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The cell cycle and seed germination

Published online by Cambridge University Press:  22 February 2007

Jorge M. Vázquez-Ramos*
Affiliation:
Departamento de Bioquímica, Facultad de Química, UNAM, México 04510 DF, México
María de la Paz Sánchez
Affiliation:
Departamento de Bioquímica, Facultad de Química, UNAM, México 04510 DF, México
*
*Correspondence Fax: +52 56225284, Email: [email protected]

Abstract

The cell cycle is the series of molecular events that allows cells to duplicate and segregate their chromosomes to form new cells. The finding that a protein kinase, the product of the yeast cdc2 gene, was fundamental in the regulation of the G2/M and G1/S transitions, associated with unstable proteins named cyclins, opened a very exciting and dynamic research area. The number of gene products that participate in the development and regulation of the cell cycle may be in the hundreds, and there is a high degree of conservation in protein sequences and regulatory pathways among eukaryotes. Although there are clear differences between plants and animals in cell structure, organization, growth, development and differentiation, the same types of proteins and very similar regulatory pathways seem to exist. Seed germination appears to be an excellent model system for studying the cell cycle in plants. Imbibition will reactivate meristematic cells – most initially with a G1 DNA content – into the cell cycle in preparation for seedling establishment. Early events include a thorough survey of DNA status, since the drying process and seed storage conditions reduce chromosomal integrity. The initiation of cell cycle events leading to G1 and S phases, and of the germination process itself, may depend on a G1 checkpoint control. Most, if not all, cell cycle proteins appear to be already present in unimbibed embryos, although there is evidence of protein turnover in the early hours, suggesting the need for de novo protein synthesis. Regulation also may occur at the level of protein modification, because existing G1, S and G2 cell cycle proteins appear to be activated at precise times during germination. Thus, cell cycle control during seed germination may be exerted at multiple levels; however, knowledge of cell cycle events and their importance for germination is still scarce and fragmentary, and different species may have developed unique control mechanisms, more suited to specific germination characteristics and habitat.

Type
Invited Review
Copyright
Copyright © Cambridge University Press 2003

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References

Ach, R.A., Durfee, T., Miller, A.B., Taranto, P., Hanley Bowdoin, L., Zambryski, P.C. and Gruissem, W. (1997) RRB1 and RRB2 encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and geminivirus replication protein. Molecular and Cellular Biology 17, 50775086.Google Scholar
Albani, D., Mariconti, L., Ricagno, S., Pitto, L., Moroni, C., Helin, K. and Cella, R. (2000) DcE2F, a functional plant E2F-like transcriptional activator from Daucus carota. Journal of Biological Chemistry 275, 1925819267.CrossRefGoogle ScholarPubMed
Al-Rashdi, J. and Bryant, J.A. (1994) Purification of a DNA binding protein from a multi-protein complex associated with DNA polymerase α in pea. Journal of Experimental Botany 45, 18671871.CrossRefGoogle Scholar
Ashraf, M. and Bray, C.M. (1993) DNA synthesis in osmoprimed leek (Allium porrum L.) seeds and evidence for repair and replication. Seed Science Research 3, 1523.Google Scholar
Baíza, A.M., Vázquez-Ramos, J.M. and Sánchez de Jiménez, E. (1989) DNA synthesis and cell division in embryonic maize tissues during germination. Journal of Plant Physiology 135, 416421.CrossRefGoogle Scholar
Bartek, J. and Lukas, J. (2001) Mammalian G1- and S- phase checkpoints in response to DNA damage. Current Opinion in Cell Biology 13, 738747.CrossRefGoogle ScholarPubMed
Benedetto, J.P., Ech-Chaoui, R., Plissonneau, J., Laquel, P., Litvak, S. and Castroviejo, M. (1996) Changes of enzymes and factors involved in DNA synthesis during wheat embryo germination. Plant Molecular Biology 31, 12171225.CrossRefGoogle ScholarPubMed
Bewley, J.D. and Black, M. (1994) Seeds: Physiology of development and germination (2nd edition). New York, Plenum.Google Scholar
BinoR.J., De R.J., De, Vries, J.N., Kraak, H.L. and Van Pijlen, J.G. (1992) Flow cytometric determination of nuclear replication stages in tomato seeds during priming and germination. Annals of Botany 69, 231236.Google Scholar
