Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The ins and outs of the plant cell cycle

Key Points

  • In contrast to animals, plants continuously generate new organs throughout their lifespan. This developmental plasticity requires a strict temporal and spatial control of the cell cycle.

  • Cell-cycle activation in quiescent cells is correlated with a change in chromatin structure and requires the activation of the retinoblastoma (RB)–E2F pathway.

  • The gain of a new cell fate is characterized by the occurrence of asymmetric divisions. The phytohormone auxin is a key regulator of asymmetric divisions in the root.

  • Cell-cycle exit is correlated with a decrease in cyclin-dependent kinase (CDK) activity. The molecular mechanisms by which differentiation and CDK activity interconnect are poorly understood.

  • Cells exit their cell cycle in response to environmental cues. Recently, a novel class of CDK inhibitory proteins has been described that putatively links the cell cycle and stress responses.

  • Cells arrest their cell cycle upon DNA damage through the activation of the ataxia-telangiectasia-mutated (ATM) and ATM- and Rad3-related (ATR) kinase pathways. In plants, transcriptional activation of the WEE1 gene (which encodes the CDC25-counteracting WEE1 kinase) represents the prevailing pathway that arrests the cell cycle under conditions that cause single- or double-stranded DNA breaks.

Abstract

Plant growth and development are driven by the continuous generation of new cells. Whereas much has been learned at a molecular level about the mechanisms that orchestrate progression through the different cell-cycle phases, little is known about how the cell-cycle machinery operates in the context of an entire plant and contributes to growth, cell differentiation and the formation of new tissues and organs. Here, we discuss how intrinsic developmental signals and environmental cues affect cell-cycle entry and exit.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The possible role of chromatin remodelling in switching from the quiescent to dividing state.
Figure 2: Auxin-induced asymmetric division during lateral root initiation.
Figure 3: Model for control of cell differentiation by CDK activity.
Figure 4: Inhibition of entry into mitosis by DNA damage in mammals versus plants.

Similar content being viewed by others

References

  1. Inzé, D. & De Veylder, L. The plant cell cycle. Annu. Rev. Plant Biol. 54, 235–264 (2006).

    Google Scholar 

  2. Jürgens, G. Cytokinesis in higher plants. Annu. Rev. Plant Biol. 56, 281–299 (2005).

    Article  CAS  PubMed  Google Scholar 

  3. Jakoby, M. & Schnittger, A. Cell cycle and differentiation. Curr. Opin. Plant Biol. 7, 661–669 (2004).

    Article  CAS  PubMed  Google Scholar 

  4. Gutierrez, C. Coupling cell proliferation and development in plants. Nature Cell Biol. 7, 535–541 (2005).

    Article  CAS  PubMed  Google Scholar 

  5. Traas, J. & Bohn-Courseau, I. Cell proliferation patterns at the shoot apical meristem. Curr. Opin. Plant Biol. 8, 587–592 (2005).

    Article  CAS  PubMed  Google Scholar 

  6. Hall, R. D. et al. A high efficiency technique for the generation of transgenic sugar beets from stomatal guard cells. Nature Biotech. 14, 1133–1138 (1996).

    Article  CAS  Google Scholar 

  7. Zhao, J. et al. Two phases of chromatin decondensation during dedifferentiation of plant cells. Distinction between competence for cell fate switch and a commitment for S phase. J. Biol. Chem. 276, 22772–22778 (2001).

    Article  CAS  PubMed  Google Scholar 

  8. Williams, L. et al. Chromatin reorganization accompanying cellular dedifferentiation is associated with modifications of histone H3, redistribution of HP1, and activation of E2F-target genes. Dev. Dyn. 228, 113–120 (2003).

    Article  CAS  PubMed  Google Scholar 

  9. Williams, L. & Grafi, G. The retinoblastoma protein — a bridge to heterochromatin. Trends Plant Sci. 5, 239–240 (2000).

