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:

Direct control of shoot meristem activity by a cytokinin-activating enzyme

Nature volume 445, pages 652–655 (2007)Cite this article

Abstract

The growth of plants depends on continuous function of the meristems. Shoot meristems are responsible for all the post-embryonic aerial organs, such as leaves, stems and flowers1. It has been assumed that the phytohormone cytokinin has a positive role in shoot meristem function2,3,4. A severe reduction in the size of meristems in a mutant that is defective in all of its cytokinin receptors has provided compelling evidence that cytokinin is required for meristem activity5,6. Here, we report a novel regulation of meristem activity, which is executed by the meristem-specific activation of cytokinins. The LONELY GUY (LOG) gene of rice is required to maintain meristem activity and its loss of function causes premature termination of the shoot meristem. LOG encodes a novel cytokinin-activating enzyme that works in the final step of bioactive cytokinin synthesis. Revising the long-held idea of multistep reactions, LOG directly converts inactive cytokinin nucleotides to the free-base forms, which are biologically active, by its cytokinin-specific phosphoribohydrolase activity. LOG messenger RNA is specifically localized in shoot meristem tips, indicating the activation of cytokinins in a specific developmental domain. We propose the fine-tuning of concentrations and the spatial distribution of bioactive cytokinins by a cytokinin-activating enzyme as a mechanism that regulates meristem activity.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: log mutant phenotypes.
Figure 2: Positional cloning of LOG.
Figure 3: Expression pattern of LOG mRNA.
Figure 4: Enzymatic function of LOG as a cytokinin nucleoside 5′-monophosphate phosphoribohydrolase.

Similar content being viewed by others

References

  1. Steeves, T. A. & Sussex, I. M. Patterns in Plant Development (Cambridge Univ. Press, Cambridge, UK, 1989)

    Book  Google Scholar 

  2. Werner, T. et al. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15, 2532–2550 (2003)

    Article  CAS  Google Scholar 

  3. Helliwell, C. A. et al. The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell 13, 2115–2125 (2001)

    Article  CAS  Google Scholar 

  4. Ashikari, M. et al. Cytokinin oxidase regulates rice grain production. Science 309, 741–745 (2005)

    Article  ADS  CAS  Google Scholar 

  5. Higuchi, M. et al. In planta functions of the Arabidopsis cytokinin receptor family. Proc. Natl Acad. Sci. USA 101, 8821–8826 (2004)

    Article  ADS  CAS  Google Scholar 

  6. Nishimura, C. et al. Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16, 1365–1377 (2004)

    Article  CAS  Google Scholar 

  7. Howell, S. H., Lall, S. & Che, P. Cytokinins and shoot development. Trends Plant Sci. 8, 453–459 (2003)

    Article  CAS  Google Scholar 

  8. Ferreira, F. J. & Kieber, J. J. Cytokinin signaling. Curr. Opin. Plant Biol. 8, 518–525 (2005)

    Article  CAS  Google Scholar 

  9. 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 

  10. Sakakibara, H. Cytokinins: activity, biosynthesis, and translocation. Annu. Rev. Plant Biol. 57, 431–449 (2006)

    Article  CAS  Google Scholar 

  11. Giulini, A., Wang, J. & Jackson, D. Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1. Nature 430, 1031–1034 (2004)

    Article  ADS  CAS  Google Scholar 

  12. To, J. P. et al. Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16, 658–671 (2004)

    Article  CAS  Google Scholar 

  13. Takei, K. et al. AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol. 45, 1053–1062 (2004)

    Article  CAS  Google Scholar 

  14. Miyawaki, K., Matsumoto-Kitano, M. & Kakimoto, T. Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J. 37, 128–138 (2004)

    Article  CAS  Google Scholar 

  15. Werner, T., Köllmer, I., Bartrina, I., Holst, K. & Schmülling, T. New insights into the biology of cytokinin degradation. Plant Biol. (Stuttg.) 8, 371–381 (2006)

    Article  CAS  Google Scholar 

  16. Sentoku, N. et al. Regional expression of the rice KN1-type homeobox gene family during embryo, shoot, and flower development. Plant Cell 11, 1651–1664 (1999)

    Article  CAS  Google Scholar 

  17. Moriguchi, K. et al. The complete nucleotide sequence of a plant root-inducing (Ri) plasmid indicates its chimeric structure and evolutionary relationship between tumor-inducing (Ti) and symbiotic (Sym) plasmids in Rhizobiaceae. J. Mol. Biol. 307, 771–784 (2001)

    Article  CAS  Google Scholar 

  18. Crespi, M., Vereecke, D., Temmerman, W., Van Montagu, M. & Desomer, J. The fas operon of Rhodococcus fascians encodes new genes required for efficient fasciation of host plants. J. Bacteriol. 176, 2492–2501 (1994)

