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Plant Physiology 147:1527-1543 (2008) © 2008 American Society of Plant Biologists Regulation of Membrane Trafficking, Cytoskeleton Dynamics, and Cell Polarity by ROP/RAC GTPases1,[W]Department of Plant Sciences, Tel Aviv University, Tel Aviv 69978, Israel (S.Y., D.B., N.S.); and Department of Plant Biology and Forest Genetics, Swedish Agricultural University, Uppsala SE–75007, Sweden (B.K.)
Rho of plants (ROP) proteins, also known as RAC proteins, are Rho-related GTPases that function as molecular switches in a multitude of signaling cascades involved in the regulation of the actin and microtubule cytoskeleton, of vesicle trafficking, and of plant responses to hormones, stresses, or light (Yang, 2002
Based on cell biological studies in animals, the Rho superfamily was initially divided into three major subfamilies designated Rho, Rac, and Cdc42 (Ridley and Hall, 1992  ; Ridley et al., 1992; Hall, 1998). With the increased availability of sequence information, the Rho family has been expanded and is currently suggested to include eight to nine subfamilies (Boureux et al., 2007; Vega and Ridley, 2007). Two methods of ROP/RAC classification are described in the literature. One classification placed ROP/RAC GTPases as a branch in the Rac subfamily and divided them into two subgroups, designated type I and type II, according to the structure of the C-terminal hypervariable domain (Winge et al., 1997). The second classification method, which is based on nucleotide sequences, suggested that ROP/RAC GTPases diverged as a separate group prior to the separation between Rac and Cdc42 and can be divided into four subgroups, which were designated I, II, III, and IV. Subgroups I and II correspond to type II ROP/RAC GTPases, and subgroups III and IV correspond to type I ROP/RAC GTPases of the first classification method (Yang, 2002; Christensen et al., 2003; Vernoud et al., 2003). Recent sequence analysis of the Rho superfamily in different eurkaryotes (Boureux et al., 2007) may solve the existing discrepancy in the literature. This analysis suggests that Rac GTPases were the originating family of all Rho GTPases and that the Rho and Cdc42 families diverged from the Rac family later in evolution. The additional Rho subfamilies were created by diversification of the family in vertebrates, primarily in mammals (Boureux et al., 2007). Thus, both earlier analyses are correct. ROP/RAC GTPases are indeed more closely related to Rac, but they diverged as a separate Rac group prior to the divergence of Rac, Rho, and Cdc42. The unique features discovered in high-resolution three-dimensional structures of AtROP9/RAC7 (Sormo et al., 2006) and AtROP4/RAC5 (Thomas et al., 2007) support the notion that ROP/RAC GTPases form a unique subgroup of the Rho GTPases (Berken and Wittinghofer, 2008). In this review, the classification of ROP/RAC GTPases into type I and type II according to their hypervariable domain will be used to discuss differences in lipid modification and subcellular targeting existing between these two types.
Similar to other Rho GTPases, ROP/RAC GTPases contain a G-domain, which is responsible for GTP binding/hydrolysis and for interaction with effector proteins, and a hypervariable domain, which determines subcellular targeting. ROP/RAC GTPases have a molecular mass of 21 to 24 kD and consist of around 200 amino acids. High-resolution three-dimensional structures of Arabidopsis (Arabidopsis thaliana) AtROP9/RAC7 (Sormo et al., 2006 ) and AtROP4/RAC5 (Thomas et al., 2007) show that these ROP/RAC GTPases contain a β-sheet core composed of six β-sheets surrounded by four  -helices. The β-sheets and -helices are connected by five loops that contain five highly conserved G-box motifs (G1–G5) responsible for GTP/Mg2+ binding and GTP hydrolysis (Bourne et al., 1991; Vetter and Wittinghofer, 2001; Berken and Wittinghofer, 2008).