    Article  CAS  PubMed  Google Scholar 

  10. Wu, J. & Grunstein, M. 25 years after the nucleosome model: chromatin modifications. Trends Biochem. Sci. 25, 619–623 (2000).

    Article  CAS  PubMed  Google Scholar 

  11. Rossi, V. et al. A maize histone deacetylase and retinoblastoma-related protein physically interact and cooperate in repressing gene transcription. Plant Mol. Biol. 51, 401–413 (2003).

    Article  CAS  PubMed  Google Scholar 

  12. Rossi, V. & Varotto, S. Insights into the G1/S transition in plants. Planta 215, 345–356 (2002).

    Article  CAS  PubMed  Google Scholar 

  13. Masubelele, N. H. et al. D-type cyclins activate division in the root apex to promote seed germination in Arabidopsis. Proc. Natl Acad. Sci. USA 102, 15694–15699 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Barrôco, R. M. et al. The role of the cell cycle machinery in resumption of postembryonic development. Plant Physiol. 137, 127–140 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Desvoyes, B., Ramirez-Parra, E., Xie, Q., Chua, N.-H. & Gutierrez, C. Cell type-specific role of the retinoblastoma/E2F pathway during Arabidopsis leaf development. Plant Physiol. 140, 67–80 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wildwater, M. et al. The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123, 1337–1349 (2005). An important study demonstrating that the RBR pathway regulates the size of the stem-cell population in roots.

    Article  CAS  PubMed  Google Scholar 

  17. Wyrzykowska, J., Schorderet, M., Pien, S., Gruissem, W. & Fleming, A. J. Induction of differentiation in the shoot apical meristem by transient overexpression of a retinoblastoma-related protein. Plant Physiol. 141, 1338–1348 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mosquna, A., Katz, A., Shochat, S., Grafi, G. & Ohad, N. Interaction of FIE, a Polycomb protein, with pRB: a possible mechanism regulating endosperm development. Mol. Genet. Genomics 271, 651–657 (2004).

    Article  CAS  PubMed  Google Scholar 

  19. Köhler, C. et al. Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J. 22, 4804–4814 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ebel, C., Mariconti, L. & Gruissem, W. Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429, 776–780 (2004).

    Article  CAS  PubMed  Google Scholar 

  21. Tio, M., Udolph, G., Yang, X. & Chia, W. cdc2 links the Drosophila cell cycle and asymmetric division machineries. Nature 409, 1063–1067 (2001).

    Article  CAS  PubMed  Google Scholar 

  22. Yu, Y., Steinmetz, A., Meyer, D., Brown, S. & Shen, W.-H. The tobacco A-type cyclin, Nicta;CYCA3;2, at the nexus of cell division and differentiation. Plant Cell 15, 2763–2777 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Boudolf, V. et al. B1-type cyclin-dependent kinases are essential for the formation of stomatal complexes in Arabidopsis thaliana. Plant Cell 16, 945–955 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ohashi-Ito, K. & Bergmann, D. C. Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18, 2493–2505 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. MacAlister, C. A., Ohashi-Ito, K. & Bergmann, D. C. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445, 537–540 (2007).

    Article  CAS  PubMed  Google Scholar 

  26. Pillitteri, L. J., Sloan, D. B., Bogenschutz, N. L. & Torii, K. U. Termination of asymmetric cell division and differentiation of stomata. Nature 445, 501–505 (2007).

    Article  CAS  PubMed  Google Scholar 

  27. del Pozo, J. C., Lopez-Matas, M. A., Ramirez-Parra, E. & Gutierrez, C. Hormonal control of the plant cell cycle. Physiol. Plant. 123, 173–183 (2005)

    Article  CAS  Google Scholar 

  28. Blilou, I. et al. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39–44 (2005).

    Article  CAS  PubMed  Google Scholar 

  29. Aida, M. et al. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109–120 (2004). Reports the identification of the first class of auxin-induced transcription factors that are required for stem-cell specification.

