Skip to main content
SpringerLink
Log in

Developmental control of cell division patterns in the shoot apex

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The shoot apical meristem is a group of rapidly dividing cells that generate all aerial parts of the plant. It is a highly organised structure, which can be divided into functionally distinct domains, characterised by specific proliferation rates of the individual cells. Genetic studies have enabled the identification of regulators of meristem function. These factors are involved in the formation and maintenance of the meristem, as well as in the formation of the primordia. Somehow, they must also govern cell proliferation rates within the shoot apex. Possible links between meristem regulators and the cell cycle machinery will be discussed. In order to analyse the role of cell proliferation in development, cell cycle gene expression has been perturbed using transgenic approaches and mutation. The effect of these alterations on growth and development at the shoot apex will be presented. Together, these studies give a first insight into the regulatory networks controlling the cell cycle and into the significance of cell proliferation in plant development.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aida, M., Ishida, T. Fukaki, H., Fujisawa, H. and Tasaka, M. 1997. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9: 841–857.

    PubMed  Google Scholar 

  • Aida, M., Ishida, T. and Tasaka, M. 1999. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interactions among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126: 1563–1570.

    PubMed  Google Scholar 

  • Bai, C., Sen, P., Hofmann, K., Ma, L., Goebl, M., Harper, J.W. and Elledge, S.J. 1996. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86: 263–274.

    PubMed  Google Scholar 

  • Barton M.K. and Poethig, R.S. 1993. Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild-type and the shoot meristemless mutant. Development 119: 823–831.

    Google Scholar 

  • Chuck, G., Lincoln, C. and Hake, S. 1996. KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant cell 8: 1277–1289.

    PubMed  Google Scholar 

  • Clark, S.E., Running, M.P. and Meyerowitz, E.M. 1993. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119: 397–418.

    PubMed  Google Scholar 

  • Clark, S.E., Running, M.P. and Meyerowitz, E.M. 1995. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same process as CLAVATA1. Development 121: 2057–2067.

    Google Scholar 

  • Clark, S.E., Jacobsen, S.E., Levin, J.Z. and Meyerowitz, E.M. 1996. The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122: 1567–1575.

    PubMed  Google Scholar 

  • Clark, S.E., Williams, R.W. and Meyerowitz, E.M. 1997. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89: 575–585.

    PubMed  Google Scholar 

  • Cleary, A.L. and Smith, L.G. 1998. The TANGLED1 gene is required for spatial control of cytoskeletal arrays associated with cell division during maize leaf development. Plant Cell 10: 1875–88.

    PubMed  Google Scholar 

  • Doerner, P., Jorgensen, J.E., You, R., Steppuhn, J. and Lamb, C.1996. Control of root growth and development by cyclin overexpression. Nature 308: 520–523.

    Google Scholar 

  • Doonan, J.H. 1998. Cell division during floral morphogenesis in Antirrhinum majus. In: D. Francis, D. Dudits and D. Inzé (Eds.) Plant Cell Division, Portland Press, London, pp. 207–222.

    Google Scholar 

  • Doonan, J.H. and Fobert, P. 1997. Conserved and novel regulators of the plant cell cycle. Curr. Opin. Cell Biol. 9: 824–839.

    PubMed  Google Scholar 

  • Elliott, R.C., Betzner, A.S., Huttner, E., Oakes, M.P., Tucker, W.Q.J., Gerentes, D., Perez, P. and Smith, D. R. 1996. AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8: 155–168.

    PubMed  Google Scholar 

  • Endrizzi, K., Moussian, B., Haecker, A., Levin, J. and Laux, T. 1996. The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristem and acts at a different level than the meristem genes WUSCHEL and ZWILLE. Plant J. 10: 967–979.

    PubMed  Google Scholar 

  • Evans, M.M.S. and Barton, M.K. 1997. Genetics of angiosperm shoot apical meristem development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 673–701.

    PubMed  Google Scholar 

  • Fleming, A.J., McQueen-Mason, S., Mandel, T. and Kuhlemeier, C.1997. Induction of leaf primordia by the cell wall protein expansin. Science 276: 1415–1418.

