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:

Two-component circuitry in Arabidopsis cytokinin signal transduction

Abstract

Cytokinins are essential plant hormones that are involved in shoot meristem and leaf formation, cell division, chloroplast biogenesis and senescence. Although hybrid histidine protein kinases have been implicated in cytokinin perception in Arabidopsis, the action of histidine protein kinase receptors and the downstream signalling pathway has not been elucidated to date. Here we identify a eukaryotic two-component signalling circuit that initiates cytokinin signalling through distinct hybrid histidine protein kinase activities at the plasma membrane. Histidine phosphotransmitters act as signalling shuttles between the cytoplasm and nucleus in a cytokinin-dependent manner. The short signalling circuit reaches the nuclear target genes by enabling nuclear response regulators ARR1, ARR2 and ARR10 as transcription activators. The cytokinin-inducible ARR4, ARR5, ARR6 and ARR7 genes encode transcription repressors that mediate a negative feedback loop in cytokinin signalling. Ectopic expression in transgenic Arabidopsis of ARR2, the rate-limiting factor in the response to cytokinin, is sufficient to mimic cytokinin in promoting shoot meristem proliferation and leaf differentiation, and in delaying leaf senescence.

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

Access options

Buy this article

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

Figure 1: Cytokinin signalling is initiated by multiple histidine protein kinase receptors.
Figure 2: AHP acts as a shuttle between the cytoplasm and nucleus in cytokinin signalling.
Figure 3: Opposite regulations of cytokinin primary response gene transcription by two types of ARR protein.
Figure 4: Ectopic expression of ARR2 is sufficient to promote cytokinin responses in transgenic tissues and plants.
Figure 5: Model of the cytokinin signal transduction pathway in Arabidopsis.

Similar content being viewed by others

References

  1. Davies, P. J. Plant Hormones; Physiology, Biochemistry and Molecular Biology (ed. Davies, P. J.) (Kluwer Academic, The Netherlands, 1995).

    Google Scholar 

  2. Mok, D. W. & Mok, M. C. Cytokinin metabolism and action. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 89–118 (2001).

    Article  MathSciNet  CAS  Google Scholar 

  3. Kakimoto, T. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274, 982–985 (1996).

    Article  ADS  CAS  Google Scholar 

  4. Kiba, T. et al. Differential expression of genes for response regulators in response to cytokinins and nitrate in Arabidopsis thaliana. Plant Cell Physiol. 40, 767–771 (1999).

    Article  CAS  Google Scholar 

  5. D'Agostino, I. B., Deruere, J. & Kieber, J. J. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol. 124, 1706–1717 (2000).

    Article  CAS  Google Scholar 

  6. Inoue, T. et al. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409, 1060–1063 (2001).

    Article  ADS  CAS  Google Scholar 

  7. Sakakibara, H., Taniguchi, M. & Sugiyama, T. His-Asp phosphorelay signaling: a communication avenue between plants and their environment. Plant Mol. Biol. 42, 273–278 (2000).

    Article  CAS  Google Scholar 

  8. Stock, A. M., Robinson, V. L. & Goudreau, P. N. Two-component signal transduction. Annu. Rev. Biochem. 69, 183–215 (2000).

    Article  CAS  Google Scholar 

  9. Thomason, P. & Kay, R. Eukaryotic signal transduction via histidine-aspartate phosphorelay. J. Cell Sci. 113, 3141–3150 (2000).

    CAS  PubMed  Google Scholar 

  10. Wurgler-Murphy, S. M. & Saito, H. Two-component signal transducers and MAPK cascades. Trends Biochem. Sci. 22, 172–176 (1997).

    Article  CAS  Google Scholar 

  11. Urao, T., Yamaguchi-Shinozaki, K. & Shinozaki, K. Two-component systems in plant signal transduction. Trends Plant Sci. 5, 67–74 (2000).