    Article  CAS  PubMed  Google Scholar 

  30. Sabatini, S., Heidstra, R., Wildwater, M. & Scheres, B. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis meristem. Genes Dev. 17, 354–358 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Sarkar, A. K. et al. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811–814 (2007).

    Article  CAS  PubMed  Google Scholar 

  32. Himanen, K. et al. Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14, 2339–2351 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. del Pozo, J. C., Diaz-Trivino, S., Cisneros, N. & Gutierrez, C. The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 18, 2224–2235 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Vanneste, S. et al. Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17, 3035–3050 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. del Pozo, J. C., Boniotti, M. B. & Gutierrez, C. Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCFAtSKP2 pathway in response to light. Plant Cell 14, 3057–3071 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. De Veylder, L. et al. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13, 1653–1668 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Beemster, G. T. S. et al. Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol. 138, 734–743 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Dewitte, W. et al. Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15, 79–92 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Imai, K. K. et al. The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18, 382–396 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Boudolf, V. et al. The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa–DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell 16, 2683–2692 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Verkest, A. et al. The cyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 17, 1723–1736 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Weinl, C. et al. Novel functions of plant cyclin-dependent kinase inhibitors, ICK1/KRP1, can act non-cell-autonomously and inhibit entry into mitosis. Plant Cell 17, 1704–1722 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Umeda, M., Umeda-Hara, C. & Uchimiya, H. A cyclin-dependent kinase-activating kinase regulates differentiation of root initial cells in Arabidopsis. Proc. Natl Acad. Sci. USA 97, 13396–13400 (2000). A comprehensive study illustrating that the level of CDK activity controls the differentiation status of root initial cells.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sieberer, T., Hauser, M.-T., Seifert, G. J. & Luschnig, C. PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr. Biol. 13, 837–842 (2003).

    Article  CAS  PubMed  Google Scholar 

  45. Frank, M. et al. TUMOROUS SHOOT DEVELOPMENT (TSD) genes are required for co-ordinated plant shoot development. Plant J. 29, 73–85 (2002).

    Article  CAS  PubMed  Google Scholar 

  46. Faure, J.-D. et al. The PASTICCINO genes of Arabidopsis thaliana are involved in the control of cell division and differentiation. Development 125, 909–918 (1998).

    CAS  PubMed  Google Scholar 

  47. Da Costa, M. et al. Arabidopsis PASTICCINO2 is an antiphosphatase involved in regulation of cyclin-dependent kinase A. Plant Cell 18, 1426–1437 (2006). Identifies the PAS2 antiphosphatase as a novel CDK regulatory protein. PAS2 interacts specifically with tyrosine-phosphorylated CDKA;1, thereby shielding this particular CDK from putative activating phosphatases. The interaction between PAS2 and CDKA;1 probably marks the onset of cell differentiation.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Mariconti, L. et al. The E2F family of transcription factors from Arabidopsis thaliana. Novel and conserved components of the retinoblastoma/E2F pathway in plants. J. Biol. Chem. 277, 9911–9919 (2002).

    Article  CAS  PubMed  Google Scholar 

  49. Vandepoele, K. et al. Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14, 903–916 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Vlieghe, K. et al. The DP-E2F-like DEL1 gene controls the endocycle in Arabidopsis thaliana. Curr. Biol. 15, 59–63 (2005).

    Article  CAS  PubMed  Google Scholar 

  51. Ramirez-Parra, E., López-Matas, M. A., Fründt, C. & Gutierrez, C. Role of an atypical E2F transcription factor in the control of Arabidopsis cell growth and differentiation. Plant Cell 16, 2350–2363 (2004). Presents evidence for a role of the atypical E2F transcription factor E2Ff/DEL3 in post-mitotic cell elongation. Inhibition of cell expansion is probably controlled by the selective repression of cell-wall biosynthesis genes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Krizek, B. A. Ectopic expression of AINTEGUMENTA in Arabidopsis plants results in increased growth of floral organs. Dev. Genet. 25, 224–236 (1999).

