Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1995 Jan;7(1):85–103. doi: 10.1105/tpc.7.1.85

A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif.

R Soni 1, J P Carmichael 1, Z H Shah 1, J A Murray 1
PMCID: PMC160767  PMID: 7696881

Abstract

A new family of three related cyclins has been identified in Arabidopsis by complementation of a yeast strain deficient in G1 cyclins. Individual members show tissue-specific expression and are conserved in other plant species. They form a distinctive group of plant cyclins, which we named delta-type cyclins to indicate their similarities with mammalian D-type cyclins. The sequence relationships between delta and D cyclins include the N-terminal sequence LXCXE. This motif was originally identified in certain viral oncoproteins and is strongly implicated in binding to the retinoblastoma protein pRb. By analogy to mammalian cyclin D, these plant homologs may mediate growth and phytohormonal signals into the plant cell cycle. In support of this hypothesis, we show that, on restimulation of suspension-cultured cells, cyclin delta 3 is rapidly induced by the plant growth regulator cytokinin and cyclin delta 2 is induced by carbon source.

Full Text

The Full Text of this article is available as a PDF (3.5 MB).

Selected References

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

  1. Ando K., Ajchenbaum-Cymbalista F., Griffin J. D. Regulation of G1/S transition by cyclins D2 and D3 in hematopoietic cells. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9571–9575. doi: 10.1073/pnas.90.20.9571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Atherton-Fessler S., Hannig G., Piwnica-Worms H. Reversible tyrosine phosphorylation and cell cycle control. Semin Cell Biol. 1993 Dec;4(6):433–442. doi: 10.1006/scel.1993.1051. [DOI] [PubMed] [Google Scholar]
  3. Baldin V., Lukas J., Marcote M. J., Pagano M., Draetta G. Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev. 1993 May;7(5):812–821. doi: 10.1101/gad.7.5.812. [DOI] [PubMed] [Google Scholar]
  4. Colasanti J., Cho S. O., Wick S., Sundaresan V. Localization of the Functional p34cdc2 Homolog of Maize in Root Tip and Stomatal Complex Cells: Association with Predicted Division Sites. Plant Cell. 1993 Sep;5(9):1101–1111. doi: 10.1105/tpc.5.9.1101. [DOI] [PMC free article] [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. Conia J., Alexander R. G., Wilder M. E., Richards K. R., Rice M. E., Jackson P. J. Reversible accumulation of plant suspension cell cultures in g(1) phase and subsequent synchronous traverse of the cell cycle. Plant Physiol. 1990 Dec;94(4):1568–1574. doi: 10.1104/pp.94.4.1568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Crowell D. N., Kadlecek A. T., John M. C., Amasino R. M. Cytokinin-induced mRNAs in cultured soybean cells. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8815–8819. doi: 10.1073/pnas.87.22.8815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Day I. S., Reddy A. S. Cloning of a family of cyclins from Arabidopsis thaliana. Biochim Biophys Acta. 1994 May 17;1218(1):115–118. doi: 10.1016/0167-4781(94)90112-0. [DOI] [PubMed] [Google Scholar]
  9. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dirick L., Nasmyth K. Positive feedback in the activation of G1 cyclins in yeast. Nature. 1991 Jun 27;351(6329):754–757. doi: 10.1038/351754a0. [DOI] [PubMed] [Google Scholar]
  11. Dowdy S. F., Hinds P. W., Louie K., Reed S. I., Arnold A., Weinberg R. A. Physical interaction of the retinoblastoma protein with human D cyclins. Cell. 1993 May 7;73(3):499–511. doi: 10.1016/0092-8674(93)90137-f. [DOI] [PubMed] [Google Scholar]
  12. Epstein C. B., Cross F. R. Genes that can bypass the CLN requirement for Saccharomyces cerevisiae cell cycle START. Mol Cell Biol. 1994 Mar;14(3):2041–2047. doi: 10.1128/mcb.14.3.2041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Evans L. S., Van't Hof J. Promotion of cell arrest in G2 in root and shoot meristems in Pisum by a factor from the cotyledons. Exp Cell Res. 1974 Aug;87(2):259–264. doi: 10.1016/0014-4827(74)90479-0. [DOI] [PubMed] [Google Scholar]
