Skip to main content

Cell Cycle Modules in Plants for Entry into Proliferation and for Mitosis

  • Chapter
  • First Online:

Abstract

Cell cycle is an orderly progression through a series of events culminating in the duplication of chromosomes during S-phase and in the segregation of chromosomes into daughter cells during mitosis. The S-and M-phases are the so called active phases which are preceded by preparatory phases, called gap phases, when regulatory inputs are pereceived; G1 and G2, respectively (Fig. 6.1). Chromosomes during G1-, S and G2-phases (interphase) are decondensed within the nuclei but intephase chromosomes are still known to occupy distinct territories within the nuclei and this organisation is important for replication, transcription, repair and recombination processes (Schubert and Shaw 2011). Mitosis is a cell cycle period packed with morphological events subdivided into pro-, meta-, ana- and telophases followed by cytokinesis. Within this chapter we will focus on the central regulators of the cell cycle phase transitions, but before we get onto the regulators in large details we first summarise what are being regulated during these cell cycle phases with an aim to pinpoint conserved and plant specific mechanisms.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Andersen SU, Buechel S, Zhao Z, Ljung K, Novak O, Busch W, Schuster C, Lohmann JU (2008) Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana. Plant Cell 20:88–100

    Article  PubMed  CAS  Google Scholar 

  • Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F, De Milde L, Muhlenbock P, Skirycz A, Gonzalez N, Beemster GT, Inze D (2012) Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Dev Cell 22:64–78

    Article  PubMed  CAS  Google Scholar 

  • Araki S, Ito M, Soyano T, Nishihama R, 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

    Article  PubMed  CAS  Google Scholar 

  • Aslanian A, Iaquinta PJ, Verona R, Lees JA (2004) Repression of the Arf tumor suppressor by E2F3 is required for normal cell cycle kinetics. Genes Dev 18:1413–1422

    Article  PubMed  CAS  Google Scholar 

  • Aw SJ, Hamamura Y, Chen Z, Schnittger A, Berger F (2010) Sperm entry is sufficient to trigger division of the central cell but the paternal genome is required for endosperm development in Arabidopsis. Development 137:2683–2690

    Article  PubMed  CAS  Google Scholar 

  • Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, dePamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA, Ashton NW, Axtell MJ, Barker E, Barker MS, Bennetzen JL, Bonawitz ND, Chapple C, Cheng C, Correa LG, Dacre M, DeBarry J, Dreyer I, Elias M, Engstrom EM, Estelle M, Feng L, Finet C, Floyd SK, Frommer WB, Fujita T, Gramzow L, Gutensohn M, Harholt J, Hattori M, Heyl A, Hirai T, Hiwatashi Y, Ishikawa M, Iwata M, Karol KG, Koehler B, Kolukisaoglu U, Kubo M, Kurata T, Lalonde S, Li K, Li Y, Litt A, Lyons E, Manning G, Maruyama T, Michael TP, Mikami K, Miyazaki S, Morinaga S, Murata T, Mueller-Roeber B, Nelson DR, Obara M, Oguri Y, Olmstead RG, Onodera N, Petersen BL, Pils B, Prigge M, Rensing SA, Riano-Pachon DM, Roberts AW, Sato Y, Scheller HV, Schulz B, Schulz C, Shakirov EV, Shibagaki N, Shinohara N, Shippen DE, Sorensen I, Sotooka R, Sugimoto N, Sugita M, Sumikawa N, Tanurdzic M, Theissen G, Ulvskov P, Wakazuki S, Weng JK, Willats WW, Wipf D, Wolf PG, Yang L, Zimmer AD, Zhu Q, Mitros T, Hellsten U, Loque D, Otillar R, Salamov A, Schmutz J, Shapiro H, Lindquist E, Lucas S, Rokhsar D, Grigoriev IV (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960–963

    Article  PubMed  CAS  Google Scholar 

  • Bartolini F, Gundersen GG (2006) Generation of noncentrosomal microtubule arrays. J Cell Sci 119:4155–4163

    Article  PubMed  CAS  Google Scholar 

  • Berckmans B, Lammens T, Van Den Daele H, Magyar Z, Bogre L, De Veylder L (2011a) Light-dependent regulation of DEL1 is determined by the antagonistic action of E2Fb and E2Fc. Plant Physiol 157:1440–1451

    Article  PubMed  CAS  Google Scholar 

  • Berckmans B, Vassileva V, Schmid SP, Maes S, Parizot B, Naramoto S, Magyar Z, Kamei CL, Koncz C, Bogre L, Persiau G, De Jaeger G, Friml J, Simon R, Beeckman T, De Veylder L (2011b) Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell 23:3671–3683

    Article  PubMed  CAS  Google Scholar 

  • Binarová P, Doležel J, Dráber P, Heberle-Bors E, Strnad M, Bogre L (1998) Treatment of Vicia faba root tip cells with specific inhibitors to cyclin-dependent kinases leads to abnormal spindle formation. Plant J 16:697–707

    Article  PubMed  Google Scholar 

  • Binárova P, Cenklová V, Hause B, Kubatová E, Lysák M, Doležel J, Bogre L, Dráber P (2000) Nuclear gamma-tubulin during acentriolar plant mitosis. Plant Cell 12:433–442

    PubMed  Google Scholar 

  • Binarová P, Cenklová V, Procházková J, Doskočilová A, Volc J, Vrlik M, Bogre L (2006) Gamma-tubulin is essential for acentrosomal microtubule nucleation and coordination of late mitotic events in Arabidopsis. Plant Cell 18:1199–1212

    Article  PubMed  CAS  Google Scholar 

  • Bisova K, Krylov DM, Umen JG (2005) Genome-wide annotation and expression profiling of cell cycle regulatory genes in Chlamydomonas reinhardtii. Plant Physiol 137:475–491