    Article  CAS  PubMed  Google Scholar 

  53. Mizukami, Y. & Fischer, R. L. Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc. Natl Acad. Sci. USA 97, 942–947 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Hu, Y., Xie, Q. & Chua, N.-H. The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 15, 1951–1961 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Dinneny, J. R., Yadegari, R., Fischer, R. L., Yanofsky, M. F. & Weigel, D. The role of JAGGED in shaping lateral organs. Development 131, 1101–1110 (2003).

    Article  CAS  Google Scholar 

  56. Ohno, C. K., Reddy, G. V., Heisler, M. G. B. & Meyerowitz, E. M. The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development 131, 1111–1122 (2003).

    Article  CAS  Google Scholar 

  57. Kim, J. H., Choi, D. & Kende, H. The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J. 36, 94–104 (2003).

    Article  CAS  PubMed  Google Scholar 

  58. Horiguchi, G., Kim, G.-T. & Tsukaya, H. The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J. 43, 68–78 (2005).

    Article  CAS  PubMed  Google Scholar 

  59. Disch, S. et al. The E3 ubiquitin ligase BIG BROTHER controls Arabidopsis organ size in a dosage-dependent manner. Curr. Biol. 16, 272–279 (2006).

    Article  CAS  PubMed  Google Scholar 

  60. Burssens, S. et al. Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211, 632–640 (2000).

    Article  CAS  PubMed  Google Scholar 

  61. West, G., Inzé, D. & Beemster, G. T. S. Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol. 135, 1050–1058 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Schuppler, U., He, P.-H., John, P. C. L. & Munns, R. Effect of water stress on cell division and cell-division-cycle 2-like cell-cycle kinase activity in wheat leaves. Plant Physiol. 117, 667–678 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Granier, C., Inzé, D. & Tardieu, F. Spatial distribution of cell division rate can be deduced from that of p34cdc2 kinase activity in maize leaves grown at contrasting temperatures and soil water conditions. Plant Physiol. 124, 1393–1402 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Logemann, E. et al. Gene activation by UV light, fungal elicitor or fungal infection in Petroselinum crispum is correlated with repression of cell cycle-related genes. Plant J. 8, 865–876 (1995).

    Article  CAS  PubMed  Google Scholar 

  65. Kadota, Y. et al. Crosstalk between elicitor-induced cell death and cell cycle regulation in tobacco BY-2 cells. Plant J. 40, 131–142 (2004).

    Article  CAS  PubMed  Google Scholar 

  66. Jang, S. J. et al. Effects of abiotic stresses on cell cycle progression in tobacco BY-2 cells. Mol. Cells 20, 136–141 (2005).

    CAS  PubMed  Google Scholar 

  67. Reichheld, J.-P., Vernoux, T., Lardon, F., Van Montagu, M. & Inzé, D. Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant J. 17, 647–656 (1999).

    Article  CAS  Google Scholar 

  68. Kadota, Y. et al. Cell cycle dependence of elicitor-induced signal transduction in tobacco BY-2 cells. Plant Cell Physiol. 46, 156–165 (2005).

    Article  CAS  PubMed  Google Scholar 

  69. Swiatek, A., Azmi, A., Stals, H., Inzé, D. & Van Onckelen, H. Jasmonic acid prevents the accumulation of cyclin B1;1 and CDK-B in synchronized tobacco BY-2 cells. FEBS Lett. 572, 118–122 (2004).

    Article  CAS  PubMed  Google Scholar 

  70. Swiatek, A., Lenjou, M., Van Bockstaele, D., Inzé, D. & Van Onckelen, H. Differential effect of jasmonic acid and abscisic acid on cell cycle progression in tobacco BY-2 cells. Plant Physiol. 128, 201–211 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Wang, H. et al. 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 (1998).

