Cell polarity signaling in Arabidopsis

Abstract

Cell polarization is intimately linked to plant development, growth, and responses to the environment. Major advances have been made in our understanding of the signaling pathways and networks that regulate cell polarity in plants owing to recent studies on several model systems, e.g., tip growth in pollen tubes, cell morphogenesis in the leaf epidermis, and polar localization of PINs. From these studies we have learned that plant cells use conserved mechanisms such as Rho family GTPases to integrate both plant-specific and conserved polarity cues and to coordinate the cytoskeketon dynamics/reorganization and vesicular trafficking required for polarity establishment and maintenance. This review focuses upon signaling mechanisms for cell polarity formation in Arabidopsis, with an emphasis on Rho GTPase signaling in polarized cell growth and how these mechanisms compare with those for cell polarity signaling in yeast and animal systems.

Figure 1

A unifying principle underlying the formation of cell polarity in eukaryotic cells. (a) A general signaling mechanism for cell polarity formation. (b) A simplified phylogenetic tree showing the major subfamilies of the Rho family small GTPases. All 11 members of the Arabidopsis Rho-related GTPase from plants (ROP) family are shown, but only representative members of the Cdc42, Rac, and Rho subfamilies are included.

Figure 2

Model cell polarity systems in plants. (a) Tip growth model: the pollen tube. (Left) A schematic of the top portion of a pistil with growing pollen tubes. (Right) A schematic showing the polarized cellular structure of pollen tubes. (b) Epidermal cells as a model for the study of planar cell polarity and/or the polarity of diffuse growth. (Left) Single-cell leaf trichome. (Middle) Trichoblast and root hairs. (Right) Pavement cells. (c) The polar localization of PINs (PIN-FORMED proteins), which directs auxin flow and produces auxin gradients, is used as a model for the study of asymmetric distribution of molecules within a cell. (d ) Guard cell differentiation as a model for the investigation of the polarity of cell division.

Figure 3

A model for a signaling network regulating the formation of the jigsaw-puzzle appearance of Arabidopsis leaf pavement cells (PC). (a) The development of PC can be separated into three stages and is associated both with cortical fine actin microfilaments (F-actin) (red patches) and with microtubules (MT) (green lines) (Fu et al. 2002, 2005). Near-square PC initials first elongate slightly to form near-rectangular cells (stage I), which produce alternating small bumps and indentations, generating cells with multiple shallow lobes and indentations (also termed sinuses or necks) (stage II). Reiterative outgrowing and indenting continue, producing highly lobed interlocking PC that often contain secondary lobes (stage III). From Fu et al. (2005) with permission. (b) A model for the ROP GTPase–dependent signaling mechanism for PC morphogenesis. This model includes known components (ROP2, RIC4, F-actin, RIC1, MT, SPK1), speculative factors (auxin and a PIN protein), and their interactions in the ROP (Rho-related GTPase from plants)-signaling network underlying PC morphogenesis. Solid arrows indicate pathways well supported by experiments. Dotted arrows indicate speculative steps/pathways. ER denotes endoplasmic reticulum.

Figure 4

A model for the generation and maintenance of the dynamic and oscillating apical cap of active ROP1 (where ROP refers to Rho-related GTPase from plants) in pollen tubes. (a) A time series of images showing the localization of a green fluorescent protein (GFP)-based active ROP1 reporter in a tobacco pollen tube transiently expressing this marker, i.e., GFP fused to the N terminus of a RIC4 deletion mutant (Hwang et al. 2005). Numbers at the bottom of each pollen tube image indicate seconds in the time series shown in the graph at the bottom of this figure. (Bottom) Graphs show the oscillation of plasma membrane (PM)-localized GFP-RIC4ΔC. Modified from figure 3 of Hwang et al. (2005). (b) Models for positive feedback–mediated lateral propagation of the apical ROP1 activity and for negative feedback–mediated global ROP1 downregulation by the REN1 GTPase–activating protein (RhoGAP) and lateral inhibition by cortical microtubules (MT) and phospholipase C (PLC). Solid arrows indicate pathways supported by experimental evidence. Dotted arrows indicate speculative pathways lacking experimental support. Abbreviations used: CDPK, calcium-dependent protein kinase; F-actin, actin microfilaments; RIC, ROP-interactive Cdc42/Rac-interactive binding (CRIB) motif–containing protein.

Figure 5

A schematic model for a unifying concept of the mechanisms underlying the control of cell morphogenesis through tip growth or polarized diffuse growth. I propose that the primary mechanism for the control of cell polarity in tip growth is the tip-localized ROP (Rho-related GTPase from plants) activation of actin dynamics, which promotes targeted exocytosis, whereas microtubule (MT)-mediated lateral inhibition plays a secondary role in polarity control. In contrast, MT-dependent mechanisms play a primary role in the control of cell polarity of diffuse growth, whereas ROP activation of actin microfilaments (F-actin) plays a secondary role in polarity control. Cortical MT–mediated polarity control involves its role in aligning cellulose microfibrils and suppression of the ROP-actin pathway. The ROP-actin pathway and the cortical MT counteract one another to fine-tune cell polarity and cell shape formation.