The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis

Plant Cell

Volumn 18, Issue 4, 2006, Pages 893-906

  Menges, Margit ^a   Samland, Anne K ^a,b   Planchais, Séverine ^a,c   Murray, James A H ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF STUTTGART   (Germany)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; GENES; MUTAGENESIS; PHASE TRANSITIONS; PROTEINS; SUGAR (SUCROSE);

ARABIDOPSIS THALIANA; MITOTIC GENES; SYNCHRONIZED CULTURES; TRANSGENIC PLANTS;

PLANTS (BOTANY);

CELLS; GENES; MUTAGENS; PHASE TRANSITION; PLANTS; PROTEINS; SUGAR;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 33745448542     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.039636     Document Type: Article

References (52)

1. Araki, S., Ito, M., Soyano, T., Nishihama, R., and Machida, Y. (2004). Mitotic cyclins stimulate the activity of c-Myb-like factors for transactivation of G(2)/M-phase-specific genes in tobacco. J. Biol. Chem. 279, 32979-32988.
2. Barroco, R.M., Van Poucke, K., Bergervoet, J.H.W., De Veylder, L., Groot, S.P.C., Inze, D., and Engler, G. (2005). The role of the cell cycle machinery in resumption of postembryonic development. Plant Physiol. 137, 127-140.
3. Boonstra, J. (2003). Progression through the G(1)-phase of the ongoing cell cycle. J. Cell. Biochem. 90, 244-252.
4. Boucheron, E., Healy, J.M.S., Bajon, C., Sauvanet, A., Rembur, J., Noin, M., Sekine, M., Riou-Khamlichi, C., Murray, J.A.H., Van Onckelen, H., and Chriqui, D. (2005). Ectopic expression of Arabidopsis CycD2 and CycD3 in tobacco has distinct effects on the structural organization of the shoot apical meristem. J. Exp. Bot. 56, 123-134.
5. Cockcroft, C.E., den Boer, B.C., Healy, J.M., and Murray, J.A.H. (2000). Cyclin D control of growth rate in plants. Nature 405, 575-579.
6. Contento, A.L., Kim, S.-J., Diane, C., and Bassham, D.C. (2004). Transcriptome profiling of the response of Arabidopsis suspension culture cells to Sue starvation. Plant Physiol. 135, 2330-2347.
7. Dewitte, W., and Murray, J.A.H. (2003). The plant cell cycle. Annu. Rev. Plant Biol. 54, 235-264.
8. Dewitte, W., Riou-Khamlichi, C., Scofield, S., Healy, J.M., Jacqmard, A., Kilby, N.J., and Murray, J.A.H. (2003). Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15, 79-92.
9. Diehl, J.A., Cheng, M.G., Roussel, M.F., and Sherr, C.J. (1998). Glycogen synthase kinase 3 beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 12, 3499-3511.
10. Diehl, J.A., and Sherr, C.J. (1997). A dominant-negative cyclin D1 mutant prevents nuclear import of cyclin-dependent kinase 4 (Cdk4) and its phosphorylation by Cdk-activating kinase. Mol. Cell. Biol. 17, 7362-7374.
11. Diehl, J.A., Zindy, F., and Sherr, C.J. (1997). Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev. 11, 957-972.
12. Ekholm, S.V., and Reed, S.I. (2000). Regulation of G(1) cyclin dependent kinases in the mammalian cell cycle. Curr. Opin. Cell Biol. 12, 676-684.
13. Germain, D., Russell, A., Thompson, A., and Hendley, J. (2000). Ubiquitination of free cyclin D1 is independent of phosphorylation on threonine 286. J. Biol. Chem. 275, 12074-12079.
14. Gleave, A.P. (1992). A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20, 1203-1207.
15. Granier, C., and Tardieu, F. (1998). Spatial and temporal analyses of expansion and cell cycle in sunflower leaves. A common pattern of development for all zones of a leaf and different leaves of a plant. Plant Physiol. 116, 991-1001.
16. Healy, J.M.S., Menges, M., Doonan, J.H., and Murray, J.A.H. (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, 7041-7047.
17. Hu, Y., Bao, F., and Li, J. (2000). Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis. Plant J. 24, 693-701.
18. Huntley, R., et al. (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, 155-169.
19. Imoto, M., Doki, Y., Jiang, W., Han, E.K.H., and Weinstein, I.B. (1997). Effects of cyclin D1 overexpression on G1 progression-related events. Exp. Cell Res. 236, 173-180.
20. Ito, M., Araki, S., Matsunaga, S., Itoh, T., Nishihama, R., Machida, Y., Doonan, J.H., and Watanabe, A. (2001). G2/M-phase-specific transcription during the plant cell cycle is mediated by c-Myb-like transcription factors. Plant Cell 13, 1891-1905.
21. Jiang, W., Kahn, S.M., Zhou, P., Zhang, Y.J., Cacace, A.M., Infante, A.S., Doi, S., Santella, R.M., and Weinstein, I.B. (1993). Overexpression of cyclin D1 in rat fibroblasts causes abnormalities in growth control, cell cycle progression and gene expression. Oncogene 8, 3447-3457.
22. Kono, A., Umeda-Hara, C., Lee, J., Ito, M., Uchimiya, H., and Umeda, M. (2003). Arabidopsis D-type cyclin CycD4;1 is a novel cyclin partner of B2-type cyclin-dependent kinase. Plant Physiol. 132, 1315-1321.