    Article  PubMed  CAS  Google Scholar 

  • Bogre L (2011) Sensing microtubule states through the mitogen-activated protein kinase pathway during mitosis and morphogenesis. New Phytol 189:897–900

    Article  PubMed  CAS  Google Scholar 

  • Bogre L, Magyar Z, Lopez-Juez E (2008) New clues to organ size control in plants. Genome Biol 9:226

    Article  PubMed  CAS  Google Scholar 

  • Borghi L, Gutzat R, Futterer J, Laizet Y, Hennig L, Gruissem W (2010) Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22:1792–1811

    Article  PubMed  CAS  Google Scholar 

  • Boruc J, Van den Daele H, Hollunder J, Rombauts S, Mylle E, Hilson P, Inze D, De Veylder L, Russinova E (2010) Functional modules in the Arabidopsis core cell cycle binary protein-protein interaction network. Plant Cell 22:1264–1280

    Article  PubMed  CAS  Google Scholar 

  • Bosco G (2010) Cell cycle: retinoblastoma, a trip organizer. Nature 466:1051–1052

    Article  PubMed  CAS  Google Scholar 

  • Bosco G, Du W, Orr-Weaver TL (2001) DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat Cell Biol 3:289–295

    Article  PubMed  CAS  Google Scholar 

  • Boudolf V, Vlieghe K, Beemster GT, Magyar Z, Torres Acosta JA, Maes S, Van Der Schueren E, Inze D, De Veylder L (2004a) 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

    Article  PubMed  CAS  Google Scholar 

  • Boudolf V, Barroco R, Engler Jde A, Verkest A, Beeckman T, Naudts M, Inze D, De Veylder L (2004b) B1-type cyclin-dependent kinases are essential for the formation of stomatal complexes in Arabidopsis thaliana. Plant Cell 16:945–955

    Article  PubMed  CAS  Google Scholar 

  • Boudolf V, Lammens T, Boruc J, Van Leene J, Van Den Daele H, Maes S, Van Isterdael G, Russinova E, Kondorosi E, Witters E, De Jaeger G, Inze D, De Veylder L (2009) CDKB1;1 forms a functional complex with CYCA2;3 to suppress endocycle onset. Plant Physiol 150:1482–1493

    Article  PubMed  CAS  Google Scholar 

  • Buendia-Monreal M, Renteria-Canett I, Guerrero-Andrade O, Bravo-Alberto CE, Martinez-Castilla LP, Garcia E, Vazquez-Ramos JM (2011) The family of maize D-type cyclins: genomic organization, phylogeny and expression patterns. Physiol Plant 143:297–308

    Article  PubMed  CAS  Google Scholar 

  • Caillaud MC, Paganelli L, Lecomte P, Deslandes L, Quentin M, Pecrix Y, Le Bris M, Marfaing N, Abad P, Favery B (2009) Spindle assembly checkpoint protein dynamics reveal conserved and unsuspected roles in plant cell division. PLoS One 4:e6757

    Article  PubMed  CAS  Google Scholar 

  • Carmena M, Earnshaw WC (2003) The cellular geography of aurora kinases. Nat Rev Mol Cell Biol 4:842–854

    Article  PubMed  CAS  Google Scholar 

  • Cayirlioglu P, Bonnette PC, Dickson MR, Duronio RJ (2001) Drosophila E2f2 promotes the conversion from genomic DNA replication to gene amplification in ovarian follicle cells. Development 128:5085–5098

    PubMed  CAS  Google Scholar 

  • Cayirlioglu P, Ward WO, Silver Key SC, Duronio RJ (2003) Transcriptional repressor functions of Drosophila E2F1 and E2F2 cooperate to inhibit genomic DNA synthesis in ovarian follicle cells. Mol Cell Biol 23:2123–2134

    Article  PubMed  CAS  Google Scholar 

  • Chen HZ, Tsai SY, Leone G (2009) Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat Rev Cancer 9:785–797

    Article  PubMed  CAS  Google Scholar 

  • Chong JL, Wenzel PL, Saenz-Robles MT, Nair V, Ferrey A, Hagan JP, Gomez YM, Sharma N, Chen HZ, Ouseph M, Wang SH, Trikha P, Culp B, Mezache L, Winton DJ, Sansom OJ, Chen D, Bremner R, Cantalupo PG, Robinson ML, Pipas JM, Leone G (2009) E2f1-3 switch from activators in progenitor cells to repressors in differentiating cells. Nature 462:930–934

    Article  PubMed  CAS  Google Scholar 

  • Cools T, De Veylder L (2009) DNA stress checkpoint control and plant development. Curr Opin Plant Biol 12:23–28

    Article  PubMed  CAS  Google Scholar 

  • Costas C, MdlP S, Sequeira-Mendes J, Gutierrez C (2011a) Progress in understanding DNA replication control. Plant Sci 181:203–209

    Article  PubMed  CAS  Google Scholar 

  • Costas C, Desvoyes B, Gutierrez C (2011b) A chromatin perspective of plant cell cycle progression. Biochim Biophys Acta 1809:379–387

    Article  PubMed  CAS  Google Scholar 

  • Costas C, Sanchez M De La Paz, Stroud H, Yu Y, Oliveros JC, Feng S, Benguria A, Lopez-Vidriero I, Zhang X, Solano R, Jacobsen SE, Gutierrez C (2011c) Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nat Struct Mol Biol 18:395–400

    Article  PubMed  CAS  Google Scholar 

  • Coudreuse D, Nurse P (2010) Driving the cell cycle with a minimal CDK control network. Nature 468:1074–1079

