Abstract
Cyclins are cell cycle regulators whose proteins oscillate dramatically during the cell cycle. Cyclin steady-state mRNA levels also fluctuate, and there are indications that both their rate of transcription and mRNA stability are under cell cycle control. Here, we demonstrate the transcriptional regulation of higher eukaryote cyclins throughout the whole cell cycle with a high temporal resolution. The promoters of two Arabidopsis cyclins, cyc3aAt and cyc1At, mediated transcriptional oscillation of the beta-glucuronidase (gus) reporter gene in stably transformed tobacco BY-2 cell lines. The rate of transcription driven by the cyc3aAt promoter was very low during G1, slowly increased during the S phase, peaked at the G2 phase and G2-to-M transition, and was down-regulated before early metaphase. In contrast, the rate of the cyc1At-related transcription increased upon exit of the S phase, peaked at the G2-to-M transition and during mitosis, and decreased upon exit from the M phase. This study indicates that transcription mechanisms that seem to be conserved among species play a significant role in regulating the mRNA abundance of the plant cyclins. Furthermore, the transcription patterns of cyc3aAt and cyc1At were coherent with their slightly higher sequence similarity to the A and B groups of animal cyclins, respectively, suggesting that they may fulfill comparable roles during the cell cycle.
Full text
PDF




Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- An G. High efficiency transformation of cultured tobacco cells. Plant Physiol. 1985 Oct;79(2):568–570. doi: 10.1104/pp.79.2.568. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cogswell J. P., Godlevski M. M., Bonham M., Bisi J., Babiss L. Upstream stimulatory factor regulates expression of the cell cycle-dependent cyclin B1 gene promoter. Mol Cell Biol. 1995 May;15(5):2782–2790. doi: 10.1128/mcb.15.5.2782. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coppock D. L., Pardee A. B. Control of thymidine kinase mRNA during the cell cycle. Mol Cell Biol. 1987 Aug;7(8):2925–2932. doi: 10.1128/mcb.7.8.2925. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ferreira P. C., Hemerly A. S., Engler J. D., van Montagu M., Engler G., Inzé D. Developmental expression of the arabidopsis cyclin gene cyc1At. Plant Cell. 1994 Dec;6(12):1763–1774. doi: 10.1105/tpc.6.12.1763. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ferreira P., Hemerly A., de Almeida Engler J., Bergounioux C., Burssens S., Van Montagu M., Engler G., Inzé D. Three discrete classes of Arabidopsis cyclins are expressed during different intervals of the cell cycle. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11313–11317. doi: 10.1073/pnas.91.24.11313. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fobert P. R., Coen E. S., Murphy G. J., Doonan J. H. Patterns of cell division revealed by transcriptional regulation of genes during the cell cycle in plants. EMBO J. 1994 Feb 1;13(3):616–624. doi: 10.1002/j.1460-2075.1994.tb06299.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Girard F., Strausfeld U., Fernandez A., Lamb N. J. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell. 1991 Dec 20;67(6):1169–1179. doi: 10.1016/0092-8674(91)90293-8. [DOI] [PubMed] [Google Scholar]
- Henglein B., Chenivesse X., Wang J., Eick D., Bréchot C. Structure and cell cycle-regulated transcription of the human cyclin A gene. Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5490–5494. doi: 10.1073/pnas.91.12.5490. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hirt H., Mink M., Pfosser M., Bögre L., Györgyey J., Jonak C., Gartner A., Dudits D., Heberle-Bors E. Alfalfa cyclins: differential expression during the cell cycle and in plant organs. Plant Cell. 1992 Dec;4(12):1531–1538. doi: 10.1105/tpc.4.12.1531. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jefferson R. A., Kavanagh T. A., Bevan M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987 Dec 20;6(13):3901–3907. doi: 10.1002/j.1460-2075.1987.tb02730.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- King R. W., Jackson P. K., Kirschner M. W. Mitosis in transition. Cell. 1994 Nov 18;79(4):563–571. doi: 10.1016/0092-8674(94)90542-8. [DOI] [PubMed] [Google Scholar]