23. Koroleva, O.A., Tomlinson, M., Parinyapong, P., Sakvarelidze, L., Leader, D., Shaw, P., and Doonan, J.H. (2004). CycD1, a putative G1 cyclin from Antirrhinum majus, accelerates the cell cycle in cultured tobacco BY-2 cells by enhancing both G1/S entry and progression through S and G2 phases. Plant Cell 16, 2364-2379.
24. Leng, X., Connell-Crowley, L., Goodrich, D., and Harper, J.W. (1997). S-phase entry upon ectopic expression of G1 cyclin-dependent kinases in the absence of retinoblastoma protein phosphorylation. Curr. Biol. 7, 709-712.
25. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408.
26. Masubelele, N.H., Dewitte, W., Menges, M., Maughan, S., Collins, C., Huntley, R., Nieuwland, J., Scofield, S., and Murray, J.A.H. (2005). D-type cyclins activate division in the root apex to promote seed germination in Arabidopsis. Proc. Natl. Acad. Sci. USA 102, 15694-15699.
27. May, M.J., and Leaver, C.J. (1993). Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. Plant Physiol. 103, 621-627.
28. Meijer, M., and Murray, J.A.H. (2001). Cell cycle controls and the development of plant form. Curr. Opin. Plant Biol. 4, 44-49.
29. Menges, M., De Jager, S.M., Gruissem, W., and Murray, J.A.H. (2005). Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J. 41, 546-566.
30. Menges, M., Hennig, L., Gruissem, W., and Murray, J.A.H. (2002). Cell cycle-regulated gene expression in Arabidopsis. J. Biol. Chem. 277, 41987-42002.
31. Menges, M., Hennig, L., Gruissem, W., and Murray, J.A.H. (2003). Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol. Biol. 53, 423-442.
32. Menges, M., and Murray, J.A.H. (2002). Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J. 30, 203-212.
33. Menges, M., and Murray, J.A.H. (2004). Cryopreservation of transformed and wild-type Arabidopsis and tobacco cell suspension cultures. Plant J. 37, 635-644.
34. Moriyasu, Y., and Ohsumi, Y. (1996). Autophagy in tobacco suspension-cultured cells in response to sucrose starvation. Plant Physiol. 111, 1233-1241.
35. Nakagami, H., Kawamura, K., Sugisaka, K., Sekine, M., and 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, 1847-1857.
36. Oakenfull, E.A., Riou-Khamlichi, C., and Murray, J.A.H. (2002). Plant D-type cyclins and the control of G1 progression. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 749-760.
37. Ohtsubo, M., and Roberts, J.M. (1993). Cyclin-dependent regulation of G(1) in mammalian fibroblasts. Science 259, 1908-1912.
38. Planchais, S., Samland, A.K., and Murray, J.A.H. (2004). Differential stability of Arabidopsis D-type cyclins: CycD3;1 is a highly unstable protein degraded by a proteasome-dependent mechanism. Plant J. 38, 616-625.
39. Quelle, D.E., Ashmun, R.A., Shurtleff, S.A., Kato, J.Y., Barsagi, D., Roussel, M.F., and Sherr, C.J. (1993). Overexpression of mouse D-type cyclins accelerates G(1) phase in rodent fibroblasts. Genes Dev. 7, 1559-1571.
40. Rechsteiner, M., and Rogers, S.W. (1996). PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21, 267-271.
41. Resnitzky, D., Gossen, M., Bujard, H., and Reed, S.I. (1994). Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol. 14, 1669-1679.
42. Riou-Khamlichi, C., Huntley, R., Jacqmard, A., and Murray, J.A.H. (1999). Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283, 1541-1544.
43. Riou-Khamlichi, C., Menges, M., Healy, J.M., and Murray, J.A.H. (2000). Sugar control of the plant cell cycle: Differential regulation of Arabidopsis D-type cyclin gene expression. Mol. Cell. Biol. 20, 4513-4521.
44. Schneider, B.L., Zhang, J., Markwardt, J., Tokiwa, G., Volpe, T., Honey, S., and Futcher, B. (2004). Growth rate and cell size modulate the synthesis of, and requirement for, G(1)-phase cyclins at start. Mol. Cell. Biol. 24, 10802-10813.
45. Schnittger, A., Schobinger, U., Bouyer, D., Weinl, C., Stierhof, Y.D., and Hulskamp, M. (2002). Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. Proc. Natl. Acad. Sci. USA 99, 6410-6415.
46. Sherr, C.J. (1995). D-type cyclins. Trends Biochem. Sci. 20, 187-190.
47. Sherr, C.J. (2000). The Pezcoller Lecture. Cancer cell cycles revisited. Cancer Res. 60, 3689-3695.
48. Soni, R., Carmichael, J.P., Shah, Z.H., and Murray, J.A.H. (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, 85-103.
49. Tarayre, S., Vinardell, J.M., Cebolla, A., Kondorosi, A., and Kondorosi, E. (2004). Two classes of the CDHH1-type activators of the anaphase-promoting complex in plants: Novel functional domains and distinct regulation. Plant Cell 16, 422-434.
50. Vandepoele, K., Raes, J., De Veylder, L., Rouze, P., Rombauts, S., and Inze, D. (2002). Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14, 903-916.
51. Verwoerd, T.C., Dekker, B.M.M., and Hoekema, A. (1989). A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 17, 2362.
52. Vierstra, R.D. (2003). The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. 8, 135-142.