Microtubule cortical array organization and plant cell morphogenesis
Introduction
Plant cell growth is achieved by cell wall expansion that is driven by high internal pressure, or turgor. To acquire specific shapes that are important for cell function and organized multicellular development, the cell wall has to yield to uniformly applied internal pressure in a non-uniform, or anisotropic, pattern. Plant cell morphogenesis is influenced by both the microtubule and actin cytoskeletal networks and the signaling mechanisms that control their organization. Interphase microtubule cortical arrays assume a variety of configurations that vary by cell type and shape. In cells that are destined to undergo rapid axial elongation, such as those in the root axis or the etiolated hypocotyl, the cortical array assumes a high degree of order, with polymers lying roughly in parallel to each other and oriented transversely or obliquely relative to the cell axis [1]. By contrast, in highly lobed pavement cells, there is no global orientation of microtubules but rather local and periodic patches of parallel polymers that are correlated with the sinuses of the undulating cell perimeter [2••]. It is likely that basic mechanisms for the creation of cortical array organization apply in all cell types, and that modifications and variations of these mechanisms operate in cells that have specialized shape. The molecular mechanisms by which cortical microtubule patterns are established and maintained are not yet known, but new insights are arriving from a combination of genetic, biochemical, and live-cell-imaging studies.
What are the functions of the plant cortical microtubule array? In 1962, Paul Green [3] reported that colchicine, a drug known to disrupt the fibers in mitotic spindles, caused uniform swelling of algal cells and loss of cell wall birefringence as measured by polarization microscopy. He hypothesized that colchicine-sensitive fibers were somehow responsible for organizing the direction in which the major structural polymers in the cell wall were deposited, the orientation of these wall fibers being the basis of the material anisotropy responsible for the direction of cell wall expansion. A year later, Ledbetter and Porter [4] observed the first cortical microtubules in plant cells, noting that they lay just under the plasma membrane and were often parallel to each other, and coining the name ‘microtubule’ because of their annular appearance in cross section. These authors and others observed that microtubules were often parallel to fibers in the cell wall [5, 6], supporting Green's original idea. Many studies with both drugs and mutants have supported the microfibril guidance hypothesis (reviewed in [7]), but microtubule orientation and cellulose orientation can become uncoupled [7, 8], and cellulose microfibrils can be laid down in a parallel fashion without an intact cortical array [9]. These observations suggest that the function of microtubules in cell wall organization might be more complicated than simple one-on-one guidance of cellulose orientation. Here, we review recent progress in our understanding of interphase cortical microtubule organization and the function of this array in building the cell wall and regulating cell wall expansion pattern.
Section snippets
Cortical microtubule nucleation
Most current evidence suggests that interphase microtubules are first polymerized then organized into the cortical array. In the course of normal root axis development, microtubules appear at the cortex of post-mitotic cells in random orientations before the array attains a high degree of order. Likewise, when cortical microtubules are depolymerized with drugs then allowed to recover, the array is initially disorganized and gradually regains an ordered appearance, showing that microtubules are
Visualization of dynamic cellulose synthase
As described in the introduction to this review, it is proposed that cortical array organization is important because it guides the deposition of cell wall cellulose microfibrils, thus generating material anisotropy in the cell wall that is the basis for directional cell expansion during turgor-driven growth. Although parallelism between microtubules and cellulose has long been noted [7], the uncoupling of these polymer arrays has also been observed [9]. A limitation to understanding the true
Conclusions
The plant cortical microtubule array is emerging as a dynamic structure in which individual polymers are constantly being destroyed, rebuilt and repositioned by polymer treadmilling. Dynamic polymers can assemble into bundles to form more stable elements of the cortical array that are required to perform work required for cell morphogenesis, such as localization and guidance of cellulose synthase. The mechanisms by which particular array structures are created, how the microtubules and actin
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
The authors would like to thank Jordi Chan and Clive Lloyd and R Malcolm Brown Jr for sharing data before publication, and Clive Lloyd, Malcom Brown, Herman Höfte, Andrew Staehelin, Sid Shaw, Tim Stearns, Chris Somerville and John Sedbrook for stimulating discussions about microtubule organization and cellulose biosynthesis.
References (59)
- et al.
A new spring for plant cell biology: microtubules as dynamic helices
Trends Biochem Sci
(1985) - et al.
Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis
Cell
(2005) Microtubule-organizing centers in higher plants: evolving concepts
Bot Acta
(1995)- et al.
Gamma-tubulin is essential for microtubule organization and development in Arabidopsis
Plant Cell
(2006) - et al.
Interactions of tobacco microtubule-associated protein MAP65-1b with microtubules
Plant J
(2004) - et al.
How the geometrical model for plant cell wall formation enables the production of a random texture
Cellulose
(2004) - et al.
Developing prolamine protein bodies are associated with the cortical cytoskeleton in rice endosperm cells
Planta
(2000) Mechanism for plant cell morphogenesis
Science
(1962)- et al.
A ‘microtubule’ in plant cell fine structure
J Cell Biol
(1963) - et al.
The cytoskeleton underlying side walls and cross walls in plants: molecules and macromolecular assemblies
J Cell Sci Suppl
(1985)