Skip to main content
SpringerLink
Log in

CHRK1, a chitinase-related receptor-like kinase, plays a role in plant development and cytokinin homeostasis in tobacco

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

CHRK1 encodes a receptor-like kinase that contains a chitinase-related sequence in the extracellular domain in Nicotiana tabacum. In this study, we showed that CHRK1 is mainly expressed in the shoot apex region including leaf primordia and young leaves, and germinating seedlings and vascular tissues, based on GUS activity of transgenic tobacco plants carrying the CHRK1promoter-GUS fusion gene. Transgenic tobacco plants in which CHRK1 expression was suppressed exhibited pleiotrophic developmental abnormality, including formation of proliferating shooty calli from emerging seedlings and severely altered seedling development. At the cellular level, ectopic cell proliferation, reduced cell specificity, and aberrant chloroplast development were observed. The transgenic lines contained 3-fold higher level of cytokinin than the wild-type plants. Consistently, the transgenic seedlings exhibited a typical cytokinin response in the absence of hormone, such as deetiolation under the dark. Based on these results, we propose that CHRK1 is involved in a developmental signaling pathway regulating cell proliferation/differentiation and the endogenous cytokinin levels in tobacco.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bakkers, J., Semino, C.E., Stroband, H., Kline, J.W. and Robbins, P.W. 1997. An important developmental role for oligosaccharides during early embryogenesis of cyprind fish. Proc. Natl. Acad. Sci. USA 94: 7982–7986.

    PubMed  Google Scholar 

  • Benhamou, N. 1996. Elicitor-induced plant defence pathways. Trends Plant Sci. 1: 233–240.

    Google Scholar 

  • Binns, A.N., Labliola, J. and Black, R.C. 1987. Initiation of auxin autonomy in Nicotiana glutinosa cells by the cytokininbiosynthesis gene from Agrobacterium tumefaciens. Planta 171: 539–548.

    Google Scholar 

  • Bollag, D.M., Rozycki, M.D. and Edelstein, S.J. 1996. Protein Methods. Wiley-Liss, New York.

    Google Scholar 

  • Broglie, K., Chet, I., Hollyday, M., Cressman, R., Biddle, P., Knowlton, S., Mauvais, C.J. and Broglie, R. 1991. Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254: 1194–1197.

    Google Scholar 

  • Brunner, F., Stintzi, A., Fritig, B. and Legrand, M. 1998. Substrate specificity of tobacco chitinases. Plant J. 14: 225–234.

    PubMed  Google Scholar 

  • Cary, A.J., Liu, W. and Howell, S.H. 1995. Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol. 107: 1075-1082.

    PubMed  Google Scholar 

  • Chaudhury, A.M., Letham, S., Craig, S. and Dennis, E.S. 1993. amp1-a mutation with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis, and precocious flowering. Plant J. 4: 907–916.

    Google Scholar 

  • Chory, J., Reinecke, D., Sim, S., Washburn, T. and Brenner, M. 1994. A role for 29 cytokinins in de-etiolation in Arabidopsis. Plant Physiol. 104: 339–347.

    PubMed  Google Scholar 

  • Coenen, C. and Lomax, T.L. 1998. The diageotropica gene differentially affects auxin and cytokinin responses throughout development in tomato. Plant Physiol. 117: 63–72.

    PubMed  Google Scholar 

  • de Jong, A.J., Cordewener, J., Lo Schiavo, F., Terzi, M., Vandekerckhove, J., van Kammen, A. and de Vries, S.C. 1992. A carrot somatic embryo mutant is rescued by chitinase. Plant Cell 4: 425–433.

    PubMed  Google Scholar 

  • de Jong, A.J., Heldstra, R., Spaink, H.P., Hartog, M.V., Meijer, E.A., Hendriks, T., Lo Schiavo, F., Terzi, M., Bisseling, T., van Kammen, A. and de Vries, S.C. 1993. Rhizobium lipooligosaccharides rescue a carrot somatic embryo mutant. Plant Cell 5: 615–620.