Like corresponding mutations in Ras (Lowy and Willumsen, 1993
In addition to the G-domain and hypervariable regions, all Rho proteins contain a helical domain called the insert region, labeled
As in all members of the Rho family, the hypervariable domain is located at the C-terminal end of ROP/RAC GTPases. In type I ROP/RAC GTPases, the hypervariable domain consists of a canonical CaaL box, which is prenylated primarily by geranylgeranyltransferase I (PGGT; Sorek et al., 2007
ROP/RAC subcellular localization has been investigated by indirect immunofluorescence, GFP tagging, and cell fractionation/immunoblotting. Imaging experiments have shown that these GTPases are associated with the plasma membrane in a variety of cell types and display enhanced membrane association at growth sites in pollen tubes, root hairs, and leaf epidermal cells (Ivanchenko et al., 2000 ; Molendijk et al., 2001; Fu et al., 2002; Jones et al., 2002; Lavy et al., 2002, 2007; Bloch et al., 2005; Lavy and Yalovsky, 2006; Sorek et al., 2007). By immunoblotting, ROP/RAC GTPases were exclusively detected in the membrane fraction of extracts of vegetative cells (Sorek et al., 2007), whereas they were found in both the membrane and the cytoplasmic fraction of pollen tube extracts (Kost et al., 1999).
The subcellular localization of ROP/RAC GTPases is primarily determined by their C-terminal hypervariable domain. However, recent findings show that activation-dependent S-acylation of one or more G-domain Cys residues is associated with partitioning of ROP/RAC GTPases into nonionic detergent-resistant membranes (DRMs; Sorek et al., 2007
Prenylation and CaaX Processing of Type I ROP/RAC GTPases
The CaaL box Cys of type I ROP/RAC GTPases is prenylated in the cytoplasm primarily by PGGT (Caldelari et al., 2001
Membrane-associated type I GTPases partition between nonionic detergent-soluble (Triton X-100-soluble membrane [TSM]) and insoluble (DRM) fractions (Fig. 1A; Sorek et al., 2007
The hypervariable domain of type II ROP/RAC GTPases consists of a unique sequence motif designated the GCCG box and a proximal polybasic domain. The GCCG box is composed of two Cys residues that undergo S-acylation (Fig. 1D; Lavy et al., 2002
The polybasic domain has two essential functions: (1) it enhances PGGT-mediated prenylation by about one order of magnitude (James et al., 1995
Removal of the polybasic domain of the Arabidopsis type II ROP/RAC AtROP8 abrogated its interaction with the membrane (Lavy and Yalovsky, 2006
S-Acylation and RhoGDI
Under physiological conditions, prenylation facilitates the interaction between Rho proteins and RhoGDI (Di-Poi et al., 2001
The findings on the activation-dependent transient S-acylation of AtROP6 and its consequential partitioning in DRMs have interesting regulatory implications. S-Acylation involves an unstable and reversible thioester bond, in contrast to prenylation, which is based on an irreversible thioether linkage (Fig. 1B). Due to its reversibility, S-acylation was suggested to play an important regulatory role in signaling processes (Smotrys and Linder, 2004 ). DRMs, often referred to as lipid rafts, are sterol- and sphingolipid-rich membrane microdomains that attract specific groups of proteins (Fig. 1B). Given their properties, lipid rafts were suggested to function as signaling hubs that can change their size and composition in response to external stimuli, favoring certain protein-protein interactions (Simons and Toomre, 2000). Characterization of DRMs in plants showed that, like their counterparts in animal cells and in yeast, they are enriched in sterols and sphingolipids. Furthermore, they contain characteristic glycosylphosphatidylinositol-anchored proteins and, importantly, a type I ROP/RAC protein (NtRAC5; Mongrand et al., 2004; Borner et al., 2005; Morel et al., 2006). In animal cells, S-acylated (palmitoylated) proteins partition into DRMs (Melkonian et al., 1999). Thus, transient S-acylation induces temporal partitioning of AtROP6 and likely other ROP/RAC GTPases to DRMs, where they potentially can interact with other proteins. Because constitutively active GTP-bound Atrop6CA, which was always found to be both prenylated and S-acylated, localized exclusively in DRMs (Sorek et al., 2007), it is likely that type I ROP/RAC GTPases signal mostly from these membrane microdomains.
