Plant Molecular Biology

, Volume 60, Issue 6, pp 947–961 | Cite as

Expression of Cell Cycle Genes in Shoot Apical Meristems

  • Vasilis C. Gegas
  • John H. DoonanEmail author


This article reviews cell proliferation in the shoot apical meristem. The morphology and function of the meristem depends on the positional control of cell growth and division. The review describes the historical framework of research in this area and then discusses the regulatory pathways that might link developmental controls to the core cell cycle machinery.


auxin cell cycle cell proliferation cyclin-dependent protein kinases cyclins cytokinin E2F meristem 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ach, R.A., Taranto, P., Gruissem, W. 1997A conserved␣family of WD-40 proteins binds to the retinoblastoma protein in both plants and animalsPlant Cell915951606PubMedCrossRefGoogle Scholar
  2. Araki, S., Ito, M., Soyano, T., Nishihama, R., Machida, Y. 2004Mitotic cyclins stimulate the activity of c-Myb-like factors for transactivation of G2/M phase-specific genes in tobaccoJ. Biol. Chem.2793297932988PubMedCrossRefGoogle Scholar
  3. Barroco, R.M., Poucke, K., Bergervoet, J.H., Veylder, L., Groot, S.P., Inze, D., Engler, G. 2005The role of the cell cycle machinery in resumption of postembryonic developmentPlant Physiol.137127140PubMedCrossRefGoogle Scholar
  4. Besnard-Wibaut, C. 1977Histoautoradiographic analysis of the thermoinductive processes in the shoot apex of Arabidopsis thaliana L. Heynh, vernalized at different stages of developmentPlant Cell Physiol.18949962Google Scholar
  5. Boucheron, E., Guivarc’h, A., Azmi, A., Dewitte, W., Onckelen, H., Chriqui, D. 2002Competency of Nicotiana tabacum L. stem tissues to dedifferentiate is associated with differential levels of cell cycle gene expression and endogenous cytokininsPlanta215267278PubMedCrossRefGoogle Scholar
  6. Boucheron, E., Healy, J.H., Bajon, C., Sauvanet, A., Rembur, J., Noin, M., Sekine, M., Riou Khamlichi, C., Murray, J.A., Onckelen, H., Chriqui, D. 2005Ectopic expression of Arabidopsis CYCD2 and CYCD3 in tobacco has distinct effects on the structural organization of the shoot apical meristemJ. Exp. Bot.56123134PubMedGoogle Scholar
  7. Boudolf, V., Barroco, R., Engler Jde, A., Verkest, A., Beeckman, T., Naudts, M., Inze, D., Veylder, L. 2004B1-type cyclin-dependent kinases are essential for the formation of stomatal complexes in Arabidopsis thaliana Plant Cell16945955PubMedCrossRefGoogle Scholar
  8. Breuil-Broyer, S., Morel, P., Almeida-Engler, J., Coustham, V., Negrutiu, I., Trehin, C. 2004High-resolution boundary analysis during Arabidopsis thaliana flower developmentPlant J.38182192PubMedCrossRefGoogle Scholar
  9. Broadhvest, J., Baker, S.C., Gasser, C.S. 2000SHORT INTEGUMENTS 2 promotes growth during Arabidopsis reproductive developmentGenetics155899907PubMedGoogle Scholar
  10. Castellano, M.M., del Pozo, J.C., Ramirez-Parra, E., Brown, S., Gutierrez, C. 2001Expression and stability of Arabidopsis CDC6 are associated with endoreplicationPlant Cell1326712686PubMedCrossRefGoogle Scholar
  11. Chaboute, M.E., Clement, B., Philipps, G. 2002S phase and meristem-specific expression of the tobacco RNR1b gene is mediated by an E2F element located in the 5′ leader sequenceJ. Biol. Chem.2771784517851PubMedCrossRefGoogle Scholar
  12. Chuck, G., Lincoln, C., Hake, S. 1996KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis Plant Cell812771289PubMedCrossRefGoogle Scholar
