Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1993 Dec;5(12):1711–1723. doi: 10.1105/tpc.5.12.1711

cdc2a expression in Arabidopsis is linked with competence for cell division.

A S Hemerly 1, P Ferreira 1, J de Almeida Engler 1, M Van Montagu 1, G Engler 1, D Inzé 1
PMCID: PMC160398  PMID: 8305869

Abstract

A key regulator of the cell cycle is a highly conserved protein kinase whose catalytic subunit, p34(cdc2), is encoded by the cdc2 gene. We studied the control of the expression of the Arabidopsis cdc2a gene in cell suspensions and during plant development. In cell cultures, arrest of the cell cycle did not significantly affect cdc2a mRNA levels, but nutrient conditions were important for cdc2a expression. During plant development, the pattern of cdc2a expression was strongly correlated with the cell proliferation potential. The effects of external signals on cdc2a expression were analyzed. Wounding induced expression in leaves. Lack of light altered temporal regulation of cdc2a in the apical but not root meristem of seedlings. Differential cdc2a responses were obtained after different hormone treatments. Signals present only in intact plants were necessary to mediate these responses. Although other control levels have yet to be analyzed, these results suggest that the regulation of cdc2a expression may contribute greatly to spatial and temporal regulation of cell division in plants. Our results also show that cdc2a expression is not always coupled with cell proliferation but always precedes it. We propose that cdc2a expression may reflect a state of competence to divide, and that the release of other controls is necessary for cell division to occur.