Black, A.R. and Azizkhan-Clifford, J. (1999) Regulation of E2F: a family of transcription factors involved in proliferation control. Gene 237, 281302.CrossRefGoogle ScholarPubMed
Bradford, K.J. (1986) Manipulations of seed water relations via osmotic priming to improve germination under stress conditions. Hortscience 21, 11051112.CrossRefGoogle Scholar
Bray, C.M., Davison, P.A., Ashraf, M. and Taylor, R.M. (1989) Biochemical changes during osmopriming of leek seeds. Annals of Botany 63, 185193.CrossRefGoogle Scholar
Brehm, A. and Kouzarides, T. (1999) Retinoblastoma protein meets chromatin. Trends in Biochemical Sciences 24, 142145.CrossRefGoogle ScholarPubMed
Breyne, P., Dreesen, R., Vandepoele, K., De Veylder, L., Van Breusegem, F., Callewaert, L., Rombauts, S., Raes, J., Cannoot, B., Engler, G., Inzé, D. and Zabeau, M. (2002) Transcriptome analysis during cell division in plants. Proceedings of the National Academy of Sciences, USA 12, 1482514830.CrossRefGoogle Scholar
Bryant, J.A., Fitchett, P.N., Hughes, S.G. and Sibson, D.R. (1992) DNA polymerase α in pea is part of a large multiprotein complex. Journal of Experimental Botany 43, 3140.Google Scholar
Castellano, M.M., del Pozo, J.C., Ramírez-Parra, E., Brown, S. and Gutierrez, C. (2001) Expression and stability of Arabidopsis CDC6 are associated with endoreplication. Plant Cell 13, 26712686.CrossRefGoogle ScholarPubMed
Castroviejo, M., Tharaud, D., Tarrago-Litvak, L. and Litvak, S. (1979) Multiple deoxyribonucleic acid polymerases from quiescent wheat embryos. Purification and characterization of three enzymes from the soluble cytoplasm and one from purified mitochondria. Biochemical Journal 181, 183191.CrossRefGoogle ScholarPubMed
Castroviejo, M., Gatius, M.T. and Litvak, S. (1990) A low molecular weight DNA polymerase from wheat embryos. Plant Molecular Biology 15, 383397.CrossRefGoogle ScholarPubMed
Chabouté, M.E., Clement, B., Sekine, M., Philipps, G. and Chaubet-Gigot, N. (2000) Cell cycle regulation of the tobacco ribonucleotide reductase small subunit gene is mediated by E2F-like elements. Plant Cell 12, 19871999.CrossRefGoogle ScholarPubMed
Cheah, K.S.E. and Osborne, D.J. (1978) DNA lesions occur with loss of viability in embryos of aging rye seed. Nature 272, 593599.Google Scholar
Citterio, S., Sgorbati, S., Levi, M., Colombo, B.M. and Sparvoli, E. (1992) PCNA and total nuclear protein content as markers of cell proliferation in pea tissue. Journal of Cell Science 102, 7178.Google Scholar
Coello, P. and Vázquez-Ramos, J.M. (1995a) Studies on the processivity of maize DNA polymerase 2, an α-type enzyme. Plant Physiology 109, 645650.CrossRefGoogle ScholarPubMed
Coello, P. and Vázquez-Ramos, J.M. (1995b) Maize DNA polymerase 2 is a phosphoprotein with increasing activity during germination. European Journal of Biochemistry 231, 99103.CrossRefGoogle ScholarPubMed
Coello, P. and Vázquez-Ramos, J.M. (1996) Maize DNA polymerase 2 (an α-type enzyme) suffers major damage after seed deterioration. Seed Science Research 6, 17.Google Scholar
Coello, P., Rodríguez, R., García, E. and Vázquez-Ramos, J.M. (1992) A DNA polymerase from maize axes: its purification and possible role. Plant Molecular Biology 20, 11591168.Google Scholar
Colasanti, J., Tyers, M. and Sundaresan, V. (1991) Isolation and characterization of cDNA clones encoding a functional p34cdc2 homolog from Zea mays. Proceedings of the National Academy of Sciences, USA 88, 33773381.CrossRefGoogle Scholar
Colasanti, J., Cho, S., Wick, S. and Sundaresan, V. (1993) Localization of the functional p34cdc2 homolog of maize in root tip and stomatal complex cells: association with predicted division sites. Plant Cell 5, 11011111.Google Scholar
Collins, J.T.B., Cannon, G.C. and Heinhorst, S. (1998) Nucleotide sequence of a cDNA (Accession No. AF020193) for DNA polymerase Δ from soybean (Glycine max). Plant Physiology. 117, 333.Google Scholar
Conger, B.V. and Carabia, J.V. (1976) Microspectrophotometric determination of the 2C and 4C nuclear complement in the root and shoot of the dormant maize embryo. Environmental and Experimental Botany 16, 171175.Google Scholar
Coolbear, P. and Grierson, D. (1979) Studies on the changes in the major nucleic acid components of tomato seeds (Lycopersicon esculentum Mill.) resulting from osmotic presowing treatment. Journal of Experimental Botany 30, 11531162.Google Scholar
Cruz-García, F., Jiménez, L.F. and Vázquez-Ramos, J.M. (1995) Biochemical and cytological studies in osmoprimed maize seeds. Seed Science Research 5, 1523.CrossRefGoogle Scholar