  13. Clark, S.E., Jacobsen, S.E., Levin, J.Z., Meyerowitz, E.M. 1996The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis Development12215671575PubMedGoogle Scholar
  14. Cockcroft, C.E., Boer, B.G., Healy, J.M., Murray, J.A. 2000Cyclin D control of growth rate in plantsNature405575579PubMedCrossRefGoogle Scholar
  15. Corellou, F., Camasses, A., Ligat, L., Peaucellier, G., Bouget, F.Y. 2005Atypical regulation of a green lineage-specific B-type cyclin-dependent kinasePlant Physiol.13816271636PubMedCrossRefGoogle Scholar
  16. Cubas, P., Lauter, N., Doebley, J., Coen, E. 1999The TCP domain: a motif found in proteins regulating plant growth and developmentPlant J.18215222PubMedCrossRefGoogle Scholar
  17. Cunninghame, M.E., Lyndon, R.F. 1986.The relationship between the distribution of perclinal cell divisions in the shoot apex and leaf initiationAnn. Bot.57737746Google Scholar
  18. Dawe, R.K., Freeling, M. 1991Cell lineage and its consequences in higher plantsPlant J.138CrossRefGoogle Scholar
  19. Day, I.S., Reddy, A.S. 1998Isolation and characterization of two cyclin-like cDNAs from Arabidopsis Plant Mol. Biol.36451461PubMedCrossRefGoogle Scholar
  20. Veylder, L., Beeckman, T., Beemster, G.T., Krols, L., Terras, F., Landrieu, I., Schueren, E., Maes, S., Naudts, M., Inze, D. 2001aFunctional analysis of cyclin-dependent kinase inhibitors of Arabidopsis Plant Cell1316531668CrossRefGoogle Scholar
  21. Veylder, L., Beemster, G.T., Beeckman, T., Inze, D. 2001bCKS1At overexpression in Arabidopsis thaliana inhibits growth by reducing meristem size and inhibiting cell-cycle progressionPlant J.25617626CrossRefGoogle Scholar
  22. Veylder, L., Segers, G., Glab, N., Casteels, P., Montagu, M., Inze, D. 1997The Arabidopsis Cks1At protein binds the cyclin-dependent kinases Cdc2aAt and Cdc2bAtFEBS Lett.412446452PubMedCrossRefGoogle Scholar
  23. del Pozo, J.C., Boniotti, M.B., Gutierrez, C. 2002 Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin–SCF(AtSKP2) pathway in response to lightPlant Cell1430573071PubMedCrossRefGoogle Scholar
  24. Dewitte, W., Riou-Khamlichi, C., Scofield, S., Healy, J.M., Jacqmard, A., Kilby, N.J., Murray, J.A. 2003Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3Plant Cell157992PubMedCrossRefGoogle Scholar
  25. Dinneny, J.R., Yadegari, R., Fischer, R.L., Yanofsky, M.F., Weigel, D. 2004The role of JAGGED in shaping lateral organsDevelopment13111011110PubMedCrossRefGoogle Scholar
  26. Doebley, J., Stec, A., Gustus, C. 1995Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominanceGenetics141333346PubMedGoogle Scholar
  27. Doerner, P., Jorgensen, J.E., You, R., Steppuhn, J., Lamb, C. 1996Control of root growth and development by cyclin expressionNature380520523PubMedCrossRefGoogle Scholar
  28. Egelkrout, E.M., Mariconti, L., Settlage, S.B., Cella, R., Robertson, D., Hanley-Bowdoin, L. 2002Two E2F elements regulate the proliferating cell nuclear antigen promoter differently during leaf developmentPlant Cell1432253236PubMedCrossRefGoogle Scholar
  29. Elliott, R.C., Betzner, A.S., Huttner, E., Oakes, M.P., Tucker, W.Q., Gerentes, D., Perez, P., Smyth, D.R. 1996AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growthPlant Cell8155168PubMedCrossRefGoogle Scholar
  30. Faure, J.D., Vittorioso, P., Santoni, V., Fraisier, V., Prinsen, E., Barlier, I., Onckelen, H., Caboche, M., Bellini, C. 1998The PASTICCINO genes of Arabidopsis thaliana are involved in the control of cell division and differentiationDevelopment125909918PubMedGoogle Scholar
  31. Ferreira, P.C., Hemerly, A.S., Engler, J.D., Montagu, M., Engler, G., Inze, D. 1994Developmental expression of the Arabidopsis cyclin gene cyc1AtPlant Cell617631774PubMedCrossRefGoogle Scholar
  32. Fitzpatrick, C.A., Sharkov, N.V., Ramsay, G., Katzen, A.L. 2002 Drosophila myb exerts opposing effects on S phase, promoting proliferation and suppressing endoreduplicationDevelopment12944974507PubMedGoogle Scholar
  33. Fletcher, J.C. 2002Coordination of cell proliferation and cell fate decisions in the angiosperm shoot apical meristemBioessays242737PubMedCrossRefGoogle Scholar
  34. Foard, D.E. 1971.The initial protrusion of a leaf primordium can form without concurrent periclinal cell divisionsCan. J.␣Bot.49694702Google Scholar
  35. Fobert, P.R., Coen, E.S., Murphy, G.J., Doonan, J.H. 1994Patterns of cell division revealed by transcriptional regulation of genes during the cell cycle in plantsEMBO J.13616624PubMedGoogle Scholar
  36. Fobert, P.R., Gaudin, V., Lunness, P., Coen, E.S., Doonan, J.H. 1996Distinct classes of cdc2-related genes are differentially expressed during the cell division cycle in plantsPlant Cell814651476PubMedCrossRefGoogle Scholar
  37. Fuerst, R.A., Soni, R., Murray, J.A., Lindsey, K. 1996Modulation of cyclin transcript levels in cultured cells of Arabidopsis thaliana Plant Physiol.11210231033PubMedCrossRefGoogle Scholar
  38. Furner, I.J., Pumfrey, J.E. 1992Cell fate in the shoot apical␣meristem of Arabidopsis thaliana Development115755764Google Scholar
  39. Gallois, J.L., Woodward, C., Reddy, G.V., Sablowski, R. 2002Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis Development12932073217PubMedGoogle Scholar
  40. Gaudin, V., Lunness, P.A., Fobert, P.R., Towers, M., Riou-Khamlichi, C., Murray, J.A., Coen, E., Doonan, J.H. 2000The expression of D-cyclin genes defines distinct developmental zones in snapdragon apical meristems and is locally regulated by the Cycloidea genePlant Physiol.12211371148PubMedCrossRefGoogle Scholar
  41. Grandjean, O., Vernoux, T., Laufs, P., Belcram, K., Mizukami, Y., Traas, J. 2004In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis Plant Cell167487PubMedCrossRefGoogle Scholar
  42. Han, W., Rhee, H.I., Cho, J.W., Ku, M.S., Song, P.S., Wang, M.H. 2005Overexpression of Arabidopsis ACK1 alters leaf morphology and retards growth and developmentBiochem. Biophys. Res. Commun.330887890PubMedCrossRefGoogle Scholar
  43. Harrar, Y., Bellec, Y., Bellini, C., Faure, J.D. 2003Hormonal control of cell proliferation requires PASTICCINO genesPlant Physiol.13212171227PubMedCrossRefGoogle Scholar
  44. He, S.S., Liu, J., Xie, Z., O’Neill, D., Dotson, S. 2004 Arabidopsis E2Fa plays a bimodal role in regulating cell division and cell growthPlant. Mol. Biol.56171184PubMedCrossRefGoogle Scholar
  45. Helliwell, C.A., Chin-Atkins, A.N., Wilson, I.W., Chapple, R., Dennis, E.S., Chaudhury, A. 2001The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidasePlant Cell1321152125PubMedCrossRefGoogle Scholar
  46. Hemerly, A.S., Ferreira, P., Almeida Engler, J., Montagu, M., Engler, G., Inze, D. 1993cdc2a expression in Arabidopsis is linked with competence for cell divisionPlant Cell517111723PubMedCrossRefGoogle Scholar