Full Text

The Full Text of this article is available as a PDF (3.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. A simple and general method for transferring genes into plants. Science. 1985 Mar 8;227(4691):1229–1231. doi: 10.1126/science.227.4691.1229. [DOI] [PubMed] [Google Scholar]
  2. Alliotte T., Tiré C., Engler G., Peleman J., Caplan A., Van Montagu M., Inzé D. An Auxin-Regulated Gene of Arabidopsis thaliana Encodes a DNA-Binding Protein. Plant Physiol. 1989 Mar;89(3):743–752. doi: 10.1104/pp.89.3.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Atanassova R., Chaubet N., Gigot C. A 126 bp fragment of a plant histone gene promoter confers preferential expression in meristems of transgenic Arabidopsis. Plant J. 1992 May;2(3):291–300. doi: 10.1111/j.1365-313x.1992.00291.x. [DOI] [PubMed] [Google Scholar]
  4. Bergounioux C., Perennes C., Hemerly A. S., Qin L. X., Sarda C., Inze D., Gadal P. A cdc2 gene of Petunia hybrida is differentially expressed in leaves, protoplasts and during various cell cycle phases. Plant Mol Biol. 1992 Dec;20(6):1121–1130. doi: 10.1007/BF00028898. [DOI] [PubMed] [Google Scholar]
  5. Colasanti J., Tyers M., Sundaresan V. Isolation and characterization of cDNA clones encoding a functional p34cdc2 homologue from Zea mays. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3377–3381. doi: 10.1073/pnas.88.8.3377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Deblaere R., Bytebier B., De Greve H., Deboeck F., Schell J., Van Montagu M., Leemans J. Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucleic Acids Res. 1985 Jul 11;13(13):4777–4788. doi: 10.1093/nar/13.13.4777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Durkacz B., Carr A., Nurse P. Transcription of the cdc2 cell cycle control gene of the fission yeast Schizosaccharomyces pombe. EMBO J. 1986 Feb;5(2):369–373. doi: 10.1002/j.1460-2075.1986.tb04221.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ferreira P. C., Hemerly A. S., Villarroel R., Van Montagu M., Inzé D. The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell. 1991 May;3(5):531–540. doi: 10.1105/tpc.3.5.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Furukawa Y., Piwnica-Worms H., Ernst T. J., Kanakura Y., Griffin J. D. cdc2 gene expression at the G1 to S transition in human T lymphocytes. Science. 1990 Nov 9;250(4982):805–808. doi: 10.1126/science.2237430. [DOI] [PubMed] [Google Scholar]
  10. Green T. R., Ryan C. A. Wound-induced Proteinase Inhibitor in Tomato Leaves: Some Effects of Light and Temperature on the Wound Response. Plant Physiol. 1973 Jan;51(1):19–21. doi: 10.1104/pp.51.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hashimoto J., Hirabayashi T., Hayano Y., Hata S., Ohashi Y., Suzuka I., Utsugi T., Toh-e A., Kikuchi Y. Isolation and characterization of cDNA clones encoding cdc2 homologues from Oryza sativa: a functional homologue and cognate variants. Mol Gen Genet. 1992 May;233(1-2):10–16. doi: 10.1007/BF00587555. [DOI] [PubMed] [Google Scholar]
  12. Hemerly A., Bergounioux C., Van Montagu M., Inzé D., Ferreira P. Genes regulating the plant cell cycle: isolation of a mitotic-like cyclin from Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3295–3299. doi: 10.1073/pnas.89.8.3295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Imajuku Y., Hirayama T., Endoh H., Oka A. Exon-intron organization of the Arabidopsis thaliana protein kinase genes CDC2a and CDC2b. FEBS Lett. 1992 Jun 8;304(1):73–77. doi: 10.1016/0014-5793(92)80592-5. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. John P. C., Sek F. J., Carmichael J. P., McCurdy D. W. p34cdc2 homologue level, cell division, phytohormone responsiveness and cell differentiation in wheat leaves. J Cell Sci. 1990 Dec;97(Pt 4):627–630. doi: 10.1242/jcs.97.4.627. [DOI] [PubMed] [Google Scholar]
  16. Krek W., Nigg E. A. Structure and developmental expression of the chicken CDC2 kinase. EMBO J. 1989 Oct;8(10):3071–3078. doi: 10.1002/j.1460-2075.1989.tb08458.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lee M. G., Norbury C. J., Spurr N. K., Nurse P. Regulated expression and phosphorylation of a possible mammalian cell-cycle control protein. Nature. 1988 Jun 16;333(6174):676–679. doi: 10.1038/333676a0. [DOI] [PubMed] [Google Scholar]
  18. Logemann J., Schell J., Willmitzer L. Improved method for the isolation of RNA from plant tissues. Anal Biochem. 1987 May 15;163(1):16–20. doi: 10.1016/0003-2697(87)90086-8. [DOI] [PubMed] [Google Scholar]
  19. Maller J. L. Mitotic control. Curr Opin Cell Biol. 1991 Apr;3(2):269–275. doi: 10.1016/0955-0674(91)90151-n. [DOI] [PubMed] [Google Scholar]
  20. Martinez M. C., Jørgensen J. E., Lawton M. A., Lamb C. J., Doerner P. W. Spatial pattern of cdc2 expression in relation to meristem activity and cell proliferation during plant development. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7360–7364. doi: 10.1073/pnas.89.16.7360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McGowan C. H., Russell P., Reed S. I. Periodic biosynthesis of the human M-phase promoting factor catalytic subunit p34 during the cell cycle. Mol Cell Biol. 1990 Jul;10(7):3847–3851. doi: 10.1128/mcb.10.7.3847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Miao G. H., Hong Z., Verma D. P. Two functional soybean genes encoding p34cdc2 protein kinases are regulated by different plant developmental pathways. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):943–947. doi: 10.1073/pnas.90.3.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nurse P. Universal control mechanism regulating onset of M-phase. Nature. 1990 Apr 5;344(6266):503–508. doi: 10.1038/344503a0. [DOI] [PubMed] [Google Scholar]
  24. Reed S. I. The selection of S. cerevisiae mutants defective in the start event of cell division. Genetics. 1980 Jul;95(3):561–577. doi: 10.1093/genetics/95.3.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Saiki R. K., Scharf S., Faloona F., Mullis K. B., Horn G. T., Erlich H. A., Arnheim N. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 1985 Dec 20;230(4732):1350–1354. doi: 10.1126/science.2999980. [DOI] [PubMed] [Google Scholar]
  26. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Smyth D. R., Bowman J. L., Meyerowitz E. M. Early flower development in Arabidopsis. Plant Cell. 1990 Aug;2(8):755–767. doi: 10.1105/tpc.2.8.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Theologis A., Ray P. M. Early auxin-regulated polyadenylylated mRNA sequences in pea stem tissue. Proc Natl Acad Sci U S A. 1982 Jan;79(2):418–421. doi: 10.1073/pnas.79.2.418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Valvekens D., Van Montagu M., Van Lijsebettens M. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5536–5540. doi: 10.1073/pnas.85.15.5536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Van Haute E., Joos H., Maes M., Warren G., Van Montagu M., Schell J. Intergeneric transfer and exchange recombination of restriction fragments cloned in pBR322: a novel strategy for the reversed genetics of the Ti plasmids of Agrobacterium tumefaciens. EMBO J. 1983;2(3):411–417. doi: 10.1002/j.1460-2075.1983.tb01438.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Zulauf E., Sánchez F., Tobin S. L., Rdest U., McCarthy B. J. Developmental expression of a Drosophila actin gene encoding actin I. Nature. 1981 Aug 6;292(5823):556–558. doi: 10.1038/292556a0. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES