Physcomitrella cyclin-dependent kinase a links cell cycle reactivation to other cellular changes during reprogramming of leaf cells

Plant Cell

Volumn 23, Issue 8, 2011, Pages 2924-2938

  Ishikawa, Masaki ^a   Murata, Takashi ^b,c   Sato, Yoshikatsu ^a,f   Nishiyama, Tomoaki ^a,d   Hiwatashi, Yuji ^b,c   Imai, Akihiro ^a,b   Kimura, Mina ^a   Sugimoto, Nagisa ^a   Akita, Asaka ^a   Oguri, Yasuko ^a   Friedman, William E ^e,g   Hasebe, Mitsuyasu ^a,b,c   Kubo, Minoru ^a,b  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^d KANAZAWA UNIVERSITY   (Japan)

^e UNIVERSITY OF COLORADO   (United States)

^f NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^g HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRYOPHYTA; CHLORONEMA; PHYSCOMITRELLA; PHYSCOMITRELLA PATENS;

EID: 80053213807     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.088005     Document Type: Article

References (82)

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 G2/M phase-specific genes in tobacco. J. Biol. Chem. 279: 32979-32988.
2. Banks, J.A., et al. (2011). The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332: 960-963.
3. Berger, C., Pallavi, S.K., Prasad, M., Shashidhara, L.S., and Technau, G.M. (2005). A critical role for cyclin E in cell fate determination in the central nervous system of Drosophila melanogaster. Nat. Cell Biol. 7: 56-62.
4. Birnbaum, K.D., and Sánchez Alvarado, A. (2008). Slicing across kingdoms: Regeneration in plants and animals. Cell 132: 697-710.
5. Borghi, L., Gutzat, R., Futterer, J., Laizet, Y., Hennig, L., and Gruissem, W. (2010). Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22: 1792-1811.
6. Budirahardja, Y., and Gonczy, P. (2009). Coupling the cell cycle to development. Development 136: 2861-2872.
7. Che, P., Gingerich, D.J., Lall, S., and Howell, S.H. (2002). Global and hormone-induced gene expression changes during shoot development in Arabidopsis. Plant Cell 14: 2771-2785.
8. Che, P., Lall, S., Nettleton, D., and Howell, S.H. (2006a). Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture. Plant Physiol. 141: 620-637.
9. Che, P., Love, T.M., Frame, B.R., Wang, K., Carriquiry, A.L., and Howell, S.H. (2006b). Gene expression patterns during somatic embryo development and germination in maize Hi II callus cultures. Plant Mol. Biol. 62: 1-14.
10. Chen, S., Bohrer, L.R., Rai, A.N., Pan, Y., Gan, L., Zhou, X., Bagchi, A., Simon, J.A., and Huang, H. (2010). Cyclin-dependent kinases regulate epigenetic gene silencing through phosphorylation of EZH2. Nat. Cell Biol. 12: 1108-1114.
11. Chiu, W.-l., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., and Sheen, J. (1996). Engineered GFP as a vital reporter in plants. Curr. Biol. 6: 325-330.
12. Chopra, R.N., and Kumra, P.K. (1988). Biology of Bryophytes. (New Delhi, India: Wiley Eastern).
13. Colasanti, J., Tyers, M., and Sundaresan, V. (1991). Isolation and characterization of cDNA clones encoding a functional p34cdc2 homologue from Zea mays. Proc. Natl. Acad. Sci. USA 88: 3377-3381.
14. Cove, D., Bezanilla, M., Harries, P., and Quatrano, R. (2006). Mosses as model systems for the study of metabolism and development. Annu. Rev. Plant Biol. 57: 497-520.
15. De Smet, I., Vanneste, S., Inzé, D., and Beeckman, T. (2006). Lateral root initiation or the birth of a new meristem. Plant Mol. Biol. 60: 871-887.
16. De Veylder, L., Beeckman, T., Beemster, G.T., Krols, L., Terras, F., Landrieu, I., van der Schueren, E., Maes, S., Naudts, M., and Inzé, D. (2001). Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13: 1653-1668.