  47. Hemerly, A.S., Ferreira, P.C., Montagu, M., Engler, G., Inze, D. 2000Cell division events are essential for embryo patterning and morphogenesis: studies on dominant-negative␣cdc2aAt mutants of Arabidopsis Plant J.23123130PubMedCrossRefGoogle Scholar
  48. Hennig, L., Taranto, P., Walser, M., Schonrock, N., Gruissem, W. 2003 Arabidopsis MSI1 is required for epigenetic maintenance of reproductive developmentDevelopment13025552565PubMedCrossRefGoogle Scholar
  49. Hewelt, A., Prinsen, E., Schell, J., Onckelen, H., Schmulling, T. 1994Promoter tagging with a promoterless ipt gene leads to cytokinin-induced phenotypic variability in transgenic tobacco plants: implications of gene dosage effectsPlant J.6879891PubMedCrossRefGoogle Scholar
  50. Himanen, K., Reuzeau, C., Beeckman, T., Melzer, S., Grandjean, O., Corben, L., Inze, D. 2003The Arabidopsis locus RCB mediates upstream regulation of mitotic gene expressionPlant Physiol.13318621872PubMedCrossRefGoogle Scholar
  51. Hu, Y., Bao, F., Li, J. 2000Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis Plant J.24693701PubMedCrossRefGoogle Scholar
  52. Hu, Y., Xie, Q., Chua, N.H. 2003The Arabidopsis auxin-inducible gene ARGOS controls lateral organ sizePlant Cell1519511961PubMedCrossRefGoogle Scholar
  53. Hubbard, L., McSteen, P., Doebley, J., Hake, S. 2002Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinteGenetics16219271935PubMedGoogle Scholar
  54. Huntley, R., Healy, S., Freeman, D., Lavender, P., Jager, S., Greenwood, J., Makker, J., Walker, E., Jackman, M., Xie, Q., Bannister, A.J., Kouzarides, T., Gutierrez, C., Doonan, J.H., Murray, J.A 1998The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteinsPlant Mol. Biol.37155169PubMedCrossRefGoogle Scholar
  55. Ingram, G.C., Goodrich, J., Wilkinson, M.D., Simon, R., Haughn, G.W., Coen, E.S. 1995Parallels between UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum Plant Cell715011510PubMedCrossRefGoogle Scholar
  56. Ito, M. 2005Conservation and diversification of three-repeat Myb transcription factors in plantsJ. Plant Res.1186169PubMedCrossRefGoogle Scholar
  57. Ito, M., Araki, S., Matsunaga, S., Itoh, T., Nishihama, R., Machida, Y., Doonan, J.H., Watanabe, A. 2001G2/M-phase-specific transcription during the plant cell cycle is mediated by c-Myb-like transcription factorsPlant Cell1318911905PubMedCrossRefGoogle Scholar
  58. Iwakawa, H., Shinmyo, A.,  et al. 2006Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis.Plant J.45819831PubMedCrossRefGoogle Scholar
  59. Jasinski, S., Perennes, C., Bergounioux, C., Glab, N. 2002aComparative molecular and functional analyses of the tobacco cyclin-dependent kinase inhibitor NtKIS1a and its spliced variant NtKIS1bPlant Physiol.13018711882CrossRefGoogle Scholar
  60. Jasinski, S., Piazza, P., Craft, J., Hay, A., Woolley, L., Rieu, I., Phillips, A., Hedden, P., Tsiantis, M. 2005KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activitiesCurr. Biol.1515601565PubMedCrossRefGoogle Scholar
  61. Jasinski, S., Riou-Khamlichi, C., Roche, O., Perennes, C., Bergounioux, C., Glab, N. 2002bThe CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3; 1-overexpressing plantsJ. Cell Sci.115973982Google Scholar
  62. Jung, J.H., Yun, J., Seo, Y.H., Park, C.M. 2005Characterization of an Arabidopsis gene that mediates cytokinin signaling in shoot apical meristem developmentMol. Cells19342349PubMedGoogle Scholar
  63. Kaya, H., Shibahara, K.I., Taoka, K.I., Iwabuchi, M., Stillman, B., Araki, T. 2001FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristemsCell104131142PubMedCrossRefGoogle Scholar