    Article  PubMed  CAS  Google Scholar 

  • Cross FR, Buchler NE, Skotheim JM (2011) Evolution of networks and sequences in eukaryotic cell cycle control. Philos Trans Roy Soc Lond B Bio 366:3532–3544

    Article  PubMed  CAS  Google Scholar 

  • Danielian PS, Friesenhahn LB, Faust AM, West JC, Caron AM, Bronson RT, Lees JA (2008) E2f3a and E2f3b make overlapping but different contributions to total E2f3 activity. Oncogene 27:6561–6570

    Article  PubMed  CAS  Google Scholar 

  • De Veylder L, Beeckman T, Beemster GT, de Almeida EJ, Ormenese S, Maes S, Naudts M, Van Der Schueren E, Jacqmard A, Engler G, Inze D (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J 21:1360–1368

    Article  PubMed  Google Scholar 

  • De Veylder L, Beeckman T, Inze D (2007) The ins and outs of the plant cell cycle. Nat Rev Mol Cell Biol 8:655–665

    Article  PubMed  CAS  Google Scholar 

  • del Pozo JC, Boniotti MB, Gutierrez C (2002) Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light. Plant Cell 14:3057–3071

    Article  PubMed  CAS  Google Scholar 

  • del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C (2006) 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

    Article  PubMed  CAS  Google Scholar 

  • Demidov D, Van Damme D, Geelen D, Blattner FR, Houben A (2005) Identification and dynamics of two classes of aurora-like kinases in Arabidopsis and other plants. Plant Cell 17:836–848

    Article  PubMed  CAS  Google Scholar 

  • Demidov D, Hesse S, Tewes A, Rutten T, Fuchs J, Ashtiyani RK, Lein S, Fischer A, Reuter G, Houben A (2009) Aurora1 phosphorylation activity on histone H3 and its cross-talk with other post-translational histone modifications in Arabidopsis. Plant J 59:221–230

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dimova DK, Stevaux O, Frolov MV, Dyson NJ (2003) Cell cycle-dependent and cell cycle-independent control of transcription by the Drosophila E2F/RB pathway. Genes Dev 17:2308–2320

    Article  PubMed  CAS  Google Scholar 

  • Dissmeyer N, Weimer AK, Pusch S, De Schutter K, Alvim Kamei CL, Nowack MK, Novak B, Duan GL, Zhu YG, De Veylder L, Schnittger A (2009) Control of cell proliferation, organ growth, and DNA damage response operate independently of dephosphorylation of the Arabidopsis Cdk1 homolog CDKA;1. Plant Cell 21:3641–3654

    Article  PubMed  CAS  Google Scholar 

  • Dissmeyer N, Weimer AK, De Veylder L, Novak B, Schnittger A (2010) The regulatory network of cell-cycle progression is fundamentally different in plants versus yeast or metazoans. Plant Signal Behav 5:1613–1618

    Article  PubMed  Google Scholar 

  • Doonan JH, Sablowski R (2010) Walls around tumours—why plants do not develop cancer. Nat Rev Cancer 10:794–802

    Article  PubMed  CAS  Google Scholar 

  • Dryková D, Cenklová V, Sulimenko V, Volc J, Dráber P, Binarová P (2003) Plant gamma-tubulin interacts with alphabeta-tubulin dimers and forms membrane-associated complexes. Plant Cell 15:465–480

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Edgar BA, Orr-Weaver TL (2001) Endoreplication cell cycles: more for less. Cell 105:297–306

    Article  PubMed  CAS  Google Scholar 

  • Fleury D, Himanen K, Cnops G, Nelissen H, Boccardi TM, Maere S, Beemster GT, Neyt P, Anami S, Robles P, Micol JL, Inze D, Van Lijsebettens M (2007) The Arabidopsis thaliana homolog of yeast BRE1 has a function in cell cycle regulation during early leaf and root growth. Plant Cell 19:417–432

    Article  PubMed  CAS  Google Scholar 

  • Fulop K, Tarayre S, Kelemen Z, Horvath G, Kevei Z, Nikovics K, Bako L, Brown S, Kondorosi A, Kondorosi E (2005) Arabidopsis anaphase-promoting complexes: multiple activators and wide range of substrates might keep APC perpetually busy. Cell Cycle 4:1084–1092

    Article  PubMed  CAS  Google Scholar 

  • Gaamouche T, Manes CLD, Kwiatkowska D, Berckmans B, Koumproglou R, Maes S, Beeckman T, Vernoux T, Doonan JH, Traas J, Inze D, De Veylder L (2010) Cyclin-dependent kinase activity maintains the shoot apical meristem cells in an undifferentiated state. Plant J 64:26–37

    PubMed  CAS  Google Scholar 

  • Goshima G, Mayer M, Zhang N, Stuurman N, Vale RD (2008) Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J Cell Biol 181:421–429

    Article  PubMed  CAS  Google Scholar 

  • Guo J, Song J, Wang F, Zhang XS (2007) Genome-wide identification and expression analysis of rice cell cycle genes. Plant Mol Biol 64:349–360

    Article  PubMed  CAS  Google Scholar 

  • Haga N, Kato K, Murase M, Araki S, Kubo M, Demura T, Suzuki K, Muller I, Voss U, Jürgens G, Ito M (2007) R1R2R3-Myb proteins positively regulate cytokinesis through activation of KNOLLE transcription in Arabidopsis thaliana. Development 134:1101–1110

    Article  PubMed  CAS  Google Scholar 

  • Haga N, Kobayashi K, Suzuki T, Maeo K, Kubo M, Ohtani M, Mitsuda N, Demura T, Nakamura K, Jürgens G, Ito M (2011) Mutations in MYB3R1 and MYB3R4 cause pleiotropic developmental defects and preferential down-regulation of multiple G2/M-specific genes in Arabidopsis. Plant Physiol 157:706–707, 717