  14. Ewen M. E., Sluss H. K., Sherr C. J., Matsushime H., Kato J., Livingston D. M. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell. 1993 May 7;73(3):487–497. doi: 10.1016/0092-8674(93)90136-e. [DOI] [PubMed] [Google Scholar]
  15. Fang F., Newport J. W. Evidence that the G1-S and G2-M transitions are controlled by different cdc2 proteins in higher eukaryotes. Cell. 1991 Aug 23;66(4):731–742. doi: 10.1016/0092-8674(91)90117-h. [DOI] [PubMed] [Google Scholar]
  16. Feiler H. S., Jacobs T. W. Cell division in higher plants: a cdc2 gene, its 34-kDa product, and histone H1 kinase activity in pea. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5397–5401. doi: 10.1073/pnas.87.14.5397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Fisher R. P., Morgan D. O. A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell. 1994 Aug 26;78(4):713–724. doi: 10.1016/0092-8674(94)90535-5. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Glotzer M., Murray A. W., Kirschner M. W. Cyclin is degraded by the ubiquitin pathway. Nature. 1991 Jan 10;349(6305):132–138. doi: 10.1038/349132a0. [DOI] [PubMed] [Google Scholar]
  21. Hadwiger J. A., Wittenberg C., Richardson H. E., de Barros Lopes M., Reed S. I. A family of cyclin homologs that control the G1 phase in yeast. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6255–6259. doi: 10.1073/pnas.86.16.6255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hannon G. J., Demetrick D., Beach D. Isolation of the Rb-related p130 through its interaction with CDK2 and cyclins. Genes Dev. 1993 Dec;7(12A):2378–2391. doi: 10.1101/gad.7.12a.2378. [DOI] [PubMed] [Google Scholar]
  23. Hartwell L. H. Saccharomyces cerevisiae cell cycle. Bacteriol Rev. 1974 Jun;38(2):164–198. doi: 10.1128/br.38.2.164-198.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hata S., Kouchi H., Suzuka I., Ishii T. Isolation and characterization of cDNA clones for plant cyclins. EMBO J. 1991 Sep;10(9):2681–2688. doi: 10.1002/j.1460-2075.1991.tb07811.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Hirayama T., Imajuku Y., Anai T., Matsui M., Oka A. Identification of two cell-cycle-controlling cdc2 gene homologs in Arabidopsis thaliana. Gene. 1991 Sep 15;105(2):159–165. doi: 10.1016/0378-1119(91)90146-3. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Hirt H., Páy A., Györgyey J., Bakó L., Németh K., Bögre L., Schweyen R. J., Heberle-Bors E., Dudits D. Complementation of a yeast cell cycle mutant by an alfalfa cDNA encoding a protein kinase homologous to p34cdc2. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1636–1640. doi: 10.1073/pnas.88.5.1636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ito M., Kodama H., Komamine A. Identification of a novel S-phase-specific gene during the cell cycle in synchronous cultures of Catharanthus roseus cells. Plant J. 1991 Sep;1(2):141–148. doi: 10.1111/j.1365-313x.1991.00141.x. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. John P. C., Sek F. J., Lee M. G. A homolog of the cell cycle control protein p34cdc2 participates in the division cycle of Chlamydomonas, and a similar protein is detectable in higher plants and remote taxa. Plant Cell. 1989 Dec;1(12):1185–1193. doi: 10.1105/tpc.1.12.1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kapros T., Bögre L., Németh K., Bakó L., Györgyey J., Wu S. C., Dudits D. Differential Expression of Histone H3 Gene Variants during Cell Cycle and Somatic Embryogenesis in Alfalfa. Plant Physiol. 1992 Feb;98(2):621–625. doi: 10.1104/pp.98.2.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kato J., Matsushime H., Hiebert S. W., Ewen M. E., Sherr C. J. Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Genes Dev. 1993 Mar;7(3):331–342. doi: 10.1101/gad.7.3.331. [DOI] [PubMed] [Google Scholar]
  35. Knoblich J. A., Sauer K., Jones L., Richardson H., Saint R., Lehner C. F. Cyclin E controls S phase progression and its down-regulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell. 1994 Apr 8;77(1):107–120. doi: 10.1016/0092-8674(94)90239-9. [DOI] [PubMed] [Google Scholar]
  36. Koff A., Ohtsuki M., Polyak K., Roberts J. M., Massagué J. Negative regulation of G1 in mammalian cells: inhibition of cyclin E-dependent kinase by TGF-beta. Science. 1993 Apr 23;260(5107):536–539. doi: 10.1126/science.8475385. [DOI] [PubMed] [Google Scholar]
