Actin-Based Domains of the “Cell Periphery Complex” and their Associations with Polarized “Cell Bodies” in Higher Plants

Abstract

Nascent cellulosic cell wall microfibrils and transverse (with respect of cell growth axis) arrays of cortical microtubules (MTs) beneath the plasma membrane (PM) are two well established features of the periphery of higher plant cells. Together with transmembrane synthase complexes, they represent the most characteristic form of a “cell periphery complex” of higher plant cells which determines the orientation of the diffuse (intercalary) type of their cell growth. However, there are some plant cell types having distinct cell cortex domains which are depleted of cortical MTs. These particular cell cortex domains are, instead, typically enriched with components of the actin-based cytoskeleton. In higher plants, this feature is prominent at extending apices of two cell types displaying tip growth - pollen tubes and root hairs. In the latter cell type, highly dynamic F-actin meshworks accumulate at extending tips, and they appear to be critical for the apparently motile character of these subcellular domains. Importantly, tip growth of both root hairs and pollen tubes is immediately stopped when the most dynamic F-actin population is depolymerized with low levels of anti-F-actin drugs. Intriguingly, MTs of tip-growing plant cells are organized in the form of longitudinal arrays, throughout the cytoplasm, which interconnect the extending tips with the subapical nuclei. This suggests that actin-rich cell cortex domains polarize plant “cell bodies” represented by nucleus-MTs complexes. A similar polarization of “cell bodies” is typical of mitotic and cytokinetic plant cells. A further type of MT-depleted and actomyosin-enriched plant cell cortex domain comprises the plasmodesmata. Primary plasmodesmata are formed during cytokinesis as part of the myosin VIII-enriched callosic cell plates, representing “juvenile” forms of the plant “cell periphery complex”. In phylogenetic terms the association between F-actin and the PM may be considered for a more “primitive” form of cellular organization than does the association of cortical MTs with the PM. We hypothesize that the actin cytoskeleton is a natural partner of the PM in all eukaryotic cells. In most plant cells, however, it was replaced by a tubulin-based “cell periphery apparatus” which regulates, via still unknown mechanisms, the spatial deposition of nascent cellulosic microfibrils synthesized by PM-associated synthase complexes.

Abbreviations

AFs: actin filaments

ER: endoplasmic reticulum

MTs: microtubules

PM: plasma membrane

Key words

Actin - callose - cell cortex - cell plate - cytokinesis - microtubules - myosin - phragmoplast - plant “cell body” - plant cell polarity - plasmodesmata - tip growth

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Section Editor: T. Nagata