Advertisement

Control of the G1/S Phase Transition in Tobacco BY-2 Cells

  • Masami Sekine
  • Atsuhiko Shinmyo
Part of the Biotechnology in Agriculture and Forestry book series (AGRICULTURE, volume 53)

Abstract

The ability of cells to clonally replicate is central to life, and the co-ordinated regulation of cell division with cell growth and differentiation is required for the development of multicellular organisms. The cell division cycle consists of DNA replication and the allocation of identical genetic information to two daughter cells through mitosis and cell division. As in other eukaryotic cells, the plant cell cycle consists of four different phases representing DNA synthesis (S phase) and mitosis (M phase) separated by two gaps, the G1 and G2 phases, such that cells pass in order through M, G1, S, and G2 phases. Although progression through the cell cycle is regulated at both the G1/S and G2/M phase transitions, the major checkpoint of cell division commitment occurs at the G1 phase. Once cells have passed through this checkpoint, they become irreversibly committed to complete the cell cycle (Murray et al. 2001; Oakenful et al. 2002).

Keywords

Proliferate Cell Nuclear Antigen Curr Opin Plant Biol Plant Cell Cycle Exhibit Transactivation Activity Geminivirus Replication Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ach RA, Durfee T, Miller AB, Taranto P, Hanley-Bowdoin L, Zambryski P, Gruissem W (1997) RRB1and RRB2encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and geminivirus replication protein. Mol Cell Biol 17: 5077–5086Google Scholar
  2. Albani D, Mariconti L, Ricagno S, Pitto L, Moroni C, Helin K, Cella R (2000) DcE2F, a functional plant E2F-like transcriptional activator from Daucus carota. J Biol Chem 275: 19258–19267PubMedCrossRefGoogle Scholar
  3. Boniotti MB, Gutierrez C (2001) A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex. Plant J 28: 341–350Google Scholar
  4. Boniotti MB, Griffith ME (2002) “Cross-talk” between cell division cycle and development in plants. Plant Cell 14:11–16Google Scholar
  5. Chabouté M-E, Clément B, Sekine M, Philipps G (2000) Cell cycle regulation of the tobacco ribonucleotide reductase small subunit gene is mediated by E2F-like elements. Plant Cell 12: 1987–1999PubMedGoogle Scholar
  6. Cockcroft CE, den Boer BG, Healy JM, Murray JAH (2000) Cyclin D control of growth rate in plants. Nature 405: 575–579PubMedCrossRefGoogle Scholar
  7. Combettes B, Reichheld JP, Chabouté M-E, Philipps G, Shen WH, Chaubet-Gigot N (1999) Study of phase-specific gene expression in synchronized tobacco cells. Methods Cell Sci 21: 109–121PubMedCrossRefGoogle Scholar
  8. de Jager SM, Murray JAH (1999) Retinoblastoma proteins in plants. Plant Mol Biol 41:295–309Google Scholar
  9. de Jager SM, Menges M, Bauer UM, Murray JAH (2001) Arabidopsis E2F1 binds a sequence present in the promoter of S-phase-regulated gene AtCDC6 and is a member of a multigene family with differential activities. Plant Mol Biol 47: 555–568Google Scholar
  10. den Boer BGW, Murray JAH (2000a) Triggering the cell cycle in plants. Trends Cell Biol 10:245– 250Google Scholar
  11. den Boer BGW, Murray JAH (2000b) Control of plant growth and development through manipulation of cell-cycle genes. Curr Opin Biotech 11: 138–145CrossRefGoogle Scholar
  12. De Veylder L, Beeckman T, Beemster G, Krols L, Terras F, Landrieu I, Van Der Schueren E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13: 1653–1668PubMedGoogle Scholar
  13. De Veylder L, Beeckman T, Beemster GTS, de Almeida Engler J, Ormenese S, Maes S, Naudts M, Van Der Schueren E, Jacqmard A, Engler G, Inzé D (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J 21: 1360–1368PubMedCrossRefGoogle Scholar
  14. Dewitte W, Murray JMH (2003) The plant cell cycle. Ann Rev Plant Biol 54: 235–264CrossRefGoogle Scholar
