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The integration of cell proliferation and growth in leaf morphogenesis

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Abstract

A number of recent publications have assessed the outcome on leaf development of targeted manipulation of cell proliferation. The results of these investigations have awakened interest in the long-standing debate in plant biology on the precise role of cell division in morphogenesis. Does cell proliferation drive morphogenesis (cell theory) or is it subservient to a mechanism which acts at the whole organ level to regulate morphogenesis (organismal theory)? In this review, the central role of growth processes (distinct from cell proliferation) in morphogenesis is highlighted and the limitations in our understanding of the basic mechanisms of plant growth control are highlighted. Finally, an attempt is made to demonstrate how sequential local co-ordination of growth might provide an interpretation of some of the recent observations on cell proliferation and leaf morphogenesis.

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References

  • Beemster GTS, Fiorani F, Inzé D (2003) Cell cycle: the key to plant growth control? Trends Plant Sci 8:154–158

    Article  PubMed  Google Scholar 

  • Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jürgens G, Friml J (2004) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  Google Scholar 

  • Bharathan G, Goliber T, Moore C, Kessler S, Pham T, Sinha NR (2002) Homologies in leaf form inferred from KNOXL gene expression during development. Science 296:1858–1860

    Article  PubMed  Google Scholar 

  • Byrne ME (2005) Networks in leaf development. Curr Opin Plant Biol 8:59–66

    Article  PubMed  Google Scholar 

  • Campanomi P, Nick P (2005) Auxin-dependent cell division and cell elongation. 1-naphthaleneacetic acid and 2,4-dichlorophenoxyacetic acid activate different pathways. Plant Physiol 137:939–948

    Article  PubMed  Google Scholar 

  • Chen J-G, Ullah H, Young JC, Sussman MR, Jones AM (2001) ABP1 Is required for organized cell elongation and division in Arabidopsis embryogenesis. Genes Dev 15:902–911

    Article  PubMed  Google Scholar 

  • Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326

    Article  PubMed  Google Scholar 

  • Curaba J, Herzog M, Vachon G (2003) GeBP, the first member of a new gene family in Arabidopsis, encodes a nuclear protein with DNA binding activity and is regulated by KNAT1. Plant J 33:305–317

    Article  PubMed  Google Scholar 

  • Dengler NG, Dengler RE, Kaplan DR (1982) The mechanism of plication inception in Palm leaves: histogenic observations on the pinnate leaf of Chryalidocarpus lutescens. Can J Bot 60:2976–2998

    Google Scholar 

  • Doonan J (2000) Social controls on cell proliferation in plants. Curr Opin Plant Biol 3:482–487

    Article  PubMed  Google Scholar 

  • De Veylder L, Beeckman T, Beemster GTS, Engler JD, Ormenese S, Maes S, Naudts M, Van der Schueren E, Jacqmard A, Engler G, Inzé 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, Beemster GTS, Krols L, Terras F, Landrieu I, Van Der Schueren E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1667

    Article  PubMed  Google Scholar 

  • Fingar DC, Salama S, Tsou C, Harlow E, Blenis J (2002) Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev 16:1472–1478

    Article  PubMed  Google Scholar 

  • Fleming AJ (2002). The mechanism of leaf morphogenesis. Planta 216:17–22

    PubMed  Google Scholar 

  • Folkers U, Kirik V, Scöbinger U, Falk S, Krishnakumar S, Pollock MA, Oppenheimer DG, Day I, Reddy AR, Jürgens G, Hülskamp M (2002) The cell morphogenesis gene ANGUSTOFOLIA encodes a CtBP/BARS-like protein and is involved in the control of the microtubule cytoskeleton. EMBO J 21:1280–1288

    Article  PubMed  Google Scholar 

  • Harrison CJ, Corley SB, Moylan EC, Alexander DL, Scotland RW, Langdale JA (2005) Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434:509–514

    Article  PubMed  Google Scholar 

  • Hay A, Kaur H, Phillips A, Hedden P, Hake S, Tsiantis M (2002) The gibberelin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol 12:1557–1565

