GIGAS CELL1, a novel negative regulator of the anaphase-promoting complex/cyclosome, is required for proper mitotic progression and cell fate determination in Arabidopsis

Plant Cell

Volumn 23, Issue 12, 2011, Pages 4382-4393

  Iwata, Eriko ^a   Ikeda, Saki ^a   Matsunaga, Sachihiro ^b   Kurata, Mariko ^a   Yoshioka, Yasushi ^a   Criqui, Marie Claire ^c   Genschik, Pascal ^c   Ito, Masaki ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b TOKYO UNIVERSITY OF SCIENCE   (Japan)

^c INST DE BIOL MOLEC DES PLANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84856431074     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.092049     Document Type: Article

References (61)

1. Adachi, S., et al. (2011). Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. Proc. Natl. Acad. Sci. USA 108: 10004-10009.
2. Aoyama, T., and Chua, N.H. (1997). A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11: 605-612.
3. Barford, D. (2011). Structure, function and mechanism of the anaphase promoting complex (APC/C). Q. Rev. Biophys. 44: 153-190.
4. Beemster, G.T., De Veylder, L., Vercruysse, S., West, G., Rombaut, D., Van Hummelen, P., Galichet, A., Gruissem, W., Inzé, D., and Vuylsteke, M. (2005). Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol. 138: 734-743.
5. Boudolf, V., Barrôco, R., Engler, Jde.A., Verkest, A., Beeckman, T., Naudts, M., Inzé, D., and De Veylder, L. (2004). B1-type cyclindependent kinases are essential for the formation of stomatal complexes in Arabidopsis thaliana. Plant Cell 16: 945-955.
6. Breuer, C., Ishida, T., and Sugimoto, K. (2010). Developmental control of endocycles and cell growth in plants. Curr. Opin. Plant Biol. 13: 654-660.
7. Cebolla, A., Vinardell, J.M., Kiss, E., Oláh, B., Roudier, F., Kondorosi, A., and Kondorosi, E. (1999). The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J. 18: 4476-4484.
8. D'Amato, F. (1984). Role of polyploidy in reproductive organs and tissues. In Embryology of the Angiosperms, B.M. Johri, ed (Berlin: Springer-Verlag), pp. 519-566.
9. d'Erfurth, I., Jolivet, S., Froger, N., Catrice, O., Novatchkova, M., and Mercier, R. (2009). Turning meiosis into mitosis. PLoS Biol. 7: e1000124.
10. De Veylder, L., Larkin, J.C., and Schnittger, A. (2011). Molecular control and function of endoreplication in development and physiology. Trends Plant Sci. 16: 624-634.
11. Edgar, B.A., and Orr-Weaver, T.L. (2001). Endoreplication cell cycles: More for less. Cell 105: 297-306.
12. Eigsti, O.J. (1938). A cytological study of colchicine effects in the induction of polyploidy in plants. Proc. Natl. Acad. Sci. USA 24: 56-63.
13. Eloy, N.B., de Freitas Lima, M., Van Damme, D., Vanhaeren, H., Gonzalez, N., De Milde, L., Hemerly, A.S., Beemster, G.T., Inzé, D., and Ferreira, P.C. (2011). The APC/C subunit 10 plays an essential role in cell proliferation during leaf development. Plant J. 68: 351-363.
14. Falbel, T.G., Koch, L.M., Nadeau, J.A., Segui-Simarro, J.M., Sack, F.D., and Bednarek, S.Y. (2003). SCD1 is required for cytokinesis and polarized cell expansion in Arabidopsis thaliana [corrected]. Development 130: 4011-4024.
15. Grosskortenhaus, R., and Sprenger, F. (2002). Rca1 inhibits APCCdh1(Fzr) and is required to prevent cyclin degradation in G2. Dev. Cell 2: 29-40.
16. Haga, N., Kato, K., Murase, M., Araki, S., Kubo, M., Demura, T., Suzuki, K., Müller, I., Voss, U., Jürgens, G., and Ito, M. (2007). R1R2R3-Myb proteins positively regulate cytokinesis through activation of KNOLLE transcription in Arabidopsis thaliana. Development 134: 1101-1110.
17. Haga, N., Kobayashi, K., Suzuki, T., Maeo, K., Kubo, M., Ohtani, M., Mitsuda, N., Demura, T., Nakamura, K., Jürgens, G., and Ito, M. (2011). Mutations in MYB3R1 and MYB3R4 cause pleiotropic developmental defects and preferential down-regulation of multiple G2/Mspecific genes in Arabidopsis. Plant Physiol. 157: 706-717.