    Article  PubMed  Google Scholar 

  72. Pettkó-Szandtner, A. et al. Activation of an alfalfa cyclin-dependent kinase inhibitor by calmodulin-like domain protein kinase. Plant J. 46, 111–123 (2006).

    Article  CAS  PubMed  Google Scholar 

  73. Minami, E. et al. Two novel genes rapidly and transiently activated in suspension-cultured rice cells by treatment with N-acetylchitoheptaose, a biotic elicitor for phytoalexin production. Plant Cell Physiol. 37, 563–567 (1996).

    Article  CAS  PubMed  Google Scholar 

  74. Churchman, M. L. et al. SIAMESE, a novel plant-specific cell cycle regulator controls endoreplication onset in Arabidopsis thaliana. Plant Cell 18, 3145–3157 (2006). Describes a novel group of CDK inhibitory proteins. One member, designated SIAMESE, has a prominent role at the mitosis-to-endocycle transition in trichome cells.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Walker, J. D., Oppenheimer, D. G., Concienne, J. & Larkin, J. C. SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development 127, 3931–3940 (2000).

    CAS  PubMed  Google Scholar 

  76. Amino, S.-I. & Nagata, T. Caffeine-induced uncoupling of mitosis from DNA replication in tobacco BY-2 cells. J. Plant Res. 109, 219–222 (1996).

    Article  CAS  Google Scholar 

  77. Garcia, V. et al. AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15, 119–132 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Culligan, K., Tissier, A. & Britt, A. ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 16, 1091–1104 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Boudolf, V., Inzé, D. & De Veylder, L. What if higher plants lack a CDC25 phosphatase? Trends Plant Sci. 11, 474–479 (2006).

    Article  CAS  PubMed  Google Scholar 

  80. Corellou, F. et al. A S/M DNA replication checkpoint prevents nuclear and cytoplasmic events of cell division including centrosomal axis alignment and inhibits activation of cyclin-dependent kinase-like proteins in fucoid zygotes. Development 127, 1651–1660 (2000).

    CAS  PubMed  Google Scholar 

  81. De Schutter, K. et al. The WEE1 kinase of Arabidopsis thaliana controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell 19, 211–225 (2007). Shows that the A. thaliana WEE1 gene is not rate limiting for cell-cycle progression under normal growth conditions, but instead is a critical target of the ATR/ATM signalling cascades that inhibit the cell cycle following activation of the DNA integrity checkpoints.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Chen, I-P., Haehnel, U., Altschmied, L., Schubert, I. & Puchta, H. The transcriptional response of Arabidopsis to genotoxic stress — a high-density colony array study (HDCA). Plant J. 35, 771–786 (2003).

    Article  CAS  PubMed  Google Scholar 

  83. Culligan, K. M., Robertson, C. E., Foreman, P., Doerner, P. & Britt, A. B. ATR and ATM play both distinct and additive roles in response to ionizing radiation. Plant J. 48, 947–961 (2006).

    Article  CAS  PubMed  Google Scholar 

  84. Hefner, E., Huefner, N. & Britt, A. B. Tissue-specific regulation of cell-cycle responses to DNA damage in Arabidopsis seedlings. DNA Repair 5, 102–110 (2006).

    Article  CAS  PubMed  Google Scholar 

  85. Ramirez-Parra, E. & Gutierrez, C. E2F regulates FASCIATA1, a chromatin assembly gene whose loss switches on the endocycle and activates gene expression by changing the epigenetic status. Plant Physiol. 144, 105–120 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Riha, K., McKnight, T. D., Griffing, L. R. & Shippen, D. E. Living with genome instability: plant responses to telomere dysfunction. Science 291, 1797–1800 (2001).

