On growth and formins

Abstract

Development of the plant aerial organs epidermis involves a complex interplay of cytoskeletal rearrangements, membrane trafficking-dependent cell surface expansion, and intra-and intercellular signaling, resulting in a pattern of perfectly interlocking pavement cells. While recent detailed in vivo observations convincingly identify microtubules rather than actin as key players at the early stages of development of pavement cell lobes in Arabidopsis, mutations affecting the actin-nucleating ARP2/3 complex are long known to reduce pavement cell lobing, suggesting a central role for actin. We have now shown that functional impairment of the Arabidopsis formin FH1 enhances both microtubule dynamics and pavement cell lobing. While formins are best known for their ability to nucleate actin, many members of this old gene family now emerge as direct or indirect regulators of the microtubule cytoskeleton, and our findings suggest that they might co-ordinate action of the two cytoskeletal systems during pavement cell morphogenesis.Abbreviations: ABP1, auxin binding protein 1; ARP2/3, actin-related proteins 2 and 3; DAG, days after germination; FH1, formin homolog 1; FH2, formin homology domain 2; FH17, formin homolog 17; ICR1, interactor of constitutively active ROPs 1; PIN, pin-formed; PTEN, phosphatase and tensin homolog; RIC, RHO-interacting CRIB; RHO, RAS homolog; ROP, RHO of plants; SMIFH2, small molecule inhibitor of FH2

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

“…Unless the effects of the fh1 mutation differ between trichomes and pavement cells, a possible explanation of the apparent paradox is that increased microtubule mobility in fh1 mutants may promote generation of transient microtubular structures required for branch initiation, while microtubule stabilization increases the lifetime of such structures. This would be consistent with our hypothesis explaining increased pavement cell lobing in fh1 mutants by enhanced generation of microtubule bundles at future pavement cell lobe necks (Cvrčková et al, 2016). Additional observations, focusing on cytoskeletal dynamics during early stages of trichome ontogeny, are needed to test this hypothesis.…”

“…Arabidopsis mutants with impaired actin nucleation commonly exhibit altered pavement cell shape and size (e.g. Li et al, 2003;Mathur et al, 2003a;Mathur et al, 2003b;El-Assal et al, 2004;Basu et al, 2004;Basu et al, 2005;Rosero et al, 2016;Sahi et al, 2018;Oulehlová et al, 2019), again consistent with microfilaments contributing to early microtubule rearrangements that establishes the lobe layout (compare Cvrčková et al, 2016), albeit cytoskeletal organization and dynamics during early pavement cell development in these mutants remains to be characterized.…”

“…At the first glance, the observed effects of actin nucleator impairment on the cytoskeletal organization and dynamics were not mirrored in cell shape properties in the double fh1 arpc5 mutants. Microtubules, which are essential for pavement cell lobe and trichome branch initiation, are more dynamic in fh1 mutants and thus prone to re-organize more readily into structures that establish the layout of a complex cell shape (Rosero et al, 2016;Cvrčková et al, 2016). In the double mutants the microtubule cytoskeleton is as dynamic as in single fh1 mutants but resulting cell shapes are less complex, resembling instead single arpc5 mutants.…”

A new kymogram-based method reveals unexpected effects of marker protein expression and spatial anisotropy of cytoskeletal dynamics in plant cell cortex

“…Using static image analysis and manual tracking of filaments labeled with several different marker proteins, we have previously shown that fh1 mutants exhibit increased microfilament bundling and thus increased actin structure lifetime both in rhizodermis and in cotyledon pavement cells [25, 26], possibly as a consequence of weakening the trans-plasmalemma attachment of cortical microfilaments to the cell wall [48] that may allow for easier lateral movement and thus bundling of individual microfilaments [49]. QuACK analyses convincingly confirmed increased lifetime of actin structures in fh1 mutants.…”

Mapping and Functional Characterization of Stigma Exposed 1, a DUF1005 Gene Controlling Petal and Stigma Cells in Mungbean (Vigna radiata)

“…LOC100273612 and At4g29310 were annotated as formin-like protein 18 ( Figure 2D). Formin is an essential regulator of cytoskeleton and directly controls cell division and expansion (Cao et al, 2016;Cvrckova et al, 2016;Rosero et al, 2016). However, DUF1005 did not possess the basic FH2 (Formin Homology 2) domain of forminlike protein (Dominguez, 2009).…”