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:

Synthetic control of flowering in rice independent of the cultivation environment

Nature Plants volume 3, Article number: 17039 (2017) Cite this article

Subjects

Abstract

For genetically homogeneous crops, the timing of flowering is determined largely by the cultivation environment and is strongly associated with the yield and quality of the harvest1. Flowering time and other agronomical traits are often tightly correlated, which can lead to difficulty excluding the effects of flowering time when evaluating the characteristics of different genetic varieties2. Here, we describe the development of transgenic rice plants whose flowering time can be controlled by specific agrochemicals. We first developed non-flowering rice plants by overexpressing a floral repressor gene, Grain number, plant height and heading date 7 (Ghd7)3,4, to inhibit any environmentally induced spontaneous flowering. We then co-transformed plants with a rice florigen gene, Heading date 3a (Hd3a)5, which is induced by the application of specific agrochemicals. This permitted the flowering time to be experimentally controlled regardless of the cultivation environment: some transgenic plants flowered only after agrochemical treatment. Furthermore, plant size and yield-related traits could, in some cases, be increased owing to both a longer duration of vegetative growth and an increased panicle size. This ability to control flowering time experimentally, independently of environmental variables, may lead to production of crops suitable for growth in different climates and facilitate breeding for various agronomical traits.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

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

Figure 1: Non-flowering plants and improved yield-related traits by overexpression of a floral repressor, Ghd7, in a rice variety.
Figure 2: Rescue of delayed flowering in Ghd7-overexpressing plants by ectopic florigen expression and a system for inducing florigen expression by agrochemical treatment.
Figure 3: Agrochemical induction of flowering in rice.
Figure 4: Robustness of floral induction by agrochemicals in rice.

Similar content being viewed by others

References

  1. Jung, C. & Müller, A. E. Flowering time control and applications in plant breeding. Trends Plant Sci. 14, 563–573 (2009).

    Article  CAS  Google Scholar 

  2. Yamamoto, T., Yonemaru, J. & Yano, M. Towards the understanding of complex traits in rice: substantially or superficially? DNA Res. 16, 141–154 (2009).

    Article  CAS  Google Scholar 

  3. Xue, W. et al. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40, 761–767 (2008).

    Article  CAS  Google Scholar 

  4. Weng, X. et al. Grain number, plant height, and heading date7 is a central regulator of growth, development, and stress response. Plant Physiol. 164, 735–747 (2014).

    Article  CAS  Google Scholar 

  5. Doi, K. et al. Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev. 18, 926–936 (2004).

    Article  CAS  Google Scholar 

  6. Kojima, S. et al. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. 43, 1096–1105 (2002).

    Article  CAS  Google Scholar 

  7. Ogiso-Tanaka, E. et al. Natural variation of the RICE FLOWERING LOCUS T 1 contributes to flowering time divergence in rice. PLoS ONE 8, e75959 (2013).

    Article  CAS  Google Scholar 

  8. Komiya, R., Yokoi, S. & Shimamoto, K. A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136, 3443–3450 (2009).

    Article  CAS  Google Scholar 

  9. Itoh, H., Nonoue, Y., Yano, M. & Izawa, T. A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nat. Genet. 42, 635–638 (2010).

    Article  CAS  Google Scholar 

  10. Itoh, H. & Izawa, T. The coincidence of critical day length recognition for florigen gene expression and floral transition under long-day conditions in rice. Mol. Plant 6, 635–649 (2013).

    Article  CAS  Google Scholar 

  11. Hung, H. Y. et al. ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc. Natl Acad. Sci. USA 109, E1913–E1921 (2012).

    Article  CAS  Google Scholar 

  12. Yang, S. et al. Sorghum phytochrome B inhibits flowering in long days by activating expression of SbPRR37 and SbGHD7, repressors of SbEHD1, SbCN8 and SbCN12. PLoS ONE 9, e105352 (2014).

    Article  Google Scholar 

  13. Komiya, R., Ikegami, A., Tamaki, S., Yokoi, S. & Shimamoto, K. Hd3a and RFT1 are essential for flowering in rice. Development 135, 767–774 (2008).

    Article  CAS  Google Scholar 

  14. Matsubara, K. et al. Ehd3, encoding a plant homeodomain finger-containing protein, is a critical promoter of rice flowering. Plant J. 66, 603–612 (2011).

    Article  CAS  Google Scholar 

  15. Hori, K. et al. Hd16, a gene for casein kinase I, is involved in the control of rice flowering time by modulating the day-length response. Plant J. 76, 36–46 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Oikawa, T. & Kyozuka, J. Two-step regulation of LAX PANICLE1 protein accumulation in axillary meristem formation in rice. Plant Cell 21, 1095–1108 (2009).

    Article  CAS  Google Scholar 

  17. Miyoshi, K. et al. PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc. Natl Acad. Sci. USA 101, 875–880 (2004).

    Article  CAS  Google Scholar 

  18. Nemoto, Y., Nonoue, Y., Yano, M. & Izawa, T. Hd1, a CONSTANS ortholog in rice, functions as an Ehd1 repressor through interaction with monocot-specific CCT-domain protein Ghd7. Plant J. 86, 221–233 (2016).