    Article  CAS  PubMed  Google Scholar 

  87. Wang, G. et al. Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol. 135, 1084–1099 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Verkest, A., Weinl, C., Inzé, D., De Veylder, L. & Schnittger, A. Switching the cell cycle. Kip-related proteins in plant cell cycle control. Plant Physiol. 139, 1099–1106 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Capron, A., Ökrész, L. & Genschik, P. First glance at the plant APC/C, a highly conserved ubiquitin-protein ligase. Trends Plant Sci. 8, 83–89 (2003).

    Article  CAS  PubMed  Google Scholar 

  90. Shimotohno, A., Umeda-Hara, C., Bisova, K., Uchimiya, H. & Umeda, M. The plant specific kinase CDKF;1 is involved in activating phosphorylation in cyclin-dependent kinase-activating kinases in Arabidopsis. Plant Cell 16, 2954–2966 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Breyne, P. et al. Transcriptome analysis during cell division in plants. Proc. Natl Acad. Sci. USA 99, 14825–14830 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Menges, M., Hennig, L., Gruissem, W. & Murray, J. A. H. Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol. Biol. 53, 423–442 (2003).

    Article  CAS  PubMed  Google Scholar 

  93. Boniotti, M. B. & Gutierrez, C. A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex. Plant J. 28, 341–350 (2001).

    Article  CAS  PubMed  Google Scholar 

  94. Nakagami, H., Kawamura, K., Sugisaka, K., Sekine, M. & Shinmyo, A. 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 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. De Veylder, L. et al. Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa/DPa transcription factor. EMBO J. 21, 1360–1368 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Kosugi, S. & Ohashi, Y. Constitutive E2F expression in tobacco plants exhibits altered cell cycle control and morphological change in a cell type-specific manner. Plant Physiol. 132, 2012–2022 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Sozzani, R. et al. Interplay between Arabidopsis activating factors E2Fb and E2Fa in cell cycle progression and development. Plant Physiol. 140, 1355–1366 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Vandepoele, K. et al. Genome-wide identification of potential plant E2F target genes. Plant Physiol. 139, 316–328 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Ramirez-Parra, E., Fründt, C. & Gutierrez, C. A genome-wide identification of E2F-regulated genes in Arabidopsis. Plant J. 33, 801–811 (2003).

    Article  CAS  PubMed  Google Scholar 

  100. Ito, M. et al. A novel cis-acting element in promoters of plant B-type cyclin genes activates M phase-specific transcription. Plant Cell 10, 331–341 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Ito, M. et al. G2/M-phase-specific transcription during the plant cell cycle is mediated by c-Myb-like transcription factors. Plant Cell 13, 1891–1905 (2001). References 100 and 101 describe the characterization of a novel cis -acting element (MSA box) that controls G2–M-phase-specific expression of plant cell-cycle genes, and the identification of c-MYB-like proteins as MSA-binding transcription factors, respectively.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Araki, S., Ito, M., Soyano, T., Nishihama, R. & Machida, Y. 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 (2005).

    Article  Google Scholar 

  103. Nagl, W. DNA endoreduplication and polyteny understood as evolutionary strategies. Science 261, 614–615 (1976).

    CAS  Google Scholar 

  104. Barow, M. & Meister, A. Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant Cell Environ. 26, 571–584 (2003).

    Article  Google Scholar 

  105. Sugimoto-Shirasu, K. & Roberts, K. 'Big it up': endoreduplication and cell-size control in plants. Curr. Opin. Plant Biol. 6, 544–553 (2003).

    Article  CAS  PubMed  Google Scholar 

  106. Vlieghe, K., Inzé, D. & De Veylder, L. in Cell Cycle Control and Plant Development (Annual Plant Reviews Vol. 32) Ch. 10 (ed. D. Inzé) 227–248 (Blackwell Publishing, Oxford, 2007).

    Book  Google Scholar 

  107. Park, J.-A. et al. Retinoblastoma protein regulates cell proliferation, differentiation, and endoreduplication in plants. Plant J. 42, 153–163 (2005).

