Formins: Linking Cytoskeleton and Endomembranes in Plant Cells

Abstract

The cytoskeleton plays a central part in spatial organization of the plant cytoplasm, including the endomebrane system. However, the mechanisms involved are so far only partially understood. Formins (FH2 proteins), a family of evolutionarily conserved proteins sharing the FH2 domain whose dimer can nucleate actin, mediate the co-ordination between actin and microtubule cytoskeletons in multiple eukaryotic lineages including plants. Moreover, some plant formins contain transmembrane domains and participate in anchoring cytoskeletal structures to the plasmalemma, and possibly to other membranes. Direct or indirect membrane association is well documented even for some fungal and metazoan formins lacking membrane insertion motifs, and FH2 proteins have been shown to associate with endomembranes and modulate their dynamics in both fungi and metazoans. Here we summarize the available evidence suggesting that formins participate in membrane trafficking and endomembrane, especially ER, organization also in plants. We propose that, despite some methodological pitfalls inherent to in vivo studies based on (over)expression of truncated and/or tagged proteins, formins are beginning to emerge as candidates for the so far somewhat elusive link between the plant cytoskeleton and the endomembrane system.

Division of Labor Between Two Actin Nucleators—the Formin FH1 and the ARP2/3 Complex—in Arabidopsis Epidermal Cell Morphogenesis

“…Binding of formins to microtubules has been documented also in plants (Deeks et al, 2010;Li et al, 2010;Yang et al, 2011;Wang et al, 2013). Some formins are associated with membranes and modulate endomembrane dynamics (see Gurel et al, 2014;Cvrčková et al, 2014). Typical plant Class I formins are transmembrane proteins that can anchor cytoskeletal structures to the plasmalemma, its distinct domains, and/or endomembranes (e.g., Deeks et al, 2010;Martinière et al, 2011;Diao et al, 2018;Oulehlová et al, 2019).…”

HLB1 Is a Tetratricopeptide Repeat Domain-Containing Protein That Operates at the Intersection of the Exocytic and Endocytic Pathways at the TGN/EE in Arabidopsis

“…Many of these proteins, such as the ARP2/3 complex, profilin, formins, and capping proteins, which localize to the PM and various membranes of organelles within the endomembrane system, have orthologs in other eukaryotes (Zhang et al, 2010Sun et al, 2013;Jimenez-Lopez et al, 2014;Cvr cková et al, 2015). In fact, some of the mechanisms by which F-actin on membranes is nucleated and polymerized in plants mirror those of animals and yeast, where small GTPases of the Rho family directly activate membrane-localized actin nucleators (Takenawa and Suetsugu, 2007).…”

Arabidopsis Class II Formins AtFH13 and AtFH14 Can Form Heterodimers but Exhibit Distinct Patterns of Cellular Localization

“…Formins are an evolutionarily ancient family of proteins [10][11][12] that can nucleate, cap, and bundle actin filaments, but also bind microtubules, resulting in an ability to modulate actin and microtubule organization and dynamics [7,9], well documented also in plants [8,[25][26][27]. Angiosperm plants possess two clades of formins whose members often exhibit characteristic domain organization.…”

“…While Class I formins are usually, though not always, integral membrane proteins [11,28], their Class II counterparts often harbor an N-terminal domain related to the mammalian PTEN (phosphatase and tensin homolog) lipid/protein phosphatase that was proposed to mediate membrane binding [11] and later shown to be responsible for membrane association and specific intracellular localization of Class II formins in the moss Physcomitrella patens [19,24] and in rice [21]. Thus, typical formins of both Class I and Class II are capable of membrane localization (reviewed in References [25,29]). In case of Class I formins, plasmalemma or endomembrane localization, as well as cytoskeletal, especially microtubule, association is well documented (e.g., References [6,[30][31][32][33][34][35]).…”