Cruz-García, F., Zuñiga-Aguilar, J.J. and Vázquez-Ramos, J.M. (1998) Effect of stimulating maize germination on cell cycle proteins. Physiologia Plantarum 102, 573581.CrossRefGoogle Scholar
Dahl, M., Meskiene, I., Bögre, L., Ha, D.T.C., Swoboda, I., Hubmann, R., Hirt, H. and Heberle-Bors, E. (1995) The D-type alfalfa cyclin gene cycMs4 complements G1 cyclin-deficient yeast and is induced in the G1 phase of the cell cycle. Plant Cell 7, 18471857.Google Scholar
de Castro, R.D., Zheng, X., Bergervoet, J.H.W., De Vos, C.H.R. and Bino, R.J. (1995) β-Tubulin accumulation and DNA replication in imbibing tomato seeds. Plant Physiology 109, 499504.CrossRefGoogle ScholarPubMed
de Castro, R.D., Bino, R.J., Jing, H.C., Kieft, H. and Hilhorst, H.W.M. (2001) Depth of dormancy in tomato (Lycopersicon esculentum Mill.) seeds is related to the progression of the cell cycle prior to the induction of dormancy. Seed Science Research 11, 4554.CrossRefGoogle Scholar
Deltour, R. and Jacqmard, A. (1975) Relation between water stress and DNA synthesis during germination of Zea mays L. Annals of Botany 38, 529534.CrossRefGoogle Scholar
De Veylder, L., Engler, J. D., Burssens, S., Manevski, A., Lescure, B., Van Montagu, M., Engler, G. and Inzé, D. (1999) A new D-type cyclin of Arabidopsis thaliana expressed during lateral root primordia formation. Planta 208, 453462.CrossRefGoogle ScholarPubMed
Egelkrout, E.M., Robertson, D. and 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, 14371452.CrossRefGoogle ScholarPubMed
Elder, R.H. and Osborne, D.J. (1993) Function of DNA synthesis and DNA repair in the survival of embryos during early germination and in dormancy. Seed Science Research 3, 4353.CrossRefGoogle Scholar
Elder, R.H., Dell'Aquila, A., Mezzina, M., Sarasin, A. and Osborne, D.J. (1987) DNA ligase in repair and replication in the embryos of rye, Secale cereale. Mutation Research 181, 6171.Google Scholar
Fabian, T., Lorbiecke, R., Umeda, M. and Sauter, M. (2000) The cell cycle genes cycA1;1 and cdc2Os-3 are coordinately regulated by gibberellin in planta. Planta 211, 376383.Google Scholar
Feiler, H.S. and Jacobs, T.W. (1991) Cloning of the pea cdc2 homolog by efficient immunological screening of PCR products. Plant Molecular Biology 17, 321333.CrossRefGoogle Scholar
Ferreira, P.C.G., Hemerly, A.S., Villarroel, R., Van Montagu, M. and Inzé, D. (1991) The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell 3, 531540.Google Scholar
Fobert, P.R., Gaudin, V., Lunness, P., Coen, E.S. and Doonan, J.H. (1996) Distinct classes of cdc2-related genes are differentially expressed during the cell division cycle in plants. Plant Cell 8, 14651476.Google ScholarPubMed
Fuerst, R.A.U.A., Soni, R., Murray, J.A.H. and Lindsey, K. (1996) Modulation of cyclin transcript levels in cultured cells of Arabidopsis thaliana. Plant Physiology 112, 10231033.CrossRefGoogle ScholarPubMed
Fujita, M. (1999) Cell cycle regulation of DNA replication initiation proteins in mammalian cells. Frontiers in Bioscience 4, 816823.CrossRefGoogle ScholarPubMed
Gallardo, K., Job, C., Groot, S.P.C., Puype, M., Demol, H., Vandekerckhove, J. and Job, D. (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiology 126, 835848.Google Scholar
García, E., Orjuela, D., Camacho, Y., Zúñiga, J.J., Plasencia, J. and Vázquez-Ramos, J.M. (1997) Comparison among DNA polymerases 1, 2 and 3 from maize embryo axes. A DNA primase activity copurifies with DNA polymerase 2. Plant Molecular Biology 33, 445455.CrossRefGoogle Scholar
García-Maya, M.M. and Buck, K.W. (1998) Purification and properties of a DNA primase from Nicotiana tabacum. Planta 204, 9399.CrossRefGoogle ScholarPubMed
Genschik, P., Criqui, M.C., Parmentier, Y., Derevier, A. and Fleck, J. (1998) Cell cycle dependent proteolysis in plants. Identification of the destruction box pathway and metaphase arrest produced by the proteasome inhibitor MG132. Plant Cell 10, 20632075.Google ScholarPubMed
Georgieva, E.I., López-Rodas, G. and Loidl, P. (1994a) Maize embryo germination. II. Proteins related to nuclear proto-oncogene- and tumor suppressor gene-products. Planta 192, 125129.CrossRefGoogle Scholar
Georgieva, E.I., López-Rodas, G., Hittmair, A., Feichtinger, H., Brosch, G. and Loidl, P. (1994b) Maize embryo germination. I. Cell cycle analysis. Planta 129, 118124.Google Scholar
Gómez, E. and Vázquez-Ramos, J.M. (2003) Maize DNA polymerase alpha is phosphorylated by a PCNA-associated cyclin/CDK kinase: effect of benzyladenine. Journal of Plant Physiology. (in press).Google Scholar