    Google Scholar 

  • Fletcher, J.C., Brand, U., Running, M.P., Simon, R. and Meyerowitz, E.M. 1999. Signaling of cell fate decision by CLAVATA3 in Arabidopsis shoot meristem. Science 283: 1911–1914.

    PubMed  Google Scholar 

  • Foard, D.E. 1971. The initial protrusion of a leaf primordium can form without concurrent periclinal cell divisions. Can. J. Bot. 49: 694–702.

    Google Scholar 

  • Fobert, P.R., Coen, E.S., Murphy, G.J.P. and Doonan, J.H. 1994. Patterns of cell division revealed by transcriptional regulation of genes during the cell cycle in plants. EMBO J. 13: 616–624.

    PubMed  Google Scholar 

  • Fobert, P.R., Gaudin, V., Lunness, P., Coen, E.S. and Doonan, J. H. 1996. Distinct classes of cdc2-related genes are differentially expressed during the cell division cycle in plants. Plant Cell 8:1465–1476.

    PubMed  Google Scholar 

  • Hemerly, A., Ferreira, P., de Almeida Engler, J., Van Montagu, M., Engler, G. and Inzé, D. 1993. cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5: 1711–1723.

    Article  PubMed  Google Scholar 

  • Hemerly, A., de Almeida Engler, J., Bergounioux, C., Van Montagu, M., Engler, G., Inzé, D. and Ferreira, P. 1995. Dominant negative mutant of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J. 14: 3925–3936.

    PubMed  Google Scholar 

  • Ingram, G.C., Goodrich, J., Wilkinson, M.D., Simon, R. Haughn, G.W. and Coen, E.S. 1995. Parallels between UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum. Plant Cell 7: 1501–1510.

    PubMed  Google Scholar 

  • Ingram, G.C., Doyle, S., Carpenter, R., Schultz, E.A., Simon, R. and Coen, E. S. 1997. Dual role for FIMBRIATA in regulating floral homeotic genes and cell division in Antirrhinum. EMBO J. 16: 6521–6534.

    PubMed  Google Scholar 

  • Johnston, L.A. 1998. Uncoupling growth from the cell cycle. Bioessays 20: 283–286.

    PubMed  Google Scholar 

  • Kayes, J.M. and Clark, S.E. 1998. CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125: 3843–3851.

    PubMed  Google Scholar 

  • Kiyokawa, H., Kineman, R., Manova-Todorova, K., Soares, V., Hoffman, E., Ono, M. Khanam, D, Hayday, A., Frohman, L. and Koff, A. 1996. Enhanced growth of mice lacking the cyclin dependent kinase inhibitor function of p27 (kip1) Cell 31: 721–732

    Google Scholar 

  • Kerstetter, R.A., Laudencia-Chingcuanco, D., Smith, L.G. and Hake, S. 1997. Loss-of-function mutation in the maize homeobox gene, KNOTTED1, are defective in shoot meristem maintenance. Development 124: 3045–3054.

    PubMed  Google Scholar 

  • Klucher, K., Chow, H., Reiser, L. and Fischer, R. 1996. The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8: 137–153.

    PubMed  Google Scholar 

  • Laufs, P., Grandjean, O., Jonak, C., Kieu, K. and Traas, J. 1998a. Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 10: 1375–1390.

    PubMed  Google Scholar 

  • Laufs, P., Jonak, C. and Traas, J. 1998b. Cells and domains: two views of the shoot meristem in Arabidopsis. Plant Physiol. Biochem. 36: 33–45.

    Google Scholar 

  • Laux, T. and Juergens G. 1997. Embryogenesis: a new start in life. Plant Cell 9: 989–1000.

    PubMed  Google Scholar 

  • Laux, T., Mayer, K.F.X., Berger, J. and Juergens, G. 1996. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122: 87–96.

    PubMed  Google Scholar 

  • Lee, I., Wolf, D.S., Nilsson, O. and Weigel, D. 1997. A LEAFY coregulator encoded by UNUSUAL FLORAL ORGANS. Curr. Biol. 7: 95–104.

    PubMed  Google Scholar 

  • Lenhard, M. and Laux, T. 1999. Shoot meristem formation and maintenance. Curr. Opin. Plant Biol. 2: 44–50.

    PubMed  Google Scholar 

  • Levin, J.Z. and Meyerowitz, E.M. 1995. UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell 7: 529–548.

