Arabidopsis Interdigitating Cell Growth Requires Two Antagonistic Pathways with Opposing Action on Cell Morphogenesis

Abstract

Coordinating growth and communication between adjacent cells is a critical yet poorly understood aspect of tissue development and organ morphogenesis. We report a Rho GTPase signaling network underlying the jigsaw puzzle appearance of Arabidopsis leaf pavement cells, in which localized outgrowth in one cell is coordinated with localized inhibition of outgrowth of the adjacent cell to form interdigitating lobes and indentations. Locally activated ROP2, a Rho-related GTPase from plants, activates RIC4 to promote the assembly of cortical actin microfilaments required for localized outgrowth. Meanwhile, ROP2 inactivates another target RIC1, whose activity promotes well-ordered cortical microtubules. RIC1-dependent microtubule organization not only locally inhibits outgrowth but in turn suppresses ROP2 activation in the indentation zones. Thus, outgrowth-promoting ROP2 and outgrowth-inhibiting RIC1 pathways antagonize each other. We propose that the counteractivity of these two pathways demarcates outgrowing and indenting cortical domains, coordinating a process that gives rise to interdigitations between adjacent pavement 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].…”

“…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]. The generation of the jigsaw puzzle-like shape of leaf pavement cells appears to be at least partly regulated by ROP-RIC signaling pathways [47]. RIC4 acts downstream of ROP2 and ROP4 to promote the assembly of cortical actin filaments in developing lobes, thus facilitating localized growth of these lobes.…”

Patterning of plant cell wall deposition by cortical microtubules

“…This mechanism is elegantly demonstrated in the morphogenesis of pavement cells in plants with a jigsaw-puzzle like appearance. Plasma membrane localized active ROP2 interacts with RIC4 to promote F-actin and thereby cell outgrowth, whereas ROP2-RIC1 promotes ordering of the microtubule array suppressing local cell growth 122 .…”