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Review
. 2015 Jan 8;5:786.
doi: 10.3389/fpls.2014.00786. eCollection 2014.

Organization and Regulation of the Actin Cytoskeleton in the Pollen Tube

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Free PMC article
Review

Organization and Regulation of the Actin Cytoskeleton in the Pollen Tube

Xiaolu Qu et al. Front Plant Sci. .
Free PMC article

Abstract

Proper organization of the actin cytoskeleton is crucial for pollen tube growth. However, the precise mechanisms by which the actin cytoskeleton regulates pollen tube growth remain to be further elucidated. The functions of the actin cytoskeleton are dictated by its spatial organization and dynamics. However, early observations of the distribution of actin filaments at the pollen tube apex were quite perplexing, resulting in decades of controversial debate. Fortunately, due to improvements in fixation regimens for staining actin filaments in fixed pollen tubes, as well as the adoption of appropriate markers for visualizing actin filaments in living pollen tubes, this issue has been resolved and has given rise to the consensus view of the spatial distribution of actin filaments throughout the entire pollen tube. Importantly, recent descriptions of the dynamics of individual actin filaments in the apical region have expanded our understanding of the function of actin in regulation of pollen tube growth. Furthermore, careful documentation of the function and mode of action of several actin-binding proteins expressed in pollen have provided novel insights into the regulation of actin spatial distribution and dynamics. In the current review, we summarize our understanding of the organization, dynamics, and regulation of the actin cytoskeleton in the pollen tube.

Keywords: ADF; actin; actin-binding protein; fimbrin; formin; pollen tube; villin.

Figures

FIGURE 1
FIGURE 1
Spatial distribution of actin filaments in the pollen tube. (A) Schematic showing the spatial distribution of actin filaments in the pollen tube. At the apex, actin filaments are less abundant. In the subapical region, actin filaments form the regular actin collar structure. In the shank region, actin filaments are axially packed into cables, termed longitudinal actin cables. These actin structures are believed to perform distinct functions. Longitudinal actin cables provide the molecular tracks for movement of large organelles and vesicles from the base to the tip. The organelles and vesicles reverse direction at the subapical region and return to the base via the middle of the pollen tube, giving rise to the reverse-fountain cytoplasmic streaming pattern. These large organelles never enter the tip, resulting in the formation of the optical smooth zone at the tip referred to as the “clear zone”. However, this region is filled with small vesicles. Therefore, actin filaments at the apical region are believed to be important for vesicle targeting and fusion events. The black arrows indicate the direction of cytoplasmic streaming. (B) Spatial distribution of ARA7-positive vesicles and RabA4b-positive vesicles in pollen tubes. ARA7-positive vesicles do not invade the apical region, whereas RabA4b-positive vesicles enter the apical region. Scale bar = 10 μm. (C) ABD2-GFP decorates longitudinal actin cables. Scale bar = 10 μm. (D) Actin filaments in Arabidopsis pollen tubes were revealed by decoration with Lifeact-mEGFP. Images showing the cortical plane, the middle plane, and a projection of a representative pollen tube are presented. Actin filaments in the shank region, subapical region, and apical region are indicated by green dots, yellow dots, and red dots, respectively. Scale bar = 10 μm.
FIGURE 2
FIGURE 2
Actin dynamics in the pollen tube. (A) Actin filaments are constantly generated from the apical membrane within the apical dome. The images presented are maximally projected time-lapse images. Emerging individual actin filaments are marked by two dots of the same color. Yellow triangles indicate the origination of actin polymerization events, and movement of the filaments from the apex to the apical flank is indicated by orange arrows. Images are a higher magnification of the boxed region of the whole pollen tube shown in the far right panel. Scale bars = 4 μm. (B) Corresponding single optical slices of images shown in (A) allowing clear visualization of single actin filament dynamics. Actin filaments are highlighted by two dots of the same color. Red arrows indicate filament elongation events, green arrows indicate filament shrinking events, and white scissors indicate severing events. Scale bar = 4 μm. (C) Schematic describing the dynamics of actin filaments within the apical dome. Figure adapted from Qu et al. (2013).With the permission from American Society of Plant Biologists (www.plantcell.org). For a detailed description, see the associated text and Qu et al. (2013). 1, 2, and 3 mark actin filaments that were nucleated from the membrane at the extreme apex, that moved from apex to the apical flank, and that were nucleated from the membrane at the apical flank, respectively. (D,E) Dynamic formation of actin bundles in the shank region. (D) Filament debundling events. Yellow dots highlight actin bundles that split into two bundles highlighted with red dots and green dots. The bundle marked by red dots is subjected to severing (indicted by scissors) and depolymerization. Images are a higher magnification of the boxed region shown in the far right panel. (E) Bundling event. Actin filaments marked by green dots and red dots were brought together via “zipping” to form the larger bundle indicated by yellow dots. Scale bars = 4 μm.
FIGURE 3
FIGURE 3
Schematic describing the regulation of actin dynamics in the pollen tube based on the functional characterization of ABPs derived mainly from Arabidopsis. (A) Intracellular localization of several ABPs in the pollen tube. For methods used to determine the localization of FIMBRIN5, ADF7, and VILLIN5, see descriptions in previous studies ( Wu et al., 2010; Qu et al., 2013; Zheng et al., 2013). Scale bar = 10 μm. (B) Schematic describing the intracellular localization and function of various ABPs in the pollen tube. For detailed information regarding the intracellular localization and function of each ABP, see the description in the text.

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