    Article  CAS  Google Scholar 

  12. D'Agostino, I. B. & Kieber, J. J. Phosphorelay signal transduction: the emerging family of plant response regulators. Trends Biochem. Sci. 24, 452–456 (1999).

    Article  CAS  Google Scholar 

  13. Yeh, K. C. & Lagarias, J. C. Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl Acad. Sci. USA 95, 13976–13981 (1998).

    Article  ADS  CAS  Google Scholar 

  14. Urao, T. et al. A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11, 1743–1754 (1999).

    Article  CAS  Google Scholar 

  15. Bleecker, A. B. & Kende, H. Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. 16, 1–18 (2000).

    Article  CAS  Google Scholar 

  16. Maeda, T., Wurgler-Murphy, S. M. & Saito, H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369, 242–245 (1994).

    Article  ADS  CAS  Google Scholar 

  17. Posas, F. et al. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 ‘two-component’ osmosensor. Cell 86, 865–875 (1996).

    Article  CAS  Google Scholar 

  18. Posas, F. & Saito, H. Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator. EMBO J. 17, 1385–1394 (1998).

    Article  CAS  Google Scholar 

  19. Clark, K. L., Larsen, P. B., Wang, X. & Chang, C. Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc. Natl Acad. Sci. USA 95, 5401–5406 (1998).

    Article  ADS  CAS  Google Scholar 

  20. Gamble, R. L., Coonfield, M. L. & Schaller, G. E. Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. Proc. Natl Acad. Sci. USA 95, 7825–7829 (1998).

    Article  ADS  CAS  Google Scholar 

  21. Suzuki, T. et al. The Arabidopsis sensor his-kinase, ahk4, can respond to cytokinins. Plant Cell Physiol. 42, 107–113 (2001).

    Article  CAS  Google Scholar 

  22. Frank, M. et al. Hormone autotrophic growth and differentiation identifies mutant lines of Arabidopsis with altered cytokinin and auxin content or signaling. Plant Physiol. 122, 721–729 (2000).

    Article  CAS  Google Scholar 

  23. Mahonen, A. P. et al. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 14, 2938–2943 (2000).

    Article  CAS  Google Scholar 

  24. Ueguchi, C., Koizumi, H., Suzuki, T. & Mizuno, T. Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol. 42, 231–235 (2001).

    Article  CAS  Google Scholar 

  25. Elbein, A. D. Inhibitors of the biosynthesis and processing of N-linked oligosaccharides. CRC Crit. Rev. Biochem. 16, 21–49 (1984).

    Article  CAS  Google Scholar 

  26. Suzuki, T., Imamura, A., Ueguchi, C. & Mizuno, T. Histidine-containing phosphotransfer (HPt) signal transducers implicated in His-to-Asp phosphorelay in Arabidopsis. Plant Cell Physiol. 39, 1258–1268 (1998).

    Article  CAS  Google Scholar 

  27. Suzuki, T. et al. Compilation and characterization of histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in plants: AHP signal transducers of Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 64, 2486–2489 (2000).

    Article  CAS  Google Scholar 

  28. Imamura, A. et al. Compilation and characterization of Arabidopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction. Plant Cell Physiol. 40, 733–742 (1999).

    Article  CAS  Google Scholar 

  29. Urao, T., Miyata, S., Yamaguchi-Shinozaki, K. & Shinozaki, K. Possible His to Asp phosphorelay signaling in an Arabidopsis two-component system. FEBS Lett. 478, 227–232 (2000).

    Article  CAS  Google Scholar 

  30. Suzuki, T., Sakurai, K., Ueguchi, C. & Mizuno, T. Two types of putative nuclear factors that physically interact with histidine-containing phosphotransfer (Hpt) domains, signaling mediators in His-to-Asp phosphorelay, in Arabidopsis thaliana. Plant Cell Physiol. 42, 37–45 (2001).

    Article  CAS  Google Scholar 

  31. Lohrmann, J. et al. The response regulator ARR2: a pollen-specific transcription factor involved in the expression of nuclear genes for components of mitochondrial complex I in Arabidopsis. Mol. Genet. Genomics 265, 2–13 (2001).