The lipid raft hypothesis is still bitterly debated (Munro, 2003
Predictions based on modeling of the Ras-activated mitogen-activated protein kinase pathway in mammalian cells suggest that nanoclustering of Ras facilitates a mechanism that converts graded ligand inputs into fixed outputs. The model predicts that cells form Ras nanoclusters in direct proportion to the concentration of the input signal (e.g. epidermal growth factor), creating a high-fidelity signaling relay across the membrane. The concentration of the epidermal growth factor, which is analog like in its nature, is turned into a digital-like on/off reaction by the Ras switch. The signal is transmitted from Ras to the mitogen-activated protein kinase pathway, recreating an analog-like signal. The signal transmission is predicted to be fully dependent on Ras nanoclustering (Tian et al., 2007
Mathematical models of Rho, Rac, and Cdc42 functions in cellular polarization predict that cycling between active and inactive states, together with fast diffusion to the cytosol of GDP-bound protein in complex with RhoGDI, are essential for obtaining robust spatial polarization rather than traveling waves (Maree et al., 2006 ; Jilkine et al., 2007). Models of Cdc42 function during bud formation in yeast predict that the energy obtained from GTP hydrolysis, along with RhoGDI-mediated relocation of GDP-bound Cdc42 to the cytoplasm, are required for polar bud growth and for the development of a single bud (Goryachev and Pokhilko, 2008). These models imply that discrete localization of polarizing factors, without cycling of Rho proteins between active and inactive states and relocation of the inactive form, is not sufficient to establish cell polarity. Mechanistically, the Rho switch mechanism that enables the binding and release of effectors, along with the spatial separation of the active and inactive states, form the basis for maintaining cell polarization.
Consistent with the theoretical models, numerous studies have demonstrated that the expression of constitutively active forms of both type I and type II ROP/RAC GTPases depolarizes cell expansion (Kost et al., 1999
Figure 2 summarizes the current knowledge concerning factors involved in polarized ROP/RAC activation and downstream signaling, which is primarily based on studies in pollen tubes and root hairs. In pollen tubes, fluorescent ROP/RAC fusion proteins accumulate at the plasma membrane of the growing tip (Kost et al., 1999
Similar mechanisms appear to be involved in the polarization of ROP/RAC activity during root hair elongation. Indirect immunofluorescence and GFP tagging showed that ROP/RAC accumulation at a specific domain of the trichoblast plasma membrane, which is determined by an auxin gradient in the root epidermis, precedes root hair outgrowth (Molendijk et al., 2001
Consistent with the proposed RhoGDI function in the control of polarized ROP/RAC activation in pollen tubes, a minor proportion (less than 50%) of the ROP/RAC proteins in tobacco pollen tube protein extracts were detected in the insoluble fraction, whereas the rest were found in the soluble fraction (Kost et al., 1999 ROP/RAC targeting seems to depend particularly strongly on GDI function in tip-growing pollen tubes, whereas the GDI-bound soluble ROP/RAC fraction in other cell types appears to be below the detection limit of biochemical assays. Identification in these cell types of small fractions of GDI-bound soluble ROP/RAC GTPases undergoing rapid cycling between the cytoplasm and the plasma membrane may require sensitive fluorescence imaging techniques, such as spot fluorescence recovery after photobleaching, which can differentiate between lateral diffusion within membranes and movement on/off membranes, or total internal reflection fluorescence, which enables monitoring of fluorescent structures in close proximity of the plasma membrane.
Plants contain a unique family of ROP/RAC-GEFs named PRONE (for plant-specific ROP nucleotide exchanger) after their catalytic domain (Berken et al., 2005
Given the theoretical models described above and available experimental data, the following model could be suggested (Fig. 2). ROP/RAC GTPases are recruited to highly specific membrane domains, for example by a morphogen (auxin) gradient, as in the case of root hairs (Fischer et al., 2006 Through the regulation of the actin and microtubule cytoskeleton, and of membrane trafficking, activated ROP/RAC GTPases promote the establishment of robust cellular polarity.
An important function of Rho GTPases in animal and yeast cells is the control of membrane trafficking. Yeast Rho GTPases accumulate at the plasma membrane at sites of directional cell expansion, where they promote localized secretion required for this process (Brennwald and Rossi, 2007 ). In animal cells, activated Rho GTPases are not only associated with the plasma membrane but also with intracellular compartments, including the Golgi and endosomal organelles. At these locations, Rho GTPases positively or negatively regulate specific membrane-trafficking events required for secretion, clathrin-dependent and -independent endocytosis, Golgi-to-ER transport, or recycling from endosomes back to the plasma membrane (Symons and Rusk, 2003; Ridley, 2006).