GórnikK., De K., De, Castro, R.D., Liu, Y., Bino, R.J. and Groot, S.P.C. (1997) Inhibition of cell division during cabbage (Brassica oleracea L.) seed germination. Seed Science Research 7, 333340.Google Scholar
Grafi, G., Burnett, R.J., Helentjaris, T., Larkins, B.A., De Caprio, J.A., Sellers, W.R. and Kaelin, W.G. (1996) A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication. Proceedings of the National Academy of Sciences, USA 93, 89628967.Google Scholar
Gurusinghe, S.H., Cheng, Z. and Bradford, K.J. (1999) Cell cycle activity during seed priming is not essential for germination advancement in tomato. Journal of Experimental Botany 50, 101106.Google Scholar
Gutiérrez, G., Cruz, F., Moreno, J., González-Hernández, V.A. and Vázquez-Ramos, J.M. (1993) Natural and artificial seed ageing in maize: Germination and DNA synthesis. Seed Science Research 3, 279285.CrossRefGoogle Scholar
Hashimoto, J., Hirabayashi, T., Hayano, Y., Hata, S., Ohashi, Y., Suzuka, I., Utsugi, T., Tohe, A. and Kikuchi, Y. (1992) Isolation and characterization of cDNA clones encoding cdc2 homologs from Oryza sativa: a functional homolog and cognate variants. Molecular and General Genetics 233, 1016.CrossRefGoogle Scholar
Hata, S., Kouchi, H., Suzuka, I. and Ishii, T. (1991) Isolation and characterization of cDNA clones for plant cyclins. EMBO Journal 10, 26812688.Google Scholar
Hata, S., Kouchi, H., Tanaka, Y., Minami, E., Matsumoto, T., Suzuka, I. and Hashimoto, J. (1992) Identification of carrot cDNA clones encoding a second putative proliferating cell-nuclear antigen, DNA polymerase delta auxiliary protein. European Journal of Biochemistry 203, 367371.Google Scholar
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. Journal of Biological Chemistry 276, 70417047.CrossRefGoogle ScholarPubMed
Herrera-Teigeiro, I., Jiménez-García, L.F. and Vázquez-Ramos, J.M. (1999) Benzyladenine promotes early activation of p34cdc2-like kinase(s) during maize germination. Seed Science Research 9, 5562.CrossRefGoogle Scholar
Herrera, I., Sanchez, M.D., Molina, J., Plasencia, J. and Vázquez-Ramos, J.M. (2000) Proliferating cell nuclear antigen expression in maize seed development and germination: Regulation by phytohormones and its association with putative cell cycle proteins. Physiologia Plantarum 110, 127134.Google Scholar
Heydecker, W. and Coolbear, P. (1977) Seed treatments for improved performance – survey and attempted prognosis. Seed Science and Technology 5, 353425.Google Scholar
Hirt, H., Pay, A., Bogre, L., Meskiene, I. and Heberle-Bors, E. (1993) cdc2MsB, a cognate cdc2 gene from alfalfa, complements the G1/S but not the G2/M transition of budding yeast cdc28 mutants. Plant Journal 4, 6169.CrossRefGoogle Scholar
Holding, D.R. and Springer, P.S. (2002) The Arabidopsis gene PROLIFERA is required for proper cytokinesis during seed development. Planta 214, 373382.Google Scholar
Houssa, C., Jacqmard, A. and Bernier, G. (1990) Activation of replicon origins as a possible target for cytokinins in shoot meristems of Sinapis. Planta 181, 324326.CrossRefGoogle ScholarPubMed
Houssa, C., Bernier, G., Pieltain, A., Kinet, J.-M. and Jacqmard, A. (1994) Activation of latent DNA-replication origins: a universal effect of cytokinins. Planta 193, 247250.Google Scholar
Hu, Y., Bao, F. and Li, J. (2000) Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis. Plant Journal 24, 693701.Google Scholar
Huntley, R.P. and Murray, J.A.H. (1999) The plant cell cycle. Current Opinion in Plant Biology 2, 440446.CrossRefGoogle ScholarPubMed
Huntley, R., Healy, S., Freeman, D., Lavender, P., de Jager, S., Greenwod, J., Makker, J., Walker, E., Jackman, M., Xie, Q., Bannister, A.J., Kouzarides, T., Gutierrez, C., Doonan, J.H. and Murray, J.A.H. (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 Molecular Biology 37, 155169.Google Scholar
Ito, M., Criqui, M-C., Sakabe, M., Ohno, T., Hata, S., Kouchi, H., Hashimoto, J., Fukuda, H., Komamine, A. and Watanabe, A. (1997) Cell cycle regulated transcription of A- and B-type plant cyclin genes in synchronous cultures. Plant Journal 11, 983992.Google Scholar
John, P.C.L., Sek, F.J. and Lee, M.G. (1989) 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 1, 11851193.Google Scholar
Joubés, J., Chevalier, C., Dudits, D., Heberle-Bors, E., Inzé, D., Umeda, M. and Renaudin, J.P. (2000) CDK-related protein kinases in plants. Plant Molecular Biology 43, 607620.CrossRefGoogle ScholarPubMed
Kelman, Z. (1997) PCNA: structure, functions and interactions. Oncogene 14, 629640.Google Scholar