18. Hajdukiewicz, P., Svab, Z., and Maliga, P. (1994). The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25: 989-994.
19. Hara, K., Yokoo, T., Kajita, R., Onishi, T., Yahata, S., Peterson, K.M., Torii, K.U., and Kakimoto, T. (2009). Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol. 50: 1019-1031.
20. Hase, Y., Trung, K.H., Matsunaga, T., and Tanaka, A. (2006). A mutation in the uvi4 gene promotes progression of endo-reduplication and confers increased tolerance towards ultraviolet Blight. Plant J. 46: 317-326.
21. Hemerly, A.S., Ferreira, P., de Almeida Engler, J., Van Montagu, M., Engler, G., and Inzé, D. (1993). Cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5: 1711-1723.
22. Imai, K.K., Ohashi, Y., Tsuge, T., Yoshizumi, T., Matsui, M., Oka, A., and Aoyama, T. (2006). The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18: 382-396.
23. Inzé, D., and De Veylder, L. (2006). Cell cycle regulation in plant development. Annu. Rev. Genet. 40: 77-105.
24. Jürgens, G. (2005). Plant cytokinesis: Fission by fusion. Trends Cell Biol. 15: 277-283.
25. Kosetsu, K., Matsunaga, S., Nakagami, H., Colcombet, J., Sasabe, M., Soyano, T., Takahashi, Y., Hirt, H., and Machida, Y. (2010). The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell 22: 3778-3790.
26. Kubo, M., Udagawa, M., Nishikubo, N., Horiguchi, G., Yamaguchi, M., Ito, J., Mimura, T., Fukuda, H., and Demura, T. (2005). Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev. 19: 1855-1860.
27. Kevei, Z., Baloban, M., Da Ines, O., Tiricz, H., Kroll, A., Regulski, K., Mergaert, P., and Kondorosi, E. (2011). Conserved CDC20 cell cycle functions are carried out by two of the five isoforms in Arabidopsis thaliana. PLoS ONE 6: e20618.
28. Kurihara, D., Matsunaga, S., Uchiyama, S., and Fukui, K. (2008). Live cell imaging reveals plant aurora kinase has dual roles during mitosis. Plant Cell Physiol. 49: 1256-1261.
29. Kuromori, T., Hirayama, T., Kiyosue, Y., Takabe, H., Mizukado, S., Sakurai, T., Akiyama, K., Kamiya, A., Ito, T., and Shinozaki, K. (2004). A collection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J. 37: 897-905.
30. Lammens, T., Boudolf, V., Kheibarshekan, L., Zalmas, L.P., Gaamouche, T., Maes, S., Vanstraelen, M., Kondorosi, E., La Thangue, N.B., Govaerts, W., Inzé, D., and De Veylder, L. (2008). Atypical E2F activity restrains APC/CCCS52A2 function obligatory for endocycle onset. Proc. Natl. Acad. Sci. USA 105: 14721-14726.
31. Larson-Rabin, Z., Li, Z., Masson, P.H., and Day, C.D. (2009). FZR2/CCS52A1 expression is a determinant of endoreduplication and cell expansion in Arabidopsis. Plant Physiol. 149: 874-884.
32. Lee, H.O., Davidson, J.M., and Duronio, R.J. (2009). Endoreplication: Polyploidy with purpose. Genes Dev. 23: 2461-2477.
33. Levan, A. (1938). The effect of colchicine on root mitoses in Allium. Hereditas 24: 471-486.
34. Lilly, M.A., and Duronio, R.J. (2005). New insights into cell cycle control from the Drosophila endocycle. Oncogene 24: 2765-2775.
35. Machida, Y.J., and Dutta, A. (2007). The APC/C inhibitor, Emi1, is essential for prevention of rereplication. Genes Dev. 21: 184-194.
36. Madgwick, S., Hansen, D.V., Levasseur, M., Jackson, P.K., and Jones, K.T. (2006). Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. J. Cell Biol. 174: 791-801.
37. Marrocco, K., Bergdoll, M., Achard, P., Criqui, M.C., and Genschik, P. (2010). Selective proteolysis sets the tempo of the cell cycle. Curr. Opin. Plant Biol. 13: 631-639.
38. Marrocco, K., Thomann, A., Parmentier, Y., Genschik, P., and Criqui, M.C. (2009). The APC/C E3 ligase remains active in most post-mitotic Arabidopsis cells and is required for proper vasculature development and organization. Development 136: 1475-1485.
39. Nadeau, J.A. (2009). Stomatal development: New signals and fate determinants. Curr. Opin. Plant Biol. 12: 29-35.
40. Nadeau, J.A., and Sack, F.D. (2002). Control of stomatal distribution on the Arabidopsis leaf surface. Science 296: 1697-1700.
