760 (2015).

    CAS  Article  Google Scholar 

  7. 7.

    Spielmeyer, W., Ellis, M. H. & Chandler, P. M. Proc. Natl Acad. Sci. USA 99, 9043–9048 (2002).

    CAS  Article  Google Scholar 

  8. 8.

    Harberd, N. P. et al. Nature 400, 256–261 (1999).

    Article  Google Scholar 

  9. 9.

    Sakamoto, T. et al. Nat. Biotechnol. 21, 909–913 (2003).

    CAS  Article  Google Scholar 

  10. 10.

    Hedden, P. & Thomas, S. G. Biochem. J. 444, 11–25 (2012).

    CAS  Article  Google Scholar 

  11. 11.

    Kaneko, M. et al. Plant J. 35, 104–115 (2003).

    CAS  Article  Google Scholar 

  12. 12.

    Furutani, I., Sukegawa, S. & Kyozuka, J. Plant J. 46, 503–511 (2006).

    CAS  Article  Google Scholar 

  13. 13.

    Doi, K. et al. Genes Dev. 18, 926–936 (2004).

    CAS  Article  Google Scholar 

  14. 14.

    Brambilla, V. et al. Plant Cell 29, 2801–2816 (2017).

    CAS  Article  Google Scholar 

  15. 15.

    Miao, J. et al. Cell Res. 23, 1233–1236 (2013).

    CAS  Article  Google Scholar 

  16. 16.

    Hoshikawa, K. The Growing Rice Plant (Nobunkyo, 1989).

  17. 17.

    Itoh, J. I., Kitano, H., Matsuoka, M. & Nagato, Y. Plant Cell 12, 2161–2174 (2000).

    CAS  Article  Google Scholar 

  18. 18.

    Sentoku, N. et al. Plant Cell 11, 1651–1664 (1999).

    CAS  Article  Google Scholar 

  19. 19.

    Tsuda, K., Ito, Y., Sato, Y. & Kurata, N. Plant Cell 23, 4368–4381 (2011).

    CAS  Article  Google Scholar 

  20. 20.

    Itoh, H., Ueguchi-Tanaka, M., Sato, Y., Ashikari, M. & Matsuoka, M. Plant Cell 14, 57–70 (2002).

    CAS  Article  Google Scholar 

  21. 21.

    Sakamoto, T. et al. Plant Physiol. 125, 1508–1516 (2001).

    CAS  Article  Google Scholar 

  22. 22.

    Nagai, K. et al. AoB Plants 6, plu028 (2014).

    Article  Google Scholar 

  23. 23.

    Gómez-Ariza, J. et al. J. Exp. Bot. 66, 2027–2039 (2015).

    Article  Google Scholar 

  24. 24.

    Fornara, F. et al. Plant Physiol. 135, 2207–2219 (2004).

    CAS  Article  Google Scholar 

  25. 25.

    Kim, D. et al. Genome Biol. 14, R36 (2013).

    Article  Google Scholar 

  26. 26.

    Langmead, B. & Salzberg, S. L. Nat. Methods 9, 357–359 (2012).

    CAS  Article  Google Scholar 

  27. 27.

    Anders, S., Pyl, P. T. & Huber, W. Bioinformatics 31, 166–169 (2015).

    CAS  Article  Google Scholar 

  28. 28.

    Robinson, M. D., McCarthy, D. J. & Smyth, G. K. Bioinformatics 26, 139–140 (2010).

    CAS  Article  Google Scholar 

  29. 29.

    Gentleman, R. C. et al. Genome Biol. 5, R80 (2004).

    Article  Google Scholar 

  30. 30.

    Mi, H., Muruganujan, A., Casagrande, J. T. & Thomas, P. D. Nat. Protoc. 8, 1551–1566 (2013).

    Article  Google Scholar 

  31. 31.

    Hiei, Y., Ohta, S., Komari, T. & Kumashiro, T. Plant J. 6, 271–282 (1994).

    CAS  Article  Google Scholar 

  32. 32.

    Wild, M. et al. Dev. Cell 37, 190–200 (2016).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We are grateful to S. Tamaki for technical assistance with some experiments. The pACTIN vector was kindly provided by L. Dreni (IBMCP, CSIC, University of Valencia, Valencia) and the CRISPR–Cas9 vector by L.-J. Qu (Peking University and National Plant Gene Research Center, Beijing). We thank A. Costa and the NOLIMITS microscopy facility for technical support. This work was supported by an ERC Starting Grant (no. 260963) to F.F.

Author information

Affiliations

  1. Department of Biosciences, University of Milan, Milan, Italy

    Jorge Gómez-Ariza, Vittoria Brambilla, Giulio Vicentini, Martina Landini, Martina Cerise, Roshi Shrestha, Francesca Galbiati, Elisabetta Caporali & Fabio Fornara

  2. Department of Agricultural and Environmental Sciences—Production, Territory, Agroenergy, University of Milan, Milan, Italy

    Vittoria Brambilla & Remo Chiozzotto

  3. Instituto de Biologıa Molecular y Celular de Plantas (IBMCP), Universidad Politecnica de Valencia-Consejo Superior de Investigaciones Cientıficas (CSIC), Valencia, Spain

    Esther Carrera & Isabel López Díaz

Authors
  1. Jorge Gómez-Ariza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vittoria Brambilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giulio Vicentini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martina Landini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martina Cerise
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Esther Carrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Roshi Shrestha
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Remo Chiozzotto
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Francesca Galbiati
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Elisabetta Caporali
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Isabel López Díaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Fabio Fornara
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.G.-A., V.B., G.V., M.L., M.C., R.S. and F.G. performed the experiments, generated and analysed the transgenic plants and performed the hormone treatments. R.C. analysed the RNA-seq data. E.Carrera and I.L.D. quantified the bioactive GAs. E.Caporali performed the scanning electron microscopy. F.F. and J.G.-A. conceived the project and wrote the manuscript.

Corresponding author

Correspondence to Fabio Fornara.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Journal peer review information Nature Plants thanks Junko Kyozuka and other anonymous reviewers for their contribution to the peer review of this work.

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figures 1–10 and Supplementary Table 1.

Reporting Summary

Dataset S1

RNA-seq of Nipponbare and T65 shoot apices during meristem commitment.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gómez-Ariza, J., Brambilla, V., Vicentini, G. et al. A transcription factor coordinating internode elongation and photoperiodic signals in rice. Nat. Plants 5, 358–362 (2019). https://doi.org/10.1038/s41477-019-0401-4

Download citation

Further reading

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