  64. Kerstetter, R.A., Hake, S.L. 1997Shoot meristem formation in vegetative developmentPlant Cell910011010PubMedCrossRefGoogle Scholar
  65. Klucher, K.M., Chow, H., Reiser, L., Fischer, R.L. 1996The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2Plant Cell8137153PubMedCrossRefGoogle Scholar
  66. Kono, A., Umeda-Hara, C., Lee, J., Ito, M., Uchimiya, H., Umeda, M. 2003 Arabidopsis D-type cyclin CYCD4;1 is a novel cyclin partner of B2-type cyclin-dependent kinasePlant Physiol.13213151321PubMedCrossRefGoogle Scholar
  67. Kosugi, S., Ohashi, Y. 2002aDNA binding and dimerization specificity and potential targets for the TCP protein familyPlant J.30337348CrossRefGoogle Scholar
  68. Kosugi, S., Ohashi, Y. 2002bE2F 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 promotersPlant J.294559CrossRefGoogle Scholar
  69. Kosugi, S., Ohashi, Y. 2003Constitutive E2F expression in␣tobacco plants exhibits altered cell cycle control and morphological change in a cell type-specific mannerPlant Physiol.13220122022PubMedCrossRefGoogle Scholar
  70. Kouchi, H., Sekine, M., Hata, S. 1995Distinct classes of mitotic cyclins are differentially expressed in the soybean shoot apex during the cell cyclePlant Cell711431155PubMedCrossRefGoogle Scholar
  71. Lance, A. 1957Recherches cytologiques sur l’evolution de quelques meristems apicaux et sur ses variations provoquees par des traitements photoperiodiqueAnn. Sci. Nat. Bot.1891421Google Scholar
  72. Landrieu, I., da Costa, M., Veylder, L., Dewitte, F., Vandepoele, K., Hassan, S., Wieruszeski, J.M., Corellou, F., Faure, J.D., Montagu, M., Inze, D., Lippens, G. 2004A small CDC25 dual-specificity tyrosine-phosphatase isoform in Arabidopsis thaliana Proc. Natl. Acad. Sci. U.S.A1011338013385PubMedCrossRefGoogle Scholar
  73. Laufs, P., Coen, E., Kronenberger, J., Traas, J., Doonan, J. 2003Separable roles of UFO during floral development revealed by conditional restoration of gene functionDevelopment130785796PubMedCrossRefGoogle Scholar
  74. Laufs, P., Grandjean, O., Jonak, C., Kieu, K., Traas, J. 1998Cellular parameters of the shoot apical meristem in Arabidopsis The Plant Cell1013751389PubMedCrossRefGoogle Scholar
  75. Lenhard, M., Jurgens, G., Laux, T. 2002The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulationDevelopment12931953206PubMedGoogle Scholar
  76. Li, C., Potuschak, T., Colon-Carmona, A., Gutierrez, R.A., Doerner, P. 2005 Arabidopsis TCP20 links regulation of growth and cell division control pathwaysProc. Natl. Acad. Sci. U.S.A1021297812983PubMedCrossRefGoogle Scholar
  77. Long, J.A., Barton, M.K. 1998The development of apical embryonic pattern in Arabidopsis Development12530273035PubMedGoogle Scholar
  78. Lui, H., Wang, H., Delong, C., Fowke, L.C., Crosby, W.L., Fobert, P.R. 2000The Arabidopsis Cdc2a-interacting protein ICK2 is structurally related to ICK1 and is a potent inhibitor of cyclin-dependent kinase activity in vitroPlant J.21379385PubMedCrossRefGoogle Scholar
  79. Lyndon, R.F. 1970Rates of cell division in the shoot apical meristem of Pisum Ann. Bot.34117Google Scholar
  80. Magyar, Z., Atanassova, A., Veylder, L., Rombauts, S., Inze, D. 2000Characterization of two distinct DP-related genes from Arabidopsis thaliana FEBS Lett.4867987PubMedCrossRefGoogle Scholar