    Article  PubMed  CAS  Google Scholar 

  • He SS, Liu J, Xie Z, O’Neill D, Dotson S (2004) Arabidopsis E2Fa plays a bimodal role in regulating cell division and cell growth. Plant Mol Biol 56:171–184

    Article  PubMed  CAS  Google Scholar 

  • Hendrickson TW, Yao J, Bhadury S, Corbett AH, Joshi HC (2001) Conditional mutations in gamma-tubulin reveal its involvement in chromosome segregation and cytokinesis. Mol Biol Cell 12:2469–2481

    PubMed  CAS  Google Scholar 

  • Henriques R, Magyar Z, Monardes A, Khan S, Zalejski C, Orellana J, Szabados L, de la Torre C, Koncz C, Bogre L (2010) Arabidopsis S6 kinase mutants display chromosome instability and altered RBR1-E2F pathway activity. EMBO J 29:2979–2993

    Article  PubMed  CAS  Google Scholar 

  • Hernando E, Nahle Z, Juan G, Diaz-Rodriguez E, Alaminos M, Hemann M, Michel L, Mittal V, Gerald W, Benezra R, Lowe SW, Cordon-Cardo C (2004) Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature 430:797–802

    Article  PubMed  CAS  Google Scholar 

  • Himanen K, Reuzeau C, Beeckman T, Melzer S, Grandjean O, Corben L, Inze D (2003) The Arabidopsis locus RCB mediates upstream regulation of mitotic gene expression. Plant Physiol 133:1862–1872

    Article  PubMed  CAS  Google Scholar 

  • Hirt H, Pay A, Gyorgyey J, Bako L, Nemeth K, Bogre L, Schweyen RJ, Heberle-Bors E, Dudits D (1991) Complementation of a yeast cell cycle mutant by an alfalfa cDNA encoding a protein kinase homologous to p34cdc2. Proc Natl Acad Sci USA 88:1636–1640

    Article  PubMed  CAS  Google Scholar 

  • Ho CM, Hotta T, Kong Z, Zeng CJ, Sun J, Lee YR, Liu B (2011) Augmin plays a critical role in organizing the spindle and phragmoplast microtubule arrays in Arabidopsis. Plant Cell 23:2606–2618

    Article  PubMed  CAS  Google Scholar 

  • Hochegger H, Takeda S, Hunt T (2008) Cyclin-dependent kinases and cell-cycle transitions: does one fit all? Nat Rev Mol Cell Biol 9:910–916

    Article  PubMed  CAS  Google Scholar 

  • Hoog G, Zarrizi R, von Stedingk K, Jonsson K, Alvarado-Kristensson M (2011) Nuclear localization of gamma-tubulin affects E2F transcriptional activity and S-phase progression. FASEB J 25:3815–3827

    Article  PubMed  CAS  Google Scholar 

  • Hořejši B, Vinopal S, Sladková V, Dráberová E, Sulimenko V, Sulimenko T, Vosecká V, Philimonenko A, Hozák P, Katsetos CD, Dráber P (2012) Nuclear gamma-tubulin associates with nucleoli and interacts with tumor suppressor protein C53. J Cell Physiol 227:367–382

    Article  PubMed  CAS  Google Scholar 

  • Hsu LC, Doan TP, White RL (2001) Identification of a gamma-tubulin-binding domain in BRCA1. Cancer Res 61:7713–7718

    PubMed  CAS  Google Scholar 

  • Hu X, Cheng X, Jiang H, Zhu S, Cheng B, Xiang Y (2010) Genome-wide analysis of cyclins in maize (Zea mays). Genet Mol Res 9:1490–1503

    Article  PubMed  CAS  Google Scholar 

  • Hubert T, Vandekerckhove J, Gettemans J (2011) Cdk1 and BRCA1 target gamma-tubulin to microtubule domains. Biochem Biophys Res Commun 414:240–245

    Article  PubMed  CAS  Google Scholar 

  • Hughes SE, Beeler JS, Seat A, Slaughter BD, Unruh JR, Bauerly E, Matthies HJ, Hawley RS (2011) Gamma-tubulin is required for bipolar spindle assembly and for proper kinetochore microtubule attachments during prometaphase I in Drosophila oocytes. PLoS Genet 7:e1002209

    Article  PubMed  CAS  Google Scholar 

  • Huysman MJ, Martens C, Vandepoele K, Gillard J, Rayko E, Heijde M, Bowler C, Inze D, Van de Peer Y, De Veylder L, Vyverman W (2010) Genome-wide analysis of the diatom cell cycle unveils a novel type of cyclins involved in environmental signaling. Genome Biol 11:R17

    Article  PubMed  CAS  Google Scholar 

  • Imai KK, Ohashi Y, Tsuge T, Yoshizumi T, Matsui M, Oka A, Aoyama T (2006) The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18:382–396

    Article  PubMed  CAS  Google Scholar 

  • Infante A, Laresgoiti U, Fernandez-Rueda J, Fullaondo A, Galan J, Diaz-Uriarte R, Malumbres M, Field SJ, Zubiaga AM (2008) E2F2 represses cell cycle regulators to maintain quiescence. Cell Cycle 7:3915–3927

    Article  PubMed  CAS  Google Scholar 

  • Inze D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40:77–105

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa M, Murata T, Sato Y, Nishiyama T, Hiwatashi Y, Imai A, Kimura M, Sugimoto N, Akita A, Oguri Y, Friedman WE, Hasebe M, Kubo M (2011) Physcomitrella cyclin-dependent kinase A links cell cycle reactivation to other cellular changes during reprogramming of leaf cells. Plant Cell 23:2924–2938