    PubMed  Google Scholar 

  • Frugis, G., Giannino, D., Mele, G., Nicolodi, C., Chiappetta, A., Bitonti, M.B., Innocenti, A.M., Dewitte, W., van Onckelen, H. and Mariotti, D. 2001. Overexpression of KNAT1 in lettuce shifts leaf determinate growth to a shoot-like indeterminate growth associated with an accumulation of isopentenyl-type cytokinins. Plant Physiol. 126: 1370–1380.

    PubMed  Google Scholar 

  • Goldberg, R.B., Barker, S.J. and Perez-Grau, L. 1989. Regulation of gene expression during plant embryogenesis. Cell 56: 149–160.

    PubMed  Google Scholar 

  • Gu, T., Mazzurco, M., Sulaman, W., Matias, D.D. and Goring, D.R. 1998. Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc. Natl. Acad. Sci. USA 95: 382–387.

    PubMed  Google Scholar 

  • Hakala, B.E., White, C. and Recklies, A.D. 1993. Human cartilage gp-39, a major secretory product of articular chondrocytes and synovial cells, is a mammalian member of a chitinase protein family. J. Biol. Chem. 268: 25803–25810.

    PubMed  Google Scholar 

  • Helliwell, C.A., Chin-Atkins, A.N., Wilson, I.W., Chapple, R. and Dennis, E.S. 2001. The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell 13: 2115–2125.

    PubMed  Google Scholar 

  • Jach, G., Görnhardt, B., Mundy, J., Logemann, J., Pinsdorf, E., Leah, R., Schell, J. and Maas, C. 1995. Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. Plant J. 8: 97–109.

    PubMed  Google Scholar 

  • Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. 1987. GUS fusion: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901–3907.

    PubMed  Google Scholar 

  • Kim, Y.S., Lee, J.H., Yoon, G.M., Cho, H.S., Park, S.-W., Suh, M.C., Choi, D., Ha, H.J., Liu, J.R. and Pai, H.-S. 2000. CHRK1, a chitinase-related receptor-like kinase in tobacco. Plant Physiol. 123: 905–915.

    PubMed  Google Scholar 

  • Kim, M., Cho, H.S., Lee, J.H. and Pai, H.-S. 2003. CHRK1, a chitinase-related receptor-like kinase, interacts with NtARC1, an armadillo repeat protein, in tobacco. Biochim. Biophys. Acta 1651: 50–59.

    PubMed  Google Scholar 

  • Neuhaus, J.-M., Fritig, B., Linthorst, H.J.M., Meins, F., Mikkelsen, J.D. and Ryals, J. 1996. A revised nomenclature for chitinase genes. Plant Mol. Biol. Rep. 14: 102–104.

    Google Scholar 

  • Renkema, G.H., Boot, R.G., Au, F.L., Donker-Koopman, W.E., Strijland, A., Muijsers, A.O., Hrebicek, M. and Aerts, J.M. 1998. Chitotriosidase, a chitinase, and the 39-kDa human cartilage glycoprotein, a chitin-binding lectin, are homologues of family 18 glycosyl hydrolases secreted by human macrophages. Eur. J. Biochem. 251: 504–509.

    PubMed  Google Scholar 

  • Riou-Khamlichi, C., Huntley, R., Jacqmard, A. and Murray, J.A.H. 1999. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544.

    PubMed  Google Scholar 

  • Semino, C.E., Specht, C.A., Raimondi, A. and Robbins, P.W. 1996. Homologs of the Xenopus developmental gene DG42 are present in zebrafish and mouse and are involved in the synthesis of Nodlike chitin oligosaccharides during early embryogenesis. Proc. Natl. Acad. Sci. USA 93: 4548–4553.

    PubMed  Google Scholar 

  • Shiu, S.H. and Bleecker, A.B. 2001. Plant receptor-like kinase gene family: diversity, function and signaling. Science's STKE 2001 (113) re22.