  15. Diehl JA, Zindy F, Sherr CJ (1997) A dominant-negative cyclin D1 mutant prevents nuclear import of cyclin-dependent kinase 4 (CDK4) and its phosphorylation by CDK activating kinase. Genes Dev 11: 957–972PubMedCrossRefGoogle Scholar
  16. Doonan J, Fobert P (1997) Conserved and novel regulators of the plant cell cycle. Curr Opin Cell Biol 9: 824–830PubMedCrossRefGoogle Scholar
  17. Durfee T, Feiler HS, Gruissem W (2000) Retinoblastoma-related proteins in plants: homologues or orthologues of their metazoan counterparts? Plant Mol Biol 43: 635–642PubMedCrossRefGoogle Scholar
  18. Egelkrout EM, Robertson D, Hanley-Bowdoin L (2001) Proliferating Cell Nuclear Antigen transcription is repressed through an E2F consensus element and activated by geminivirus infection in mature leaves. Plant Cell 13: 1437–1452PubMedGoogle Scholar
  19. Geelen DNV, Inzé D (2001) A bright future for the Bright Yellow-2 cell culture. Plant Physiol 127: 1375–1379PubMedCrossRefGoogle Scholar
  20. Grafi G, Burnett RJ, Helentjaris T, Larkins BA, DeCaprio JA, Sellers WR, Kaelin WG (1996) A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication. Proc Natl Acad Sci USA 93: 8962–8967PubMedCrossRefGoogle Scholar
  21. Gutierrez C (1998) The retinoblastoma pathway in plant cell cycle and development. Curr Opin Plant Biol 1: 492–497PubMedCrossRefGoogle Scholar
  22. Gutierrez C, Ramirez-Parra E, Castellano MM, del Pozo JC (2002) G1 to Stransition: more than a cell cycle engine switch. Curr Opi Plant Biol 5: 480–486CrossRefGoogle Scholar
  23. Harbour JW, Dean DC (2000) The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev 14: 2393–2409PubMedCrossRefGoogle Scholar
  24. Hasezawa S, Nagata T (1991) Dynamic organization of plant microtubules at the 3 distinct transition points during the cell-cycle progression of synchronized tobacco BY-2 cells. Bot Acta 104: 206–211Google Scholar
  25. Healey JMS, Menges M, Doonan JH, Murray JAH (2001) The Arabidopsis D-type cyclins, CycD2 and CycD3, both interact in vivo with the PSTAIRE cyclin dependent kinase, Cdc2a, but are differentially controlled. J Biol Chem 276: 7041–7047CrossRefGoogle Scholar
  26. Huntley R, Murray JAH (1999) The plant cell cycle. Curr Opin Plant Biol 2: 440–446PubMedCrossRefGoogle Scholar
  27. Huntley R, Healy JMS, Freeman D, Lavender P, de Jager S, Greenwood J, Makker J, Walker E, Jackman M, Xie Q, Bannister AJ, Kouzarides T, Gutierrez C, Doonan JH, Murray JAH (1998) The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D ( CycD) proteins. Plant Mol Biol 37: 155–169Google Scholar
  28. Joubes J, Chevalier C, Dudits D, Heberle-Bors E, Inzé D, Umeda M, Renaudin JP (2000) CDKrelated protein kinases in plants. Plant Mol Biol 43: 607–621PubMedCrossRefGoogle Scholar
  29. Kong L-J, Orozco BM, Roe JL, Nagar S, Ou S, Feiler HS, Durfee T, Miller AB, Gruissem W, Robertson D, Hanley-Bowdoin L (2000) A geminivirus replication protein interacts with the retinoblastoma protein through a novel domain to determine symptoms and tissue specificity of infection in plants. EMBO J 19: 3485–3495PubMedCrossRefGoogle Scholar
  30. Kosugi S, Ohashi Y (2002a) E2F sites that can interact with E2F proteins cloned from rice are required for meristematic tissue-specific expression of rice and tobacco proliferating cell nuclear antigen promoters. Plant J 29: 45–59PubMedCrossRefGoogle Scholar
  31. Kosugi S, Ohashi Y (2002b) Interaction of the Arabidopsis E2F and DP proteins confers their concomitant nuclear translocation and transactivation. Plant Physiol 128: 833–843PubMedCrossRefGoogle Scholar
  32. Kosugi S, Ohashi Y (2002c) E2Ls, E2F-like repressors of Arabidopsis that bind to E2F sites in a monomeric form. J Biol Chem 277: 16553–16558PubMedCrossRefGoogle Scholar
  33. Laureys F, Dewitte W, Witters E, Van Montagu M, Inzé D, Van Onckelen H (1998) Zeatin is indispensable for the G2-M transition in tobacco BY-2 cells. FEBS Lett 426: 29–32PubMedCrossRefGoogle Scholar