Although the molecular mechanisms by which activated Rho GTPases control membrane trafficking in animal and yeast cells are not fully understood, Rho-induced F-actin reorganization clearly plays a key role in these regulatory processes. Animal and yeast Rho GTPases promote F-actin nucleation via direct interactions with formins (Kovar, 2006
In yeast and animal cells, active Rho GTPases stimulate secretion not only via F-actin reorganization but also by directly interacting with and activating components of the exocyst. The exocyst is an octameric complex implicated in the tethering of post-Golgi vesicles, which promotes the fusion of these vesicles with the plasma membrane (TerBush et al., 1996
Additional regulatory mechanisms by which animal Rho GTPases modulate membrane trafficking include the direct or indirect interaction with coat proteins (clathrin, coatmer/COP-1) involved in the formation and cargo loading of transport vesicles (Yang et al., 2001
The polarized growth of plant cells has long been thought to depend on internal turgor pressure built up by water accumulation in the large central vacuole and on microtubule-directed deposition of cell wall-reinforcing cellulose microfibrils. These cellulose microfibrils can restrict cell expansion in all directions other than the main growth axes. In recent years, it has become increasingly clear that F-actin structures and membrane trafficking controlled by ROP/RAC GTPases also play key roles in the directional expansion of plant cells (Smith and Oppenheimer, 2005 ; Hussey et al., 2006; Mathur, 2006).
Most plant cells undergo diffuse growth (i.e. they expand in all directions to some extent), although growth occurs mainly along one or more main axes. Diffuse cell growth has been shown to be associated with a network of actin cables and filaments extending throughout the cytoplasm, which displays a net alignment along growth axes, and with diffuse cortical F-actin structures underlying the plasma membrane at growth sites (Dong et al., 2001
A dense cortical F-actin network similar to the one underlying the plasma membrane in lamellipodia of motile animal cells has not been identified in expanding plant cells, indicating that membrane protrusion driven by actin polymerization does not play a role in the polarized growth of these cells. Rather, F-actin structures seem to promote membrane trafficking required for the local deposition of new cell wall material in the extracellular matrix at sites where plant cells expand (Wasteneys and Galway, 2003
ROP/RAC GTPases clearly have important functions in the control of both diffuse cell expansion and tip growth. Overexpression of constitutively active ROP/RAC GTPases enhances and depolarizes diffuse cell growth (Molendijk et al., 2001
Accumulating evidence summarized in the following sections strongly suggests that ROP/RAC GTPases control polarized cell growth by regulating membrane trafficking both via the control of actin organization and via actin-independent pathways. An important function of ROP/RAC-regulated F-actin structures in membrane trafficking has also been demonstrated during pathogen defense reactions. The prevention of the penetration of resistant barley (Hordeum vulgare) cells by the fungus powdery mildew was shown to involve ROP/RAC-dependent formation of actin filaments polarized toward the site of fungal attack. These actin filaments are thought to promote membrane trafficking required for the deposition of additional cell wall material and of defense compounds at this site (Opalski et al., 2005 ).
Overexpression of constitutively active GFP-AtROP11/RAC10CA in transgenic Arabidopsis plants was shown to block the uptake of the styryl dye FM4-64, an established tracer of endocytic membrane internalization, in root hairs and to interfere with the formation of brefeldin A (BFA) compartments in these and other cells (Bloch et al., 2005 ). BFA compartments are formed in plant cells treated with the Arf-GEF inhibitor BFA by the aggregation of aberrant endocytic endosomes and secretory (trans-Golgi network) organelles. These compartments have been shown to contain plasma membrane proteins and lipids that normally undergo endocytic recycling (Nebenführ et al., 2002; Geldner et al., 2003; Grebe et al., 2003). The effects of ROP/RAC overexpression on FM4-64 uptake by transgenic root hairs are shown in Figure 3. In nontransformed root hairs and in transgenic root hairs expressing GFP fused to wild-type AtROP11/RAC10, massive FM4-64 internalization was observed within minutes (Fig. 1, A and B). By contrast, FM4-64 internalization was not detectable even after prolonged incubation at room temperature in swollen root hairs expressing GFP fused to constitutively active AtROP11/RAC10CA (Fig. 3, C–E; Bloch et al., 2005). Together, these observations strongly suggest a role of ROP/RAC GTPases in the control of endocytic membrane uptake. Considering the proposed function of lipid rafts in the regulation of endocytosis in animal and yeast cells (Hancock, 2006), it will be interesting to test whether the accumulation of activated ROP/RAC GTPases in DRMs has a function in the control of membrane internalization in plants.
