Plant Microtubules: Their Role in Growth and Development

Abstract

The close association of cortical microtubules with cell walls is a characteristic of immobile plant cells. In interphase, the cortical array helps organize the cell wall and before division is replaced by a narrower preprophase band that forecasts where the new cross‐wall will be attached after mitosis. The mitotic spindle is essentially similar to the general eukaryotic model but the lack of centrosomes at the poles means that the plant spindle looks different, having broader poles and reduced astral microtubules. During cytokinesis, the rigid cellulose‐rich wall does not contract inwards to separate the divided chromosomes; instead, a new cross‐wall is laid down by a ring of phragmoplast microtubules that expands outwards until it fuses with the parent wall at the site predicted by the preprophase band. In plants, microtubules therefore have a particularly direct connection with morphogenesis.

Key concepts:

  • Plant cells are immobile – their shape held by a cellulose‐rich cell wall.

  • The passive entry of water into the vacuole generates the turgor pressure that drives cell expansion.

  • The direction of cell expansion is regulated according to the way that inelastic cellulose microfibrils are oriented in the cell wall.

  • Cortical microtubules attached to the cytoplasmic face of the plasma membrane channel the movement of the enzyme complexes as they extrude cellulose microfibrils into the wall.

  • Plant microtubules are highly dynamic, moving by a modified form of treadmilling in which new tubulin subunits are added at one end, as other subunits are lost from the opposite end.

  • The cortical array of microtubules arises out of the self‐organization of microtubules that emerge from multiple, scattered nucleation sites.

  • The plane of cell division is forecast by the preprophase band. This transient, cortical structure contains microtubules, actin, endoplasmic reticulum and Golgi vesicles.

  • In higher plants, which have no centrioles, the mitotic spindle has broad poles and few astral microtubules.

  • The cytokinetic apparatus, the phragmoplast, is comprised of two interdigitating circlets of microtubules and actin filaments. Golgi vesicles are directed to the line of overlap to deposit the cell plate.

  • The new cross‐wall grows out centrifugally, like a ripple in a pond, until it contacts the parental wall previously marked by the preprophase band.

Keywords: cytoskeleton; microtubules; morphogenesis; cell cycle; preprophase band; cytokinesis

Figure 1.

The cell wall controls the direction of expansion. (a) The wall‐less cell (the protoplast) swells as a sphere and does not elongate. (b) When a cell wall is present, circumferentially wrapped cellulose microfibrils constrain the protoplast from expanding sideways. Adjacent turns of cellulose can, however, be separated, so that the cell expands perpendicularly to the orientation of the cellulose microfibrils.

Figure 2.

Model for the influence of microtubules on the orientation of cellulose biosynthesis. Cortical microtubules are attached to the plasma membrane by cross‐linking proteins; they are also bridged to each other by the microtubule‐associated protein, MAP65. Cellulose is synthesized from multienzyme complexes that sit in the plasma membrane's lipid bilayer in the form of hexagonal rosettes. Cellulose microfibrils are extruded from these rosettes; this drives the rosettes along the fluid membrane in lanes provided by the underlying microtubules. Credit: P Huey, Science. From Lloyd C (2006) Microtubules make tracks for cellulose. Science312: 1482–1483.

Figure 3.

The microtubule cycle in tobacco suspension cells. (a) Fluorescently labelled cortical microtubules wrap around the cortex of an interphase cell. Here they form an oblique array. They can also be longitudinal but in elongating cells they tend to be transverse. (b) The cortical microtubules are beginning to ‘bunch‐up’ to form the preprophase band that predicts the division plane, where the cell plate will attach to the parental wall after mitosis. (c) In metaphase, the cortical microtubules have depolymerized. The spindle is barrel‐shaped without centrosomes at the spindle poles and without astral microtubules. (d) In cytokinesis, the phragmoplast, which contains mirror‐image sets of microtubules, deposits vesicles at the dark line along its equator. These vesicles contain complex oolysaccharides more flexible than the cellulose microfibrils that will strengthen the wall when mature. The disc‐like cell plate expands outwards until it contacts the parental wall at the site forecast by the preprophase band. Photographs from Henrik Buschmann.

Figure 4.

Division in vacuolated cells. During preprophase, the cell constructs a cytoplasmic raft across vacuolated cells. The nucleus is held in the centre of this raft, which is called the phragmosome. Radial strands containing microtubules and actin filaments connect the nucleus to the cortex. At the cortex, the division plane is predicted by the preprophase band, which also contains microtubules and actin filaments. Therefore, both radial and cortical cytoskeletal structures of the phragmosome initially define the plane in which the cell will divide. Perpendicular to this is the spindle axis marked by polar strands and polar caps of various antigens, such as γ‐tubulin.

Figure 5.

The phragmoplast. (a) The phragmoplast is a double circle of short microtubules whose circumference increases as it deposits a central disc – the cell plate. (b) Seen from above, the circular phragmoplast grows outwards (centrifugally) until the cell plate fuses with the parental cell wall at the site predicted by the preprophase band in the run‐up to division. (c) Phragmoplast microtubules are oppositely directed, with both sets of fast‐growing (‘plus’) ends directed to the midline. Actin filaments run parallel with the microtubules. Vesicles derived from the Golgi apparatus move along these cytoskeletal elements and fuse at the midline to form the cell plate, which grows outwards at its edge.

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Further Reading

Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annual Review of Cell and Developmental Biology 21: 203–222.

Chan J, Calder G, Fox S and Lloyd C (2007) Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nature Cell Biology 9: 171–175.

Dixit R and Cyr R (2004) Encounters between dynamic cortical microtubules promotes ordering of the cortical array through angle‐dependent modifications of microtubule behavior. Plant Cell 16: 3274–3284.

Ehrhardt D and Shaw SL (2006) Microtubule dynamics and organization in the plant cortical array. Annual Review of Plant Biology 57: 859–875.

Jürgens G (2005) Cytokinesis in higher plants. Annual Review of Plant Biology 56: 281–299.

Lloyd CW and Chan J (2006) Not so divided: the common basis of plant and animal mitosis. Nature Reviews. Molecular Cell Biology 7: 147–152.

Murata T, Sonobe S, Baskin TI et al. (2005) Microtubule‐dependent microtubule nucleation based on recruitment of γ‐tubulin in higher plants. Nature Cell Biology 7: 961–968.

Paredez AR, Somerville CR and Ehrhardt D (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312: 1491–1495.

Segui‐Simarro JM, Austin JR, White EA and Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high‐pressure freezing. Plant Cell 16: 836–856.

Van Damme D and Geleen D (2008) Demarcation of the cortical division zone in dividing plant cells. Cell Biology International 32: 178–187.

Walker KL, Muller S, Moss D, Ehrhardt DW and Smith LG (2007) Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Current Biology 17: 1827–1836.

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How to Cite close
Lloyd, Clive W(Sep 2009) Plant Microtubules: Their Role in Growth and Development. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001685.pub2]