Kimura, S., Ishibashi, T., Hatanaka, M., Sakakibara, Y., Hashimoto, J. and Sakaguchi, K. (2000) Molecular cloning and characterization of a plant homologue of the origin recognition complex 1 (ORC1). Plant Science 158, 3339.CrossRefGoogle Scholar
Kodama, H., Ito, M., Ohnishi, N., Suzuka, I. and Komamine, A. (1991) Molecular cloning of the gene for plant proliferating-cell nuclear antigen and expression of this gene during the cell cycle in synchronous cultures of Catharanthus roseus cells. European Journal of Biochemistry 197, 495503.Google Scholar
Kornberg, A. and Baker, T. (1992) DNA replication. (2nd edition). New York, W.H. Freeman.Google Scholar
Kosugi, S. and Ohashi, Y. (2002) 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 Journal 29, 4559.CrossRefGoogle ScholarPubMed
Lanteri, S., Kraak, H.L., de Vos, C.H.R. and Bino, R.J. (1993) Effects of osmotic preconditioning on nuclear replication activity in seeds of pepper (Capsicum annuum). Physiologia Plantarum 89, 433440.Google Scholar
Lanteri, S., Saracco, F., Kraak, H.L. and Bino, R.J. (1994) The effects of priming on nuclear replication activity and germination in pepper (Capsicum annuum) and tomato (Lycopersicon esculentum) seeds. Seed Science Research 4, 8187.CrossRefGoogle Scholar
Lanteri, S., Nada, E., Belletti, P., Quagliotti, L. and Bino, R.J. (1996) Effects of controlled deterioration and osmoconditioning on germination and nuclear replication in seeds of pepper (Capsicum annuum L.). Annals of Botany 77, 591597.Google Scholar
Lanteri, S., Portis, E., Bergervoet, H.W. and Groot, S.P.C. (2000) Molecular markers for the priming of pepper seeds (Capsicum annuum L.). Journal of Horticultural Science and Biotechnology 75, 607611.CrossRefGoogle Scholar
Lapidot-Lieson, Y., Patinkin, D., Prody, C.A., Ehrlich, G., Seidman, S., Ben-Aziz, R., Benseler, F., Eckstein, F., Zakut, H. and Soreq, H. (1992) Cloning and antisense oligodeoxynucleotide inhibition of a human homolog of cdc2 required in hematopoiesis. Proceedings of the National Academy of Sciences, USA 89, 579583.Google Scholar
Laquel, P., Castroviejo, M. and Litvak, S. (1990) Further biochemical characterization of wheat DNA primase: possible functional implication of copurification with DNA polymerase A. Nucleic Acids Research 18, 48674876.Google Scholar
Laquel, P., Litvak, S. and Castroviejo, M. (1993) Mammalian proliferating cell nuclear antigen stimulates the processivity of two wheat embryo DNA polymerases. Plant Physiology 102, 107114.Google Scholar
Laquel, P., Litvak, S. and Castroviejo, M. (1994) Wheat DNA primase. RNA primer synthesis in vitro, structural studies by photochemical cross-linking, and modulation of primase activity by DNA polymerases. Plant Physiology 105, 6979.Google Scholar
López, I., Khan, S., Vázquez, J. and Hussey, P.J. (1995) Molecular cloning of a maize cDNA clone encoding a putative proliferating cell nuclear antigen. Biochimica et Biophysica Acta 1260, 119121.Google Scholar
Luque, A.E., Benedetto, J.P. and Castroviejo, M. (1998) Wheat DNA polymerase CI: a homologue of rat DNA polymerase beta. Plant Molecular Biology 38, 647654.CrossRefGoogle Scholar
Magyar, Z., Meszaros, T., Miskolezi, P., Deak, M., Feher, A., Brown, S., Kondorosi, E., Athanasiadis, A., Pongor, S., Bilgin, M., Bako, L., Konez, C. and Dudits, D. (1997) Cell cycle phase specificity of putative cyclin-dependent kinase variants in synchronized alfalfa cells. Plant Cell 9, 223235.Google ScholarPubMed
Magyar, Z., Atanassova, A., de Veylder, L., Rombauts, S. and Inze, D. (2000) Characterization of two distinct DP-related genes from Arabidopsis thaliana. FEBS Letters 486, 7987.CrossRefGoogle ScholarPubMed
Mariconti, L., Pellegrini, B., Cantoni, R., Stevens, R., Bergounioux, C., Cella, R. and Albani, D. (2002) The E2F family of transcription factors from Arabidopsis thaliana. Novel and conserved components of the retinoblastoma/E2F pathway in plants. Journal of Biological Chemistry 277, 99119919.CrossRefGoogle ScholarPubMed
Matsumoto, T., Hata, S., Suzuka, I. and Hashimoto, J. (1994) Expression of functional proliferating cell nuclear antigen from rice (Oryza sativa) in Escherichia coli. Activity in association with human DNA polymerase delta. European Journal of Biochemistry 23, 179187.CrossRefGoogle Scholar
Matsushime, H., Roussel, M.F., Ashmun, R.A. and Sherr, C.J. (1991) Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 65, 701713.Google Scholar
Meijer, M. and Murray, J.A.H. (2000) The role and regulation of D-type cyclins in the plant cell cycle. Plant Molecular Biology 43, 621633.Google Scholar