17. De Veylder, L., Beeckman, T., and Inze, D. (2007). The ins and outs of the plant cell cycle. Nat. Rev. Mol. Cell Biol. 8: 655-665.
18. den Boer, B.G., and Murray, J.A. (2000). Triggering the cell cycle in plants. Trends Cell Biol. 10: 245-250.
19. Dolezel, J., and Bartos, J. (2005). Plant DNA flow cytometry and estimation of nuclear genome size. Ann. Bot. (Lond.) 95: 99-110.
20. Doonan, J.H., Cove, D.J., and Lloyd, C.W. (1988). Microtubules and microfilaments in tip growth - Evidence that microtubules impose polarity on protonemal growth in Physcomitrella patens. J. Cell Sci. 89: 533-540.
21. Dubrovsky, J.G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, M. G., Friml, J., Shishkova, S., Celenza, J., and Benkova, E. (2008). Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc. Natl. Acad. Sci. USA 105: 8790-8794.
22. Ferreira, P.C., Hemerly, A.S., Villarroel, R., Van Montagu, M., and Inzé, D. (1991). The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell 3: 531-540.
23. Finka, A., Schaefer, D.G., Saidi, Y., Goloubinoff, P., and Zryd, J.P. (2007). In vivo visualization of F-actin structures during the development of the moss Physcomitrella patens. New Phytol. 174: 63-76.
24. Friedman, W.E. (1991). Double fertilization in Ephedra trifurca, a nonflowering seed plant: the relationship between fertilization events and the cell cycle. Protoplasma 165: 106-120.
25. Gaamouche, T., Manes, C.L., Kwiatkowska, D., Berckmans, B., Koumproglou, R., Maes, S., Beeckman, T., Vernoux, T., Doonan, J.H., Traas, J., Inzé, D., and De Veylder, L. (2010). Cyclin-dependent kinase activity maintains the shoot apical meristem cells in an undifferentiated state. Plant J. 64: 26-37.
26. Gilbert, S.F. (2006). Developmental Biology. (Sunderland, MA: Sinauer Associates).
27. Gordon, S.P., Heisler, M.G., Reddy, G.V., Ohno, C., Das, P., and Meyerowitz, E.M. (2007). Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134: 3539-3548.
28. Guerineau, F., Brooks, L., Meadows, J., Lucy, A., Robinson, C., and Mullineaux, P. (1990). Sulfonamide resistance gene for plant transformation. Plant Mol. Biol. 15: 127-136.
29. Gutierrez, C. (2005). Coupling cell proliferation and development in plants. Nat. Cell Biol. 7: 535-541.
30. Harashima, H., Shinmyo, A., and Sekine, M. (2007). Phosphorylation of threonine 161 in plant cyclin-dependent kinase A is required for cell division by activation of its associated kinase. Plant J. 52: 435-448.
31. Harrison, C.J., Roeder, A.H., Meyerowitz, E.M., and Langdale, J.A. (2009). Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Curr. Biol. 19: 461-471.
32. Hemerly, A., Engler Jde, A., Bergounioux, C., Van Montagu, M., Engler, G., Inzé, D., and Ferreira, P. (1995). Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J. 14: 3925-3936.
33. 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.
34. Hemerly, A.S., Ferreira, P.C., Van Montagu, M., Engler, G., and Inzé, D. (2000). Cell division events are essential for embryo patterning and morphogenesis: studies on dominant-negative cdc2aAt mutants of Arabidopsis. Plant J. 23: 123-130.
35. Himanen, K., Boucheron, E., Vanneste, S., de Almeida Engler, J., Inzé, D., and Beeckman, T. (2002). Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14: 2339-2351.
36. Hirayama, T., Imajuku, Y., Anai, T., Matsui, M., and Oka, A. (1991). Identification of two cell-cycle-controlling cdc2 gene homologs in Arabidopsis thaliana. Gene 105: 159-165.
37. Hiwatashi, Y., Obara, M., Sato, Y., Fujita, T., Murata, T., and Hasebe, M. (2008). Kinesins are indispensable for interdigitation of phragmoplast microtubules in the moss Physcomitrella patens. Plant Cell 20: 3094-3106.