    Article  CAS  Google Scholar 

  19. Ito, Y. & Kurata, N. Disruption of KNOX gene suppression in leaf by introducing its cDNA in rice. Plant Sci. 174, 357–365 (2008).

    Article  CAS  Google Scholar 

  20. Shimono, M. et al. Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19, 2064–2076 (2007).

    Article  CAS  Google Scholar 

  21. Umemura, K. et al. Contribution of salicylic acid glucosyltransferase, OsSGT1, to chemically induced disease resistance in rice plants. Plant J. 57, 463–472 (2009).

    Article  CAS  Google Scholar 

  22. Günl, M., Liew, E. F., David, K. & Putterill, J. Analysis of a post-translational steroid induction system for GIGANTEA in Arabidopsis. BMC Plant Biol. 9, 141 (2009).

    Article  Google Scholar 

  23. Krzymuski, M. et al. The dynamics of FLOWERING LOCUS T expression encodes long-day information. Plant J. 83, 952–961 (2015).

    Article  CAS  Google Scholar 

  24. Yeoh, C. C., Balcerowicz, M., Laurie, R., Macknight, R. & Putterill, J. Developing a method for customized induction of flowering. BMC Biotechnol. 11, 36 (2011).

    Article  CAS  Google Scholar 

  25. Saijo, T. & Nagasawa, A. Development of a tightly regulated and highly responsive copper-inducible gene expression system and its application to control of flowering time. Plant Cell Rep. 33, 47–59 (2014).

    Article  CAS  Google Scholar 

  26. Zhang, H. et al. Precocious flowering in trees: the FLOWERING LOCUS T gene as a research and breeding tool in Populus. J. Exp. Bot. 61, 2549–2560 (2010).

    Article  CAS  Google Scholar 

  27. Kim, S. L., Choi, M., Jung, K. H. & An, G. Analysis of the early-flowering mechanisms and generation of T-DNA tagging lines in Kitaake, a model rice cultivar. J. Exp. Bot. 64, 4169–4182 (2013).

    Article  CAS  Google Scholar 

  28. Izawa, T. et al. Os-GIGANTEA confers robust diurnal rhythms on the global transcriptome of rice in the field. Plant Cell 23, 1741–1755 (2011).

    Article  CAS  Google Scholar 

  29. Breitling, R., Armengaud, P., Amtmann, A. & Herzyk, P. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett. 573, 83–92 (2004).

    Article  CAS  Google Scholar 

  30. 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 

  31. Endo-Higashi, N. & Izawa, T. Flowering time genes Heading date 1 and Early heading date 1 together control panicle development in rice. Plant Cell Physiol. 52, 1083–1094 (2011).

    Article  CAS  Google Scholar 

  32. Sugio, T., Satoh, J., Matsuura, H., Shinmyo, A. & Kato, K. The 5′-untranslated region of the Oryza sativa alcohol dehydrogenase gene functions as a translational enhancer in monocotyledonous plant cells. J. Biosci. Bioeng. 105, 300–302 (2008).

    Article  CAS  Google Scholar 

  33. Ochman, H., Gerber, A. S. & Hartl, D. L. Genetic applications of an inverse polymerase chain reaction. Genetics 120, 621–623 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Taoka, K. et al. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476, 332–335 (2011).

    Article  CAS  Google Scholar 

  35. 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 

Download references

Acknowledgements

This work was supported by grants from MAFF, Japan (Genomics for Agricultural Innovation, GPN-1001; Genomics-based Technology for Agricultural Improvement, GMO-1005; PFT-1001) to T.I.

Author information

Author notes

  1. Ryo Okada, Yasue Nemoto & Naokuni Endo-Higashi

    Present address: †Present addresses: Department of Biological Mechanisms and Functions, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan (R.O.); Field Omics Unit, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan (Y.N.); Japan Grain Inspection Association, Tyuohu-ku, Tokyo 103-0026, Japan (N.E.-H.).,

Authors and Affiliations

  1. Functional Plant Research Unit, National Institute of Agrobiological Sciences, Tsukuba, 305-8602, Ibaraki, Japan

    Ryo Okada, Yasue Nemoto, Naokuni Endo-Higashi & Takeshi Izawa

  2. Department of Agriculture, Laoratory of Plant Breeding & Genetics, University of Tokyo, Bunkyo-ku, 113-8657, Tokyo, Japan

    Takeshi Izawa

Authors
  1. Ryo Okada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yasue Nemoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Naokuni Endo-Higashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takeshi Izawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T.I. conceived and conducted the entire experiments of this work. R.O. performed most of experiments in this work. Y.N. performed the analysis of Ghd7-overexpressing plant in rice. N.E.-H. performed the effect of Hd3a ectopic expression in the Ghd7-overexpressing plant in rice. T.I. and R.O. wrote the manuscript and the others revised it.

Corresponding author

Correspondence to Takeshi Izawa.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Okada, R., Nemoto, Y., Endo-Higashi, N. et al. Synthetic control of flowering in rice independent of the cultivation environment. Nature Plants 3, 17039 (2017). https://doi.org/10.1038/nplants.2017.39

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2017.39

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