  • Smigocki, A.C. and Owens, L.D. 1989. Cytokinin to auxin ratios and morphology of shoots and tissues transformed by chimeric isopentenyltransferase gene. Plant Physiol. 91: 808–811.

    Google Scholar 

  • Stone, S.L., Anderson, E.M., Mullen, R.T. and Goring, D.R. 2003. ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15: 885–898.

    PubMed  Google Scholar 

  • Stone, S.L., Arnoldo, M. and Goring, D.R. 1999. A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science 286: 1729–1731.

    PubMed  Google Scholar 

  • Suh, M.C., Choi, D. and Liu, J.R. 1998. Cadmium resistance in transgenic tobacco plants expressing the Nicotiana glutinosa L. metallothionein-like gene. Mol. Cells 8: 678–684.

    PubMed  Google Scholar 

  • Takei, K., Sakakibara, H., Taniguchi, M. and Sugiyama, T. 2001. Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol. 42: 85–93.

    PubMed  Google Scholar 

  • Tamaoki, M., Kusaba, S., Kano-Murakami, Y. and Matsuoka, M. 1997. Ectopic expression of a tobacco homeobox gene, NTH15, dramatically alters leaf morphology and hormone levels in transgenic tobacco. Plant Cell Physiol. 38: 917–927.

    PubMed  Google Scholar 

  • Thomas, J.C., Smigocki, A.C. and Bohnert, H.J. 1995. Lightinduced expression of ipt gene from Agrobacterium tumefaciens results in cytokinnin accumulation and osmotic stress symptoms in transgenic tobacco. Plant Mol. Biol. 27: 225–235.

    PubMed  Google Scholar 

  • van Loon, L.C., Pierpoint, W.S., Boller, T. and Conejero, V. 1994. Recommendations for naming plant pathogenesis-related proteins. Plant Mol. Biol. Rep. 12: 245–264.

    Google Scholar 

  • Zhong, R., Kays, S.J., Schroeder, B.P. and Ye, Z.-H. 2002. Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14: 165–179.

    PubMed  Google Scholar 

  • Zhu, Y., Maher, E.A., Masoud, S., Dixon, R.A. and Lamb, C.J. 1994. Enhanced protection against fungal attack by constitutive coexpression of chitinase and glucanase genes in transgenic tobacco. Bio/technology 12: 807–812.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Plant Genomics and 2Laboratory of Plant Cell Biotechnology, Korea Research Institute of Bioscience and Biotechnology, Yusong, Taejon, 305-333, Korea

    Jeong Hee Lee, Hye Sun Cho, Do Myung Kim, Youn Sung Kim & Hyun-Sook Pai

  2. Department of Horticulture, Chungnam University, Taejon, 305-764, Korea

    Jeong Hee Lee & Yong Pyo Lim

  3. Plant Science Center, Institute of Physical and Chemical Research, 1-7-22, Suehiro, Tsurumi, Yokohama, 230-0045, Japan

    Kentaro Takei & Hitoshi Sakakibara

  4. Biotechnology, Yusong, Taejon, 305-333, Korea

    Sung Ran Min

  5. Department of Biology, Yonsei University, Seoul, 120-749, Korea

    Woo Taek Kim

  6. Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Chinju, 660-701, Korea

    Dae Young Sohn

  7. Division of Biosciences and Bioinformatics, Myongji University, San 38-2, Namdong, Yongin, Kyonggi-do, 449-728, Korea

    Hyun-Sook Pai

Authors
  1. Jeong Hee Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kentaro Takei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hitoshi Sakakibara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hye Sun Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Do Myung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Youn Sung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sung Ran Min
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Woo Taek Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Dae Young Sohn
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yong Pyo Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hyun-Sook Pai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hyun-Sook Pai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lee, J.H., Takei, K., Sakakibara, H. et al. CHRK1, a chitinase-related receptor-like kinase, plays a role in plant development and cytokinin homeostasis in tobacco. Plant Mol Biol 53, 877–890 (2003). https://doi.org/10.1023/B:PLAN.0000023668.34205.a8

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PLAN.0000023668.34205.a8

Search

Navigation