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:

Differential regulation of EIN3 stability by glucose and ethylene signalling in plants

Nature volume 425, pages 521–525 (2003)Cite this article

Abstract

Glucose is a global regulator of growth and metabolism that is evolutionarily conserved from unicellular microorganisms to multicellular animals and plants1. In photosynthetic plants, glucose shows hormone-like activities and modulates many essential processes, including embryogenesis, germination, seedling development, vegetative growth, reproduction and senescence2,3. Genetic and phenotypic analyses of Arabidopsis mutants with glucose-insensitive (gin) and glucose-oversensitive (glo) phenotypes have identified an unexpected antagonistic interaction between glucose and the plant stress hormone ethylene. The ethylene-insensitive etr1 and ein2 mutants have glo phenotypes, whereas the constitutive ethylene signalling mutant ctr1 is allelic to gin4 (refs 4, 5). The precise molecular mechanisms underlying the complex signalling network that governs plant growth and development in response to nutrients and plant hormones are mostly unknown. Here we show that glucose enhances the degradation of ETHYLENE-INSENSITIVE3 (EIN3), a key transcriptional regulator in ethylene signalling6,7, through the plant glucose sensor hexokinase8. Ethylene, by contrast, enhances the stability of EIN3. The ein3 mutant has a glo phenotype, and overexpression of EIN3 in transgenic Arabidopsis decreases glucose sensitivity.

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: Functional analysis of EIN3 in maize protoplasts.
Figure 2: Glucose accelerates EIN3 degradation.
Figure 3: Differential glucose and ethylene signalling.
Figure 4: Opposite effects of ethylene and glucose on EIN3 stability in Arabidopsis.

Similar content being viewed by others

References

  1. Rolland, F., Winderickx, J. & Thevelein, J. M. Glucose-sensing mechanisms in eukaryotic cells. Trends Biochem. Sci. 26, 310–317 (2001)

    Article  CAS  Google Scholar 

  2. Smeekens, S. Sugar-induced signal transduction in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 49–81 (2000)

    Article  CAS  Google Scholar 

  3. Rolland, F., Moore, B. & Sheen, J. Sugar sensing and signaling in plants. Plant Cell 14, S185–S205 (2002)

    Article  CAS  Google Scholar 

  4. Zhou, L., Jang, J.-C., Jones, T. L. & Sheen, J. Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc. Natl Acad. Sci. USA 95, 10294–10299 (1998)

    Article  ADS  CAS  Google Scholar 

  5. Cheng, W.-H. et al. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and function. Plant Cell 14, 2723–2743 (2002)

    Article  CAS  Google Scholar 

  6. Chao, Q. et al. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSTIVE3 and related proteins. Cell 89, 1133–1144 (1997)

    Article  CAS  Google Scholar 

  7. Solano, R., Stepanova, A., Chao, Q. & Ecker, J. R. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSTIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 12, 3703–3714 (1998)

    Article  CAS  Google Scholar 

  8. Moore, B. et al. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light and hormonal signaling. Science 300, 332–336 (2003)

    Article  ADS  CAS  Google Scholar 

  9. Chang, C., Kwok, S. F., Bleecker, A. B. & Meyerowitz, E. M. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262, 539–544 (1993)

    Article  ADS  CAS  Google Scholar 

  10. Alonso, J. M. et al. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284, 2148–2152 (1999)

    Article  CAS  Google Scholar 

  11. Jang, J.-C. & Sheen, J. Sugar sensing in higher plants. Plant Cell 6, 1665–1679 (1994)

    Article  CAS  Google Scholar 

  12. Zuo, J., Niu, Q.-W. & Chua, N.-H. An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24, 265–273 (2000)

    Article  CAS  Google Scholar 

  13. Sheen, J. Protein phosphatase activity is required for light-inducible gene expression in maize. EMBO J. 12, 3497–3505 (1993)

    Article  CAS  Google Scholar 

  14. Yanagisawa, S. & Sheen, J. Involvement of maize DOF zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10, 75–89 (1998)

    Article  CAS  Google Scholar 

  15. Hwang, I. & Sheen, J. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383–389 (2001)

    Article  ADS  CAS  Google Scholar 

  16. Kosugi, S. & Ohashi, Y. Cloning and DNA-binding properties of a tobacco ethylene-insensive3 (EIN3) homolog. Nucleic Acids Res. 28, 960–967 (2000)