  34. Lui H, Wang H, Delong C, Fowke LC, Crosby WL, Fobert PR (2000) The Arabidopsis Cdc2ainteracting protein ICK2 is structurally related to ICK1 and is a potent inhibitor of cyclindependent kinase activity in vitro. Plant J 21: 379–385PubMedCrossRefGoogle Scholar
  35. Magyar Z, Meszaros T, Miskolczi P, Deak M, Feher A, Brown S, Kondorosi E, Athanasiadis A, Pongor S, Bilgin M, Bako L, Koncz C, Dudits D (1997) Cell cycle phase specificity of putative cyclin-dependent kinase variants in synchronized alfalfa cells. Plant Cell 9: 223–235PubMedGoogle Scholar
  36. Magyar Z, Atanassova A, De Veylder L, Rombauts S, Inzé D (2000) Characterization of two distinct DP-related genes from Arabidopsis thaliana. FEBS Lett 486: 79–87PubMedCrossRefGoogle Scholar
  37. Mariconti L, Pellegrini B, Cantoni R, Stevens R, Bergounioux C, Cella R, Albani D (2002) The E2F family of transcription factors from Arabidopsis thaliana: novel and conserved components of the retinoblastoma/E2F pathway in plants. J Biol Chem 277: 9911–9919PubMedCrossRefGoogle Scholar
  38. Meijer M, Murray JAH (2000) The role and regulation of D-type cyclins in the plant cell cycle. Plant Mol Biol 43: 621–633PubMedCrossRefGoogle Scholar
  39. Meijer M, Murray JAH (2001) Cell cycle controls and the development of plant form. Curr Opin Plant Biol 4: 44–49PubMedCrossRefGoogle Scholar
  40. Menges M, Murray JAH (2002) Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J 30: 203–212PubMedCrossRefGoogle Scholar
  41. Mironov V, De Veylder L, Van Montagu M, Inzé D (1999) Cyclin-dependent kinases and cell division in plants–the nexus. Plant Cell 3: 29–41Google Scholar
  42. Murray JAH, Doonan J, Riou-Khamlichi C, Meijer M, Oakenfull EA (2001) G1 cyclins, cytokinins and the regulation of the G1/S transition. In: Francis D (ed) The plant cell cycle and its interfaces. CRC Press, Sheffield, pp 19–41Google Scholar
  43. Nagata T, Nemoto Y, Hasezawa S (1992) Tobacco BY-2 cell line as the “Helâ cell in the cell biology of higher plants. Int Rev Cytol 132: 1–30CrossRefGoogle Scholar
  44. Nakagami H, Sekine M, Murakami H, Shinmyo A (1999) Tobacco retinoblastoma-related protein phosphorylated by a distinct cyclin-dependent kinase complex with Cdc2/cyclin D in vitro. Plant J 18: 243–252PubMedCrossRefGoogle Scholar
  45. Nakagami H, Kawamura K, Sugisaka K, Sekine M, Shinmyo A (2002) Phosphorylation of retinoblastoma-related protein by the cyclin D/cyclin-dependent kinase complex is activated at the G1/S-phase transition in tobacco. Plant Cell 14: 1847–1857PubMedCrossRefGoogle Scholar
  46. Nevins JR (2001) The Rb/E2F pathway and cancer. Hum Mol Genet 10: 699–703PubMedCrossRefGoogle Scholar
  47. Oakenfull EA, Riou-Khamlichi C, Murray JAH (2002) Plant D-type cyclins and the control of G1 progression. Philos Trans R Soc Lond B Biol Sci 357: 749–760PubMedCrossRefGoogle Scholar
  48. Pines J (1995) Cyclins and cyclin-dependent kinases: a biochemical review. Biochem J 308:697– 711Google Scholar
  49. Planchaisa S, Glab N, Inzé D, Bergounioux C (2000) Chemical inhibitors: a tool for plant cell cycle studies. FEBS Lett 476: 78–83CrossRefGoogle Scholar
  50. Porceddu A, Stals H, Reichheld J-P, Segers G, De Veylder L, de Pinho Barroco R, Casteels P, Van Montagu M, Inzé D, Mironov V (2001) A plant-specific cyclin-dependent kinase is involved in the control of G2/M progression in plants. J Biol Chem 276: 36354–36360PubMedCrossRefGoogle Scholar
  51. Ramirez-Parra E, Xie Q, Boniotti MB, Gutierrez C (1999) The cloning of plant E2F, a retinoblastoma-binding protein, reveals unique and conserved features with animal G(1)/S regulators. Nucleic Acids Res 27: 3527–3533PubMedCrossRefGoogle Scholar
  52. Reichheld JP, Sonobe S, Clement B, Chaubet N, Gigot C (1995) Cell cycle regulated histone gene-expression in synchronized plant cells. Plant J 7: 245–252CrossRefGoogle Scholar
