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An upstream region of the Arabidopsis thaliana CDKA;1 (CDC2aAt) gene directs transcription during trichome development

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Abstract

The cell cycle of eukaryotes is tightly regulated through the activity of cyclin-dependent kinases. The Arabidopsis thaliana CDKA;1 (CDC2aAt) gene is thought to encode such a protein kinase, since it is actively transcribed in proliferating tissues and can complement defects in the Schizosaccharomyces pombe cdc2 gene. We analyzed the functional structure of the CDKA;1 promoter, using fusion genes between various upstream regions of CDKA;1 and the Escherichia coli β-glucuronidase (GUS) gene. A 595 bp DNA fragment upstream from the transcription start site conferred GUS activity on developing trichomes, but not on proliferating tissues. On the other hand, another upstream fragment extending to the 5′ non-coding transcribed region gave GUS activity to both proliferating tissues and developing trichomes. Against the gl2 mutant background, GUS activity directed by the 595 bp fragment was detected in single-stalk cells, but not in giant cells without obvious polar extension growth. These results revealed that the 595 bp fragment lacks cis element(s) essential for proliferating-cell-specific promoter activity, but can direct transcription in a specific period during trichome development, which does not include cell division. This suggests that CDKA;1 functions during cell morphogenesis as well as cell proliferation.

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REFERENCES

  • Aoyama, T., Takanami, M. and Oka, A. 1989. Signal structure for transcriptional activation in the upstream regions of virulence genes on the hairy-root-inducing plasmid A4. Nucl. Acids Res. 17: 8711–8725.

    Google Scholar 

  • Bechtold, N., Ellis, J. and Pelletier, G. 1993. In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis plants. C.R. Acad. Sci. Paris. Life Sci. 316: 1194–1199.

    Google Scholar 

  • Blangy, A., Lane, H. A., d'Herin P., Harper, M., Kress, M. and Nigg, E. A. 1995. Phosphorylation by p34cdc2 regulates spindle association of human Eg5, kinesin-related motor essential for bipolar spindle formation in vivo. Cell 83: 1159–1169.

    Google Scholar 

  • Burssens, S., Van Montagu, M. and Inzé, D. 1998. The cell cycle in Arabidopsis. Plant Physiol. Biochem. 36: 9–19.

    Google Scholar 

  • Chaubet, N., Flenet, M., Clement, B., Brignon, P. and Gigot, C. 1996. Identification of cis-elements regulating the expression of an Arabidopsis histone H4 gene. Plant J. 10: 425–435.

    Google Scholar 

  • Dolan, L. Janmaat, K., Willemsen, V., Linstead P., Poething, S., Roberts, K. and Scheres, B. 1993. Cellular organization of the Arabidopsis thaliana root. Development 119: 71–84.

    Google Scholar 

  • Ferreira, P. C. G., Hemerly, A. S., Villarroel, R., Van Montagu, M. and Inzé, D. 1991. The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell 3: 531–540.

    Google Scholar 

  • Fobert, P. R., Gaudin, V., Lunness, P., Coen, E. S. and Doonan, J.H. 1996. Distinct classes of cdc2-related genes are differentially expressed during the cell division cycle in plants. Plant Cell 8: 1465–1476.

    Google Scholar 

  • Forsburg, S. and Nurse, P. 1991. Cell cycle regulation in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Annu. Rev. Cell Biol. 7: 227–256.

    Google Scholar 

  • Gendreau, E., Traas, J., Desnos, T., Grandjean, O., Caboche, M. and Hofte, H. 1997. Cellular basis of hypocotyl growth in Arabidopsis. Plant Physiol. 114: 295–305.

    Google Scholar 

  • Hemerly, A. S., Ferreira, P., de Almeida Engler, J., Van Montagu, M., Engler, G. and Inzé, D. 1993. cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5: 1711–1723.

    Google Scholar 

  • Hirayama, T., Imajuku, Y., Anai, T., Matsui, M. and Oka, A. 1991. Identification of two cell-cycle-controlling cdc2 gene homologs in Arabidopsis thaliana. Gene 105: 159–165.

    Google Scholar 

  • Hulskamp, M., Misera, S. and Jugens, G. 1994. Genetic dissection of trichome cell development in Arabidopsis. Cell 76: 555–566.

    Google Scholar 

  • Hulskamp, M., Folkers U. and Grini, P. E. 1998. Cell morphogenesis in Arabidopsis. Bioessays 20: 20–29.

    Google Scholar 

  • Imajuku, Y., Hirayama, T., Endoh, H. and Oka, A. 1992. Exonintron organization of the Arabidopsis thaliana protein kinase genes CDC2a and CDC2b. FEBS Lett. 304: 73–77.

    Google Scholar 

  • Jacqmard, A., De Veylder, L., Segers, G., de Almeida Engler, J., Bernier, G., Van Montagu, M. and Inzé, D. 1999. Expression of CKS1At in Arabidopsis thaliana indicates a role for the protein in both the mitotic and the endoreduplication cycle. Planta 207: 496–504.

    Google Scholar 

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

    Google Scholar 

  • Joubes, J., Chevalier, C., Dudits, D., Heberle-Bors, E., Inzé, D., Umeda, M. and Renaudin, J.-P. 2000. CDK-related protein kinases in plants. Plant. Mol. Biol. 43: 607–620.