    Article  CAS  Google Scholar 

  17. Chang, C.-C. et al. Functional analysis of two maize cDNAs encoding T7-like RNA polymerases. Plant Cell 11, 911–926 (1999)

    Article  CAS  Google Scholar 

  18. Wang, K. L.-C., Li, H. & Ecker, J. R. Ethylene biosynthesis and signaling networks. Plant Cell 14, S131–S151 (2002)

    Article  CAS  Google Scholar 

  19. Naidoo, N., Song, W., Hunter-Ensor, M. & Sehgal, A. A role for proteasome in the light response of the timeless clock protein. Science 285, 1737–1741 (1999)

    Article  CAS  Google Scholar 

  20. Osterlund, M. T. et al. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405, 462–466 (2000)

    Article  ADS  CAS  Google Scholar 

  21. Ravid, T. et al. The ubiquitin–proteasome pathway mediates the regulated degradation of mammalian 3-hydroxy-3-methylglutaryl-coenzyme A reductase. J. Biol. Chem. 275, 35840–35847 (2000)

    Article  CAS  Google Scholar 

  22. Fujimoto, S. Y., Ohta, M., Usui, A., Shinshi, H. & Ohme-Takagi, M. Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12, 393–404 (2000)

    Article  CAS  Google Scholar 

  23. Kovtun, Y., Chiu, W.-L., Zeng, W. & Sheen, J. Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 395, 716–720 (1998)

    Article  ADS  CAS  Google Scholar 

  24. Kieber, J. J., Rothenberg, M., Gregg, R., Feldmann, K. A. & Ecker, J. R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72, 427–441 (1993)

    Article  CAS  Google Scholar 

  25. Gray, W. M., Kepinski, S., Rouse, D. & Estelle, M. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271–276 (2001)

    Article  ADS  CAS  Google Scholar 

  26. Lopez-Molina, L., Mongrand, S. & Chua, N.-H. A postgermination development arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl Acad. Sci. USA 98, 4782–4787 (2001)

    Article  ADS  CAS  Google Scholar 

  27. Silverstone, A. L. et al. Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13, 1555–1566 (2001)

    Article  CAS  Google Scholar 

  28. He, J.-X. et al. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc. Natl Acad. Sci. USA 99, 10185–10190 (2002)

    Article  ADS  CAS  Google Scholar 

  29. Vierstra, R. D. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. 8, 135–142 (2003)

    Article  CAS  Google Scholar 

  30. Sheen, J.-Y. & Bogorad, L. Expression of ribulose bisphosphate carboxylase large subunit and three small subunit genes in two cell types of maize leaves. EMBO J. 13, 3417–3422 (1986)

    Article  Google Scholar 

Download references

Acknowledgements

We thank B. Lam for help with antibody preparation and for providing plants; T. Miwa for help with generating transgenic Arabidopsis; M. V. Parthasarathy for the actin antibody; F. Rolland and B. Seed for critically reading the manuscript; J. Callis for the UBQ10–GUS construct; B. Moore for the AtXHK1 mutant; Y. Niwa for the TP–GFP construct; and Y.-H. Cho and R. Patharkar for advice. The work was supported in part by grants from the Ministry of Education, Culture, Sports, Science and Technology, Japan (to S.Y.), and the National Science Foundation and the National Institutes of Health (to J.S.).

Author information

Authors and Affiliations

  1. Research Institute for Bioresources, Okayama University, Chuo 2-20-1, 710-0046, Kurashiki, Japan

    Shuichi Yanagisawa

  2. Department of Molecular Biology, Massachusetts General Hospital, Department of Genetics, Harvard Medical School, Massachusetts, 02114, Boston, USA

    Shuichi Yanagisawa, Sang-Dong Yoo & Jen Sheen

Authors
  1. Shuichi Yanagisawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sang-Dong Yoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jen Sheen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shuichi Yanagisawa.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yanagisawa, S., Yoo, SD. & Sheen, J. Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425, 521–525 (2003). https://doi.org/10.1038/nature01984

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01984

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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