Microtubule cortical array organization and plant cell morphogenesis

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Plant cell cortical microtubule arrays attain a high degree of order without the benefit of an organizing center such as a centrosome. New assays for molecular behaviors in living cells and gene discovery are yielding insight into the mechanisms by which acentrosomal microtubule arrays are created and organized, and how microtubule organization functions to modify cell form by regulating cellulose deposition. Surprising and potentially important behaviors of cortical microtubules include nucleation from the walls of established microtubules, and treadmilling-driven motility leading to polymer interaction, reorientation, and microtubule bundling. These behaviors suggest activities that can act to increase or decrease the local level of order in the array. The SPIRAL1 (SPR1) and SPR2 microtubule-localized proteins and the radial swollen 6 (rsw-6) locus are examples of new molecules and genes that affect both microtubule array organization and cell growth pattern. Functional tagging of cellulose synthase has now allowed the dynamic relationship between cortical microtubules and the cell-wall-synthesizing machinery to be visualized, providing direct evidence that cortical microtubules can organize cellulose synthase complexes and guide their movement through the plasma membrane as they create the cell wall.

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.

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