    Google Scholar 

  • Koornneef, M. 1981. The complex syndrome of ttg mutants. Arab. Inf. Serv. 18: 45–51.

    Google Scholar 

  • Koornneef, M., Dellaert, L. W. M. and van der Veen, J. H. 1982. EMS-and radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana. Mutat. Res. 93: 109–123.

    Google Scholar 

  • MacAuley, A., Cross, J.C. and Werb, Z. 1998. Reprogramming the cell cycle for endoreduplication in rodent trophoblast cells. Mol. Biol. Cell 9: 795–807.

    Google Scholar 

  • Martinez, M. C., Jorgensen, J.-E., Lawton, M. A., Lamb, C. J. and Peter, W. D. 1992. Spatial pattern of cdc2 expression in relation to meristem activity and cell proliferation during plant development. Proc. Natl. Acad. Sci. USA 89: 7360–7364.

    Google Scholar 

  • Mathur, J., Spielhofer, P., Kost, B. and Chua, N.-H. 1999. The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126: 5559–5568.

    Google Scholar 

  • Mathur, J. and Chua, N.-H. 2000. Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes. Plant Cell 12: 465–477.

    Google Scholar 

  • Melaragno, J. E., Mehrotra, B. and Coleman, A. W. 1993. Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5: 1661–1668.

    Google Scholar 

  • Mironov, V., De Veylder, L., Van Montagu, M. and Inzé, D. 1999. Cyclin-dependent kinase and cell division in plants: the nexus. Plant Cell 11: 509–521.

    Google Scholar 

  • Nabeshima, K., Kurokawa, H., Takeuchi, M., Kinoshita, K., Nakaseko, Y. and Yanagida, M. 1995. p93dis1, which is required for sister chromatid separation, is a novel microtubule and spindle pole body-associating protein phosphorylated at the Cdc2 target sites. Genes Dev. 9: 1572–1585.

    Google Scholar 

  • Nigg, E. A. 1995. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays 17: 471–480.

    Google Scholar 

  • Nikolic, M., Dudek, H., Kwon, Y.T., Ramos, Y. F. M. and Tsai, L.-H. 1996. The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev. 10: 816–825

    Google Scholar 

  • Nikolic, M., Chou, M. M., Lu, W., Mayer, B.J. and Tsai, L.-H. 1998. The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 395: 194–198.

    Google Scholar 

  • Oppenheimer, D. G., Pollock, M. A., Vacik, J., Szmanski, D. B., Ericson, B., Feldmann, K. and Marks, M. D. 1997. Essential role of a kinesin-like protein in Arabidopsis trichome morohogenesis. Proc. Natl. Acad. Sci. USA 94: 6261–6266.

    Google Scholar 

  • Pines, J. 1993. Cyclins and cyclin-dependent kinases: take your partners. Trends Biochem. Sci. 18: 195–197.

    Google Scholar 

  • Reed, S. I. 1992. The role of p34 kinases in the G1 to S-phase transition. Annu. Rev. Cell Biol. 8: 529–561.

    Google Scholar 

  • Sambrook, J. Fritsch, E. F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.

    Google Scholar 

  • Segers, G., Gadisseur, I., Bergounioux, C., de Almeida Engler, J., Bernier, G., Jacqmard, A., Van Montagu, M. and Inzé, D. 1996. The Arabidopsis cyclin-dependent kinase gene cdc2bAt is preferentially expressed during S and G2 phases in the cell cycle. Plant J. 10: 601–612.

    Google Scholar 

  • Sigrist, S. J. and Lehner, C. F. 1997. Drosophila fizzy-related down-regulates mitotic cyclins and is required for cell proliferation arrest and entry into endocycles. Cell 90: 671–681.

    Google Scholar 

  • Stals, H., Bauwens, S., Traas, J., Van Montagu, M., Engler, G. and Inzé, D. 1997. Plant CDC2 is not only targeted to the pre-prophase band, but also co-localizes with the spindle, phragmoplast, and chromosomes. FEBS Lett. 418: 229–234.

    Google Scholar 

  • Szymanski, D. B., Jilk, R.A., Pollock, S.M. and Marks, D. 1998. Control of GL2 expression in Arabidopsis leaves and trichomes. Development 125: 1161–1171.

    Google Scholar 

  • Szymanski, D. B., Marks, M. D. and Wick, S. M. 1999. Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11: 2331–2347.

    Google Scholar 

  • Traas, J., Hulskamp, M., Gendreau, E. and Hofte, H. 1998. Endoreduplication and development: rule without dividing? Curr. Opin. Plant Biol. 1: 498–503.

    Google Scholar 

  • Valvekens, D., Van Montagu, M. and Van Lijsebettens M. 1988. Agrobacterium tumefaciens-mediated transformation of Arabidopsis root explants using kanamycin selection. Proc. Natl. Acad. Sci. USA 85: 5536–5540.

    Google Scholar 

  • Verde, F., Labbe, J. C., Doree, M. and Karsenti, E. 1990. regulation of microtubule dynamics by cdc2 protein kinase in cell-free extracts of Xenopus eggs. Nature 343: 233–238.

    Google Scholar 

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Imajuku, Y., Ohashi, Y., Aoyama, T. et al. An upstream region of the Arabidopsis thaliana CDKA;1 (CDC2aAt) gene directs transcription during trichome development. Plant Mol Biol 46, 205–213 (2001). https://doi.org/10.1023/A:1010665831955

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