Meijer, M. and Murray, J.A.H. (2001) Cell cycle controls and development of plant form. Current Opinion in Plant Biology 4, 4449.Google Scholar
Menges, M., Hennig, L., Gruissem, W. and Murray, J.A.H. (2002) Cell cycle-regulated gene expression in Arabidopsis. Journal of Biological Chemistry. 277, 4198742002.Google Scholar
Miao, G., Hong, Z. and Verma, D.P.S. (1993) Two functional soybean genes encoding p34(cdc2) protein kinases are regulated by different plant developmental pathways. Proceedings of the National Academy of Sciences, USA 90, 943947.CrossRefGoogle ScholarPubMed
Mimura, S. and Takisawa, H. (1998) Xenopus Cdc45-dependent loading of DNA polymerase alpha onto chromatin under the control of S-phase Cdk. EMBO Journal 17, 56995707.Google Scholar
Mironov, V., De Veylder, L., Van Montagu, M. and Inzé, D. (1999) Cyclin-dependent kinases and cell division in plants: the nexus. Plant Cell 11, 509521.Google Scholar
Morgan, D.O. (1997) Cyclin-dependent kinases: Engines, clocks and microprocessors. Annual Review of Cell and Developmental Biology 13, 261291.CrossRefGoogle ScholarPubMed
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 Journal 18, 243252.Google Scholar
Nurse, P. (1994) Ordering S phase and M phase in the cell cycle. Cell 79, 547550.CrossRefGoogle Scholar
Onelli, E., Citterio, S., O'Connor, J.E., Levi, M. and Sgorbati, S. (1997) Flow cytometry, sorting and immunocharacterization with proliferating cell nuclear antigen of cycling and non-cycling cells in synchronized pea root tips. Planta 202, 188195.Google Scholar
Osborne, D.J. (1983) Biochemical control systems operating in the early hours of germination. Canadian Journal of Botany 61, 35683577.CrossRefGoogle Scholar
Osborne, D.J., Sharon, R. and Ben-Ishai, R. (1980) Studies on DNA integrity and DNA repair in germinating embryos of rye (Secale cereale). Israel Journal of Botany 29, 259272.Google Scholar
Page, A.M. and Hieter, P. (1999) The anaphase-promoting complex: new subunits and regulators. Annual Review of Biochemistry 68, 583609.Google Scholar
Ramírez-Parra, E., Xie, Q., Boniotti, M.B. and Gutierrez, C. (1999) The cloning of plant E2F, a retinoblastomabinding protein, reveals unique and conserved features with animal G1/S regulators. Nucleic Acids Research 27, 35273533.Google Scholar
Reichheld, J.-P., Chaubet, N., Shen, W.H., Renaudin, J.-P. and Gigot, C. (1996) Multiple A-type cyclins express sequentially during the cell cycle in Nicotiana tabaccum BY2 cells. Proceedings of the National Academy of Sciences, USA 93, 1381913824.CrossRefGoogle Scholar
Renaudin, J.P., Doonan, J.H., Freeman, D., Hashimoto, J., Hirt, H., Inze, D., Jacobs, T., Kouchi, H., Rouze, P., Sauter, M., Savoure, A., Sorrell, D.A., Sundaresan, V. and Murray, J.A.H. (1996) Plant cyclins: A unified nomenclature for plant A-, B- and D-type cyclins based on sequence organisation. Plant Molecular Biology 32, 10031018.Google Scholar
Reyes, J., Jiménez-García, L.F., González, M.A. and Vázquez-Ramos, J.M. (1991) Benzyladenine-stimulation of nuclear DNA synthesis and cell division in germinating maize. Seed Science Research 1, 113117.Google Scholar
Rhind, N. and Russell, P. (2000) Chk1 and Cds1: linchpins of the DNA damage and replication checkpoint pathways. Journal of Cell Science 113, 38893896.Google Scholar
Richard, M.C., Litvak, S. and Castroviejo, M. (1991) DNA polymerase B from wheat embryos: a plant delta-like DNA polymerase. Archives of Biochemistry and Biophysics 287, 141150.CrossRefGoogle ScholarPubMed
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, 15411544.Google Scholar
Rossi, V. and Varotto, S. (2002) Insights into the G1/S transition in plants. Planta 215, 345356.CrossRefGoogle ScholarPubMed
Roudier, F., Fedorova, E., Gyorgyey, J., Feher, A., Brown, S., Kondorosi, A. and Kondorosi, E. (2000) Cell cycle function of a Medicago sativa A2-type cyclin interacting with a PSTAIRE-type cyclin-dependent kinase and a retinoblastoma protein. Plant Journal 23, 7383.CrossRefGoogle Scholar
Sanathkumar, M., Ghosh, B. and Sen Gupta, D.N. (1996) Isolation of mammalian pol beta-type DNA polymerase in shoot tips of germinated seedlings of IR-8 rice (Oryza sativa L.). Biochemistry and Molecular Biology International 39, 117126.Google ScholarPubMed
Sánchez, M.D.P., Torres, A., Boniotti, M.B., Gutierrez, C. and Vázquez-Ramos, J.M. (2002) PCNA protein associates to Cdk-A type protein kinases in germinating maize. Plant Molecular Biology 50, 167175.Google Scholar
