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. 1996 Sep;8(9):1465–1476. doi: 10.1105/tpc.8.9.1465

Distinct classes of cdc2-related genes are differentially expressed during the cell division cycle in plants.

P R Fobert 1, V Gaudin 1, P Lunness 1, E S Coen 1, J H Doonan 1
PMCID: PMC161291  PMID: 8837502

Abstract

cdc2 and several related genes encode the catalytic subunits of cyclin-dependent kinases, which have been implicated in a number of cellular processes, including control of cell division. As a first step in exploring their function in plants, we isolated four cdc2-related genes from Antirrhinum. Two genes, cdc2a and cdc2b, encode proteins that contain a perfectly conserved PSTAIRE motif characteristic of cdc2 homologs, whereas the products of the two remaining genes, cdc2c and cdc2d, appear to represent a new subclass of proteins that have so far only been identified in plants. Transcripts of these novel genes were localized in isolated cells dispersed throughout actively dividing regions of the inflorescence. This localization is consistent with accumulation that is specific to particular phases of the cell cycle. Correlating cell labeling with nuclear condensation and double-labeling experiments using cdc2 and histone H4 as probes indicated that cdc2c transcripts accumulate during S phase as well as during the G2 and M transition, whereas cdc2d expression was specific to the G2 and M phases. All cells labeled with cdc2d also contained cdc2c label, Indicating that expression of cdc2d completely overlapped with that of cdc2c. Transcripts of cdc2a and cdc2b were detected in all cells within actively dividing regions, but at levels that were only slightly higher than those observed in nondividing areas. These transcripts did not appear to accumulate in a cell cycle-specific fashion. The genes cdc2a and cdc2b were able to partially complement a yeast cdc2 mutation, although all four genes appeared to interfere with the sizing mechanism of yeast cells. We propose that plants contain at least two classes of cdc2-related genes that differ in structure, expression, and perhaps function.