    Article  PubMed  CAS  Google Scholar 

  • Ito M (2005) Conservation and diversification of three-repeat Myb transcription factors in plants. J Plant Res 118:61–69

    Article  PubMed  CAS  Google Scholar 

  • Ito M, Iwase M, Kodama H, Lavisse P, Komamine A, Nishihama R, Machida Y, Watanabe A (1998) A novel cis-acting element in promoters of plant B-type cyclin genes activates M phase-specific transcription. Plant Cell 10:331–341

    PubMed  CAS  Google Scholar 

  • Ito M, Araki S, Matsunaga S, Itoh T, Nishihama R, Machida Y, Doonan JH, Watanabe A (2001) G2/M-phase-specific transcription during the plant cell cycle is mediated by c-Myb-like transcription factors. Plant Cell 13:1891–1905

    PubMed  CAS  Google Scholar 

  • Iwakawa H, Shinmyo A, Sekine M (2006) Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J 45:819–831

    Article  PubMed  CAS  Google Scholar 

  • Janson ME, Setty TG, Paoletti A, Tran PT (2005) Efficient formation of bipolar microtubule bundles requires microtubule-bound gamma-tubulin complexes. J Cell Biol 169:297–308

    Article  PubMed  CAS  Google Scholar 

  • Johmura Y, Soung NK, Park JE, Yu LR, Zhou M, Bang JK, Kim BY, Veenstra TD, Erikson RL, Lee KS (2011) Regulation of microtubule-based microtubule nucleation by mammalian polo-like kinase 1. Proc Natl Acad Sci USA 108:11446–11451

    Article  PubMed  CAS  Google Scholar 

  • Johnston AJ, Kirioukhova O, Barrell PJ, Rutten T, Moore JM, Baskar R, Grossniklaus U, Gruissem W (2010) Dosage-sensitive function of retinoblastoma related and convergent epigenetic control are required during the Arabidopsis life cycle. PLoS Genet 6:e1000988

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Karsenti E, Vernos I (2001) The mitotic spindle: a self-made machine. Science 294:543–547

    Article  PubMed  CAS  Google Scholar 

  • Kasili R, Walker JD, Simmons LA, Zhou J, De Veylder L, Larkin JC (2010) SIAMESE cooperates with the CDH1-like protein CCS52A1 to establish endoreplication in Arabidopsis thaliana trichomes. Genetics 185:257–268

    Article  PubMed  CAS  Google Scholar 

  • Kato K, Galis I, Suzuki S, Araki S, Demura T, Criqui MC, Potuschak T, Genschik P, Fukuda H, Matsuoka K, Ito M (2009) Preferential up-regulation of G2/M phase-specific genes by overexpression of the hyperactive form of NtmybA2 lacking its negative regulation domain in tobacco BY-2 cells. Plant Physiol 149:1945–1957

    Article  PubMed  CAS  Google Scholar 

  • Keck JM, Jones MH, Wong CC, Binkley J, Chen D, Jaspersen SL, Holinger EP, Xu T, Niepel M, Rout MP, Vogel J, Sidow A, Yates JR III, Winey M (2011) A cell cycle phosphoproteome of the yeast centrosome. Science 332:1557–1561

    Article  PubMed  CAS  Google Scholar 

  • Kono A, Umeda-Hara C, Adachi S, Nagata N, Konomi M, Nakagawa T, Uchimiya H, Umeda M (2007) The Arabidopsis D-type cyclin CYCD4 controls cell division in the stomatal lineage of the hypocotyl epidermis. Plant Cell 19:1265–1277

    Article  PubMed  CAS  Google Scholar 

  • Korenjak M, Brehm A (2005) E2F-Rb complexes regulating transcription of genes important for differentiation and development. Curr Opin Genet Dev 15:520–527

    Article  PubMed  CAS  Google Scholar 

  • Kosugi S, Ohashi Y (2003) 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

    Article  PubMed  CAS  Google Scholar 

  • Kramer A, Maier B, Bartek J (2011) Centrosome clustering and chromosomal (in)stability: a matter of life and death. Mol Oncol 5:324–335

    Article  PubMed  CAS  Google Scholar 

  • Lammens T, Boudolf V, Kheibarshekan L, Zalmas LP, Gaamouche T, Maes S, Vanstraelen M, Kondorosi E, La Thangue NB, Govaerts W, Inze D, De Veylder L (2008) Atypical E2F activity restrains APC/CCCS52A2 function obligatory for endocycle onset. Proc Natl Acad Sci USA 105:14721–14726

    Article  PubMed  CAS  Google Scholar 

  • Larson-Rabin Z, Li Z, Masson PH, Day CD (2009) FZR2/CCS52A1 expression is a determinant of endoreduplication and cell expansion in Arabidopsis. Plant Physiol 149:874–884

    Article  PubMed  CAS  Google Scholar 

  • Leone G, Nuckolls F, Ishida S, Adams M, Sears R, Jakoi L, Miron A, Nevins JR (2000) Identification of a novel E2F3 product suggests a mechanism for determining specificity of repression by Rb proteins. Mol Cell Biol 20:3626–3632

    Article  PubMed  CAS  Google Scholar 

  • Lesca C, Germanier M, Raynaud-Messina B, Pichereaux C, Etievant C, Emond S, Burlet-Schiltz O, Monsarrat B, Wright M, Defais M (2005) DNA damage induce gamma-tubulin-RAD51 nuclear complexes in mammalian cells. Oncogene 24:5165–5172

    Article  PubMed  CAS  Google Scholar 

  • Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P (2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA 102:12978–12983

