Transmembrane formins as active cargoes of membrane trafficking

Abstract

Formins are a large, evolutionarily old family of cytoskeletal regulators whose roles include actin capping and nucleation, as well as modulation of microtubule dynamics. The plant class I formin clade is characterized by a unique domain organization, as most of its members are transmembrane proteins with possible cell wall-binding motifs exposed to the extracytoplasmic space-a structure that appears to be a synapomorphy of the plant kingdom. While such transmembrane formins are traditionally considered mainly as plasmalemma-localized proteins contributing to the organization of the cell cortex, we review, from a cell biology perspective, the growing evidence that they can also, at least temporarily, reside (and in some cases also function) in endomembranes including secretory and endocytotic pathway compartments, the endoplasmic reticulum, the nuclear envelope, and the tonoplast. Based on this evidence, we propose that class I formins may thus serve as 'active cargoes' of membrane trafficking-membrane-embedded proteins that modulate the fate of endo- or exocytotic compartments while being transported by them.

Keywords: Actin; biotic interactions; cell growth; cytokinesis; endocytosis; exocytosis; formin; microtubules; plasmalemma; tonoplast.

Fig. 1.

A simplified formin phylogeny with distribution of documented or suspected membrane trafficking-related functions. The schematic FH2 domain tree is based on Pruyne (2017), with only plant, fungal, and major metazoan formin clades labelled. Clades shown in grey correspond to major formin groups found only outside opisthokonts and plants. Branch length is not to scale. Note that the topology of relationships between major clades often lacks statistical support.

Fig. 2.

Modes of plasmalemma expansion and targeted secretion discussed in this review. (A) Plasmalemma expansion during cell growth and division. (B) Targeted secretion during biotic interactions. Destinations of exocytosis, coinciding with areas of vigorous plasmalemma turnover that correspond to activated cortical domains sensuŽárský et al. (2009), are highlighted. (B) is in part based on Rae et al. (2021).

Fig. 3.

Phylogenetic distribution of cell expansion- and membrane trafficking-related roles of class I formins. The schematic FH2 domain tree is based on previous reports (Cvrčková et al., 2004; Li et al. 2017; van Gisbergen et al., 2018; Liang et al. 2021). Highlighted branches correspond to evolutionarily conserved clades within the class I formin family; only formins discussed in this review are shown individually. Branch length is not to scale.

Fig. 4.

Endomembrane localization of Arabidopsis class I formin AtFH1. A spinning disc confocal microscopy section of the primary root elongation zone rhizodermis from a seedling expressing biologically active GFP-tagged AtFH1 in the genetic background of the fh1:CRISPR loss-of-function mutant (Cifrová et al., 2020) shows an overlap of several localization patterns found along the developmental gradient of the root tip. For expression construct description, transformation procedure, culture conditions, and imaging methods, see Oulehlová et al. (2019).

Fig. 5.

Proposed models of the role of class I formins in endomembrane dynamics. (A) The dock–ship model. (B) The active cargo hypothesis—an example of a non-processive vesicle-borne formin that steers its compartment’s movement by nucleating short actin filaments. The figure includes an anonymous drawing of a docked boat from Wikimedia Commons (https://commons.wikimedia.org/wiki/File:PSF_Q-740001.png; public domain), and an image of a towed Chinese ship by John Gray, 1878; both drawings are from OpenClipart.org and licenced under the Creative Commons Zero 1.0.