Trends in Plant Science
Volume 9, Issue 12, December 2004, Pages 583-590
Journal home page for Trends in Plant Science

Cell shape development in plants

https://doi.org/10.1016/j.tplants.2004.10.006Get rights and content

The shape of a plant cell has long been the cornerstone of diverse areas of plant research but it is only recently that molecular-genetic and cell-biological tools have been effectively combined for dissecting plant cell morphogenesis. Increased understanding of the polar growth characteristics of model cell types, the availability of many morphological mutants and significant advances in fluorescent-protein-aided live-cell visualization have provided the major impetus for these analyses. The cytoskeleton and its regulators have emerged as essential components of the scaffold involved in fabricating plant cell shape. In this article, I collate information from recent discoveries to derive a simple cytoskeleton-based operational framework for plant cell morphogenesis.

Section snippets

Shape changes result from changing the growth focus of a cell

Differential growth is best studied in easily accessible cell types such as epidermal pavement cells and leaf trichomes 7, 8, stomatal guard cells [9], root-hair cells [10], elongating pollen tubes [11] and differentiating tracheids [12], which allow experimental manipulation and can be studied in pertinent morphological mutants. Although the final shapes of these model cells differ greatly, they do share a common growth mechanism [7]. Based on the area over which growth is spread during the

Cytoskeletal elements during differential growth

In higher plants, amongst all other cellular components, the two major cytoskeleton elements actin microfilaments and microtubules 11, 13 appear to play a decisive role in the shape-determining process. Treatment of plant cells with cytoskeleton-interacting drugs has been particularly helpful in developing this view and has allowed particular changes in cell morphology to be linked to altered activity of specific cytoskeletal proteins 13, 14, 15, 16, 17, 18. The following general observations

Cortical weakening can trigger the growth process

The previous roles attributed to actin and microtubules during cell morphogenesis need to be reassessed so that we can assimilate the observations made above into a coherent operational framework that addresses how growth can be targeted to a region of the cell to make it grow differently from other regions. The observation that all plant cells initially possess a regular shape suggests an even distribution of intracellular resources and the growth machinery at this developmental stage.

Reinforcement of weak cortical sites and fixation of growth directionality requires microtubules

A continuous stream of signals feeding into the actin-mesh-loosening mechanism can potentially extend cortical weakening to the entire cell surface. A general release of growth materials by vesicles in the expanding weak region would ultimately produce an isodiametric cell shape (Figure 3). Because this does not usually happen, the further weakening of the cortex must obviously be curtailed at some stage for growth to become localized. Activation of actin-bundling proteins might counteract the

Conclusions and perspectives

Molecular-genetic and cell-biological evidence of cell morphogenesis strongly suggests that localized growth occurs as a cellular response to combat regional weakening of the cortex. The weakening is created by a localized increase in cortical actin dynamics. Polar growth directionality becomes fixed once endoplasmic microtubules approach the weak actin mesh and both reinforce it and establish the concurrence of both cytoskeletal elements at the particular cortical location. All

Acknowledgements

I thank Alice Cheung, Nancy Dengler, Patrick Hussey, Thomas Berleth, Peter Hepler and Marie-Theres Hauser for their critical comments and suggestions on the ideas presented here, and Takashi Hashimoto for sharing prepublication details.

References (81)

  • U. Mayer et al.

    Microtubule cytoskeleton: a track record

    Curr. Opin. Plant Biol.

    (2002)
  • F. Baluska

    Root hair formation: F-actin dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges

    Dev. Biol.

    (2000)
  • T. Ketelaar

    The actin-interacting protein AIP1 is essential for actin organization and plant development

    Curr. Biol.

    (2004)
  • J. Le

    Requirements for Arabidopsis AtARP2 and AtARP3 during epidermal development

    Curr. Biol.

    (2003)
  • S. El-Assal

    Arabidopsis GNARLED encodes a NAP125 homolog that positively regulates ARP2/3

    Curr. Biol.

    (2004)
  • M.J. Deeks

    Arabidopsis NAP1 is essential for ARP2/3-dependent trichome morphogenesis

    Curr. Biol.

    (2004)
  • M.J. Frank et al.

    A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells

    Curr. Biol.

    (2002)
  • M.J. Deeks et al.

    Arp2/3 and ‘the shape of things to come’

    Curr. Opin. Plant Biol.

    (2003)
  • J. Mathur

    A novel localization pattern for an EB1-like protein links microtubule dynamics to endomembrane organization

    Curr. Biol.

    (2003)
  • A.S.N. Reddy

    A novel plant calmodulin-binding protein with a kinesin heavy chain motor domain

    J. Biol. Chem.

    (1996)
  • M. Surpin et al.

    Traffic jams affect plant development and signal transduction

    Nat. Rev. Mol. Cell Biol.

    (2004)
  • S. Gilroy et al.

    Signal processing and transduction in plant cells: the end of the beginning?

    Nat. Rev. Mol. Cell Biol.

    (2001)
  • M. Hülskamp

    Plant trichomes: a model for cell differentiation

    Nat. Rev. Mol. Cell Biol.

    (2004)
  • R.J. Carol et al.

    Building a hair: tip growth in Arabidopsis thaliana root hairs

    Philos. Trans. R. Soc. London B. Biol. Sci.

    (2002)
  • P.K. Hepler

    Polarized cell growth in higher plants

    Annu. Rev. Cell Dev. Biol.

    (2001)
  • H. Fukuda

    Signals that control plant vascular cell differentiation

    Nat. Rev. Mol. Cell Biol.

    (2004)
  • G.O. Wasteneys et al.

    Remodeling the cytoskeleton for growth and form: an overview with some new views

    Annu. Rev. Plant Biol.

    (2003)
  • T.N. Bibikova

    Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana

    Plant J.

    (1999)
  • J. Mathur et al.

    Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes

    Plant Cell

    (2000)
  • D.B. Szymanski

    Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis

    Plant Cell

    (1999)
  • J. Mathur

    The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana

    Development

    (1999)
  • J. Mathur

    Simultaneous visualization of peroxisome and cytoskeletal elements reveals actin and not microtubule-based peroxisome motility in plants

    Plant Physiol.

    (2002)
  • J. Mathur

    Arabidopsis CROOKED encodes for the smallest subunit of the ARP2/3 complex and controls cell shape by region specific fine F-actin formation

    Development

    (2003)
  • D.G. Oppenheimer

    Essential role of a kinesin-like protein in Arabidopsis trichome morphogenesis

    Proc. Natl. Acad. Sci. U. S. A.

    (1997)
  • A.T. Whittington

    MOR1 is essential for organizing cortical microtubules in plants

    Nature

    (2001)
  • V. Kirik

    The Arabidopsis TUBULIN-FOLDING COFACTOR A gene is involved in the control of the alpha/beta-tubulin monomer balance

    Plant Cell

    (2002)
  • D. Twell

    MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast

    Nat. Cell Biol.

    (2002)
  • S. Thitamadee

    Microtubule basis for left-handed helical growth in Arabidopsis

    Nature

    (2002)
  • T. Abe

    Microtubule defects and cell morphogenesis in the lefty1lefty2 tubulin mutant of Arabidopsis thaliana

    Plant Cell Physiol.

    (2004)
  • K. Nakajima

    SPIRAL1 encodes a plant specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells

    Plant Cell

    (2004)
  • Cited by (0)

    View full text