    Article  CAS  Google Scholar 

  32. Sakai, H., Aoyama, T. & Oka, A. Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J. 24, 703–711 (2000).

    Article  CAS  Google Scholar 

  33. Xiang, C., Han, P., Lutziger, I., Wang, K. & Oliver, D. J. A mini binary vector series for plant transformation. Plant Mol. Biol. 40, 711–717 (1999).

    Article  CAS  Google Scholar 

  34. Sussman, M. R., Amasino, R. M., Young, J. C., Krysan, P. J. & Austin-Phillips, S. The Arabidopsis knockout facility at the University of Wisconsin-Madison. Plant Physiol. 124, 1465–1467 (2000).

    Article  CAS  Google Scholar 

  35. Nakamura, A. et al. Biochemical characterization of a putative cytokinin-responsive His-kinase, CKI1, from Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 63, 1627–1630 (1999).

    Article  CAS  Google Scholar 

  36. Urao, T., Yakubov, B., Yamaguchi-Shinozaki, K. & Shinozaki, K. Stress-responsive expression of genes for two-component response regulator-like proteins in Arabidopsis thaliana. FEBS Lett. 427, 175–178 (1998).

    Article  CAS  Google Scholar 

  37. Sakai, H., Aoyama, T., Bono, H. & Oka, A. Two-component response regulators from Arabidopsis thaliana contain a putative DNA-binding motif. Plant Cell Physiol. 39, 1232–1239 (1998).

    Article  CAS  Google Scholar 

  38. Riou-Khamlichi, C., Huntley, R., Jacqmard, A. & Murray, J. A. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283, 1541–1544 (1999).

    Article  ADS  CAS  Google Scholar 

  39. Meijer, M. & Murray, J. A. Cell cycle controls and the development of plant form. Curr. Opin. Plant Biol. 4, 44–49 (2001).

    Article  CAS  Google Scholar 

  40. Gan, S. & Amasino, R. M. Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270, 1986–1988 (1995).

    Article  ADS  CAS  Google Scholar 

  41. Ori, N. et al. Leaf senescence is delayed in tobacco plants expressing the maize homeobox gene knotted1 under the control of a senescence-activated promoter. Plant Cell 11, 1073–1080 (1999).

    Article  CAS  Google Scholar 

  42. Quirino, B. F., Noh, Y. S., Himelblau, E. & Amasino, R. M. Molecular aspects of leaf senescence. Trends Plant Sci. 5, 278–282 (2000).

    Article  CAS  Google Scholar 

  43. Tsiantis, M. Control of shoot cell fate. Beyond homeoboxes. Plant Cell 13, 733–738 (2001).

    Article  CAS  Google Scholar 

  44. Sheen, J. Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274, 1900–1902 (1996).

    Article  ADS  CAS  Google Scholar 

  45. Kovtun, Y., Chiu, W. L., Tena, G. & Sheen, J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl Acad. Sci. USA 97, 2940–2945 (2000).

    Article  ADS  CAS  Google Scholar 

  46. 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 

  47. Haseloff, J., Siemering, K. R., Prasher, D. C. & Hodge, S. Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl Acad. Sci. USA 94, 2122–2127 (1997).

    Article  ADS  CAS  Google Scholar 

  48. 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 

Download references

Acknowledgements

We would like to thank T. Kakimoto for the CKI1 cDNA clone and communicating unpublished results; C. Xiang, K. Wang and D. J. Oliver for the mini-binary vectors; J. Callis for the UBQ10–GUS plasmid; E. Schaller for the ER–GFP construct; J. Elhai, W.-L. Chiu and H. Sze for helpful discussions on the manuscript; B. Moore for help with confocal microscopy; and G. Tena for Arabidopsis plants. This work is supported by NSF and NIH grants to J.S.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jen Sheen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hwang, I., Sheen, J. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383–389 (2001). https://doi.org/10.1038/35096500

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35096500

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

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