    PubMed  Google Scholar 

  • Leyser, H.M.O. and Furner, I.J. 1992. Characterization of three shoot apical meristem mutants of Arabidopsis thaliana. Development 116: 397–403.

    Google Scholar 

  • Leyser, H.M., Lincoln, C.A., Timpte, C., Lammere, D., Turner, J. and Estelle, M. 1993. Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364: 161–164.

    Article  PubMed  Google Scholar 

  • Lincoln, C., Long, J., Yamagushi, J., Serikawa, K. and Hake, S. 1994. A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6: 1859–1876.

    PubMed  Google Scholar 

  • Long, J.A., Moan, E.I., Medford, J.I. and Barton, M.K. 1996. A member of the KNOTTED class of homeo-domain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66–69.

    PubMed  Google Scholar 

  • Long J.A., Barton M.K. 1998. The development of apical embryonic pattern in Arabidopsis. Development 125: 3027–3035.

    PubMed  Google Scholar 

  • Lyndon, R.F. 1998. The Shoot Apical Meristem: Its Growth and Development, Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Martinez, M.C., Jorgensen, J.-E., Lawton, M.A., Lamb, C.J. and Doerner, P.W. 1992. Saptial pattern of cdc2 expression in relation to meristem activity and cell proliferation during plant development. Proc. Natl. Acad. Sci. USA 89: 7360–7364.

    PubMed  Google Scholar 

  • Mayer, K.F.X., Schoof, H., Haecker, A., Lenhard, M., Juergens, G. and Laux, T. 1998. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95: 805–815.

    PubMed  Google Scholar 

  • Medford, J.I. 1992. Vegetative apical meristem. Plant Cell 4: 1029–1039.

    Article  PubMed  Google Scholar 

  • Meyerowitz, E. M. 1997. Genetic control of cell division patterns in developing plants. Cell 88: 299–308.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Nakagami, H., Sekine, M., Murakami, H. and Shinmyo A. 1999. Tobacco retinoblastoma-related protein phosphorylated by a distinct cyclin-dependent kinase complex with Cdc2/cyclin D in vitro. 18: 243–252.

    Google Scholar 

  • Nougarède, A. 1968. Experimental cytology of the shoot apical cells during vegetative growth and flowering. Int. Rev. Cytol. 21: 203–351.

    Google Scholar 

  • Parcy F., Nilsson O., Busch M.A., Lee I. and Weigel D. 1998. A genetic framework for floral patterning. Nature 395: 561–566.

    PubMed  Google Scholar 

  • Reinhardt D., Wittwer F., Mandel T., Kuhlemeier C. 1998. Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem. Plant Cell 10: 1427–1437.

    PubMed  Google Scholar 

  • Rinne, P.L.H. and van der Schoot, C. 1998. Symplastic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125: 1477–1485.

    PubMed  Google Scholar 

  • Riou-Khamlichi, C., Huntley, R., Jacqmard, A. and Murray, J.A., 1999. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544.

    PubMed  Google Scholar 

  • Sherr, C. J. 1994. G1 phase progression: cycling on cue. Cell 18: 551–555.

    Google Scholar 

  • Simon, R., Carpenter, R., Doyle, S. and Coen, E. 1994. FIMBRIATA controls flower development bymediating between meristem and floral organ identity genes. Cell 78: 99–107.

    Article  PubMed  Google Scholar 

  • Sinha, N.R., Williams, R.E. and Hake, S. 1993. Overexpression of the maize homeobox gene KNOTTED1, causes a switch from determinate to indeterminate cell fates. Genes Dev. 7: 787–795.

    PubMed  Google Scholar 

  • Sinha, N. 1999. Leaf development in angiosperms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 419–446.

    PubMed  Google Scholar 

  • Smith, L.G., Greene, B., Veit, B. and Hake, S. 1992. A dominant mutation of in the maize homeobox gene, KNOTTED1, causes its ectopic expression in leaf-cells with altered fates. Development 116: 21–30.

    PubMed  Google Scholar 

  • Smith, L.G., Hake, S. and Sylvester A.W. The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development 122: 481–489.

  • Soni, R., Carmichael, J.P., Shah, Z.H. and Murray, J.A.H. 1995. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7: 85–103.