  37. Lahue E. E., Smith A. V., Orr-Weaver T. L. A novel cyclin gene from Drosophila complements CLN function in yeast. Genes Dev. 1991 Dec;5(12A):2166–2175. doi: 10.1101/gad.5.12a.2166. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Léopold P., O'Farrell P. H. An evolutionarily conserved cyclin homolog from Drosophila rescues yeast deficient in G1 cyclins. Cell. 1991 Sep 20;66(6):1207–1216. doi: 10.1016/0092-8674(91)90043-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Matsushime H., Ewen M. E., Strom D. K., Kato J. Y., Hanks S. K., Roussel M. F., Sherr C. J. Identification and properties of an atypical catalytic subunit (p34PSK-J3/cdk4) for mammalian D type G1 cyclins. Cell. 1992 Oct 16;71(2):323–334. doi: 10.1016/0092-8674(92)90360-o. [DOI] [PubMed] [Google Scholar]
  42. Matsushime H., Roussel M. F., Ashmun R. A., Sherr C. J. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell. 1991 May 17;65(4):701–713. doi: 10.1016/0092-8674(91)90101-4. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Meyerson M., Faha B., Su L. K., Harlow E., Tsai L. H. The cyclin-dependent kinase family. Cold Spring Harb Symp Quant Biol. 1991;56:177–186. doi: 10.1101/sqb.1991.056.01.023. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. 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]
  47. Minami M., Huh G. H., Yang P., Iwabuchi M. Coordinate gene expression of five subclass histones and the putative transcription factors, HBP-1a and HBP-1b, of histone genes in wheat. Plant Mol Biol. 1993 Oct;23(2):429–434. doi: 10.1007/BF00029019. [DOI] [PubMed] [Google Scholar]
  48. Minet M., Dufour M. E., Lacroute F. Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 1992 May;2(3):417–422. doi: 10.1111/j.1365-313x.1992.00417.x. [DOI] [PubMed] [Google Scholar]
  49. Motokura T., Bloom T., Kim H. G., Jüppner H., Ruderman J. V., Kronenberg H. M., Arnold A. A novel cyclin encoded by a bcl1-linked candidate oncogene. Nature. 1991 Apr 11;350(6318):512–515. doi: 10.1038/350512a0. [DOI] [PubMed] [Google Scholar]
  50. Murray A. W., Solomon M. J., Kirschner M. W. The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature. 1989 May 25;339(6222):280–286. doi: 10.1038/339280a0. [DOI] [PubMed] [Google Scholar]
  51. Murray J. A. Plant cell division: the beginning of START. Plant Mol Biol. 1994 Oct;26(1):1–3. doi: 10.1007/BF00039513. [DOI] [PubMed] [Google Scholar]
  52. Nasmyth K. Control of the yeast cell cycle by the Cdc28 protein kinase. Curr Opin Cell Biol. 1993 Apr;5(2):166–179. doi: 10.1016/0955-0674(93)90099-c. [DOI] [PubMed] [Google Scholar]
  53. Nugent J. H., Alfa C. E., Young T., Hyams J. S. Conserved structural motifs in cyclins identified by sequence analysis. J Cell Sci. 1991 Jul;99(Pt 3):669–674. doi: 10.1242/jcs.99.3.669. [DOI] [PubMed] [Google Scholar]
  54. 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]
  55. Ohtsubo M., Roberts J. M. Cyclin-dependent regulation of G1 in mammalian fibroblasts. Science. 1993 Mar 26;259(5103):1908–1912. doi: 10.1126/science.8384376. [DOI] [PubMed] [Google Scholar]
  56. Pardee A. B. G1 events and regulation of cell proliferation. Science. 1989 Nov 3;246(4930):603–608. doi: 10.1126/science.2683075. [DOI] [PubMed] [Google Scholar]
  57. 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]
  58. Quelle D. E., Ashmun R. A., Shurtleff S. A., Kato J. Y., Bar-Sagi D., Roussel M. F., Sherr C. J. Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev. 1993 Aug;7(8):1559–1571. doi: 10.1101/gad.7.8.1559. [DOI] [PubMed] [Google Scholar]
  59. Rechsteiner M. PEST sequences are signals for rapid intracellular proteolysis. Semin Cell Biol. 1990 Dec;1(6):433–440. [PubMed] [Google Scholar]
  60. Reed S. I. G1-specific cyclins: in search of an S-phase-promoting factor. Trends Genet. 1991 Mar;7(3):95–99. doi: 10.1016/0168-9525(91)90279-Y. [DOI] [PubMed] [Google Scholar]
  61. 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]
  62. Richardson H. E., O'Keefe L. V., Reed S. I., Saint R. A Drosophila G1-specific cyclin E homolog exhibits different modes of expression during embryogenesis. Development. 1993 Nov;119(3):673–690. doi: 10.1242/dev.119.3.673. [DOI] [PubMed] [Google Scholar]
