Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin

Abstract

Microtubules (MTs) and actin filaments (F-actin) function cooperatively to regulate plant cell morphogenesis. However, the mechanisms underlying the crosstalk between these two cytoskeletal systems, particularly in cell shape control, remain largely unknown. In this study, we show that introduction of the MyTH4-FERM tandem into KCBP (kinesin-like calmodulin-binding protein) during evolution conferred novel functions. The MyTH4 domain and the FERM domain in the N-terminal tail of KCBP physically bind to MTs and F-actin, respectively. During trichome morphogenesis, KCBP distributes in a specific cortical gradient and concentrates at the branching sites and the apexes of elongating branches, which lack MTs but have cortical F-actin. Further, live-cell imaging and genetic analyses revealed that KCBP acts as a hub integrating MTs and actin filaments to assemble the required cytoskeletal configuration for the unique, polarized diffuse growth pattern during trichome cell morphogenesis. Our findings provide significant insights into the mechanisms underlying cytoskeletal regulation of cell shape determination.DOI: http://dx.doi.org/10.7554/eLife.09351.001

Cytoskeleton dynamics control the first asymmetric cell division in Arabidopsis zygote

“…This role likely explains the absence of zygote elongation in the pilz mutant, which is deficient in MT assembly (28). Similar roles for MT rings have been observed in directionally elongating cells, such as fern protonema (29) and Arabidopsis trichome branches (30), suggesting that MT rings play a general role in defining the zone of apical growth. Because diverse species, including flowering plants and brown algae, have vertically elongated zygotes (31)(32)(33), similar polarization might be a general strategy of plant zygotes in contrast to most animal zygotes that undergo cell division in the absence of cell growth (34).…”

“…3F), which are general features of tipgrowing cells in various plant species (25,35,36). Because fern protonema elongates in tip-growing manner (29) and Arabidopsis trichome outgrows as polarized diffuse growth (30), it is intriguing to determine which manner is used in the zygote elongation. Because tip growth is an ancient mechanism observed in the gametophytes of bryophytes (37) and budding yeasts (38), it might be natural for the zygote, the origin of sporophytic cells, to use this machinery for the first polarization step to establish the body axis.…”

The IQD Family of Calmodulin-Binding Proteins Links Calcium Signaling to Microtubules, Membrane Subdomains, and the Nucleus

“…More than 300 CaMBPs are currently known, which include transporters and channels, metabolic enzymes, transcription factors, myosins, and various proteins of undefined functions that mostly interact with either holo-CaM or apo-CaM (Reddy et al, 2011). To date, only one CaM-binding MAP has been reported, KINESIN-LIKE CaM-BINDING PROTEIN/ ZWICHEL (KCBP/ZWI; Narasimhulu and Reddy, 1998), which functions in trichome development (Hülskamp et al, 1994;Oppenheimer et al, 1997;Tian et al, 2015) and root growth (Buschmann et al, 2015;Humphrey et al, 2015). During cell division, KCBP localizes to the cortical division zone and likely functions in phragmoplast guidance and in the spatial control of cytokinesis (Buschmann et al, 2015).…”

The Cytoskeleton and Its Regulation by Calcium and Protons

“…I also draw attention to recently published work showing that KCBP interacts with actin MFs as well as MTs (Tian et al, 2015). It has been known for some years that both MTs and MFs, as well as KCBP (Oppenheimer et al, 1997), participate in the control of trichome development.…”