  81. Magyar, Z., Veylder, L., Atanassova, A., Bako, L., Inze, D., Bogre, L. 2005The role of the Arabidopsis E2FB transcription factor in regulating auxin-dependent cell divisionPlant Cell1725272541PubMedCrossRefGoogle Scholar
  82. Martienssen, R. 1997The origin of maize branches outNature386443, 445PubMedCrossRefGoogle Scholar
  83. Martinez, M.C., Jorgensen, J.E., Lawton, M.A., Lamb, C.J., Doerner, P.W. 1992Spatial pattern of cdc2 expression in relation to meristem activity and cell proliferation during plant developmentProc. Natl. Acad. Sci. U.S.A8973607364PubMedGoogle Scholar
  84. Meyerowitz, E.M. 1997Genetic control of cell division patterns in developing plantsCell88299308PubMedCrossRefGoogle Scholar
  85. Mizukami, Y., Fischer, R.L. 2000Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesisProc. Natl. Acad. Sci. U.S.A97942947PubMedCrossRefGoogle Scholar
  86. Nakagami, H., Kawamura, K., Sugisaka, K., Sekine, M., Shinmyo, A. 2002Phosphorylation of retinoblastoma-related protein by the cyclin D/cyclin-dependent kinase complex is activated at the G1/S-phase transition in tobaccoPlant Cell1418471857PubMedCrossRefGoogle Scholar
  87. Nath, U., Crawford, B.C., Carpenter, R., Coen, E. 2003Genetic control of surface curvatureScience29914041407PubMedCrossRefGoogle Scholar
  88. Nougarede, A. 1967Experimental cytology of the shoot apical cells during vegetative growth and floweringInt. Rev. Cytol.21203351PubMedCrossRefGoogle Scholar
  89. Nougarede, A., Francis, D., Rondet, P. 1991Location of the cell cycle changes in relation to morphological changes in the shoot apex in the Silene coeli-rosa immediately before sepal initiationProtoplasma165110CrossRefGoogle Scholar
  90. Nougarede, A., Rembur, J. 1978Variations of the cell cycle phases in the shoot apex of Chrysnthemum segetum LZ. Pflanzenphysiol. Bd.S379389Google Scholar
  91. Nougarede, A., Rembur, J., Saint-Come, R. 1987Rates of cell division in the young prefloral shoot apex of Chrysanthemum segetum LProtoplasma138156160CrossRefGoogle Scholar
  92. Nougarede, A., Rembur, J. 1977Determination of the cell cycle and DNA synthesis duration in the shoot apex of the Chrysanthemum segetum L. by double-labelling autoradiographic techniqueZ. Pflanzenphysiol. Bd.81283295Google Scholar
  93. Nowack, M.K., Grini, P.E.,  et al. 2006A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesisNat. Genet.386367PubMedGoogle Scholar
  94. Ohno, C.K., Reddy, G.V., Heisler, M.G., Meyerowitz, E.M. 2004The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue developmentDevelopment13111111122PubMedCrossRefGoogle Scholar
  95. Ormenese, S., Almeida Engler, J., Groodt, R., Veylder, L., Inze, D., Jacqmard, A. 2004Analysis of the spatial expression pattern of seven Kip- related proteins (KRPs) in the shoot apex of Arabidopsis thaliana Ann. Bot. (Lond)93575580CrossRefGoogle Scholar
  96. Palatnik, J.F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J.C., Weigel, D. 2003Control of leaf morphogenesis by microRNAsNature425257263PubMedCrossRefGoogle Scholar
  97. Ramirez-Parra, E., Lopez-Matas, M.A., Frundt, C., Gutierrez, C. 2004Role of an atypical E2F transcription factor in the control of Arabidopsis cell growth and differentiationPlant Cell1623502363PubMedCrossRefGoogle Scholar
  98. Reddy, G.V., Meyerowitz, E.M. 2005Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apexScience310663667PubMedCrossRefGoogle Scholar
  99. Rembur, J., Nougarede, A. 1977Duration of cell cycles in the shoot apex of Chrysanthemum segetum LZ. Pflanzenphysiol. Bd.S173179Google Scholar