- Koch C., Nasmyth K. Cell cycle regulated transcription in yeast. Curr Opin Cell Biol. 1994 Jun;6(3):451–459. doi: 10.1016/0955-0674(94)90039-6. [DOI] [PubMed] [Google Scholar]
- 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. 1995 Aug;7(8):1143–1155. doi: 10.1105/tpc.7.8.1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee H. H., Chiang W. H., Chiang S. H., Liu Y. C., Hwang J., Ng S. Y. Regulation of cyclin D1, DNA topoisomerase I, and proliferating cell nuclear antigen promoters during the cell cycle. Gene Expr. 1995;4(3):95–109. [PMC free article] [PubMed] [Google Scholar]
- Lepetit M., Ehling M., Chaubet N., Gigot C. A plant histone gene promoter can direct both replication-dependent and -independent gene expression in transgenic plants. Mol Gen Genet. 1992 Jan;231(2):276–285. doi: 10.1007/BF00279801. [DOI] [PubMed] [Google Scholar]
- Lucibello F. C., Truss M., Zwicker J., Ehlert F., Beato M., Müller R. Periodic cdc25C transcription is mediated by a novel cell cycle-regulated repressor element (CDE). EMBO J. 1995 Jan 3;14(1):132–142. doi: 10.1002/j.1460-2075.1995.tb06983.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maity A., McKenna W. G., Muschel R. J. Evidence for post-transcriptional regulation of cyclin B1 mRNA in the cell cycle and following irradiation in HeLa cells. EMBO J. 1995 Feb 1;14(3):603–609. doi: 10.1002/j.1460-2075.1995.tb07036.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morris T. D., Weber L. A., Hickey E., Stein G. S., Stein J. L. Changes in the stability of a human H3 histone mRNA during the HeLa cell cycle. Mol Cell Biol. 1991 Jan;11(1):544–553. doi: 10.1128/mcb.11.1.544. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Naeve G. S., Sharma A., Lee A. S. Temporal events regulating the early phases of the mammalian cell cycle. Curr Opin Cell Biol. 1991 Apr;3(2):261–268. doi: 10.1016/0955-0674(91)90150-w. [DOI] [PubMed] [Google Scholar]
- Ohtsubo N., Nakayama T., Terada R., Shimamoto K., Iwabuchi M. Proximal promoter region of the wheat histone H3 gene confers S phase-specific gene expression in transformed rice cells. Plant Mol Biol. 1993 Nov;23(3):553–565. doi: 10.1007/BF00019303. [DOI] [PubMed] [Google Scholar]
- Piaggio G., Farina A., Perrotti D., Manni I., Fuschi P., Sacchi A., Gaetano C. Structure and growth-dependent regulation of the human cyclin B1 promoter. Exp Cell Res. 1995 Feb;216(2):396–402. doi: 10.1006/excr.1995.1050. [DOI] [PubMed] [Google Scholar]
- Pines J., Hunter T. Human cyclin A is adenovirus E1A-associated protein p60 and behaves differently from cyclin B. Nature. 1990 Aug 23;346(6286):760–763. doi: 10.1038/346760a0. [DOI] [PubMed] [Google Scholar]
- Pines J., Hunter T. Isolation of a human cyclin cDNA: evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2. Cell. 1989 Sep 8;58(5):833–846. doi: 10.1016/0092-8674(89)90936-7. [DOI] [PubMed] [Google Scholar]
- Pines J. Protein kinases and cell cycle control. Semin Cell Biol. 1994 Dec;5(6):399–408. doi: 10.1006/scel.1994.1047. [DOI] [PubMed] [Google Scholar]
- Renaudin J. P., Colasanti J., Rime H., Yuan Z., Sundaresan V. Cloning of four cyclins from maize indicates that higher plants have three structurally distinct groups of mitotic cyclins. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7375–7379. doi: 10.1073/pnas.91.15.7375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walker D. H., Maller J. L. Role for cyclin A in the dependence of mitosis on completion of DNA replication. Nature. 1991 Nov 28;354(6351):314–317. doi: 10.1038/354314a0. [DOI] [PubMed] [Google Scholar]
- Welch P. J., Wang J. Y. Coordinated synthesis and degradation of cdc2 in the mammalian cell cycle. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):3093–3097. doi: 10.1073/pnas.89.7.3093. [DOI] [PMC free article] [PubMed] [Google Scholar]