  63. Rogers S., Wells R., Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 1986 Oct 17;234(4774):364–368. doi: 10.1126/science.2876518. [DOI] [PubMed] [Google Scholar]
  64. Schiestl R. H., Gietz R. D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet. 1989 Dec;16(5-6):339–346. doi: 10.1007/BF00340712. [DOI] [PubMed] [Google Scholar]
  65. Sewing A., Bürger C., Brüsselbach S., Schalk C., Lucibello F. C., Müller R. Human cyclin D1 encodes a labile nuclear protein whose synthesis is directly induced by growth factors and suppressed by cyclic AMP. J Cell Sci. 1993 Feb;104(Pt 2):545–555. doi: 10.1242/jcs.104.2.545. [DOI] [PubMed] [Google Scholar]
  66. 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]
  67. Solomon M. J. Activation of the various cyclin/cdc2 protein kinases. Curr Opin Cell Biol. 1993 Apr;5(2):180–186. doi: 10.1016/0955-0674(93)90100-5. [DOI] [PubMed] [Google Scholar]
  68. Soni R., Carmichael J. P., Murray J. A. Parameters affecting lithium acetate-mediated transformation of Saccharomyces cerevisiae and development of a rapid and simplified procedure. Curr Genet. 1993 Nov;24(5):455–459. doi: 10.1007/BF00351857. [DOI] [PubMed] [Google Scholar]
  69. Soni R., Murray J. A. A rapid and inexpensive method for isolation of shuttle vector DNA from yeast for the transformation of E.coli. Nucleic Acids Res. 1992 Nov 11;20(21):5852–5852. doi: 10.1093/nar/20.21.5852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Soni R., Murray J. A. Isolation of intact DNA and RNA from plant tissues. Anal Biochem. 1994 May 1;218(2):474–476. doi: 10.1006/abio.1994.1214. [DOI] [PubMed] [Google Scholar]
  71. Tamura K., Kanaoka Y., Jinno S., Nagata A., Ogiso Y., Shimizu K., Hayakawa T., Nojima H., Okayama H. Cyclin G: a new mammalian cyclin with homology to fission yeast Cig1. Oncogene. 1993 Aug;8(8):2113–2118. [PubMed] [Google Scholar]
  72. Tsai L. H., Lees E., Faha B., Harlow E., Riabowol K. The cdk2 kinase is required for the G1-to-S transition in mammalian cells. Oncogene. 1993 Jun;8(6):1593–1602. [PubMed] [Google Scholar]
  73. Tyers M., Tokiwa G., Futcher B. Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins. EMBO J. 1993 May;12(5):1955–1968. doi: 10.1002/j.1460-2075.1993.tb05845.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Wiman K. G. The retinoblastoma gene: role in cell cycle control and cell differentiation. FASEB J. 1993 Jul;7(10):841–845. doi: 10.1096/fasebj.7.10.8393817. [DOI] [PubMed] [Google Scholar]
  75. Wimmel A., Lucibello F. C., Sewing A., Adolph S., Müller R. Inducible acceleration of G1 progression through tetracycline-regulated expression of human cyclin E. Oncogene. 1994 Mar;9(3):995–997. [PubMed] [Google Scholar]
  76. Wittenberg C., Sugimoto K., Reed S. I. G1-specific cyclins of S. cerevisiae: cell cycle periodicity, regulation by mating pheromone, and association with the p34CDC28 protein kinase. Cell. 1990 Jul 27;62(2):225–237. doi: 10.1016/0092-8674(90)90361-h. [DOI] [PubMed] [Google Scholar]
  77. Won K. A., Xiong Y., Beach D., Gilman M. Z. Growth-regulated expression of D-type cyclin genes in human diploid fibroblasts. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9910–9914. doi: 10.1073/pnas.89.20.9910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Xiong Y., Beach D. Population explosion in the cyclin family. Curr Biol. 1991 Dec;1(6):362–364. doi: 10.1016/0960-9822(91)90193-z. [DOI] [PubMed] [Google Scholar]
  79. Xiong Y., Connolly T., Futcher B., Beach D. Human D-type cyclin. Cell. 1991 May 17;65(4):691–699. doi: 10.1016/0092-8674(91)90100-d. [DOI] [PubMed] [Google Scholar]
  80. Xiong Y., Menninger J., Beach D., Ward D. C. Molecular cloning and chromosomal mapping of CCND genes encoding human D-type cyclins. Genomics. 1992 Jul;13(3):575–584. doi: 10.1016/0888-7543(92)90127-e. [DOI] [PubMed] [Google Scholar]
  81. Xiong Y., Zhang H., Beach D. D type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA. Cell. 1992 Oct 30;71(3):505–514. doi: 10.1016/0092-8674(92)90518-h. [DOI] [PubMed] [Google Scholar]
  82. 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]

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

RESOURCES