    Article  PubMed  CAS  Google Scholar 

  • Lin TC, Gombos L, Neuner A, Sebastian D, Olsen JV, Hrle A, Benda C, Schiebel E (2011) Phosphorylation of the yeast gamma-tubulin Tub4 regulates microtubule function. PLoS One 6:e19700

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Ruderman JV (2006) Aurora A, mitotic entry, and spindle bipolarity. Proc Natl Acad Sci USA 103:5811–5816

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Marc J, Joshi HC, Palevitz BA (1993) A gamma-tubulin-related protein associated with the microtubule arrays of higher plants in a cell cycle-dependent manner. J Cell Sci 104:1217–1228

    PubMed  CAS  Google Scholar 

  • Liu DX, Nath N, Chellappan SP, Greene LA (2005) Regulation of neuron survival and death by p130 and associated chromatin modifiers. Genes Dev 19:719–732

    Article  PubMed  CAS  Google Scholar 

  • Lloyd C (2011) Plant cytokinesis: circles within circles. Curr Biol 21:R926–R927

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Juez E, Dillon E, Magyar Z, Khan S, Hazeldine S, de Jager SM, Murray JA, Beemster GT, Bogre L, Shanahan H (2008) Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell 20:947–968

    Article  PubMed  CAS  Google Scholar 

  • Ma HT, Poon RY (2011) Orderly inactivation of the key checkpoint protein mitotic arrest deficient 2 (MAD2) during mitotic progression. J Biol Chem 286:13052–13059

    Article  PubMed  CAS  Google Scholar 

  • Magyar Z (2008) Keeping the balance between proliferation and differentiation by the E2F transcriptional regulatory network is central to plant growth and development. In: Bogre L, Beemster GT (eds) In plant growth signaling. Springer, Berlin/Heidelberg

    Google Scholar 

  • Magyar Z, De Veylder L, Atanassova A, Bako L, Inze D, Bogre L (2005) The role of the Arabidopsis E2FB transcription factor in regulating auxin-dependent cell division. Plant Cell 17:2527–2541

    Article  PubMed  CAS  Google Scholar 

  • Magyar Z, Horvath B, Khan S, Mohammed B, Henriques R, De Veylder L, Bako L, Scheres B, Bogre L (2012) Arabidopsis E2FA stimulates proliferation and endocycle separately through RBR-bound and RBR-free complexes. EMBO J 31:1480–1493

    Article  PubMed  CAS  Google Scholar 

  • Maluszynska J, Kolano B, Sas-Nowosielska H (2013) Endopolyploidy in plants. In: Leitch IJ, Greilhuber J, Doležel J, Wendel JF (eds) Plant genome diversity, vol 2, Physical structure, behaviour and evolution of plant genomes. Springer-Verlag, Wien, pp 99–119

    Google Scholar 

  • Marti A, Wirbelauer C, Scheffner M, Krek W (1999) Interaction between ubiquitin-protein ligase SCFSKP2 and E2F-1 underlies the regulation of E2F-1 degradation. Nat Cell Biol 1:14–19

    Article  PubMed  CAS  Google Scholar 

  • Menges M, Hennig L, Gruissem W, Murray JA (2003) Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol Biol 53:423–442

    Article  PubMed  CAS  Google Scholar 

  • Menges M, de Jager SM, Gruissem W, Murray JA (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41:546–566

    Article  PubMed  CAS  Google Scholar 

  • Menges M, Pavesi G, Morandini P, Bogre L, Murray JA (2007) Genomic organization and evolutionary conservation of plant D-type cyclins. Plant Physiol 145:1558–1576

    Article  PubMed  CAS  Google Scholar 

  • Mishra RK, Chakraborty P, Arnaoutov A, Fontoura BM, Dasso M (2010) The Nup107-160 complex and gamma-TuRC regulate microtubule polymerization at kinetochores. Nat Cell Biol 12:164–169

    Article  PubMed  CAS  Google Scholar 

  • Morgan DO (2007) The cell cycle principles of control. Oxford University Press, Corby

    Google Scholar 

  • Murata T, Sonobe S, Baskin TI, Hyodo S, Hasezawa S, Nagata T, Horio T, Hasebe M (2005) Microtubule-dependent microtubule nucleation based on recruitment of gamma-tubulin in higher plants. Nat Cell Biol 7:961–968

    Article  PubMed  CAS  Google Scholar 

  • Nair JS, Ho AL, Tse AN, Coward J, Cheema H, Ambrosini G, Keen N, Schwartz GK (2009) Aurora B kinase regulates the postmitotic endoreduplication checkpoint via phosphorylation of the retinoblastoma protein at serine 780. Mol Biol Cell 20:2218–2228

    Article  PubMed  CAS  Google Scholar 

  • Nayak T, Edgerton-Morgan H, Horio T, Xiong Y, De Souza CP, Osmani SA, Oakley BR (2010) Gamma-tubulin regulates the anaphase-promoting complex/cyclosome during interphase. J Cell Biol 190:317–330

    Article  PubMed  CAS  Google Scholar 

  • Neufeld TP, de la Cruz AF, Johnston LA, Edgar BA (1998) Coordination of growth and cell division in the Drosophila wing. Cell 93:1183–1193

    Article  PubMed  CAS  Google Scholar 

  • Nieuwland J, Maughan S, Dewitte W, Scofield S, Sanz L, Murray JA (2009) The D-type cyclin CYCD4;1 modulates lateral root density in Arabidopsis by affecting the basal meristem region. Proc Natl Acad Sci U S A 106:22528–22533

    Article  PubMed  CAS  Google Scholar 

  • Nowack MK, Grini PE, Jakoby MJ, Lafos M, Koncz C, Schnittger A (2006) A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat Genet 38:63–67