Sánchez de Jiménez, E. and Aguilar, R. (1984) Protein synthesis patterns. Relevance of old and new messenger RNA in germinating maize embryos. Plant Physiology 75, 231234.Google Scholar
Sánchez de Jiménez, E., Aguilar, R. and López, S. (1981) Distinctive characteristics of protein synthesis in maize embryos during the early stages of germination. Biochemical and Biophysical Research Communications 99, 445450.Google Scholar
Sánchez-Jiménez, M.P., Cruz-García, F., Covarrubias-Robles, A. and Vázquez-Ramos, J.M. (1997) Osmoacondicionamiento de semillas de frijol: Establecimiento y caracterización. Agrociencia 31, 305311.Google Scholar
Schub, O., Rohaly, G., Smith, R.W.P., Schneider, A., Dehde, S., Dornreiter, I.L. and Nasheuer, H.-P. (2001) Multiple phosphorylation sites of DNA polymerase α-primase cooperate to regulate the initiation of DNA replication in vitro. Journal of Biological Chemistry 276, 3807638083.Google Scholar
Sen, S. and Osborne, D.J. (1974) Germination of rye embryos following hydration–dehydration treatments: enhancement of protein and RNA synthesis and earlier induction of DNA replication. Journal of Experimental Botany 25, 10101019.Google Scholar
Serizawa, H., Makela, T.P., Conaway, J.W., Conaway, R.C., Weinberg, R.A. and Young, R.A. (1995) Association of CDK-activating kinase subunits with transcription factor TFIIH. Nature 374, 280282.Google Scholar
Setiady, Y.Y., Sekine, M., Hariguchi, N., Kouchi, H. and Shinmyo, A. (1996) Molecular cloning and characterization of a cDNA clone that encodes a cdc2 homolog from Nicotiana tabacum. Plant and Cell Physiology 37, 369376.Google Scholar
Seto, H., Hatanaka, M., Kimura, S., Oshige, M., Tsuya, Y., Mizushina, Y., Sawado, T., Aoyagi, N., Matsumoto, T., Hashimoto, J. and Sakaguchi, K. (1998) Purification and characterization of a 100 kDa DNA polymerase from cauliflower inflorescence. Biochemical Journal 332, 557563.CrossRefGoogle ScholarPubMed
Sherr, C.J. (1994) G1 phase progression: cycling on cue. Cell 79, 551555.Google Scholar
Sherr, C.J. and Roberts, J.M. (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes and Development 13, 15011512.Google Scholar
Shimizu, S. and Mori, H. (1998) Analysis of cycles of dormancy and growth in pea axillary buds based on mRNA accumulation patterns of cell cycle-related genes. Plant and Cell Physiology 39, 255262.Google Scholar
Simanis, V. and Nurse, P. (1986) The cell cycle control gene cdc2+ of fission yeast encodes a protein kinase potentially regulated by phosphorylation. Cell 45, 261268.Google Scholar
Sivritepe, H.O. and Dourado, A.M. (1995) The effect of priming treatments on the viability and accumulation of chromosomal damage in aged pea seeds. Annals of Botany 75, 165171.Google Scholar
Smits, V.A.J. and Medema, R.H. (2001) Checking out the G2/M transition. Biochimica et Biophysica Acta 1519, 112.CrossRefGoogle Scholar
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, 85103.Google ScholarPubMed
Sorrell, D.A., Combettes, B., Chaubet-Gigot, N., Gigot, C. and Murray, J.A.H. (1999) Distinct cyclin D genes show mitotic accumulation or constant levels of transcripts in tobacco bright yellow-2 cells. Plant Physiology 119, 343351.Google Scholar
Spiegel, S. and Marcus, A. (1975) Polyribosome formation in early wheat embryo germination independent of either transcription or polyadenylation. Nature 256, 228230.Google Scholar
Springer, P.S., McCombie, W.R., Sundaresan, V. and Martienssen, R.A. (1995) Gene trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in Arabidopsis. Science 268, 877880.Google Scholar
Stevens, R., Mariconti, L., Rossignol, P., Perennes, C., Cella, R. and Bergounioux, C. (2002) Two E2F sites in the Arabidopsis MCM3 promoter have different roles in cell cycle activation and meristematic expression. Journal of Biological Chemistry 277, 3297832984.Google Scholar
Sun, Y., Dilkes, B.P., Zhang, C., Dante, R.A., Carneiro, N.P., Lowe, K.S., Jung, R., Gordon-Kamm, W.J. and Larkins, B.A. (1999) Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. Proceedings of the National Academy of Sciences, USA 96, 41804185.Google Scholar
Suzuka, I., Daidoji, H., Matsuoka, M., Kadowaki, K., Takasaki, Y., Nakane, P.K. and Moriuchi, T. (1989) Gene for proliferating cell nuclear antigen (DNA polymerase δ auxiliary protein) is present in both mammalian and higher plant genomes. Proceedings of the National Academy of Sciences, USA 86, 31893193.Google Scholar
Takisawa, H., Mimura, S. and Kubota, Y. (2000) Eukaryotic DNA replication: from pre-replication complex to initiation complex. Current Opinion in Cell Biology 12, 690696.Google Scholar
