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:

RETRACTED ARTICLE: Identification and role of adenylyl cyclase in auxin signalling in higher plants

A Retraction to this article was published on 26 November 1998

Abstract

Cyclic AMP is an important signalling molecule in prokaryotes and eukaryotes1, but its significance in higher plants has been generally doubted2 because they have low adenylyl cyclase activity and barely detectable amounts of cAMP3. Here we used activation T-DNA tagging to create tobacco cell lines that can proliferate in the absence of the phytohormone auxin in the culture media4,5. The sequence tagged in one line, axi 141, was used to isolate a complementary DNA encoding adenylyl cyclase, the first from a higher plant. Sequence analysis reveals that the tobacco adenylyl cyclase is probably soluble, contains characteristic leucine-rich repeats, and bears similarity with adenylyl cyclase from the yeast Schizosaccharomyces pombe. Expression of the cDNA in Escherichia coli results in an increase in endogenous cAMP levels, and in yeast its expression functionally complements the cry1 mutation. Tobacco protoplasts treated with cAMP, or the adenylyl cyclase activator forskolin, no longer require auxin to divide. This finding, together with the observation that the adenylyl cyclase inhibitor dideoxyadenosine inhibits cell proliferation in the presence of auxin, suggests that cAMP is involved in auxin-triggered cell division in higher plants.

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: T-DNA organization and axi 141 expression.
Figure 2: Functional and sequence characterizationof axi 141.
Figure 3: Functional testing of axi 141.
Figure 4: Effect of cAMP on protoplast division.

Similar content being viewed by others

References

  1. Francis, S. H. & Corbin, J. D. in Signal Transduction (eds Heldin, C.-H. & Purton, M.) 223–240 (Chapman and Hall, London, (1996).

    Google Scholar 

  2. Trewavas, A. & Gilroy, S. Signal transduction in plant cells. Trends Genet. 7, 356–361 (1991).

    Article  CAS  PubMed  Google Scholar 

  3. Assmann, S. Cyclic AMP as a second messenger in higher plants. Plant Physiol. 108, 885–889 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hayashi, H., Czaja, I., Lubenow, H., Schell, J. & Walden, R. Activation of a plant gene by T-DNA tagging: auxin-independent growth in vitro. Science 258, 1350–1353 (1992).

    Article  CAS  PubMed  ADS  Google Scholar 

  5. Walden, R. et al.Activation tagging: a means of isolating genes implicated as playing a role in plant growth and development. Plant Mol. Biol. 26, 1521–1528 (1994).

    Article  CAS  PubMed  Google Scholar 

  6. Walden, R., Hayashi, H., Lubenow, H., Czaja, I. & Schell, J. Auxin inducibility and developmental expression of axi 1: a gene directing auxin independent growth in tobacco protoplasts. EMBO J. 13, 4729–4736 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Yamawaki-Kataoka, Y., Tamaoki, T., Choe, H.-R., Tanaka, H. & Kataoka, T. Adenylate cyclases in yeast: A comparison of the genes from Schizosaccharomyces pombe and Saccaromyces cerevisiae. Proc. Natl Acad. Sci. USA 86, 5693–5697 (1989).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  8. Kroll, D. J. et al.Amultifunctional prokaryotic protein expression system: overproduction, affinity purification and selective detection. DNA Cell Biol. 12, 441–453 (1993).

    Article  CAS  PubMed  Google Scholar 

  9. Matsumoto, K., Uno, I. & Ishikawa, T. Identification of the structural gene and nonsense alleles for adenylate cyclase in Saccaromyces cerevisiae. J. Bacteriol. 157, 277–282 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kataoka, T., Broek, D. & Wigler, M. DNA sequence and characterisation of the S. cerevisiae gene encoding adenylate cyclase. Cell 43, 493–505 (1985).

    Article  CAS  PubMed  Google Scholar 

  11. Nagata, T. & Takebe, I. Cell wall regeneration and cell division in isolated tobacco mesophyll protoplasts. Planta 92, 301–308 (1993).

    Article  Google Scholar 

  12. Walden, R., Czaja, I., Schmülling, T. & Schell, J. Rol genes alter hormonal requirements for protoplast growth and modify the expression of an auxin responsive promoter. Plant Cell Rep. 12, 551–554 (1993).

    Article  CAS  PubMed  Google Scholar 

  13. Röhrig, H. et al.Convergent pathways for lipochitooligosaccharide and auxin signaling in tobacco cells. Proc. Natl Acad. Sci. USA 93, 13389–13392 (1996).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  14. Holgate, S. T., Lewis, R. A. & Austen, K. F. Role of adenylate cyclase in immunologic release of mediators from rat mast cells: agonist and antagonist effects of purine- and ribose-modified adenosine analogs. Proc. Natl Acad. Sci. USA 77, 6800–6804 (1985).