  100. Riou-Khamlichi, C., Huntley, R., Jacqmard, A., Murray, J.A. 1999Cytokinin activation of Arabidopsis cell division through a D-type cyclinScience28315411544PubMedCrossRefGoogle Scholar
  101. Rupp, H.M., Frank, M., Werner, T., Strnad, M., Schmulling, T. 1999Increased steady state mRNA levels of the STM and KNAT1 homeobox genes in cytokinin overproducing Arabidopsis thaliana indicate a role for cytokinins in the shoot apical meristemPlant J.18557563PubMedCrossRefGoogle Scholar
  102. Satina, S., Blakenlee, A.F., Avery, A.G. 1940Demonstration of the three germ layers in the shoot apex of Datura by means of induced polyploidy in the periclinal chimerasAm. J. Bot.27895905CrossRefGoogle Scholar
  103. Satina, S., Blakenlee, A.F., Avery, A.G. 1941Periclinal chimeras in Datura stramonium in relation to development of leaf and flowersAm. J. Bot.28862871CrossRefGoogle Scholar
  104. Schnittger, A., Weinl, C., Bouyer, D., Schobinger, U., Hulskamp, M. 2003Misexpression of the cyclin-dependent kinase inhibitor ICK1/KRP1 in single-celled Arabidopsis trichomes reduces endoreduplication and cell size and induces cell deathPlant Cell15303315PubMedCrossRefGoogle Scholar
  105. Shimotohno, A., Umeda-Hara, C., Bisova, K., Uchimiya, H., Umeda, M. 2004The plant-specific kinase CDKF;1 is involved in activating phosphorylation of cyclin-dependent kinase-activating kinases in Arabidopsis Plant Cell1629542966PubMedCrossRefGoogle Scholar
  106. Shpak, E.D., Berthiaume, C.T., Hill, E.J., Torii, K.U. 2004Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferationDevelopment13114911501PubMedCrossRefGoogle Scholar
  107. Smith, L.G., Greene, B., Veit, B., Hake, S. 1992A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fatesDevelopment1162130PubMedGoogle Scholar
  108. Sorrell, D.A., Marchbank, A., McMahon, K., Dickinson, J.R., Rogers, H.J., Francis, D. 2002A WEE1 homologue from Arabidopsis thaliana Planta215518522PubMedCrossRefGoogle Scholar
  109. Steeves, T.A. and Sussex, I.M. 1989. Pattern in plant development, Cambridge University PressGoogle Scholar
  110. Suchomelova, P., Velgova, D., Masek, T., Francis, D., Rogers, H.J., Marchbank, A.M., Lipavska, H. 2004Expression of the fission yeast cell cycle regulator cdc25 induces de novo shoot formation in tobacco: evidence of a cytokinin-like effect by this mitotic activatorPlant Physiol. Biochem.424955PubMedCrossRefGoogle Scholar
  111. Suzuki, T., Sakurai, K., Ueguchi, C., Mizuno, T. 2001Two types of putative nuclear factors that physically interact with histidine-containing phosphotransfer (Hpt) domains, signaling mediators in His-to-Asp phosphorelay, in Arabidopsis thaliana Plant Cell Physiol.423745PubMedCrossRefGoogle Scholar
  112. Swaminathan, K., Yang, Y., Grotz, N., Campisi, L., Jack, T. 2000An enhancer trap line associated with a D-class cyclin gene in Arabidopsis Plant Physiol.12416581667PubMedCrossRefGoogle Scholar
  113. Szymkowiak, E.J., Sussex, I.M. 1996What chimeras can tell us about plant developmentAnnu. Rev. Plant Physiol. Plant Mol. Biol.47351376PubMedCrossRefGoogle Scholar
  114. Tatematsu, K., Ward, S., Leyser, O., Kamiya, Y., Nambara, E. 2005Identification of cis-elements that regulate gene expression during initiation of axillary bud outgrowth in Arabidopsis Plant Physiol.138757766PubMedCrossRefGoogle Scholar