Another direct link between ROP/RAC GTPases and the control of membrane trafficking was established by the observation that an Arabidopsis protein called ICR1 (for interactor of constitutively active ROP1) binds directly to AtSEC3A, a homolog of the yeast regulatory exocyst component Sec3 (Lavy et al., 2007
Several ROP/RAC signaling pathways appear to regulate F-actin structures and to influence microtubular organization during polar cell expansion. One of these pathways involves the DOCK180-like ROP/RAC-GEF SPK1 along with the WAVE and Arp2/3 complexes. Other pathways are based on CRIB domain-containing ROP/RAC effectors called RICs (for ROP-interacting CRIB) or on actin-binding proteins such as ADF/cofilin. Mutations in genes coding for all these regulatory factors have profound effects on directional cell expansion. Current knowledge concerning the functions of these factors is discussed in this and the following section.
Trichomes are large cellular structures that protrude from the leaf epidermis. In Arabidopsis, they are single cells typically composed of a central stalk and three distal branches with pointed tips. Although the cell expansion mechanisms responsible for the development of the complex morphology of these cells are not fully understand, they are thought to depend in part on diffuse cell expansion and clearly require microtubules and the actin cytoskeleton (Mathur, 2005
The distorted class of Arabidopsis mutants develop deformed trichomes with abnormal F-actin organization, swollen stalks, and short, mispositioned branches. Essentially identical cellular defects are caused by the treatment of developing trichomes with drugs that interfere with F-actin stability (Mathur et al., 1999
Trichomes formed by mutants defective in the gene encoding the ROP/RAC-GEF SPK1 fail to branch (Qiu et al., 2002
Analysis of distorted mutants has shown that, in addition to aberrant trichome morphogenesis, these plants display cell expansion and cell adhesion defects, which are particularly clearly detectable in the epidermis of rapidly growing organs such as etiolated hypocotyls and cotyledons (Mathur, 2005
Interestingly, plants carrying mutant alleles of DISTORTED genes, which are ubiquitously expressed at low levels throughout plants (Mathur, 2005
Mutant spk1 and distorted alleles are normally transmitted through the male gametophyte (pollen tube) during sexual reproduction and have only weak effects on root hair morphology (Qiu et al., 2002
RICs form a plant-specific family of ROP/RAC effectors that all contain a CRIB domain but share little homology outside of this domain with each other or with any other proteins (Wu et al., 2001
Counteracting RIC1- and RIC4-dependent pathways have been proposed to underlie the ROP/RAC-dependent control of directional cell expansion in developing pavement cells in the epidermis of Arabidopsis leaves (Fu et al., 2005
Two different counteracting RIC-dependent pathways have also been proposed to participate in the control of tip growth by ROP/RAC GTPases (Gu et al., 2005 While RIC1, RIC4, and RIC3 undoubtedly play important roles as ROP/RAC effectors in the regulation of directional cell expansion, the molecular mechanisms they employ to control cytoskeletal organization and membrane trafficking remain to be identified.
Like animal and yeast Rho GTPases, ROP/RAC GTPases can also modulate F-actin organization by regulating ADF/cofilin and, possibly, formin activity. The pollen-specific tobacco ADF homolog NtADF1 associates with F-actin structures in pollen tubes and contains a conserved regulatory phosphorylation site (Ser-6) near the N terminus (Chen et al., 2003 ). NtADF1 overexpression in pollen tubes depolymerizes fine actin filaments, inhibits cell expansion, and counteracts growth depolarization induced by ROP/RAC overexpression. Interestingly, ROP/RAC overexpression results in enhanced phosphorylation of NtADF1 at Ser-6, which reduces the ability of this protein to associate with F-actin, inhibit cell expansion, and block ROP/RAC-induced growth depolarization (Chen et al., 2002, 2003). These observations suggest that, similar to the situation in animal cells, ROP/RAC activation can promote F-actin assembly not only via the stimulation of the Arp2/3 complex (see above) but also by inducing ADF phosphorylation and inactivation. Homologs of LIM kinases, which phosphorylate ADF in response to Rho activation in animal cells, are not found in plants. Instead, plant ADF was shown to be phosphorylated by calmodulin-like protein kinases (Allwood et al., 2001).