    Article  ADS  Google Scholar 

  15. Seamon, H. B., Padgett, W. & Daly, J. W. Forskolin: unique diterpine activator of adenylate cyclase in membranes and intact cells. Proc. Natl Acad. Sci. USA 78, 3363–3367 (1981).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  16. Taussig, R. & Gilman, A. G. Mammalian membrane bound adenyl cyclases. J. Biol. Chem. 270, 1–4 (1995).

    Article  CAS  PubMed  Google Scholar 

  17. Archdeacon, J., Talty, J., Boesten, B., Danchin, A., & O'Gara, F. Cloning of the second adenylate cyclase gene (cya2) from Rhizobium meliloti F34: sequence similarity to eukaryotic cyclases. FEMS Microbiol. Lett. 128, 177–184 (1995).

    Article  CAS  PubMed  Google Scholar 

  18. Macdonald, H. Auxin perception and signal transduction. Physiol. Planta 100, 423–430 (1997).

    Article  CAS  Google Scholar 

  19. Hartzell, H. C., Mery, P.-F., Fishmeister, R. & Szabo, G. Sympathetic regulation of cardiac calcium current is due exclusively to cyclic AMP-dependent phosphorylation. Nature 351, 573–576 (1991).

    Article  CAS  PubMed  ADS  Google Scholar 

  20. Lalli, E. & Sassone-Corssi, P. Signal transduction and gene regulation: The nuclear response to cAMP. J. Biol. Chem. 269, 17359–17362 (1994).

    Article  CAS  PubMed  Google Scholar 

  21. Li, W., Luan, S., Schreiber, S. L. & Assmann, S. M. Cyclic AMP stimulates K+ channel activity in mesophyll cells of Vicia faba L. Plant Physiol. 106, 957–961 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Katagiri, F., Lam, E. & Chua, N.-H. Two tobacco DNA binding proteins with homology to the nuclear factor CREB. Nature 340, 727–730 (1989).

    Article  CAS  PubMed  ADS  Google Scholar 

  23. Milner, P. A. & Clausier, B. E. G-protein coupled receptors in plants cells. J. Exp. Bot. 47, 983–992 (1996).

    Article  Google Scholar 

  24. Fritze, K., Czaja, I. & Walden, R. T-DNA tagging of genes influencing polyamine metaboism: isolation of mutant plant lines and rescue of DNA promoting growth in the presence of a polyamine biosynthetic inhibitor. Plant J. 7, 101–111 (1994).

    Google Scholar 

  25. Töpfer, R., Maas, C., Höricke-Grandpierre, C., Schell, J. & Steinbiss, H.-H. Expression vectors for high level gene expression in dicotyledonous and monocotyledonous plants. Methods Enzymol. 217, 66–78 (1993).

    Article  Google Scholar 

  26. Studier, F. W., Rosenberg, A. H., Dunn, J. J. & Dubendorf, J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185, 60–89 (1990).

    Article  CAS  PubMed  Google Scholar 

  27. Suzuki, N. et al.Leucine rich repeats and carboxyl terminus are required for interaction of yeast adenylate cyclase with RAS proteins. Proc. Natl Acad. Sci. USA 87, 8711–8715 (1990).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

Download references

Acknowledgements

We thank T. Kataoka for the yeast strain T50-3A and pYEP24-CYRI, W. Schmalenbach for technical assistance, and R. Schmidt for conversations. T.I was supported by a Alexander van Humboldt postdoctoral fellowship. C.S is supported by a DFG studentship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard Walden.

Additional information

This article was retracted. Some of the results reported in this Letter cannot be reproduced. We know that the data on protoplast division described for Figs 1a, c, 2a, band 4, and the corresponding experimental procedures described in the Methods section and the text, are wrong. In fact, the data showing that cAMP can stimulate protoplast division in the absence of auxins are not correct. Hence, we need to retract this paper. We apologize for any misunderstanding that this might have caused. Note from the Editor: One author, R.W., although concerned with the accuracy of parts of this paper, reserves judgement concerning its retraction and awaits the outcome of further experimentation.

About this article

Cite this article

Ichikawa, T., Suzuki, Y., Czaja, I. et al. RETRACTED ARTICLE: Identification and role of adenylyl cyclase in auxin signalling in higher plants. Nature 390, 698–701 (1997). https://doi.org/10.1038/37810

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/37810

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