41. Nagl, W. (1978). Endopolyploidy and Polyteny in Differentiation and Evolution. (Amsterdam: North-Holland Publishing Company).
42. Nakamura, M., Naoi, K., Shoji, T., and Hashimoto, T. (2004). Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol. 45: 1330-1334.
43. Nakamura, R.L., McKendree, W.L., Jr., Hirsch, R.E., Sedbrook, J.C., Gaber, R.F., and Sussman, M.R. (1995). Expression of an Arabidopsis potassium channel gene in guard cells. Plant Physiol. 109: 371-374.
44. Narbonne-Reveau, K., Senger, S., Pal, M., Herr, A., Richardson, H.E., Asano, M., Deak, P., and Lilly, M.A. (2008). APC/CFzr/Cdh1 promotes cell cycle progression during the Drosophila endocycle. Development 135: 1451-1461.
45. Ohashi-Ito, K., and Bergmann, D.C. (2006). Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18: 2493-2505.
46. Perazza, D., Herzog, M., Hülskamp, M., Brown, S., Dorne, A.M., and Bonneville, J.M. (1999). Trichome cell growth in Arabidopsis thaliana can be derepressed by mutations in at least five genes. Genetics 152: 461-476.
47. Pesin, J.A., and Orr-Weaver, T.L. (2008). Regulation of APC/C activators in mitosis and meiosis. Annu. Rev. Cell Dev. Biol. 24: 475-499.
48. Peters, J.M. (2006). The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 7: 644-656.
49. Pillitteri, L.J., Sloan, D.B., Bogenschutz, N.L., and Torii, K.U. (2007). Termination of asymmetric cell division and differentiation of stomata. Nature 445: 501-505.
50. Saze, H., and Kakutani, T. (2007). Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatinremodeling factor DDM1. EMBO J. 26: 3641-3652.
51. Semiarti, E., Ueno, Y., Tsukaya, H., Iwakawa, H., Machida, C., and Machida, Y. (2001). The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128: 1771-1783.
52. Soyano, T., Nishihama, R., Morikiyo, K., Ishikawa, M., and Machida, Y. (2003). NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKKmediated MAPK cascade and is required for plant cytokinesis. Genes Dev. 17: 1055-1067.
53. Ten Hove, C.A., and Heidstra, R. (2008). Who begets whom? Plant cell fate determination by asymmetric cell division. Curr. Opin. Plant Biol. 11: 34-41.
54. Van Leene, J., et al. (2010). Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 6: 397.
55. Vanstraelen, M., Baloban, M., Da Ines, O., Cultrone, A., Lammens, T., Boudolf, V., Brown, S.C., De Veylder, L., Mergaert, P., and Kondorosi, E. (2009). APC/C-CCS52A complexes control meristem maintenance in the Arabidopsis root. Proc. Natl. Acad. Sci. USA 106: 11806-11811.
56. Weingartner, M., Criqui, M.C., Mészáros, T., Binarova, P., Schmit, A.C., Helfer, A., Derevier, A., Erhardt, M., Bögre, L., and Genschik, P. (2004). Expression of a nondegradable cyclin B1 affects plant development and leads to endomitosis by inhibiting the formation of a phragmoplast. Plant Cell 16: 643-657.
57. Weiss, H., and Maluszynska, J. (2001). Molecular cytogenetic analysis of polyploidization in the anther tapetum of diploid and autotetraploid Arabidopsis thaliana plants. Ann. Bot. (Lond.) 87: 729-735.
58. Wu, G., Glickstein, S., Liu, W., Fujita, T., Li, W., Yang, Q., Duvoisin, R., and Wan, Y. (2007). The anaphase-promoting complex coordinates initiation of lens differentiation. Mol. Biol. Cell 18: 1018-1029.
59. Yang, Y., Kim, A.H., Yamada, T., Wu, B., Bilimoria, P.M., Ikeuchi, Y., de la Iglesia, N., Shen, J., and Bonni, A. (2009). A Cdc20-APC ubiquitin signaling pathway regulates presynaptic differentiation. Science 326: 575-578.
60. Zhang, Y., Wang, Z., Liu, D.X., Pagano, M., and Ravid, K. (1998). Ubiquitin-dependent degradation of cyclin B is accelerated in polyploid megakaryocytes. J. Biol. Chem. 273: 1387-1392.
61. Zielke, N., Querings, S., Rottig, C., Lehner, C., and Sprenger, F. (2008). The anaphase-promoting complex/cyclosome (APC/C) is required for rereplication control in endoreplication cycles. Genes Dev. 22: 1690-1703.