  115. Tepfer, S.S., Nougarede, A., Rondet, P. 1981Seasonal studies of vegetative buds of Helianthus tuberosus: concentration of nuclei in phase G1 during winter dormancy.Can. J. Bot.5919181927Google Scholar
  116. Torii, K.U., Mitsukawa, N., Oosumi, T., Matsuura, Y., Yokoyama, R., Whittier, R.F., Komeda, Y. 1996The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeatsPlant Cell8735746PubMedCrossRefGoogle Scholar
  117. Tremousaygue, D., Garnier, L., Bardet, C., Dabos, P., Herve, C., Lescure, B. 2003Internal telomeric repeats and ‘TCP domain’ protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cellsPlant J.33957966PubMedCrossRefGoogle Scholar
  118. Tsiantis, M., Hay, A. 2003Comparative plant development: the time of the leaf?Nat. Rev. Genet.4169180PubMedCrossRefGoogle Scholar
  119. Uemukai, K., Iwakawa, H., Kosugi, S., Uemukai, S., Kato, K., Kondorosi, E., Murray, J.A., Ito, M., Shinmyo, A., Sekine, M. 2005Transcriptional activation of tobacco E2F is repressed by co-transfection with the retinoblastoma-related protein: cyclin D expression overcomes this repressor activityPlant Mol. Biol.5783100PubMedCrossRefGoogle Scholar
  120. Vandepoele, K., Vlieghe, K., Florquin, K., Hennig, L., Beemster, G.T., Gruissem, W., Peer, Y., Inze, D., Veylder, L. 2005Genome-wide identification of potential plant E2F target genesPlant Physiol.139316328PubMedCrossRefGoogle Scholar
  121. Vroemen, C.W., Mordhorst, A.P., Albrecht, C., Kwaaitaal, M.A., Vries, S.C. 2003The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis Plant Cell1515631577PubMedCrossRefGoogle Scholar
  122. Wang, G., Kong, H., Sun, Y., Zhang, X., Zhang, W., Altman, N., DePamphilis, C.W., Ma, H. 2004Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteinsPlant Physiol.13510841099PubMedCrossRefGoogle Scholar
  123. Wang, H., Fowke, L.C., Crosby, W.L. 1997A plant cyclin-dependent kinase inhibitor geneNature386451452PubMedCrossRefGoogle Scholar
  124. Wang, H., Qi, Q., Schorr, P., Cutler, A.J., Crosby, W.L., Fowke, L.C. 1998ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acidPlant J.15501510PubMedCrossRefGoogle Scholar
  125. Wardlaw, C.W. 1957On the organization and reactivity of the shoot apex in vascular plantsAm. J. Bot.44176185CrossRefGoogle Scholar
  126. Weir, I., Lu, J., Cook, H., Causier, B., Schwarz-Sommer, Z., Davies, B. 2004CUPULIFORMIS establishes lateral␣organ boundaries in Antirrhinum Development131915922PubMedCrossRefGoogle Scholar
  127. Wyrzykowska, J., Pien, S., Shen, W.H., Fleming, A.J. 2002Manipulation of leaf shape by modulation of cell divisionDevelopment129957964PubMedGoogle Scholar
  128. Yanai, O., Shani, E., Dolezal, K., Tarkowski, P., Sablowski, R., Sandberg, G., Samach, A., Ori, N. 2005 Arabidopsis KNOXI proteins activate cytokinin biosynthesisCurr. Biol.1515661571PubMedCrossRefGoogle Scholar
  129. Yokoyama, R., Takahashi, T., Kato, A., Torii, K.U., Komeda, Y. 1998The Arabidopsis ERECTA gene is expressed in the shoot apical meristem and organ primordiaPlant J.15301310PubMedCrossRefGoogle Scholar
  130. Zhang, K., Diederich, L., John, P.C. 2005The cytokinin requirement for cell division in cultured Nicotiana plumbaginifolia cells can be satisfied by yeast Cdc25 protein tyrosine phosphatase: implications for mechanisms of cytokinin response and plant developmentPlant Physiol.137308316PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  1. 1.Department of Cell and Developmental BiologyJohn Innes CentreNorwichUK

Personalised recommendations