    Article  PubMed  Google Scholar 

  • Inze D (2005) Green light for the cell cycle. EMBO J 24:657–662

    Article  PubMed  Google Scholar 

  • Kaplan DR (2001) Fundamental concepts of leaf morphology and morphogenesis: a contribution to the interpretation of molecular genetic mutants. Int J Plant Sci 162:465–474

    Article  Google Scholar 

  • Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–708

    Article  PubMed  Google Scholar 

  • Kim GT, Shoda K, Tsuge T, Cho K-H, Uchimiya H, Yokoyama R, Nishitani K, Tsukaya H (2002) The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement ofcortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. EMBO J 21:1267–1279

    Article  PubMed  Google Scholar 

  • Kim GT, Tsukaya H, Saito Y, Uchimaya H (1999) Changes in the shape of leaves and flowers upon overexpression of cytochrome P450 in Arabidopsis. Proc Natl Acad Sci USA 96:9433–9437

    Article  PubMed  Google Scholar 

  • Kim GT, Tsukaya H., Uchimaya H (1998) The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev 12:2381–2391

    PubMed  Google Scholar 

  • Lee Y, Choi D, Kende H. (2001) Expansins: ever expanding numbers and functions. Curr Opin Plant Biol 4:527–532

    Article  PubMed  Google Scholar 

  • McConnell, Emery J, Eshed Y, Bao, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713

    Article  PubMed  Google Scholar 

  • Meyerowitz EM (1996) Plant development: local control, global patterning. Curr Opin Genet Dev 6:475–479

    Article  PubMed  Google Scholar 

  • Mele G, Ori N, Sato Y, Hake S (2003) The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes Dev 17:2088–2093

    PubMed  Google Scholar 

  • Nath U, Crawford BCW, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299:1404–1407

    Article  PubMed  Google Scholar 

  • Nieuwland J, Feron R, Huisman BAH, Fasolino A, Hilbers CW, Derksen J, Mariani C (2005) Lipid transfer proteins enhance cell wall extension in tobacco. Plant Cell 17:2009–2019

    Article  PubMed  Google Scholar 

  • Nijhout HF (2003) The control of growth. Development 130:5863–5867

    Article  PubMed  Google Scholar 

  • Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof Y-D, Kleine-Vehn J, Morris DA, Emans N, Jurgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256

    Article  PubMed  Google Scholar 

  • Rudra D, Warner JR (2004) What better measure than ribosome synthesis? Genes Dev 18:243–2436

    Article  Google Scholar 

  • Tsiantis M, Hay A (2003) Comparative plant development: the time of the leaf? Nat Rev Genetics 4:169–180

    Article  Google Scholar 

  • Tsukaya H (2002) Interpretation of mutants in leaf morphology: genetic evidence for a compensatory system in leaf morphogenesis that provides a new link between cell and organismal theories. Int Rev Cytol 217:1–39

    PubMed  Google Scholar 

  • Tsukaya H (2003) Organ shape and size: a lesson from studies of leaf morphogenesis. Curr Opin Plant Biol 6:57–62

    Article  PubMed  Google Scholar 

  • Van Lijsebettens M, Vanderhaeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M (1994) An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J 13:3378–3388

    PubMed  Google Scholar 

  • Van Volkenburgh E (1999) Leaf expansion- am integrating plant behaviour. Plant Cell Environ 22:1463–1473

    Article  Google Scholar 

  • Veit B (2004) Determination of cell fate in apical meristems. Curr Opin Plant Biol 7:57–64

    Article  PubMed  Google Scholar 

  • Zrenner R, Salanoubat M, Willmitzer L, Sonnewald U. (1995) Evidence of a crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J 7:97–107

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Work in the author’s laboratory is funded by the BBSRC, Gatsby Foundation, the Swiss Federal Institute of Technology Zurich and the Swiss Federal Agency for Science and Education.

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Correspondence to Andrew J. Fleming.

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Fleming, A.J. The integration of cell proliferation and growth in leaf morphogenesis. J Plant Res 119, 31–36 (2006). https://doi.org/10.1007/s10265-005-0240-4

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  • DOI: https://doi.org/10.1007/s10265-005-0240-4

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