Vandepoele, K., Raes, J., De Veylder, L., Rouzé, P., Rombauts, S. and Inze, D. (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14, 903916.Google Scholar
Vázquez, E., Montiel, F. and Vázquez-Ramos, J.M. (1991) DNA ligase activity in deteriorated maize embryo axes during germination: a model relating defects in DNA metabolism in seeds to loss of germinability. Seed Science Research 1, 269273.Google Scholar
Vázquez-Ramos, J.M. and Osborne, D.J. (1986) Analysis of the DNA synthesized during early germination of rye embryos using BND-cellulose chromatography. Mutation Research 166, 3947.CrossRefGoogle Scholar
Vázquez-Ramos, J.M. and Reyes-Jiménez, J. (1990) Stimulation of DNA synthesis and DNA polymerase activity by benzyladenine during early germination of maize axes. Canadian Journal of Botany 68, 25902594.CrossRefGoogle Scholar
Vázquez-Ramos, J.M., López, S., Vázquez, E. and Murillo, E. (1988) DNA integrity and DNA polymerase activity in deteriorated maize embryo axes. Journal of Plant Physiology 133, 600604.Google Scholar
Villiers, T.A. and Edgcumbe, D.J. (1975) On the cause of seed deterioration in dry storage. Seed Science and Technology 3, 761774.Google Scholar
Voitenleitner, C., Rehfuess, C., Hilmes, M., O'Rear, L., Liao, P.-C., Gage, D.A., Ott, R., Nasheuer, H.-P. and Fanning, E. (1999) Cell cycle-dependent regulation of human DNA polymerase α-primase activity by phosphorylation. Molecular and Cellular Biology 19, 646656.CrossRefGoogle ScholarPubMed
Waga, S. and Stillman, B. (1998) The DNA replication fork in eukaryotic cells. Annual Review of Biochemistry 67, 721751.Google Scholar
Waga, S., Hannon, G.J., Beach, D. and Stillman, B. (1994) The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 369, 574578.Google Scholar
Wang, H., Fowke, L.C. and Crosby, W.L. (1997) A plant cyclin-dependent kinase inhibitor gene. Nature 386, 451452.CrossRefGoogle ScholarPubMed
Wang, H., Qi, Q.G., 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 Journal 15, 501510.Google Scholar
Wang, H., Zhou, Y., Gilmer, S., Whitwill, S. and Fowke, L.C. (2000) Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant Journal 24, 613623.CrossRefGoogle ScholarPubMed
Whittle, C.-A., Beardmore, T. and Johnston, M.O. (2001) Is G1 arrest in plant seeds induced by a p53-related pathway?. Trends in Plant Science 6, 248251.CrossRefGoogle ScholarPubMed
Xie, Q., Suarez-Lopez, P. and Gutierrez, C. (1995) Identification and analysis of a retinoblastoma binding motif in the replication protein of a plant DNA virus: requirement for efficient viral DNA replication. EMBO Journal 14, 40734082.Google Scholar
Xie, Q., Sanz-Burgos, P., Hannon, G.J. and Gutiérrez, C. (1996) Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO Journal 15, 49004908.Google Scholar
Xiong, Y., Zhang, H. and Beach, D. (1992) D-Type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA. Cell 71, 505514.Google Scholar
Yanagawa, Y., Kimura, S., Takase, T., Sakaguchi, K., Umeda, M., Komamine, A., Tanaka, K., Hashimoto, J., Sato, T. and Nakagawa, H. (2002) Spatial distribution of the 26S proteasome in meristematic tissues and primordia of rice (Oryza sativa L.). Planta 214, 703707.Google Scholar
Yokoi, M., Ito, M., Izumi, M., Miyazawa, H., Nakai, H. and Hanaoka, F. (1997) Molecular cloning of the cDNA for the catalytic subunit of plant DNA polymerase alpha and its cell-cycle dependent expression. Genes to Cells 2, 695709.Google Scholar
Zaraín, M., Bernal-Lugo, I. and Vázquez-Ramos, J.M. (1987) Effect of benzyladenine on the DNA synthesis during early germination of maize embryo axes. Mutation Research 181, 103110.Google Scholar
Zhang, K., Letham, D.S. and John, P.C.L. (1996) Cytokinin controls the cell cycle at mitosis by stimulating the tyrosine dephosphorylation and activation of p34Cdc2-like histone H1 kinase. Planta 200, 212.Google Scholar
Zhou, Y., Fowke, L.C. and Wang, H. (2002) Plant CDK inhibitors: studies of interactions with cell cycle regulators in the yeast two-hybrid system and functional comparisons in transgenic Arabidopsis plants. Plant Cell Reports 20, 967975.Google Scholar
Zlatanova, J.S., Ivanov, P.S., Stoilov, L.M., Chimshirova, K.V. and Stanchev, B.S. (1987) DNA repair precedes replicative synthesis during early germination in maize. Plant Molecular Biology 10, 139144.Google Scholar
Zúñiga-Aguilar, J.J., López, I., Gómez, A. and Vázquez-Ramos, J.M. (1995) Does benzyladenine stimulate DNA metabolism by modifying gene expression during maize germination?. Seed Science Research 5, 219226.Google Scholar