    Article  PubMed  Google Scholar 

  • Souer, E., van Houwelingen, A., Kloos, D., Mol, J. and Koes, R. 1996. The NO APICAL MERISTEM gene of petunia is required for pattern formation in embryos and flowers and expressed at meristem and primordia boundaries. Cell 85: 159–170.

    PubMed  Google Scholar 

  • Stone, J.M., Trotochaud, A.E., Walker, J.C. and Clark, S.E. 1998. control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions. Plant Physiol. 117: 1217–1225.

    PubMed  Google Scholar 

  • Steeves, T.A. and Sussex, I.M. 1989. Patterns in Plant Development. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Stewart, R.N. and Dermen, H. 1975. Flexibility in ontogeny as shown by the contribution of the shoot apical layers to leaves of periclinal chimeras. Am. J. Bot. 62: 935–947.

    Google Scholar 

  • Su, T.T. and O'Farrell, P.H. 1998. Size control: cell proliferation does not equal growth. Curr. Biol. 248: 687–689.

    Google Scholar 

  • Szymkowiak, E.J. and Sussex, I.M. 1996.What chimeras can tell us about plant development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 351–376.

    PubMed  Google Scholar 

  • Traas, J., Bellini, C., Nacry, P., Kronenberger, J., Bouchez, D. and Caboche, M. 1995. Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375: 676–677.

    Google Scholar 

  • Traas, J. and Laufs, P. 1997. Cell cycle mutants in higher plants: a phenotypical overview. In: D. Francis, D. Dudits and D. Inzé (Eds.) Plant Cell Division, Portland Press, London, pp. 319–336.

    Google Scholar 

  • Trotochaud, A.E., Hao, T., Wu, G., Yang, Z. and Clark, S.E. 1999. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signalling complex that includes KAPP and a rho-related protein. Plant Cell 11: 393–405.

    PubMed  Google Scholar 

  • van der Schoot, C. and Rinne, P. 1999. Networks for shoot design. Trends Plant Sci. 4: 31–37.

    PubMed  Google Scholar 

  • Vollbrecht, E., Veit, B., Sinha, N. and Hake, S. 1991. The developmental gene KNOTTED1 is a member of a maize homeobox gene family. Nature 350: 241–243.

    PubMed  Google Scholar 

  • Weigel, D., Alvarez, J., Smith, D.R., Yanofsky, M.F. and Meyerowitz, E.M. 1992. LEAFY controls floral meristem identity in Arabidopsis. Cell 69: 843–859.

    Article  PubMed  Google Scholar 

  • Weigmann K., Cohen S.M. and Lehner C.F. 1997. Cell cycle progression, growth and patterning in imaginal discs despite inhibition of cell division after inactivation of Drosophila Cdc2 kinase. Development 124: 3555–3563.

    PubMed  Google Scholar 

  • Weinberg, R. 1995. The retinoblastoma protein and cell cycle control. Cell 81: 323–330

    Article  PubMed  Google Scholar 

  • Wilkinson, M.D. and Haughn, G.W. 1995. UNUSUAL FORAL ORGANS controls meristem identity and organ primordia fate in Arabidopsis. Plant Cell 7: 1485–1499.

    Article  PubMed  Google Scholar 

  • Williams, R.W., Wilson, J.M. and Meyerowitz, E.M. 1997. A possible role for kinase-associated protein phosphatase in Arabidopsis CLAVATA1 signaling pathway. Proc. Natl. Acad. Sci. USA 94: 10467–10472.

    PubMed  Google Scholar 

  • Xie, Q., Sanz-Burgos, A.P., Hannon, G.J. and Gutiérrez, C. 1996. Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO J. 15: 4900–4908.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Biologie Cellulaire, I.N.R.A., Route de Saint Cyr, 78026, Versailles cedex, France

    Teva Vernoux, Daphné Autran & Jan Traas

Authors
  1. Teva Vernoux
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daphné Autran
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jan Traas
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vernoux, T., Autran, D. & Traas, J. Developmental control of cell division patterns in the shoot apex. Plant Mol Biol 43, 569–581 (2000). https://doi.org/10.1023/A:1006464430936

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006464430936

Search

Navigation