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. 2012 Aug 24:3:188.
doi: 10.3389/fpls.2012.00188. eCollection 2012.

Bundling actin filaments from membranes: some novel players

Clément Thomas  1
Affiliations

Bundling actin filaments from membranes: some novel players

Clément Thomas. Front Plant Sci. .

Abstract

Progress in live-cell imaging of the cytoskeleton has significantly extended our knowledge about the organization and dynamics of actin filaments near the plasma membrane of plant cells. Noticeably, two populations of filamentous structures can be distinguished. On the one hand, fine actin filaments which exhibit an extremely dynamic behavior basically characterized by fast polymerization and prolific severing events, a process referred to as actin stochastic dynamics. On the other hand, thick actin bundles which are composed of several filaments and which are comparatively more stable although they constantly remodel as well. There is evidence that the actin cytoskeleton plays critical roles in trafficking and signaling at both the cell cortex and organelle periphery but the exact contribution of actin bundles remains unclear. A common view is that actin bundles provide the long-distance tracks used by myosin motors to deliver their cargo to growing regions and accordingly play a particularly important role in cell polarization. However, several studies support that actin bundles are more than simple passive highways and display multiple and dynamic roles in the regulation of many processes, such as cell elongation, polar auxin transport, stomatal and chloroplast movement, and defense against pathogens. The list of identified plant actin-bundling proteins is ever expanding, supporting that plant cells shape structurally and functionally different actin bundles. Here I review the most recently characterized actin-bundling proteins, with a particular focus on those potentially relevant to membrane trafficking and/or signaling.

Keywords: LIM proteins; SCAB1; THRUMIN1; V-ATPases; actin bundling; fimbrins; formins; villins.

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Figures

Figure 1
Figure 1
Main reactions controlling actin filament dynamics and organization in plant cells. The G-actin monomer binding protein profilin inhibits spontaneous actin nucleation in the cytoplasm. Nucleation is promoted de novo (1) by nucleating proteins such as formins. In addition, non-processive formins, such as Arabidopsis AtFH1, can also induce nucleation from the side of pre-existing filaments, a process which likely contributes to the initiation of actin bundles (not illustrated; Michelot et al., ; Blanchoin et al., 2010). Following nucleation, actin filaments undergo fast polymerization (2) and (2′) before being capped (3). The aging section of actin filaments (which contains ADP-loaded actin subunits, not shown) is fragmented by severing proteins such as actin-depolymerizing factors (4). The resulting fragments can be capped at their barbed end and depolymerize from their pointed (−) end to replenish the pool of monomers (5). Alternatively, they can re-elongate through polymerization (5′) although this process rarely occurs immediately following severing, suggesting intense barbed end capping activity (Staiger et al., 2009). Finally, actin fragments can serve as building blocks to assemble novel filaments by an end-joining mechanism (5″). Actin filaments are crosslinked into bundles by bundling proteins (right part of the cartoon). Both in vitro and live cell TIRFM-based analyses support that actin bundles form by a “catch and zipper” mechanism (6) (Khurana et al., 2010). Actin bundles subsequently grow by elongation of filaments at their ends (7) as well as by end-association of pre-existing filaments (7′), a process which might be facilitated by bundling proteins. Like single filaments, actin bundles are severed although at a lower frequency (Khurana et al., ; Smertenko et al., 2010). Current data support that unipolar bundles (here-exemplified) predominate in plant cells. However, the existence of bundles containing actin filaments of mixed polarity is not excluded.
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