A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes

Abstract

Tip growth in neuronal cells, plant cells, and fungal hyphae is known to require tip-localized Rho GTPase, calcium, and filamentous actin (F-actin), but how they interact with each other is unclear. The pollen tube is an exciting model to study spatiotemporal regulation of tip growth and F-actin dynamics. An Arabidopsis thaliana Rho family GTPase, ROP1, controls pollen tube growth by regulating apical F-actin dynamics. This paper shows that ROP1 activates two counteracting pathways involving the direct targets of tip-localized ROP1: RIC3 and RIC4. RIC4 promotes F-actin assembly, whereas RIC3 activates Ca2+ signaling that leads to F-actin disassembly. Overproduction or depletion of either RIC4 or RIC3 causes tip growth defects that are rescued by overproduction or depletion of RIC3 or RIC4, respectively. Thus, ROP1 controls actin dynamics and tip growth through a check and balance between the two pathways. The dual and antagonistic roles of this GTPase may provide a unifying mechanism by which Rho modulates various processes dependent on actin dynamics in eukaryotic cells.

A RHOse by any other name: a comparative analysis of animal and plant Rho GTPases

“…A growing body of evidence also points to ROP as a key player in the generation of cell polarity in plant cell growth and morphogenesis. ROPs have been shown to regulate polar growth and cell morphogenesis in several cell systems including pollen tubes, developing root hairs, and leaf pavement cells [46][47][48][49][50][51][52][53][54].…”

“…Apart from the conserved actin nucleation mechanisms, ROPs might regulate a novel mechanism for the assembly of the actin cytoskeleton [47,50]. Evidence indicates that ROP1 activates the assembly of a dynamic form of tip-localized actin microfilaments required for pollen tube growth [49].…”

“…In Arabidopsis, the RIC family comprises 11 members, which based on sequence similarity can be sorted into five subfamilies based on sequence similarity [84]. RIC's function has been studied in two model systems: pollen tubes [50] and leaf pavement cells [47]. ROP1 regulates pollen tube growth through coordination of two counteracting pathways: activation of RIC4 promotes assembly of apical F-actin in the pollen tube tip, whereas activation of RIC3 leads to disassembly of the apical F-actin through a Ca 2+ -dependent process [50].…”

“…RIC's function has been studied in two model systems: pollen tubes [50] and leaf pavement cells [47]. ROP1 regulates pollen tube growth through coordination of two counteracting pathways: activation of RIC4 promotes assembly of apical F-actin in the pollen tube tip, whereas activation of RIC3 leads to disassembly of the apical F-actin through a Ca 2+ -dependent process [50]. In turn, these two pathways appear to provide positive (RIC4) or negative (RIC3) feedback signaling to ROP1, leading to an oscillation of ROP1 activity at the pollen tube tip that is correlated with tip growth oscillation [85].…”

Deciphering the Possible Mechanism of GABA in Tobacco Pollen Tube Growth and Guidance

“…The tip growth of pollen tubes is a complex system, 16 requiring the participation of multiple signal molecules, such as the Rac/Rop protein, [17][18][19] F-actin, 20 mitogen-activated protein kinase (MAPK), 21 calmodulin-like domain protein kinase (CDPK) 22 and the 14-3-3 protein, 23 which are all involved in the growth and orientation of pollen tubes. New data are providing valuable clues to decipher the role of GABA in this intricate signaling network and its possible connection with the signal components.…”