As discussed above, animal Rho GTPases promote F-actin nucleation alternatively through the Arp2/3 complex or through formins. Because Arp2/3 functions appear to be largely restricted to trichomes and other epidermal cells in plants, it is tempting to speculate that ROP/RAC-mediated modulation of formin activity may play an important role in the control of F-actin organization during the expansion of other cells in these organisms. Members of a structurally diverse family of Arabidopsis proteins containing an FH2 domain, which is responsible for the F-actin-nucleating activity of animal and yeast formins, have been shown to display such activity in vitro and/or to promote F-actin formation in vivo (Staiger and Blanchoin, 2006
ROP/RAC GTPases have been reported to directly bind to and activate NADPH oxidase subunits (Wong et al., 2007 ). In root hairs (Foreman et al., 2003) and in pollen tubes (Potocky et al., 2007), NADPH oxidase activity responsible for the apical accumulation of reactive oxygen species (ROS) was shown to be essential for cell elongation. Through the stimulation of plasma membrane Ca2+ channels, ROS are thought to be essential for the establishment of a tip-focused Ca2+ gradient required for root hair growth (see above; Foreman et al., 2003). Interestingly, ROS levels at the root hair tip were recently shown to fluctuate periodically in coordination with oscillations in extracellular pH and in cell elongation rate (Monshausen et al., 2007).
In addition to presumably regulating actin organization and membrane trafficking, elevated Ca2+ levels at the root hair apex were recently demonstrated to stimulate NADPH oxidase activity. This creates a positive feedback loop that is likely to contribute to the maintenance of the polarity of root hair growth (Takeda et al., 2008
PtdIns 4,5-P2
As discussed above, like animal Rho GTPases, pollen tube ROP/RAC GTPases physically interact with PtdIns P-K activity, which generates the signaling lipid PtdIns 4,5-P2 (Kost et al., 1999
PtdIns 4,5-P2 hydrolysis by PLC activity associated with the pollen tube plasma membrane at the flanks of the tip appears to be required to restrict the distribution of this lipid to the apex (Dowd et al., 2006
Interestingly, PLC-mediated PtdIns 4,5-P2 hydrolysis also generates Ins 3-P, a soluble molecule well known for its ability to induce Ca2+ influx into the cytoplasm of pollen tubes (Franklin-Tong et al., 1996
While most of the evidence summarized above links ROP/RAC signaling to the control of membrane trafficking, it appears likely that membrane trafficking in turn also affects ROP/RAC signaling. As discussed above, like other Rho proteins, type I ROP/RAC GTPases presumably undergo postprenylation CaaX processing at the ER before they are transported to the plasma membrane, possibly along the secretory pathway. The promotion of secretion by ROP/RAC GTPases, along with the transport of these proteins on the surface of secretory vesicles to sites of their activation at the plasma membrane, potentially creates a positive feedback mechanism that contributes to the maintenance of cellular polarization. As exemplified by the proposed transport of diacyl glycerol from the flanks of the pollen tube tip to the apex, endocytic membrane uptake or recycling mechanisms may regulate the intracellular distribution of membrane-associated factors involved in ROP/RAC signaling, including ROP/RAC-activating transmembrane receptors or ROP/RAC-GEFs. Again, the control of such mechanisms by ROP/RAC signaling would create an excellent opportunity for positive or negative feedback regulation that could play a very important role in the control of cell polarization. Consistent with the proposed interdependence of membrane trafficking and Rho signaling, blocking secretion and/or endocytic recycling by BFA treatment prevents the polarized accumulation of type I ROP/RAC activity at the plasma membrane of root epidermal cells, which is required for root hair outgrowth (Molendijk et al., 2001 ). However, BFA did not induce the accumulation of AtROP11/RAC10 in BFA bodies or prevented its accumulation at the plasma membrane (Bloch et al., 2005). This indicated that the intracellular targeting of this protein, and possibly other type II ROP/RAC GTPases, does not depend on BFA-sensitive membrane trafficking.
Another implication of the stimulation of membrane trafficking by activated ROP/RAC GTPases is that the membrane domains with which these proteins are associated are presumably undergoing constant remodeling. At the tip of rapidly elongating pollen tubes, where membrane trafficking is particularly dynamic, GAP- and GDI-dependent ROP/RAC recycling from the flanks to the apex was proposed to be required to compensate for the constant lateral displacement of ROP/RAC activity caused by the massive fusion of secretory vesicles with the plasma membrane (Kost, 2008
Recent years have seen much progress in our understanding of the regulation of ROP/RAC function and of the downstream signaling network stimulated by their activity. Although Rho regulation and downstream signaling have remained highly conserved during evolution, plants have developed a range of unique mechanisms involved in these processes, including (1) ROP/RAC activation by plant-specific GEFs, (2) ROP/RAC-dependent signaling by plant-specific RIC and ICR1 effectors, and (3) PLC-mediated spatial restriction of PtdIns 4,5-P2 distribution. Despite these variations in the underlying signaling mechanism, a key function of all Rho proteins, including ROP/RAC GTPases, appears to be the control of membrane trafficking, either through F-actin reorganization or actin-independent pathways.