    Article  PubMed  CAS  Google Scholar 

  • Nowack MK, Shirzadi R, Dissmeyer N, Dolf A, Endl E, Grini PE, Schnittger A (2007) Bypassing genomic imprinting allows seed development. Nature 447:312–315

    Article  PubMed  CAS  Google Scholar 

  • Park JA, Ahn JW, Kim YK, Kim SJ, Kim JK, Kim WT, Pai HS (2005) Retinoblastoma protein regulates cell proliferation, differentiation, and endoreduplication in plants. Plant J 42:153–163

    Article  PubMed  CAS  Google Scholar 

  • Parvin JD (2009) The BRCA1-dependent ubiquitin ligase, gamma-tubulin, and centrosomes. Environ Mol Mutagen 50:649–653

    Article  PubMed  CAS  Google Scholar 

  • Pastuglia M, Azimzadeh J, Goussot M, Camilleri C, Belcram K, Evrard JL, Schmit AC, Guerche P, Bouchez D (2006) Gamma-tubulin is essential for microtubule organization and development in Arabidopsis. Plant Cell 18:1412–1425

    Article  PubMed  CAS  Google Scholar 

  • Petrovská B, Cenklová V, Pochylová Z, Kourová H, Doskočilová A, Plíhal O, Binarová L, Binarová P (2012) Plant Aurora kinases play a role in maintenance of primary meristems and control of endoreduplication. New Phytol 193:590–604

    Article  PubMed  Google Scholar 

  • Planchais S, Perennes C, Glab N, Mironov V, Inze D, Bergounioux C (2002) Characterization of cis-acting element involved in cell cycle phase-independent activation of Arath;CycB1;1 transcription and identification of putative regulatory proteins. Plant Mol Biol 50:111–127

    Article  PubMed  CAS  Google Scholar 

  • Prigozhina NL, Oakley CE, Lewis AM, Nayak T, Osmani SA, Oakley BR (2004) Gamma-tubulin plays an essential role in the coordination of mitotic events. Mol Biol Cell 15:1374–1386

    Article  PubMed  CAS  Google Scholar 

  • Rayman JB, Takahashi Y, Indjeian VB, Dannenberg JH, Catchpole S, Watson RJ, te Riele H, Dynlacht BD (2002) E2F mediates cell cycle-dependent transcriptional repression in vivo by recruitment of an HDAC1/mSin3B corepressor complex. Genes Dev 16:933–947

    Article  PubMed  CAS  Google Scholar 

  • Raynaud-Messina B, Merdes A (2007) Gamma-tubulin complexes and microtubule organization. Curr Opin Cell Biol 19:24–30

    Article  PubMed  CAS  Google Scholar 

  • Royzman I, Austin RJ, Bosco G, Bell SP, Orr-Weaver TL (1999) ORC localization in Drosophila follicle cells and the effects of mutations in dE2F and dDP. Genes Dev 13:827–840

    Article  PubMed  CAS  Google Scholar 

  • Sage J, Straight AF (2010) RB’s original CIN? Genes Dev 24:1329–1333

    Article  PubMed  CAS  Google Scholar 

  • Sardon T, Pache RA, Stein A, Molina H, Vernos I, Aloy P (2010) Uncovering new substrates for Aurora A kinase. EMBO Rep 11:977–984

    Article  PubMed  CAS  Google Scholar 

  • Scheres B, Xu J (2006) Polar auxin transport and patterning: grow with the flow. Genes Dev 20:922–926

    Article  PubMed  CAS  Google Scholar 

  • Schnittger A, Schobinger U, Stierhof YD, Hulskamp M (2002) Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr Biol 12:415–420

    Article  PubMed  CAS  Google Scholar 

  • Schubert I, Shaw P (2011) Organization and dynamics of plant interphase chromosomes. Trends Plant Sci 16:273–281

    Article  PubMed  CAS  Google Scholar 

  • Schuh M, Ellenberg J (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130:484–498

    Article  PubMed  CAS  Google Scholar 

  • Schweiger R, Linial M (2010) Cooperativity within proximal phosphorylation sites is revealed from large-scale proteomics data. Biol Direct 5:6

    Article  PubMed  CAS  Google Scholar 

  • Sozzani R, Maggio C, Varotto S, Canova S, Bergounioux C, Albani D, Cella R (2006) Interplay between Arabidopsis activating factors E2Fb and E2Fa in cell cycle progression and development. Plant Physiol 140:1355–1366

    Article  PubMed  CAS  Google Scholar 

  • Sterken R, Kiekens R, Coppens E, Vercauteren I, Zabeau M, Inze D, Flowers J, Vuylsteke M (2009) A population genomics study of the Arabidopsis core cell cycle genes shows the signature of natural selection. Plant Cell 21:2987–2998

    Article  PubMed  CAS  Google Scholar 

  • Stumpff J, Kellogg DR, Krohne KA, Su TT (2005) Drosophila Wee1 interacts with members of the gamma TURC and is required for proper mitotic-spindle morphogenesis and positioning. Curr Biol 15:1525–1534

    Article  PubMed  CAS  Google Scholar 

  • Takahashi I, Kojima S, Sakaguchi N, Umeda-Hara C, Umeda M (2010) Two Arabidopsis cyclin A3s possess G1 cyclin-like features. Plant Cell Rep 29:307–315

    Article  PubMed  CAS  Google Scholar 

  • Tsai MY, Zheng Y (2005) Aurora A kinase-coated beads function as microtubule-organizing centers and enhance RanGTP-induced spindle assembly. Curr Biol 15:2156–2163

    Article  PubMed  CAS  Google Scholar 

  • Tsai SY, Opavsky R, Sharma N, Wu L, Naidu S, Nolan E, Feria-Arias E, Timmers C, Opavska J, de Bruin A, Chong JL, Trikha P, Fernandez SA, Stromberg P, Rosol TJ, Leone G (2008) Mouse development with a single E2F activator. Nature 454:1137–1141