    Article  CAS  Google Scholar 

  19. Chen, C.-M. & Kristopeit, S. M. Metabolism of cytokinin: dephosphorylation of cytokinin ribonucleotide by 5′-nucleotidases from wheat germ cytosol. Plant Physiol. 67, 494–498 (1981)

    Article  CAS  Google Scholar 

  20. Chen, C.-M. & Kristopeit, S. M. Metabolism of cytokinin: Deribosylation of cytokinin ribonucleoside by adenosine nucleosidase from wheat germ. Plant Physiol. 68, 1020–1023 (1981)

    Article  CAS  Google Scholar 

  21. Jain, M., Tyagi, A. K. & Khurana, J. P. Molecular characterization and differential expression of cytokinin-responsive type-A response regulators in rice (Oryza sativa). BMC Plant Biol. 6 1 doi: 10.1186/1471-2229-6-1 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Long, J. A., Moan, E. I., Medford, J. I. & Barton, M. K. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66–69 (1996)

    Article  ADS  CAS  Google Scholar 

  23. Mayer, K. F. et al. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805–815 (1998)

    Article  CAS  Google Scholar 

  24. Leibfried, A. et al. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438, 1172–1175 (2005)

    Article  ADS  CAS  Google Scholar 

  25. Jasinski, S. et al. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 15, 1560–1565 (2005)

    Article  CAS  Google Scholar 

  26. Yanai, O. et al. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol. 15, 1566–1571 (2005)

    Article  CAS  Google Scholar 

  27. Sakamoto, T. et al. Ectopic expression of KNOX homeodomain protein induces expression of cytokinin biosynthesis gene in rice. Plant Physiol. 142, 54–62 (2006)

    Article  CAS  Google Scholar 

  28. Faiss, M., Zalubilova, J., Strnad, M. & Schmülling, T. Conditional transgenic expression of the ipt gene indicates a function for cytokinins in paracrine signaling in whole tobacco plants. Plant J. 12, 401–415 (1997)

    Article  CAS  Google Scholar 

  29. Kouchi, H., Sekine, M. & Hata, S. Distinct classes of mitotic cyclins are differentially expressed in the soybean shoot apex during the cell cycle. Plant Cell 7, 1143–1155 (1995)

    Article  CAS  Google Scholar 

  30. Takei, K., Sakakibara, H. & Sugiyama, T. Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J. Biol. Chem. 276, 26405–26410 (2001)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank L. Dennis for critical reading of this manuscript; I. Yamaguchi, T. Hashimoto and M. Nakajima for their suggestions; H. Satoh and S. Yamaki for log alleles; and T. Kuroha for sharing his unpublished results.

Author Contributions T.K., M.M., K.K., Y.N. and J.K. isolated, cloned and genetically characterized LOG, and N.U. M.K. and H.S. determined the biochemical nature of LOG. J.K. and H.S. wrote the manuscript.

Genbank accession numbers are as follows: LOG (AK071695), LOC_Os01g51210 (AK061091), LOC_Os05g46360 (AK068633), LOC_Os03g49050 (AC123974), LOC_Os09g37540 (AK062595), LOC_Os05g51390 (AK242659), LOC_Os03g64070 (AK061341), LOC_Os03g01880 (AK099538), LOC_Os10g33900 (AK108805), LOC_Os02g41770 (AP005000), LOC_Os04g43840 (AK069293), At2g28305 (NM_128389), At2g35990 (NM_129158), At2g37210 (NM_129277), At3g53450 (NM_115205), AT4G35190 (NM_119685), At5g03270 (NM_120405), At5g06300 (NM_120713), At5g11950 (NM_121233) and At5g26140 (NM_122515).

Author information

Author notes

  1. Takashi Kurakawa and Nanae Ueda: These two authors contributed equally to this work.

Authors and Affiliations

  1. Graduate School of Agricultural and Life Sciences, University of Tokyo, Yayoi, Bunkyo, Tokyo, 113-8652, Japan

    Takashi Kurakawa, Kaoru Kobayashi, Yasuo Nagato & Junko Kyozuka

  2. RIKEN Plant Science Center, Tsurumi, Yokohama, 230-0045, Japan

    Nanae Ueda, Mikiko Kojima & Hitoshi Sakakibara

  3. Research Institute for Bioresources, Okayama University, Kurashiki, Okayama, 710-0046, Japan

    Masahiko Maekawa

Authors
  1. Takashi Kurakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nanae Ueda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masahiko Maekawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kaoru Kobayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mikiko Kojima
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yasuo Nagato
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hitoshi Sakakibara
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Junko Kyozuka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hitoshi Sakakibara or Junko Kyozuka.

Ethics declarations

Competing interests

Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Table 1 and Supplementary Figure 1-6 and additional references. (PDF 264 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kurakawa, T., Ueda, N., Maekawa, M. et al. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445, 652–655 (2007). https://doi.org/10.1038/nature05504

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature05504

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