The systems biology of ROP/RAC signaling appears to be highly complex. Direct evidence has been generated for an important function of ROP/RAC GTPases in the control of F-actin reorganization, membrane trafficking, and polar cell growth. A variety of factors have been identified that link ROP/RAC activation to the regulation of these processes in different cell types. Some of these factors, including Ca2+, PtdIns 4,5-P2, and ROS, are involved in a multitude of regulatory pathways, many of which are presumably ROP/RAC independent (Fig. 4
). Spatial and/or temporal restriction of ROP/RAC activation and downstream signaling, therefore, is likely to be required to prevent nonspecific stimulation of independent pathways. To locally contain ROP/RAC signaling, plant cells appear to employ a complex network of interacting regulatory mechanisms. ROP/RAC targeting and local activation are tightly controlled by prenylation and S-acylation of the hypervariable domain, transient raft association depending on G-domain S-acylation, direct binding to PtdIns 4,5-P2, GEF-dependent activation, GAP/GDI-mediated recycling, and, possibly, membrane trafficking. Additional mechanisms contributing to the spatial and temporal restriction of ROP/RAC signaling, at least in tip-growing cells, include (1) the highly specific intracellular targeting of regulatory factors such as GEFs and GAPs by unknown processes, (2) the maintenance by PLC activity of membrane domains enriched in PtdIns 4,5-P2, which potentially acts both upstream and downstream of ROP/RAC activation, and (3) the coordinated oscillation of the activity of ROP/RAC GTPases (Hwang et al., 2005 A key challenge of ongoing and future research is to understand how cells undergoing directional expansion integrate the many regulatory mechanisms and pathways involved in localized ROP/RAC signaling to coordinate F-actin-dependent membrane trafficking underlying this process. It will be essential to investigate in detail the intracellular distribution ROP/RAC GTPases expressed in expanding cells and to further explore the possibility that some of them may be associated with endomembrane compartments. An important part of this investigation will be the further analysis of lipid modifications of different ROP/RAC GTPases and of the effects of these modifications on RhoGDI interaction as well as on intracellular targeting. GEFs and GAPs controlling ROP/RAC activity during specific cellular processes need to be identified, and their intracellular targeting needs to be studied. In addition, it will be important to further characterize (1) the exact cellular functions of ROP/RAC effectors, (2) the membrane trafficking processes involved in polar plant cell expansion, and (3) the role of different F-actin structures in these processes. Experiments based on analysis of the effects of overexpressing constitutively active or dominant negative ROP/RAC variants were instrumental in the acquisition of our current knowledge concerning the role of ROP/RAC signaling in the control of membrane trafficking and polar cell growth. Analysis of the effects of knocking out or knocking down the expression of single ROP/RAC GTPases, or of combinations of these proteins, in plant cells undergoing directional expansion will be important to confirm and extend this knowledge. Together with the experimental approaches summarized above, mathematical modeling will be required to achieve an integrated understanding of the complex regulatory mechanisms and cellular processes underlying ROP/RAC-controlled membrane trafficking during polar cell growth.
The following materials are available in the online version of this article.
Received April 27, 2008; accepted June 12, 2008; published August 6, 2008.
1 This work was supported by grants from the Israel Science Foundation (grant no. ISF 312/07), the U.S.-Israel Binational Agricultural Research and Development program (grant no. 4032/07), the German Israel Foundation (grant no. GIF 834/2005), the Deutschland Israel Program (grant no. DIP H–3.1), and the German Research Foundation. 
2 These authors contributed equally to the article. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Shaul Yalovsky (shauly{at}tauex.tau.ac.il).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.108.122150 * Corresponding author; e-mail shauly{at}tauex.tau.ac.il.
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ROP/RAC EVOLUTION
STRUCTURE AND ACTIVITY
1 inhibits pollen tube elongation (Kost et al., 1999