38. Inzé, D., and De Veylder, L. (2006). Cell cycle regulation in plant development. Annu. Rev. Genet. 40: 77-105.
39. Jefferson, R.A. (1987). Assaying chimeric genes in plants: The GUS gene fusion system. Plant Mol. Biol. Rep. 5: 387-405.
40. Kalderon, D., Richardson, W.D., Markham, A.F., and Smith, A.E. (1984). Sequence requirements for nuclear location of simian virus 40 large-T antigen. Nature 311: 33-38.
41. Kawamura, K., Murray, J.A., Shinmyo, A., and Sekine, M. (2006). Cell cycle regulated D3-type cyclins form active complexes with plantspecific B-type cyclin-dependent kinase in vitro. Plant Mol. Biol. 61: 311-327.
42. Kawasaki, S., and Murakami, Y. (2000). Genome analysis of Lotus japonicus. J. Plant Res. 113: 497-506.
43. Knoblich, J.A. (2008). Mechanisms of asymmetric stem cell division. Cell 132: 583-597.
44. Lajtha, L.G. (1979). Stem cell concepts. Differentiation 14: 23-34.
45. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408.
46. Masip, M., Veiga, A., Izpisua, J.C., and Simon, C. (2010). Reprogramming with defined factors: From induced pluripotency to induced transdifferentiation. Mol. Hum. Reprod. 16: 856-868.
47. McCusker, D., Denison, C., Anderson, S., Egelhofer, T.A., Yates III, J.R., Gygi, S.P., and Kellogg, D.R. (2007). Cdk1 coordinates cellsurface growth with the cell cycle. Nat. Cell Biol. 9: 506-515.
48. Menand, B., Calder, G., and Dolan, L. (2007a). Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomitrella patens. J. Exp. Bot. 58: 1843-1849.
49. Menand, B., Yi, K., Jouannic, S., Hoffmann, L., Ryan, E., Linstead, P., Schaefer, D.G., and Dolan, L. (2007b). An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316: 1477-1480.
50. Menges, M., Hennig, L., Gruissem, W., and Murray, J.A. (2002). Cell cycle-regulated gene expression in Arabidopsis. J. Biol. Chem. 277: 41987-42002.
51. 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.
52. Nakagami, H., Sekine, M., Murakami, H., and Shinmyo, A. (1999). Tobacco retinoblastoma-related protein phosphorylated by a distinct cyclin-dependent kinase complex with Cdc2/cyclin D in vitro. Plant J. 18: 243-252.
53. Nishiyama, T., Hiwatashi, Y., Sakakibara, I., Kato, M., and Hasebe, M. (2000). Tagged mutagenesis and gene-trap in the moss, Physcomitrella patens by shuttle mutagenesis. DNA Res. 7: 9-17.
54. Oakenfull, E.A., Riou-Khamlichi, C., and Murray, J.A. (2002). Plant Dtype cyclins and the control of G1 progression. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357: 749-760.
55. Odell, J.T., Nagy, F., and Chua, N.H. (1985). Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313: 810-812.
56. Okano, Y., Aono, N., Hiwatashi, Y., Murata, T., Nishiyama, T., Ishikawa, T., Kubo, M., and Hasebe, M. (2009). A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. Proc. Natl. Acad. Sci. USA 106: 16321-16326.
57. Osley, M.A. (1991). The regulation of histone synthesis in the cell cycle. Annu. Rev. Biochem. 60: 827-861.
58. Perroud, P.F., and Quatrano, R.S. (2008). BRICK1 is required for apical cell growth in filaments of the moss Physcomitrella patens but not for gametophore morphology. Plant Cell 20: 411-422.
59. Planchais, S., Glab, N., Inzé, D., and Bergounioux, C. (2000). Chemical inhibitors: A tool for plant cell cycle studies. FEBS Lett. 476: 78-83.
60. Planchais, S., Glab, N., Trehin, C., Perennes, C., Bureau, J.M., Meijer, L., and Bergounioux, C. (1997). Roscovitine, a novel cyclindependent kinase inhibitor, characterizes restriction point and G2/M transition in tobacco BY-2 cell suspension. Plant J. 12: 191-202.