    Article  PubMed  CAS  Google Scholar 

  • Tyson JJ, Novak B (2008) Temporal organization of the cell cycle. Curr Biol 18:R759–R768

    Article  PubMed  CAS  Google Scholar 

  • Umbrasaite J, Schweighofer A, Kazanaviciute V, Magyar Z, Ayatollahi Z, Unterwurzacher V, Choopayak C, Boniecka J, Murray JA, Bogre L, Meskiene I (2010) MAPK phosphatase AP2C3 induces ectopic proliferation of epidermal cells leading to stomata development in Arabidopsis. PLoS One 5:e15357

    Article  PubMed  CAS  Google Scholar 

  • van den Heuvel S, Dyson NJ (2008) Conserved functions of the pRB and E2F families. Nat Rev Mol Cell Biol 9:713–724

    Article  PubMed  CAS  Google Scholar 

  • Van Leene J, Hollunder J, Eeckhout D, Persiau G, Van De Slijke E, Stals H, Van Isterdael G, Verkest A, Neirynck S, Buffel Y, De Bodt S, Maere S, Laukens K, Pharazyn A, Ferreira PC, Eloy N, Renne C, Meyer C, Faure JD, Steinbrenner J, Beynon J, Larkin JC, Van de Peer Y, Hilson P, Kuiper M, De Veylder L, Van Onckelen H, Inze D, Witters E, De Jaeger G (2010) Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol Syst Biol 6:397

    PubMed  Google Scholar 

  • Van Leene J, Boruc J, De Jaeger G, Russinova E, De Veylder L (2011) A kaleidoscopic view of the Arabidopsis core cell cycle interactome. Trends Plant Sci 16:141–150

    Article  PubMed  CAS  Google Scholar 

  • Vandepoele K, Raes J, De Veylder L, Rouze P, Rombauts S, Inze D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14:903–916

    Article  PubMed  CAS  Google Scholar 

  • Vandepoele K, Vlieghe K, Florquin K, Hennig L, Beemster GT, Gruissem W, Van de Peer Y, Inze D, De Veylder L (2005) Genome-wide identification of potential plant E2F target genes. Plant Physiol 139:316–328

    Article  PubMed  CAS  Google Scholar 

  • Vandepoele K, Quimbaya M, Casneuf T, De Veylder L, Van de Peer Y (2009) Unraveling transcriptional control in Arabidopsis using cis-regulatory elements and coexpression networks. Plant Physiol 150:535–546

    Article  PubMed  CAS  Google Scholar 

  • Vanstraelen M, Baloban M, Da Ines O, Cultrone A, Lammens T, Boudolf V, Brown SC, De Veylder L, Mergaert P, Kondorosi E (2009) APC/C-CCS52A complexes control meristem maintenance in the Arabidopsis root. Proc Natl Acad Sci USA 106:11806–11811

    Article  PubMed  CAS  Google Scholar 

  • Vlieghe K, Vuylsteke M, Florquin K, Rombauts S, Maes S, Ormenese S, Van Hummelen P, Van de Peer Y, Inze D, De Veylder L (2003) Microarray analysis of E2Fa-DPa-overexpressing plants uncovers a cross-talking genetic network between DNA replication and nitrogen assimilation. J Cell Sci 116:4249–4259

    Article  PubMed  CAS  Google Scholar 

  • Weingartner M, Binarova P, Drykova D, Schweighofer A, David JP, Heberle-Bors E, Doonan J, Bogre L (2001) Dynamic recruitment of Cdc2 to specific microtubule structures during mitosis. Plant Cell 13:1929–1943

    PubMed  CAS  Google Scholar 

  • Weingartner M, Criqui MC, Meszaros T, Binarova P, Schmit AC, Helfer A, Derevier A, Erhardt M, Bogre L, 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

    Article  PubMed  CAS  Google Scholar 

  • Wenzel PL, Chong JL, Saenz-Robles MT, Ferrey A, Hagan JP, Gomez YM, Rajmohan R, Sharma N, Chen HZ, Pipas JM, Robinson ML, Leone G (2011) Cell proliferation in the absence of E2F1-3. Dev Biol 351:35–45

    Article  PubMed  CAS  Google Scholar 

  • Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123:1337–1349

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yoshizumi T, Tsumoto Y, Takiguchi T, Nagata N, Yamamoto YY, Kawashima M, Ichikawa T, Nakazawa M, Yamamoto N, Matsui M (2006) Increased level of polyploidy1, a conserved repressor of CYCLINA2 transcription, controls endoreduplication in Arabidopsis. Plant Cell 18:2452–2468

    Article  PubMed  CAS  Google Scholar 

  • Yuan L, Yang X, Makaroff CA (2011) Plant cohesins, common themes and unique roles. Curr Protein Pept Sci 12:93–104

    Article  PubMed  CAS  Google Scholar 

  • Zhu W, Giangrande PH, Nevins JR (2005) Temporal control of cell cycle gene expression mediated by E2F transcription factors. Cell Cycle 4:633–636

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

We thank Dr. Věra Cenklová for providing pictures of V. faba for Fig. 6.4.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laszlo Bogre .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Wien

About this chapter

Cite this chapter

Magyar, Z., Ito, M., Binarová, P., Mohamed, B., Bogre, L. (2013). Cell Cycle Modules in Plants for Entry into Proliferation and for Mitosis. In: Greilhuber, J., Dolezel, J., Wendel, J. (eds) Plant Genome Diversity Volume 2. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1160-4_6

Download citation

Publish with us

Policies and ethics