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Selected References

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  1. Basi G., Schmid E., Maundrell K. TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene. 1993 Jan 15;123(1):131–136. doi: 10.1016/0378-1119(93)90552-e. [DOI] [PubMed] [Google Scholar]
  2. Bradley D., Carpenter R., Sommer H., Hartley N., Coen E. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell. 1993 Jan 15;72(1):85–95. doi: 10.1016/0092-8674(93)90052-r. [DOI] [PubMed] [Google Scholar]
  3. Buck V., Russell P., Millar J. B. Identification of a cdk-activating kinase in fission yeast. EMBO J. 1995 Dec 15;14(24):6173–6183. doi: 10.1002/j.1460-2075.1995.tb00308.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carpenter R., Copsey L., Vincent C., Doyle S., Magrath R., Coen E. Control of flower development and phyllotaxy by meristem identity genes in antirrhinum. Plant Cell. 1995 Dec;7(12):2001–2011. doi: 10.1105/tpc.7.12.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carr A. M., MacNeill S. A., Hayles J., Nurse P. Molecular cloning and sequence analysis of mutant alleles of the fission yeast cdc2 protein kinase gene: implications for cdc2+ protein structure and function. Mol Gen Genet. 1989 Jul;218(1):41–49. doi: 10.1007/BF00330563. [DOI] [PubMed] [Google Scholar]
  6. Espinoza F. H., Ogas J., Herskowitz I., Morgan D. O. Cell cycle control by a complex of the cyclin HCS26 (PCL1) and the kinase PHO85. Science. 1994 Nov 25;266(5189):1388–1391. doi: 10.1126/science.7973730. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Forsburg S. L., Nurse P. Cell cycle regulation in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Annu Rev Cell Biol. 1991;7:227–256. doi: 10.1146/annurev.cb.07.110191.001303. [DOI] [PubMed] [Google Scholar]
  10. Hanks S. K. Homology probing: identification of cDNA clones encoding members of the protein-serine kinase family. Proc Natl Acad Sci U S A. 1987 Jan;84(2):388–392. doi: 10.1073/pnas.84.2.388. [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. Hata S. cDNA cloning of a novel cdc2+/CDC28-related protein kinase from rice. FEBS Lett. 1991 Feb 11;279(1):149–152. doi: 10.1016/0014-5793(91)80271-4. [DOI] [PubMed] [Google Scholar]
  13. Heichman K. A., Roberts J. M. Rules to replicate by. Cell. 1994 Nov 18;79(4):557–562. doi: 10.1016/0092-8674(94)90541-x. [DOI] [PubMed] [Google Scholar]
  14. Hemerly A. S., Ferreira P., de Almeida Engler J., Van Montagu M., Engler G., Inzé D. cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell. 1993 Dec;5(12):1711–1723. doi: 10.1105/tpc.5.12.1711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hemerly A., Engler J. de A., Bergounioux C., Van Montagu M., Engler G., Inzé D., Ferreira P. Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J. 1995 Aug 15;14(16):3925–3936. doi: 10.1002/j.1460-2075.1995.tb00064.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Kaffman A., Herskowitz I., Tjian R., O'Shea E. K. Phosphorylation of the transcription factor PHO4 by a cyclin-CDK complex, PHO80-PHO85. Science. 1994 Feb 25;263(5150):1153–1156. doi: 10.1126/science.8108735. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Lahti J. M., Xiang J., Heath L. S., Campana D., Kidd V. J. PITSLRE protein kinase activity is associated with apoptosis. Mol Cell Biol. 1995 Jan;15(1):1–11. doi: 10.1128/mcb.15.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lapidot-Lifson Y., Patinkin D., Prody C. A., Ehrlich G., Seidman S., Ben-Aziz R., Benseler F., Eckstein F., Zakut H., Soreq H. Cloning and antisense oligodeoxynucleotide inhibition of a human homolog of cdc2 required in hematopoiesis. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):579–583. doi: 10.1073/pnas.89.2.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lew J., Wang J. H. Neuronal cdc2-like kinase. Trends Biochem Sci. 1995 Jan;20(1):33–37. doi: 10.1016/s0968-0004(00)88948-3. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. McKinney J. D., Heintz N. Transcriptional regulation in the eukaryotic cell cycle. Trends Biochem Sci. 1991 Nov;16(11):430–435. doi: 10.1016/0968-0004(91)90170-z. [DOI] [PubMed] [Google Scholar]
  24. Measday V., Moore L., Ogas J., Tyers M., Andrews B. The PCL2 (ORFD)-PHO85 cyclin-dependent kinase complex: a cell cycle regulator in yeast. Science. 1994 Nov 25;266(5189):1391–1395. doi: 10.1126/science.7973731. [DOI] [PubMed] [Google Scholar]
  25. Meskiene I., Bögre L., Dahl M., Pirck M., Ha D. T., Swoboda I., Heberle-Bors E., Ammerer G., Hirt H. cycMs3, a novel B-type alfalfa cyclin gene, is induced in the G0-to-G1 transition of the cell cycle. Plant Cell. 1995 Jun;7(6):759–771. doi: 10.1105/tpc.7.6.759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Meyerson M., Enders G. H., Wu C. L., Su L. K., Gorka C., Nelson C., Harlow E., Tsai L. H. A family of human cdc2-related protein kinases. EMBO J. 1992 Aug;11(8):2909–2917. doi: 10.1002/j.1460-2075.1992.tb05360.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Meyerson M., Harlow E. Identification of G1 kinase activity for cdk6, a novel cyclin D partner. Mol Cell Biol. 1994 Mar;14(3):2077–2086. doi: 10.1128/mcb.14.3.2077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Moreno S., Klar A., Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991;194:795–823. doi: 10.1016/0076-6879(91)94059-l. [DOI] [PubMed] [Google Scholar]
  30. Pines J. Cyclins and cyclin-dependent kinases: take your partners. Trends Biochem Sci. 1993 Jun;18(6):195–197. doi: 10.1016/0968-0004(93)90185-p. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Prentice H. L. High efficiency transformation of Schizosaccharomyces pombe by electroporation. Nucleic Acids Res. 1992 Feb 11;20(3):621–621. doi: 10.1093/nar/20.3.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Reed S. I. The role of p34 kinases in the G1 to S-phase transition. Annu Rev Cell Biol. 1992;8:529–561. doi: 10.1146/annurev.cb.08.110192.002525. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Schwarz-Sommer Z., Hue I., Huijser P., Flor P. J., Hansen R., Tetens F., Lönnig W. E., Saedler H., Sommer H. Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J. 1992 Jan;11(1):251–263. doi: 10.1002/j.1460-2075.1992.tb05048.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sherr C. J. Mammalian G1 cyclins. Cell. 1993 Jun 18;73(6):1059–1065. doi: 10.1016/0092-8674(93)90636-5. [DOI] [PubMed] [Google Scholar]
  37. Shuttleworth J., Godfrey R., Colman A. p40MO15, a cdc2-related protein kinase involved in negative regulation of meiotic maturation of Xenopus oocytes. EMBO J. 1990 Oct;9(10):3233–3240. doi: 10.1002/j.1460-2075.1990.tb07522.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Simon M., Seraphin B., Faye G. KIN28, a yeast split gene coding for a putative protein kinase homologous to CDC28. EMBO J. 1986 Oct;5(10):2697–2701. doi: 10.1002/j.1460-2075.1986.tb04553.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Simon R., Carpenter R., Doyle S., Coen E. Fimbriata controls flower development by mediating between meristem and organ identity genes. Cell. 1994 Jul 15;78(1):99–107. doi: 10.1016/0092-8674(94)90576-2. [DOI] [PubMed] [Google Scholar]
  40. Soni R., Carmichael J. P., Shah Z. H., Murray J. A. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell. 1995 Jan;7(1):85–103. doi: 10.1105/tpc.7.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Staiger C., Doonan J. Cell division in plants. Curr Opin Cell Biol. 1993 Apr;5(2):226–231. doi: 10.1016/0955-0674(93)90107-2. [DOI] [PubMed] [Google Scholar]
  42. Stern B., Ried G., Clegg N. J., Grigliatti T. A., Lehner C. F. Genetic analysis of the Drosophila cdc2 homolog. Development. 1993 Jan;117(1):219–232. doi: 10.1242/dev.117.1.219. [DOI] [PubMed] [Google Scholar]
  43. Xiang J., Lahti J. M., Grenet J., Easton J., Kidd V. J. Molecular cloning and expression of alternatively spliced PITSLRE protein kinase isoforms. J Biol Chem. 1994 Jun 3;269(22):15786–15794. [PubMed] [Google Scholar]
  44. van den Heuvel S., Harlow E. Distinct roles for cyclin-dependent kinases in cell cycle control. Science. 1993 Dec 24;262(5142):2050–2054. doi: 10.1126/science.8266103. [DOI] [PubMed] [Google Scholar]

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