  53. Renaudin JP, Doonan JH, Freeman D, Hashimoto J, Hirt H, Inzé D, Jacobs T, Kouchi H, Rouze P, Sauter M, Savoure A, Sorrell DA, Sundaresan V, Murray JAH (1996) Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization. Plant Mol Biol 2: 1003–1018Google Scholar
  54. Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544PubMedCrossRefGoogle Scholar
  55. Riou-Khamlichi C, Menges M, Healy JM, Murray JAH (2000) Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol Cell Biol 20:4513– 4521Google Scholar
  56. Rossi V, Varotto S (2002) Insights into the G1/S transition in plants. Planta 215:345–356 Rossignol P, Stevens R, Perennes C, Jasinski S, Cella R, Tremousaygue D, Bergounioux C (2002)Google Scholar
  57. AtE2F-a and AtDP-a, members of the E2F family of transcription factors, induce Arabidopsis leaf cells to re-enter S phase. Mol Genet Genomics 266:995–1003Google Scholar
  58. Sekine M, Ito M, Uemukai K, Maeda Y, Nakagami H, Shinmyo A (1999) Isolation and characterization of the E2F-like gene in plants. FEBS Lett 460: 117–122PubMedCrossRefGoogle Scholar
  59. Shen W-H (2001) The plant cell cycle: G1/S regulation. Euphytica 118: 223–232CrossRefGoogle Scholar
  60. Sherr CJ, Roberts JM (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13: 1501–1512PubMedCrossRefGoogle Scholar
  61. Soni R, Carmichael JP, Shah ZH, Murray JAH (1995) A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7: 85–103PubMedGoogle Scholar
  62. Sorrell DA, Combettes B, Chaubet-Gigot N, Gigot C, Murray JAH (1999) Distinct cyclin D genes show mitotic accumulation or constant levels of transcripts in tobacco bright yellow-2 cells. Plant Physiol 119: 343–351PubMedCrossRefGoogle Scholar
  63. Sorrell DA, Menges M, Healy JMS, Deveaux Y, Amano C, Su Y, Nakagami H, Shinmyo A, Doonan JH, Sekine M, Murray JAH (2001) Cell cycle regulation of cyclin-dependent kinases in tobacco cultivar Bright Yellow-2 cells. Plant Physiol 126: 1214–1223PubMedCrossRefGoogle Scholar
  64. Stals H, Inzé D (2001) When plant cells decide to divide. Trends Plant Sci 6: 359–364PubMedCrossRefGoogle Scholar
  65. Stals H, Casteels P, Van Montagu M, Inzé D (2000) Regulation of cyclin-dependent kinases in Arabidopsis thaliana. Plant Mol Biol 43: 583–593PubMedCrossRefGoogle Scholar
  66. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815Google Scholar
  67. Trimarchi JM, Lees JA (2002) Transcription: Sibling rivalry in the E2F family. Nature Rev Mol Cell Biol 3: 11–20CrossRefGoogle Scholar
  68. Vandepoele K, Raes J, De Veylder L, Rouzé P, Rombauts S, Inzé D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14: 903–916PubMedCrossRefGoogle Scholar
  69. Wang H, Fowke LC, Crosby WL (1997) A plant cyclin-dependent kinase inhibitor gene. Nature 386: 451–452PubMedCrossRefGoogle Scholar
  70. Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL, Fowke LC (1998) Expression of the plant cyclindependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant J 15: 501–510PubMedCrossRefGoogle Scholar
  71. Wang H, Zhou Y, Gilmer S, Whitwill S, Fowke LC (2000) Expression of the plant cyclin-dependentGoogle Scholar
  72. kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant J 24:613–623Google Scholar
  73. Xie Q, Sanz-Burgos AP, Hannon GJ, Gutierrez C (1996) Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO J 15: 4900–4908PubMedGoogle Scholar
  74. Zhang S, Gavin M, Dahiya A, Postigo A, Ma D, Luo R, Harbour W, Dean D (2000) Exit from G1 and S Phase of the Cell Cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/ SNF and Rb-hSWI/SNF. Cell 101: 79–89PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2004

Authors and Affiliations

  • Masami Sekine
    • 1
  • Atsuhiko Shinmyo
    • 1
  1. 1.Nara Institute of Science and Technology (NAIST)Graduate School of Biological SciencesIkoma, NaraJapan

Personalised recommendations