61. Prigge, M.J., and Bezanilla, M. (2010). Evolutionary crossroads in developmental biology: Physcomitrella patens. Development 137: 3535-3543.
62. Quelo, A.H., Bryant, J.A., and Verbelen, J.P. (2002). Endoreduplication is not inhibited but induced by aphidicolin in cultured cells of tobacco. J. Exp. Bot. 53: 669-675.
63. Raghavan, V. (1989). Developmental Biology of Fern Gametophytes. (Cambridge, UK: Cambridge University Press).
64. Rensing, S.A., et al. (2008). The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64-69.
65. Saidi, Y., Finka, A., Chakhporanian, M., Zrÿd, J.-P., Schaefer, D.G., and Goloubinoff, P. (2005). Controlled expression of recombinant proteins in Physcomitrella patens by a conditional heat-shock promoter A tool for plant research and biotechnology. Plant Mol. Biol. 59: 697-711.
66. Sakakibara, K., Nishiyama, T., Sumikawa, N., Kofuji, R., Murata, T., and Hasebe, M. (2003). Involvement of auxin and a homeodomainleucine zipper I gene in rhizoid development of the moss Physcomitrella patens. Development 130: 4835-4846.
67. Salic, A., and Mitchison, T.J. (2008). A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl. Acad. Sci. USA 105: 2415-2420.
68. Schween, G., Gorr, G., Hohe, A., and Reski, R. (2003). Unique tissuespecific cell cycle in Physcomitrella. Plant Biol. 5: 50-58.
69. Sena, G., Wang, X., Liu, H.Y., Hofhuis, H., and Birnbaum, K.D. (2009). Organ regeneration does not require a functional stem cell niche in plants. Nature 457: 1150-1153.
70. Skoog, F., and Miller, C.O. (1957). Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 54: 118-130.
71. Slack, J.M. (2008). Origin of stem cells in organogenesis. Science 322: 1498-1501.
72. Sorrell, D.A., Menges, M., Healy, J.M., Deveaux, Y., Amano, C., Su, Y., Nakagami, H., Shinmyo, A., Doonan, J.H., Sekine, M., and Murray, J.A. (2001). Cell cycle regulation of cyclin-dependent kinases in tobacco cultivar Bright Yellow-2 cells. Plant Physiol. 126: 1214-1223.
73. Spinner, L., Pastuglia, M., Belcram, K., Pegoraro, M., Goussot, M., Bouchez, D., and Schaefer, D.G. (2010). The function of TONNEAU1 in moss reveals ancient mechanisms of division plane specification and cell elongation in land plants. Development 137: 2733-2742.
74. Sugimoto, K., Jiao, Y., and Meyerowitz, E.M. (2010). Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev. Cell 18: 463-471.
75. Sustar, A., and Schubiger, G. (2005). A transient cell cycle shift in Drosophila imaginal disc cells precedes multipotency. Cell 120: 383-393.
76. Tamura, K., Kimura, M., and Yamaguchi, I. (1995). Blasticidin S deaminase gene (BSD): A new selection marker gene for transformation of Arabidopsis thaliana and Nicotiana tabacum. Biosci. Biotechnol. Biochem. 59: 2336-2338.
77. Tilmann, C., and Kimble, J. (2005). Cyclin D regulation of a sexually dimorphic asymmetric cell division. Dev. Cell 9: 489-499.
78. Vogel, G. (2005). How does a single somatic cell become a whole plant? Science 309: 86.
79. Wang, H., Ouyang, Y., Somers, W.G., Chia, W., and Lu, B. (2007). Polo inhibits progenitor self-renewal and regulates Numb asymmetry by phosphorylating Pon. Nature 449: 96-100.
80. Wang, H., Qi, Q., Schorr, P., Cutler, A.J., Crosby, W.L., and Fowke, L. C. (1998). ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J. 15: 501-510.
81. Wirtz-Peitz, F., Nishimura, T., and Knoblich, J.A. (2008). Linking cell cycle to asymmetric division: Aurora-A phosphorylates the Par complex to regulate Numb localization. Cell 135: 161-173.
82. Zuo, J., Niu, Q.W., and Chua, N.H. (2000). Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24: 265-273.