Actin-dependent vacuolar occupancy of the cell determines auxin-induced growth repression

Abstract

The cytoskeleton is an early attribute of cellular life, and its main components are composed of conserved proteins. The actin cytoskeleton has a direct impact on the control of cell size in animal cells, but its mechanistic contribution to cellular growth in plants remains largely elusive. Here, we reveal a role of actin in regulating cell size in plants. The actin cytoskeleton shows proximity to vacuoles, and the phytohormone auxin not only controls the organization of actin filaments but also impacts vacuolar morphogenesis in an actindependent manner. Pharmacological and genetic interference with the actin-myosin system abolishes the effect of auxin on vacuoles and thus disrupts its negative influence on cellular growth. SEMbased 3D nanometer-resolution imaging of the vacuoles revealed that auxin controls the constriction and luminal size of the vacuole. We show that this actin-dependent mechanism controls the relative vacuolar occupancy of the cell, thus suggesting an unanticipated mechanism for cytosol homeostasis during cellular growth.auxin | vacuole | actin cytoskeleton | cell growth

Wortmannin-induced vacuole fusion enhances amyloplast dynamics in Arabidopsiszigzag1hypocotyls

“…Contact sites between plant subcellular organelles have been identified by electron microscopy or laser trapping, including between ER and plasma membrane (summarized in Staehelin, 1997), ER and endosomes (Stefano et al , 2015), and ER and Golgi (Sparkes et al , 2009). The vacuole has also been shown in tight association with the cytoskeleton (Scheuring et al , 2016) and the ER (Staehelin, 1997), and the latter may provide an anchoring system that may be important to regulate amyloplast sedimentation. Future analysis by electron microscopy in shoot endodermal cells may provide further support for these contact sites.…”

Auxin and ROP GTPase Signaling of Polar Nuclear Migration in Root Epidermal Hair Cells

“…Since actin organization impacts vacuole morphology in late meristematic cells (Scheuring et al, 2016), we addressed whether vacuole morphology would be strongly altered in act7-6, as observed for nuclear mispositioning in elongated trichoblasts. Strikingly, however, the mean vacuole size between the wild type and act7-6 did not differ significantly in elongating trichoblasts, although vacuole size in the act7-6 mutant was somewhat more variable than in the wild type (Supplemental Fig.…”

Auxin and Cellular Elongation

“…High doses of auxin induce smaller luminal vacuoles, which are required for the negative impact of auxin on cellular elongation (Löfke et al, 2015). This growth mechanism appears to rely on the vacuolar occupancy of the cell (Scheuring et al, 2016), suggesting that the vacuole has a space-filling function during cellular growth Löfke et al, 2015). Vacuolar morphogenesis is also highly dynamic in tip-growing cells (Hicks et al, 2004).…”

“…Vacuolar morphogenesis is also highly dynamic in tip-growing cells (Hicks et al, 2004). Intriguingly, processes that are required for auxin-dependent vacuolar morphogenesis, including vacuolar SNARES, phosphatidylinositol 4-kinases (Löfke et al, 2015), as well as actin and myosins (Scheuring et al, 2016), are also implicated in root hair expansion (Ringli et al, 2002;Preuss et al, 2006;Park and Nebenführ, 2013;Larson et al, 2014). Hence, it is tempting to speculate that vacuoles may also be important cellular effectors contributing to root hair expansion.…”