    Article  CAS  PubMed  Google Scholar 

  108. Castellano, M. M., del Pozo, J. C., Ramirez-Parra, E., Brown, S. & Gutierrez, C. Expression and stability of Arabidopsis CDC6 are associated with endoreplication. Plant Cell 13, 2671–2686 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Castellano, M. M., Boniotti, M. B., Caro, E., Schnittger, A. & Gutierrez, C. DNA replication licensing affects cell proliferation or endoreplication in a cell type-specific manner. Plant Cell 16, 2380–2393 (2004).

    CAS  Google Scholar 

  110. Bisbis, B. et al. Cyclin-dependent kinase (CDK) inhibitors regulate the CDK-cyclin complex activities in endoreduplicating cells of developing tomato fruit. J. Biol. Chem. 281, 7374–7383 (2006).

    Article  CAS  PubMed  Google Scholar 

  111. Cebolla, A. et al. The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J. 18, 4476–4484 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Tarayre, S., Vinardell, J. M., Cebolla, A., Kondorosi, A. & Kondorosi, E. Two classes of the Cdh1-type activators of the anaphase-promoting complex in plants: novel functional domains and distinct regulation. Plant Cell 16 422–434 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Yoshizumi, T. et al. INCREASED LEVEL OF POLYPLOIDY1, a conserved repressor of CYCLINA2 transcription, controls endoreduplication in Arabidopsis. Plant Cell 18, 2452–2468 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Peres, A. et al. Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses. J. Biol. Chem. 28 June 2007 (doi:10.1074/jbc.M703326200)

Download references

Acknowledgements

The authors thank M. De Cock and K. Spruyt for help with preparing the manuscript and the artwork, respectively. This work was supported by a grant from the University Poles of Attraction Programme–Belgian Science Policy and the European Union Marie Curie Research Training Networks. L.D.V. is a postdoctoral researcher of the Research Foundation–Flanders.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dirk Inzé.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Dirk Inzé's homepage

DATABASES

TAIR

CYCA3;2

CYCA2;4

ICK1

ICK2

CYCB1;1

CYCD3;1

CYCD3;2

Glossary

Stomatal guard cell

One of a pair of kidney-shaped cells that control the opening and closing of stomata.

Histone acetyltransferase

An enzyme that acetylates core histones, resulting in important regulatory effects on chromatin structure and assembly and on gene transcription.

Stomata

A specialized epidermal structure that is found on stems and leaves and permits gas exchange with the inner plant tissues.

Auxin

One of several hormones found in plants that control the growth and division of cells.

AP2 domain

A plant-specific protein domain that was originally identified in the floral homeotic protein APETALA2 and is involved in DNA binding.

Pericycle

A layer of cells located between the endodermis and the central stele from which lateral roots originate.

Protoxylem

Meristematic cells that give rise to xylem — the tissue that is specialized for the transport of water and minerals upwards through the plant.

Endoreduplication

Replication of DNA during the S phase of the cell cycle without the subsequent completion of mitosis and/or cytokinesis.

Pavement cell

A plant epidermal cell that is not part of a stomatal complex or trichome.

Phytohormone

A plant hormone.

Antiphosphatase

A non-functional protein phosphatase that is still able to bind its substrates without causing their dephosphorylation.

Expansin

A putative cell-wall-loosening enzyme that enables cell expansion.

Dicotyledonous plant

A flowering plant, the seed of which typically contains two embryonic leaves or cotyledons.

Water stress

A situation when the demand for water exceeds the available amount.

Medicago truncatula

(Barrel medic). A small forage legume that was chosen as the model organism for legume biology.

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Veylder, L., Beeckman, T. & Inzé, D. The ins and outs of the plant cell cycle. Nat Rev Mol Cell Biol 8, 655–665 (2007). https://doi.org/10.1038/nrm2227

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrm2227

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing