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The Regulatory RAB and ARF GTPases for Vesicular Trafficking

Erik Nielsen, Alice Y. Cheung, Takashi Ueda
Erik Nielsen
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Alice Y. Cheung
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Takashi Ueda
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Published August 2008. DOI: https://doi.org/10.1104/pp.108.121798

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  • © 2008 American Society of Plant Biologists

While highly conserved in structure and in fundamental regulatory aspects for their activities, the RAS superfamily of monomeric GTP-binding proteins, or small GTPases, comprise a large family of regulatory molecules that collectively regulate diverse and critical cellular processes in eukaryotes. The RAB and ARF GTPases are members of two of the RAS-related subfamilies that function in regulating vesicle trafficking, starting from regulating the formation of vesicles on donor membranes and directing trafficking specificity to and facilitating vesicle docking on target membranes (Zerial and McBride, 2001; Gillingham and Munro, 2007). Studies in yeast (Saccharomyces cerevisiae) and mammalian systems have shown that successive steps in endomembrane trafficking, from the endoplasmic reticulum (ER) to the Golgi, intra-Golgi, post-Golgi, and endocytic trafficking, are mediated by subfamilies of RAB and ARF GTPases. The fundamental roles that these small GTPases play in membrane trafficking are indicated by their conservation throughout eukaryotes and their proliferation in the more complex animal and plant systems. Structural conservation among these GTPases has facilitated a rather comprehensive identification of the corresponding gene families in plants with complete genome information, in particular those for the Arabidopsis (Arabidopsis thaliana) RABs and ARFs (Pereira-Leal and Seabra, 2001; Rutherford and Moore, 2002; Vernoud et al., 2003; Zhang et al., 2007). In most cases examined, sequence conservation among yeast, mammalian, and plant RAB GTPases has correlated with similar localization on discrete subcellular compartments of the endomembrane trafficking systems in these diverse organisms. However, while the most closely related RAB GTPases from diverse organisms appear to hold analogous positions within the endomembrane system, it is clear that experimental strategies directly targeted at examining the specific functions of these small GTPases in plants will be required to determine distinctions in how various membrane compartments are utilized and how plant-specific cargos are sorted and trafficked through these compartments. We refer readers to earlier reviews (Rutherford and Moore, 2002; Vernoud et al., 2003) and focus our discussion here on recent studies that examine the biological role for these small GTPases in specific cellular context as well as emerging studies that explore their broader regulatory networks.

NOMENCLATURE AND THE RESEARCH TOOL BOX

A comprehensive gene/protein nomenclature system that accurately reflects phylogenetic relationships as well as functional specialization is a moving target, as genomic sequences and functional information are continuously being added and refined. This is particularly the case for the plant RAB GTPases, which, like their yeast and mammalian counterparts, constitute the largest of the RAS-related superfamilies of small GTPases. Based on sequence similarity among themselves, and with their yeast and mammalian orthologs, a nomenclature system for the 57 Arabidopsis RABs that places them into eight distinct subfamilies (A to H, corresponding to the mammalian RAB GTPase classes of 11, 2, 18, 1, 8, 5, 7, and 6, respectively), each regulating distinct paths in the membrane trafficking systems, has been proposed (Pereira-Leal and Seabra, 2001). The use of numerical designation to reflect closest analogy with mammalian orthologs, e.g. RAB2 and RAB11, has been adopted for some of the studies, especially for RABs from plants other than Arabidopsis. This has the clear advantage for cross-referencing but runs the risk of obscuring aspects of these plant RAB GTPases that have evolved to best serve vesicular trafficking needs in plant cells. Development of a nomenclature system that incorporates the numbering system of the closest mammalian orthologs and at the same time preserves the designation of the eight distinct subgroups previously defined for the Arabidopsis RABs is currently under way (I. Moore, personal communication). We will use both systems, e.g. RAB11/RABA, for general discussions and retain use of the original nomenclature in most of our discussions of specific studies. We opt to test the use, however, of the system under development in the section where we discuss the RAB5/RABF and RAB7/RABG class of GTPases. Perhaps response from readers will help guide the development of a system that best serves this complex protein family.

Like all RAS-related GTP-binding proteins, RAB GTPases utilize guanine nucleotide exchange and GTP hydrolysis to switch between active (GTP-bound) and inactive (GDP-bound) conformations (Fig. 1 ). One of the features that distinguish the plant RAB GTPase family is the size of the protein family. To date, knockout mutations have not yielded functional insight for these small GTPases, most probably because of overlapping functions among members of the same subfamily or between closely related subfamilies. On the other hand, replacement of specific amino acid residues in various functional domains of RAS-related GTPases results in defined effects on guanine nucleotide binding and GTP hydrolysis. Mutations that stabilize the GTP-bound activated state, thus up-regulating their regulatory activity, are referred to as constitutively active (CA); conversely, those that render the GDP-bound inactive state to be more predominant confer a dominant negative (DN) effect on the small GTPase-regulated pathways. Much of the functional insight for the RABs and ARFs discussed below and summarized in Figure 2 is derived from studies based on these CA and DN mutations in transformed plant or cell systems.

Figure 1.
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Figure 1.

The small GTPase regulatory cycle. RAS-related GTPases cycle between an active GTP-bound and an inactive GDP-bound state. GEFs activate these small GTPases, which in turn interact with specific effectors to mediate downstream pathways. GAPs stimulate the inherent GTPase activity of these small G proteins, accelerating the inactivation of their regulatory activity.

Figure 2.
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Figure 2.

A schematic illustration for the RAB- and ARF-mediated pathways in plant cells known to date. Phragmoplast and polarized outgrowth are depicted as examples of cellular structures that require high levels of polarized secretory activities for their formation. SV, Secretory vesicles; MVE/PVC, multivesiculated endosome/prevacuolar compartment; RE, recycling endosome.

Additional important biological roles for RAB- and ARF-regulated pathways have emerged recently from studies in knockout plants defective in proteins that regulate the RAB and ARF GTPase cycle. In particular, knockouts of RAB and ARF guanine exchange factors (GEFs) that stimulate exchange of GDP for GTP, and thereby “turn on” the GTPase by allowing progression into the GTP-bound conformation (Fig. 1), have resulted in observable defects in plant growth and development (Steinmann et al., 1999; Goh et al., 2007; Teh and Moore, 2007). Another class of regulators for these small GTPases are GTPase-activating proteins (GAPs), which stimulate hydrolysis of the GTP bound in the RAB or ARF GTPases and thus “turn off” the GTPase by returning it to its GDP-bound conformation. Mutations in ARF GAP have been shown to result in abnormal vein pattern formation in Arabidopsis (Koizumi et al., 2005; Sieburth et al., 2006). Finally, some success has been gained by analysis of knockouts of downstream effector proteins that are recruited to the GTP-bound, active GTPases and are responsible for carrying out the various biological functions that these small GTPases regulate (Preuss et al., 2006; Stefano et al., 2006).

Development of fluorescent protein-labeled RABs and ARFs and cargo molecules has accelerated the ability to assign subcellular locations for these proteins within the endomembrane system (Fig. 3 ). Studies of these small GTPases in cellular and developmental processes that rely on high levels of secretion or polarized secretory activities facilitate functional association with specific cellular processes and physiological phenomena. Therefore, embryogenesis, cell plate formation, and the polar growth cells such as root hairs and pollen tubes are popular biological systems for the functional dissection of these small GTPases.

Figure 3.
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Figure 3.

Some model cell systems for the studies of regulatory small GTPases for vesicular trafficking. A, Localization of various GFP-labeled RAB GTPases in transiently transformed Arabidopsis protoplasts. B and C, Localization of NtRAB5 to endosomal compartments in tobacco epidermal cells. B, GFP-NtRAB5 (green) colocalizes on yellow punctate structures with the endocytic marker FM4-64 (red) in epidermal cells of CaMV35S-GFP-NtRab5 transformed tobacco seedlings. C, CFP-NtRAB5 (red) colocalizes with a GFP-labeled auxin efflux protein AtPIN1 (green) known to be recycled through the endosomes (see Geldner and Jürgens, 2006) on yellow punctate structures. The insets in B and C are enlarged from the structures indicated by arrows and arrowheads. The tobacco epidermal cell was transiently cotransformed by agroinfiltration (see Batoko et al., 2000). D, Colocalization of a GFP-NtRAB5 (green) with a CFP-labeled NtRAB11b (red) in an elongating pollen tube showing the polarized concentration of Rab11-labeled transport vesicles in the apex and the localization of Rab5-labeled endosomes in the subtending cytoplasm (B–D; T. Andreyeva and A.Y. Cheung, unpublished data).

RAB1/RABD AND RAB2/RABB

In mammalian cells, the early secretory pathway of ER to Golgi trafficking and intra-Golgi trafficking are mediated by RAB1 and RAB2 (Zerial and McBride, 2001). Whereas mammalian RAB1 regulates anterograde ER to Golgi trafficking, RAB2 may be more important in intra-Golgi and retrograde Golgi to ER trafficking. While homologs of both RAB1 and RAB2 are found in plants, RAB2 homologs are not found in yeast, where RAB1 alone sufficiently supports the early secretory pathway (Segev et al., 1988). Similar to mammalian RAB1 (Haubruck et al., 1989), plant RAB1/RABDs are able to complement the yeast ypt1 mutation. On the other hand, a RAB2 from soybean (Glycine max) failed to complement ypt1 (Kim et al., 1996; Park et al., 1997). The functional divergence between RAB1D and RAB2B implicated by these studies remains to be vigorously examined in plant cells.

In Arabidopsis, the RAB1/RABD family is comprised of five subspecies (Pereira-Leal and Seabra, 2001; Rutherford and Moore, 2002; Vernoud et al., 2003). One of these, RAB1b, has been localized to the ER and Golgi in transiently transformed epidermal cells expressing the GFP-labeled protein (Batoko et al., 2000). Expression of a DN RAB1b induced the accumulation of a secreted form of GFP and a Golgi-targeted N-glycosylated GFP variant in a membrane reticulate reminiscent of the ER. This and the accumulation of an endoglycosidase H-sensitive population of the Golgi-targeted GFP confirmed that trafficking from ER to the Golgi was inhibited in cells compromised in their RAB1-regulated trafficking activity as a result of DN RAB1b overexpression. Developmentally, a recent study in maritime pine (Pinus pinaster) revealed high levels of expression of a RAB1, PpRAB1, in early zygotic development followed by decline as embryos matured, suggesting a role for this small GTPase in early embryogenesis (Goncalves et al., 2007).

The RAB2/RABB GTPase family is relatively small, represented by two to four members in Arabidopsis, maize (Zea mays), and rice (Oryza sativa; Pereira-Leal and Seabra, 2001; Rutherford and Moore, 2002; Vernoud et al., 2003; Zhang et al., 2007). The functional significance of the RAB2/RABB-regulated pathway has been examined in pollen tubes, which represent one of the most dramatic polar growth cell types in nature (Cheung et al., 2002). In addition to an extensive ER system that spans the entire pollen tube cytoplasm except at the extreme apex, pollen tubes maintain a highly polarized organelle distribution pattern with an extremely high density of transport vesicles segregated to the apical cytoplasm, while larger organelles, including the Golgi bodies and the endosomes, are largely confined to the subapical and distal regions of the tube (Cheung and Wu, 2008). For a majority of the secreted proteins that have been examined, vesicles loaded with these proteins accumulate in the apical zone, presumably either in transit to fusion with the plasma membrane or as recycled vesicles after endocytosis (Parton et al., 2001). Growth perturbation unfailingly associates with disruption of the polarized organellar distribution pattern, in particular dissipation of the apical collections of vesicles. In tobacco (Nicotiana tabacum) pollen tubes, GFP-NtRAB2 associates efficiently with Golgi bodies. Expression of DN NtRAB2s substantially reduced the delivery of GFP-labeled Golgi-located cargo proteins to their destination, while cytoplasmic and a reticular membrane signal were augmented, supporting a role for NtRAB2 in the early secretory pathway. While not prohibiting cell membrane protein localization, their delivery was compromised as the normal accumulation of vesicles loaded with these cargo molecules in the tube apex and pollen tube growth rate were both reduced. In maize, hypermorphic mutations in one of its RAB2s, ZmRAB2A1, induces wart-like structures on leaf surfaces, suggesting a role in cell wall secretion in expanding leaf cells (Zhang et al., 2007).

RAB11/RABA

In both yeast and animal systems, the number of RAB11/YPT31/32-like Rab GTPases are relatively small in comparison to the entire RAB GTPase family complement, three of approximately 66 in Homo sapiens and two of 11 in yeast (Pereira-Leal and Seabra, 2001; Stenmark and Olkkonen, 2001). In contrast, 26 of the 57 RAB GTPases present in Arabidopsis are RAB11/YPT31/32-related GTPases. Intriguingly, the large number of RAB11/RABA GTPases seem to be a conserved feature in most plants, as large numbers of this class of proteins have also been identified in legumes and monocots (Borg et al., 1997; Zhang et al., 2007).

In animals, members of the RAB11 family have been found to regulate trafficking through specialized endosomal compartments called recycling endosomes (Ullrich et al., 1996), while in yeast, YPT31/32 regulate exit of secretory and endocytic cargo from the trans-Golgi cisterna (Benli et al., 1996; Jedd et al., 1997; Chen et al., 2005). More recently, roles for these RAB GTPases in aspects of yeast and animal cell cytokinesis have been identified as well (Pelissier et al., 2003; Riggs et al., 2003; Ortiz and Novick, 2006).

What role do Rab11/RABA GTPases play in growth and development of plants? Several lines of evidence suggest that at least some members of this RAB GTPase family play important roles in secretion and/or recycling of cell wall components in plants. Several RAB11/RABA GTPases have now been localized either as fluorescent fusion proteins or by cell fractionation techniques and appear to localize to compartments that partially overlap with trans-Golgi elements and endosomal compartments (Inaba et al., 2002; Preuss et al., 2004; de Graaf et al., 2005; Chow et al., 2008). Antisense inhibition of RAB11 GTPases in tomato (Solanum lycopersicum) results in complex developmental abnormalities and delayed fruit ripening, which could be attributed to impaired cell wall deposition (Lu et al., 2001). In Arabidopsis, RABA4b displays polarized distribution to membrane compartments that accumulate at the tips of growing root hair cells (Preuss et al., 2004) and, through its interaction with a pair of phosphatidylinositol 4-OH kinases, regulates proper root hair growth (Preuss et al., 2006). Additionally, in tobacco pollen, NtRAB11b localizes to vesicular congregates that, while rapidly cycling in and out of the apical zone of growing pollen tubes, concentrate at the tips of these polar growth cells (Supplemental Movie S1). Overexpression of DN and CA mutant forms of this RAB GTPase interfered with pollen tube expansion, in particular with focused growth at the tip (de Graaf et al., 2005). These results suggest a common role for members of the RAB11/RABA GTPases in the regulation of tip growth, possibly through polarized secretion of new cell wall components or through control of polar recycling events during pollen tube and root hair expansion. More recently, examination of the subcellular distribution of two other Arabidopsis RAB11/RABA, RAB-A2 and RAB-A3, has shown that these Rab GTPases localize to membranes that specifically label the margins of growing phragmoplasts. Intriguingly, the membrane compartments to which these two RAB11/RABA family members were localized could be labeled with the bulk-flow endocytic marker, FM4-64, implying that at least some members of the RAB11/RABA compartments are reached by endocytic membrane traffic. Further, in this study, inducible expression of a DN form of RAB-A2 resulted in formation of multinucleate cells and cell wall stubs consistent with a role in polarized delivery of cargo to sites of new cell wall synthesis (Chow et al., 2008).

Taken together, these results highlight a role for members of the RAB11/RABA GTPase family in trafficking events between the plant trans-Golgi network and the plasma membrane. Major challenges going forward in the study of these membrane compartments will be to determine the extent to which this large family of RAB11/RABA GTPases resides on similar or distinct compartments and to determine to what extent these compartments are involved in trafficking of secretory or endocytic cargo.

RAB8/RABE

The yeast and mammalian RAB8 homologs show functional association with polarized secretion of proteins from the Golgi apparatus to the plasma membrane, such as regulating polarized secretion during the budding process in yeast (Salminen and Novick, 1987; Goud et al., 1988) and post-Golgi basolateral membrane trafficking in mammalian epithelial cells (Huber et al., 1993b). Misregulating RAB8 activity in fibroblasts resulted in cellular protrusions and relocalization of actin to membrane protrusion sites and mislocalization of apical proteins (Peranen et al., 1996; Hattula et al., 2006; Sato et al., 2007). In immature and fully polarized neurons in culture, RAB8 preferentially localizes to axons and dendrites; antisense suppression impairs anterograde trafficking in these neurites (Huber et al., 1993a, 1995). Rab8-mediated vesicle trafficking is also critical for membrane assembly in the primary cilium, a hair-like organelle with sensory function on the surface of most vertebrate cells (Nachury et al., 2007). The Arabidopsis RAB8/RABE family is comprised of five closely related members (Rutherford and Moore, 2002; Vernoud et al., 2003). So far, functional studies have been reported only for RABE1d in transiently transformed epidermal cells. Studies based on a DN form of RABE1d in conjunction with similar mutations in the RAB5 and RAB11 class of GTPases, RABD2 and RABF2, respectively, and a large number of differentially labeled marker proteins or indicator dyes showed that the Arabidopsis RABE-regulated step is post-Golgi and that DN RABE1d inhibits anterograde trafficking to the plasma membrane and diverts secretory activity to the vacuolar pathway (Zheng et al., 2005). In tomato, a RAB8 GTPase has been identified as interacting with the avirulence factor avrPto from the pathogen Pseudomonas sp., and this interaction was dependent on the presence of the host cell resistance protein, implying a possible role in vesicular activity associated with the launch of a defense response (Bogdanove and Martin, 2000). An ethylene-induced RAB8 homolog has also been identified from tomato, suggesting a role in ethylene-regulated cell wall dissolution processes that are dependent on enhanced secretion of hydrolytic proteins (Moshkov et al., 2003). It will be important to dissect how the RAB8/RABE- and RAB11/RABA-regulated pathways intercept and diverge in the post-Golgi steps of membrane trafficking.

RAB5/RABF

The best-characterized RAB GTPase in animals is RAB5, which was initially demonstrated to regulate homotypic early endosomal fusion and fusion between plasma membrane-derived endocytic vesicles and early endosomes (Gorvel et al., 1991; Bucci et al., 1992). Later, this small GTPase was shown to be involved in a wide spectrum of endocytic events, including endosome motility along microtubules (Nielsen et al., 1999; Hoepfner et al., 2005), compartmentalization of membrane domains on endosomes through the regulation of phospholipid contents (Christoforidis et al., 1999; Miaczynska and Zerial, 2002), and direct signaling between the endosomes and nucleus (Miaczynska et al., 2004). In contrast, the physiological significance of RAB5 members in plants was not described until several years ago, though the first plant RAB5 homolog was isolated over 15 years ago (Terryn et al., 1992). This could be due to the skepticism surrounding the occurrence of endocytosis in plant cells (Aniento and Robinson, 2005). Today, however, constitutive recycling and ligand- or substrate-induced endocytosis of plasma membrane proteins and lipids have been firmly demonstrated. Endocytosis in plant cells is now recognized as an essential part of plant life (Geldner and Jürgens, 2006), which brought attention to the mechanism involving RAB5.

There are three RAB5 homologs in the Arabidopsis genome: RAB5F2a/RHA1, RAB5F2b/ARA7, and RAB5F1/ARA6 (Ueda et al., 2001; Figs. 2 and 3). The two RAB5F2 genes seem to be orthologous to animal RAB5s, because they encode GTPases with high overall similarity to animal RAB5s. In contrast, RAB5F1 harbors unique structural features, such as N-terminal fatty acylation sites instead of a C-terminal Cys motif. This particular RAB5 has not yet been identified in organisms other than plants, making its presence one of the more remarkable features of the organization of plant RAB GTPases in addition to an extremely expanded RAB11A family.

Several lines of evidence indicate that plant RAB5s function in the endocytic pathway. All three Arabidopsis RAB5F proteins localize on punctate organelles, which are labeled by the endocytosis tracer FM4-64 (Ueda et al., 2004; Takano et al., 2005; Jaillais et al., 2008; see also Fig. 3B). The internalization of FM4-64 was inhibited by overexpressed DN RAB5F2b, and endocytosed BOR1, a boron transporter whose endocytosis from the plasma membrane is induced by an elevated boron concentration, passed through the RAB5F2b-positive endosomes en route to the vacuoles (Takano et al., 2005). These results indicate the presence of an endosomal property for RAB5F-positive organelles.

It was recently reported that the plant trans-Golgi domain also harbors endosomal property. RAB11A2a- and RAB11A3-positive compartments are stained by FM4-64 before this dye reaches endosomes bearing RAB5F2 or GNOM (Chow et al., 2008). These RABA compartments partially overlap with VHA-A1-positive compartments, which are also stained by FM4-64 after a shorter period of incubation than RAB5F2 endosomes (Dettmer et al., 2006). These results likely indicate that RAB11A compartments function as earlier endosomes than RAB5F2 endosomes; it is not clear yet, however, whether RAB11A, RAB5F2, and GNOM compartments function in the same endocytic route in a sequential manner or are on different pathways. Time lapse localization of cargo proteins such as BOR1, FLS2, and PIN1, whose endocytosis can be triggered or inhibited by its ligands or substrates (Paciorek et al., 2005; Takano et al., 2005; Robatzek et al., 2006) on distinct endosomes, will be helpful to be more conclusive.

On the other hand, there are implications that RAB5F2 plays critical roles in the biosynthetic vacuolar transport pathway. Both RAB5F2 proteins colocalize with marker molecules known to be on the prevacuolar compartment or multivesiculated endosomes (Figs. 2 and 3; Sohn et al., 2003; Kotzer et al., 2004; Lee et al., 2004; Ueda et al., 2004), and overexpression of DN RAB5F2 perturbs the transport of soluble vacuolar proteins to vacuoles (Sohn et al., 2003; Kotzer et al., 2004). Thus, RAB5F2 proteins should be involved in both endocytic and vacuolar transport pathways, suggesting that these two transport pathways merge at RAB5F2-positive organelles in plant cells.

RAB5F1 and RAB5F2 localize on different populations of multivesiculated endosomes/prevacuolar compartments with considerable overlap (Ueda et al., 2004; Haas et al., 2007), suggesting that these two RAB5F groups have different functions. This is also supported by different genetic interactions with the gene encoding their common GEF, VPS9a (Goh et al., 2007), though further studies are needed. The RAB5F2 homolog is found in almost all plant lineages, which suggests that the critical roles of RAB5 in vesicular trafficking are well conserved in plants. The only known exception is a unicellular red alga with a very small genome, Cyanidioschyzon merolae, which does not harbor a RAB5-related sequence (Matsuzaki et al., 2004). It is also of interest to ask whether C. merolae carries out endocytosis and, if so, how it is performed.

RAB7/RABG

Mammalian RAB7 is known to regulate membrane fusion at the late endosomes, and its yeast counterpart, Ypt7, mediates the fusion of vacuoles. Plants also harbor genes homologous to RAB7 whose functions, however, have not yet been clearly revealed. The Arabidopsis genome encodes eight putative RAB7 proteins, seven of which localize to the vacuolar membrane (Saito et al., 2002; T. Ueda, unpublished data; Fig. 3A). The functions of the RAB7G proteins seem to be highly redundant, because multiple mutants (double, triple, and quadruple mutants) do not show any abnormal phenotype (T. Ueda, unpublished data). On the other hand, the vacuoleless1 mutant, in which a subunit of a putative downstream effector complex of RAB7G was mutated, exhibits embryonic lethality (Rojo et al., 2001), suggesting the importance of RAB7G function in plant development. RAB7G could also be involved in the stress response, as indicated by the overexpression of RAB7G3e conferring salt and osmotic stress tolerance (Mazel et al., 2004). Further biochemical and genetic analyses, as well as cytological studies, will unveil the function of this group more precisely.

SAR AND ARF GTPASES

The formation of transport vesicles on donor membranes begins with the assembly of several sets of coat protein complexes (COPs) mediated by a class of small GTPases, the SAR/ARF family. Recent studies in S. cerevisiae and mammalian cells have revealed that this class of GTPase regulates multiple sequential steps in the formation of transport vesicles, including coat recruitment, cargo sorting, completion of fission, and uncoating transport vesicles. Each transport step seems to employ specific sets of coat proteins and regulatory GTPase, for example, COPII and SAR1 in transport from the ER to the Golgi, COPI and ARF1 in transport from the Golgi to the ER or intra-Golgi traffic, and clathrin-adaptor complexes and ARFs in multiple steps in post-Golgi or endocytic pathways (for review, see Gillingham and Munro, 2007; Sato and Nakano, 2007). Most coat proteins and SAR/ARF GTPases are well conserved in plants, so the molecular framework associated with COPs and SAR/ARF seems to be also.

SAR1, now included in the ARF family, was identified as a multicopy suppressor of sec12 mutant in yeast. Sec12p was later found to be an activating GEF for Sar1p (Nakano and Muramatsu, 1989; Barlowe and Schekman, 1993). Sar1p directly binds to the COPII component, a heterodimer of Sec23p and Sec24p, which further recruits the Sec13p-Sec31p subcomplex. Sec24p also binds exposed cytoplasmic signals of transmembrane cargo, facilitating the sorting of cargo molecules into COPII vesicles. Because plant SAR1 can substitute the function of yeast Sar1p (d'Enfert et al., 1992; Takeuchi et al., 1998), the molecular function of SAR1 should be conserved in plants, whereas the spatial distribution and organization of plant ER export sites (ERES), where SAR1 is expected to act, are regulated in a distinct manner from yeasts or animals (Hanton et al., 2006).

In plants, organization of membrane trafficking pathways between the ER and Golgi compartments display important differences from animal and yeast systems. Yeast generally do not organize Golgi membranes into stacks (Preuss et al., 1992), and while in animals Golgi stacks are organized in large ribbon-like arrays around the microtubule-organizing center, plants instead contain large numbers of independent mini-stacks that display motility along bundled actin filaments (Boevink et al., 1998; Ladinsky et al., 1999). The distinctions with regard to spatial distributions of ER and Golgi membranes in these different systems have led to interesting questions regarding the roles and placement of elements of the COPII- and COPI-mediated trafficking components (Hawes, 2005). In plants, AtSAR1 proteins associate with ER membranes as well as localizing at Golgi-associated ERES and interference with SAR1 activity results in defects in trafficking from the ER to the Golgi (Bar-Peled and Raikhel, 1997; daSilva et al., 2004; Hanton et al., 2008). On the other hand, some plant COPII components display unique distributions on ER membranes. Unlike other systems, fluorescent protein fusions of several of the COPII coat proteins (Sec13, Sec23, and Sec24) have been found localized at ERES in the vicinity of mobile Golgi stacks (Yang et al., 2005; Matheson et al., 2006; Stefano et al., 2006; Hanton et al., 2007), while Sec12 is distributed uniformly over the ER (daSilva et al., 2004; Yang et al., 2005). This finding suggests that elements of the COPII vesicle coat may be assembled on areas of the ER besides the ERES at the ER/Golgi interface (Hanton et al., 2008).

ARF was first identified as a cofactor required in the ADP-ribosylation of Gαs by cholera toxin (Enomoto and Gill, 1980; Kahn and Gilman, 1984), but the ADP-ribosylation appears not to be involved in normal cellular activity. The mammalian ARF family (excluding SARs) consists of ARF and ARL (ARF-like). ARF proteins are further classified into three subclasses based on structural and functional criteria. Class-I ARF are reported to facilitate the assembly of COPI and to play a role in effective cargo sorting. However, the precise molecular mechanisms of COPI vesicle formation and cargo selection have not been clearly elucidated compared to COPII vesicles due to the lack of an in vitro reconstitution system for this process. Small GTPases structurally, but not functionally, related to ARF proteins are designated as ARL and are involved in various cellular activities. In plants, ARF1 has been shown to localize to Golgi and endosomes, and interference with this protein affects various plant functions, such as cell polarity determination, cell proliferation, cell elongation, and fertility (Gebbie et al., 2005; Xu and Scheres, 2005). Furthermore, ARFB, which shows significant homology to mammalian ARF6, localizes to the plasma membrane (Matheson et al., 2008).

Plants express a conserved family of ARF proteins consisting of ARF and ARL subgroups (Vernoud et al., 2003). Plant ARFs seem to have critical roles in multiple steps of the membrane traffic pathways, including retrograde and anterograde ER-Golgi trafficking and BP80-dependent vacuolar transport (Lee et al., 2002; Takeuchi et al., 2002; Pimpl et al., 2003). Extensive studies done recently on the ARF GEFs demonstrated that temporally and spatially regulated activation of ARF is critical for both transport through the Golgi and endosomal recycling (Richter et al., 2007; Teh and Moore, 2007). As for ARL proteins, a few reports indicate that this subgroup is also involved in various cellular functions (McElver et al., 2000; Steinborn et al., 2002; Stefano et al., 2006), but the molecular and physiological significance of most ARL members is still to be determined.

THE GTPASE CYCLE IS THE ENGINE THAT DRIVES VECTORIAL TRANSPORT

As described earlier, the molecular switch function of a small GTPase is carried out by cycling between its active GTP-bound form and the inactive GDP-bound form (Fig. 1). Switching from the inactive to active state is accomplished by replacing bound GDP with GTP, which requires GEF. Functional counterparts of Sec12p, the GEF for the yeast Sar1p, are conserved in animals and plants. ARF GEFs are distinguished by a conserved Sec7 domain. Though eukaryotic ARF GEFs are subclassed into eight groups, Arabidopsis contains only two groups of ARF-associated GEF, GBF, and BIG proteins, suggesting that there was unique evolution of plant ARF GEFs. In fact, recent studies revealed that two GBF-type ARF GEFs, GNOM and GNL1, which are likely to have derived from the common ancestral ARF GEF, are functionally differentiated; GNOM acquired a function in endosomal recycling in addition to the ancestral function on the Golgi (Richter et al., 2007; Teh and Moore, 2007). Our knowledge of the RAB GEF in plants is still limited, but VPS9a from Arabidopsis was recently found to be a specific GEF for RAB5 (Goh et al., 2007). VPS9a seems to be practically the sole RAB5 GEF that activates both plant-unique and conventional RAB5s in Arabidopsis. In contrast, many RAB5 GEFs with divergent domain structures have been shown to activate RAB5 at distinct steps in the endocytic pathway in animal cells (Carney et al., 2006). These results suggest that RAB GEFs have also evolved uniquely from the animal system.

After performing functions in their active form, GTPases are inactivated by hydrolyzing GTP to GDP, which is accelerated by the GAP (Fig. 1). GTP hydrolysis on the yeast Sar1p is facilitated by Sec23p, which also has a homolog in Arabidopsis. There are 15 putative ARF GAPs in Arabidopsis, only some of which have been characterized. For example, van3 and scarface were isolated as mutants associated with abnormal vein patterning in an independent screening and are allelic mutants of an ARF GAP (Koizumi et al., 2005; Sieburth et al., 2006). The previously mentioned GNOM was also identified as a gene responsible for a mutated vein patterning (Koizumi et al., 2000). Taken together, this suggests that a correctly regulated ARF GTPase cycle, which is also essential for proper auxin transport, is critical for normal vein patterning. Another ARF GAP, RPA, activates GTPase activity of ARF1. rpa mutants are defective in root hair development, indicating that ARF also plays an important role in tip growth (Song et al., 2006). Although RAB GAP-like activity in plant cells was detected earlier (Anai et al., 1994) and a rice RAB-GAP has been isolated (Heo et al., 2005), there is currently little information available on its physiological role.

Once inactivated, small GTPases detach from the membrane and are kept in the GDP-bound inactive state until the next round of the GTPase activation cycle begins (Fig. 1). While SAR/ARF members do not require specific factors for this process, dissociation of most RAB GTPases from membranes is mediated by a conserved protein family, the RAB GDP dissociation inhibitor (RAB GDI). The only exception to this is RAB5F1/ARA6, which is recycled from membranes independently of RAB GDI (Ueda et al., 2001). RAB GDI binds only to GDP-bound RABs and keeps them in the GDP-bound state by inhibiting GDP release. Plants also harbor functionally conserved RAB GDIs with broad substrate specificity (Ueda et al., 1996; Zarsky et al., 1997; Ueda et al., 1998), in contrast to GEFs and GAPs, which interact only with specific RAB members. A new round of the GTPase cycle begins with dissociation from the GDI and attachment to the membrane, which is mediated by GDI displacement factor. The Pra/Yip family of proteins, whose homologs are also found in plants, is proposed to undertake this function (Sivars et al., 2003) but has not yet been tested in plants.

EFFECTORS AND DOWNSTREAM FUNCTION

While GTP-binding and hydrolysis are intrinsic to RAB GTPase regulatory function, it is the recruitment and interaction of the RAB GTPases with cytosolic effector proteins that allow these RAB GTPases to carry out their regulatory functions in membrane trafficking. In animal and yeast systems, significant progress has been made in identifying RAB effector proteins (Zerial and McBride, 2001; Grosshans et al., 2006; Pfeffer, 2007). Initial models of RAB GTPase function indicated that these small GTPases played an essential role in regulation of membrane recognition events just prior to membrane fusion (Salminen and Novick, 1987; Novick and Brennwald, 1993). However, as identification of RAB effector proteins has proceeded, the functions of these effectors have highlighted additional roles for RAB GTPases in membrane-trafficking events. As a result, current models of RAB GTPase function involve roles in diverse aspects of membrane trafficking, such as vesicle formation (Carroll et al., 2001), recruitment of cytoskeletal motor proteins (Wu et al., 1998; Echard et al., 1998; Nielsen et al., 1999; Wagner et al., 2002; Hoepfner et al., 2005), and vesicle tethering and fusion (Christoforidis et al., 1999; Guo et al., 1999; Tall et al., 1999; Nielsen et al., 2000; Moyer et al., 2001).

In plants, very few RAB effector proteins have been identified and characterized. The structural heterogeneity of RAB effectors makes it unlikely that plant RAB effectors can be identified by sequence similarity alone (Zerial and McBride, 2001). However, some established RAB effectors, such as lipid kinases (Christoforidis et al., 1999), are present in Arabidopsis. One such lipid kinase, PI-4 Kβ1, has been shown to be an effector of RABA4b and plays important roles in regulation of polarized secretion in plants (Preuss et al., 2006). Additionally, specific lipid-binding domains are associated with RAB effector protein functions (Simonsen et al., 1998; Christoforidis et al., 1999), and GFP-2xFYVE domains have been shown to be selectively recruited to endosomal compartments (Voigt et al., 2005), indicating that plant endosomes also selectively accumulate PI-3P. Clearly, further identification of plant RAB effector proteins is urgently needed to expand our understanding of RAB GTPase functions during membrane trafficking in plants and will be required to elucidate the specifically tailored roles of plant RAB GTPase and their unique functions in plant-specific membrane trafficking.

PROSPECTUS

As the framework for fundamental characterization of the regulatory small GTPases for vesicular trafficking is already quite well established, future challenges lie in obtaining a precise understanding of how these plant RABs and ARFs act on the cellular level and how the processes they mediate impact overall plant growth, development, and response to the environment. How the functions of members within each of the RAB subclasses are conserved or have diverged and to what extent members from different subclasses may overlap in their functional pathways remain largely unexplored in plants. On the cell biological and biochemical levels, identification of effectors is likely to be an effective means to resolve functional divergence among related small GTPases and reveal how specificity between these small GTPases and the trafficking pathway they mediate is established. Imaging approaches that resolve dynamic interactions (see e.g. Held et al., 2008) between these small GTPases with their regulators, effectors, and their target membrane compartments should elucidate transient regulatory and functional events that are most likely to be important aspects of how vesicular trafficking pathways are regulated. While understanding of the functional significance of RAB- and ARF-regulated vesicular trafficking in cell growth and plant development is emerging, how plants rely on a responsive membrane-trafficking system to meet specific biotic and abiotic challenges, such as in response to pathogens and wounding, remains to be explored. These efforts together will reach beyond establishing RABs and ARFs as fundamental regulators of vesicular trafficking in plant cells to elucidate the roles that these small GTPases have evolved to meet needs that are unique to the growth and developmental strategies in plants.

Supplemental Data

The following materials are available in the online version of this article.

  • Supplemental Movie S1. Trafficking of GFP-NtRAB11b-labeled vesicular bodies in elongating tobacco pollen tubes showing the dynamics of vesicular trafficking in these polar growth cell types and differential localization of the RAB11-labeled vesicular structures to the apical cytoplasm. Reproduced from Cheung and Wu (2008).

Footnotes

  • 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: Alice Y. Cheung (acheung{at}biochem.umass.edu).

  • www.plantphysiol.org/cgi/doi/10.1104/pp.108.121798

  • ↵1 This work was supported by the U.S. Department of Energy (grant no. DE–FG02–0#ER15412 to E.N.), by the U.S. Department of Agriculture (grant no. CSREES 2005–35304–16030 to A.Y.C.), and by the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grants-in-Aid for Scientific Research to T.U.).

  • ↵[W] The online version of this article contains Web-only data.

  • Received April 22, 2008.
  • Accepted May 23, 2008.
  • Published August 6, 2008.

LITERATURE CITED

  1. ↵
    Anai T, Matsui M, Nomura N, Ishizaki R, Uchimiya H (1994) In vitro mutation analysis of Arabidopsis thaliana small GTP-binding proteins and detection of GAP-like activities in plant cells. FEBS Lett 346: 175–180
    OpenUrlCrossRefPubMed
  2. ↵
    Aniento F, Robinson DG (2005) Testing for endocytosis in plants. Protoplasma 226: 3–11
    OpenUrlCrossRefPubMed
  3. ↵
    Bar-Peled M, Raikhel NV (1997) Characterization of AtSEC12 and AtSAR1. Proteins likley involved in endoplasmic reticulum and Golgi transport. Plant Physiol 114: 315–324
    OpenUrlAbstract
  4. ↵
    Barlowe C, Schekman R (1993) SEC12 encodes a guanine-nucleotide-exchange factor essential for transport vesicle budding from the ER. Nature 365: 347–349
    OpenUrlCrossRefPubMed
  5. ↵
    Batoko H, Zheng HQ, Hawes C, Moore I (2000) A Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12: 2201–2217
    OpenUrlAbstract/FREE Full Text
  6. ↵
    Benli M, Doring F, Robinson DG, Yang X, Gallwitz D (1996) Two GTPase isoforms, Ypt31p and Ypt31p, are essential for Golgi function in yeast. EMBO J 15: 6460–6475
    OpenUrlPubMed
  7. ↵
    Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15: 441–447
    OpenUrlCrossRefPubMed
  8. ↵
    Bogdanove AJ, Martin GB (2000) AvrPto-dependent Pto-interacting proteins and AvrPto-interacting proteins in tomato. Proc Natl Acad Sci USA 97: 8836–8840
    OpenUrlAbstract/FREE Full Text
  9. ↵
    Borg S, Brandstrup B, Jensen TJ, Poulsen C (1997) Identification of new protein species among 33 different small GTP-binding proteins encoded by cDNAs from Lotus japonicus, and expression of corresponding mRNAs in developing root nodules. Plant J 11: 237–250
    OpenUrlCrossRefPubMed
  10. ↵
    Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70: 715–728
    OpenUrlCrossRefPubMed
  11. ↵
    Carney DS, Davies BA, Horazdovsky BF (2006) Vps9 domain-containing proteins: activators of Rab5 GTPases from yeast to neurons. Trends Cell Biol 16: 27–35
    OpenUrlCrossRefPubMed
  12. ↵
    Carroll KS, Hanna J, Simon I, Krise J, Barbero P, Pfeffer SR (2001) Role of Rab9 GTPase in facilitating receptor recruitment by TIP47. Science 292: 1373–1376
    OpenUrlAbstract/FREE Full Text
  13. ↵
    Chen SH, Chen S, Tokarev AA, Liu F, Jedd G, Segev N (2005) Ypt31/32 GTPases and their novel F-box effector protein Rcy1 regulate protein recycling. Mol Biol Cell 16: 178–192
    OpenUrlAbstract/FREE Full Text
  14. ↵
    Cheung AY, Chen CY, Glaven RH, de Graaf BH, Vidali L, Hepler PK, Wu HM (2002) Rab2 GTPase regulates vesicle trafficking between the endoplasmic reticulum and the Golgi bodies and is important to pollen tube growth. Plant Cell 14: 945–962
    OpenUrlAbstract/FREE Full Text
  15. ↵
    Cheung AY, Wu H (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59: 547–572
    OpenUrlCrossRefPubMed
  16. ↵
    Chow CM, Neto H, Foucart C, Moore I (2008) Rab-A2 and Rab-A3 GTPases define a trans-golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. Plant Cell 20: 101–123
    OpenUrlAbstract/FREE Full Text
  17. ↵
    Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, Yip SC, Waterfield MD, Backer JM, Zerial M (1999) Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1: 249–252
    OpenUrlCrossRefPubMed
  18. ↵
    d'Enfert C, Gensse M, Gaillardin C (1992) Fission yeast and a plant have functional homologues of the Sar1 and Sec12 proteins involved in ER to Golgi traffic in budding yeast. EMBO J 11: 4205–4211
    OpenUrlPubMed
  19. ↵
    daSilva LL, Snapp EL, Denecke J, Lippincott-Schwartz J, Hawes C, Brandizzi F (2004) Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16: 1753–1771
    OpenUrlAbstract/FREE Full Text
  20. ↵
    de Graaf BH, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, Wu HM (2005) Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 17: 2564–2579
    OpenUrlAbstract/FREE Full Text
  21. ↵
    Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715–730
    OpenUrlAbstract/FREE Full Text
  22. ↵
    Echard A, Jollivet F, Martinez O, Lacapere JJ, Rousselet A, Janoueix-Lerosey I, Goud B (1998) Interaction of a Golgi-associated kinesin-like protein with Rab6. Science 279: 580–585
    OpenUrlAbstract/FREE Full Text
  23. ↵
    Enomoto K, Gill DM (1980) Cholera toxin activation of adenylate cyclase. Roles of nucleoside triphosphates and a macromolecular factor in the ADP ribosylation of the GTP-dependent regulatory component. J Biol Chem 255: 1252–1258
    OpenUrlFREE Full Text
  24. ↵
    Gebbie LK, Burn JE, Hocart CH, Williamson RE (2005) Genes encoding ADP-ribosylation factors in Arabidopsis thaliana L. Heyn.; genome analysis and antisense suppression. J Exp Bot 56: 1079–1091
    OpenUrlAbstract/FREE Full Text
  25. ↵
    Geldner N, Jürgens G (2006) Endocytosis in signaling and development. Curr Opin Plant Biol 9: 589–594
    OpenUrlCrossRefPubMed
  26. ↵
    Gillingham AK, Munro S (2007) The small G proteins of the Arf family and their regulators. Annu Rev Cell Dev Biol 23: 579–611
    OpenUrlCrossRefPubMed
  27. ↵
    Goh T, Uchida W, Arakawa S, Ito E, Dainobu T, Ebine K, Takeuchi M, Sato K, Ueda T, Nakano A (2007) VPS9a, the common activator for two distinct types of Rab5 GTPases, is essential for the development of Arabidopsis thaliana. Plant Cell 19: 3504–3515
    OpenUrlAbstract/FREE Full Text
  28. ↵
    Goncalves S, Cairney J, Rodriguez MP, Canovas F, Oliveira M, Miquel C (2007) PpRab1, a Rab GTPase from maritime pine is differentially expressed during embryogenesis. Mol Genet Genomics 278: 273–282
    OpenUrlCrossRefPubMed
  29. ↵
    Gorvel JP, Chavrier P, Zerial M, Gruenberg J (1991) rab5 controls early endosome fusion in vitro. Cell 64: 915–925
    OpenUrlCrossRefPubMed
  30. ↵
    Goud B, Salminen A, Walworth NC, Novick PJ (1988) A GTP-binding protein required for secretion rapidly associates with secretory vesicles and the plasma membrane in yeast. Cell 53: 753–768
    OpenUrlCrossRefPubMed
  31. ↵
    Grosshans BL, Ortiz D, Novick P (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci USA 103: 11821–11827
    OpenUrlAbstract/FREE Full Text
  32. ↵
    Guo W, Roth D, Walch-Solimena C, Novick P (1999) The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J 15: 1071–1080
    OpenUrl
  33. ↵
    Haas TJ, Sliwinski MK, Martinez DE, Preuss M, Ebine K, Ueda T, Nielsen E, Odorizzi G, Otegui MS (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19: 1295–1312
    OpenUrlAbstract/FREE Full Text
  34. ↵
    Hanton SL, Chatre L, Matheson LA, Rossi M, Held MA, Brandizzi F (2008) Plant Sar1 isoforms with near-identical protein sequences exhibit different localizations and effects on secretion. Plant Mol Biol 67: 283–294
    OpenUrlCrossRefPubMed
  35. ↵
    Hanton SL, Chatre L, Renna L, Matheson LA, Brandizzi F (2007) De novo formation of plant endoplasmic reticulum export sites is membrane cargo induced and signal mediated. Plant Physiol 143: 1640–1650
    OpenUrlAbstract/FREE Full Text
  36. ↵
    Hanton SL, Matheson LA, Brandizzi F (2006) Seeking a way out: export of proteins from the plant endoplasmic reticulum. Trends Plant Sci 11: 335–343
    OpenUrlCrossRefPubMed
  37. ↵
    Haubruck H, Prange R, Vorgias C, Gallwitz D (1989) The ras-related ypt1 protein can functionally replace the YPT1 gene product in yeast. EMBO J 8: 1427–1432
    OpenUrlPubMed
  38. ↵
    Hattula K, Furuhjelm J, Tikkanen J, Tanhuanpaa K, Laakkonen P, Peranen J (2006) Characterization of the Rab8-specific membrane traffic route linked to protrusion formation. J Cell Sci 119: 4866–4877
    OpenUrlAbstract/FREE Full Text
  39. ↵
    Hawes C (2005) Cell biology of the plant Golgi apparatus. New Phytol 165: 29–44
    OpenUrlCrossRefPubMed
  40. ↵
    Held MA, Boulaflous A, Brandizzi F (2008) Advances in fluorescent protein-based imaging for the analysis of plant endomembranes. Plant Physiol 147: 1469–1481
    OpenUrlFREE Full Text
  41. ↵
    Heo JB, Rho HS, Kim SW, Hwang SM, Kwon HJ, Nahm MY, Bang WY, Bahk JD (2005) OsGAP1 functions as a positive regulator of OsRab11-mediated TGN to PM or vacuole trafficking. Plant Cell Physiol 46: 2005–2018
    OpenUrlAbstract/FREE Full Text
  42. ↵
    Hoepfner S, Severin F, Cabezas A, Habermann B, Runge A, Gillooly D, Stenmark H, Zerial M (2005) Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121: 437–450
    OpenUrlCrossRefPubMed
  43. ↵
    Huber LA, De Hoop MJ, Dupree P, Zerial M, Simons K (1993a) Protein transport to the dendritic plasma membrane of cultured neurons is regulated by rab8p. J Cell Biol 123: 47–55
    OpenUrlAbstract/FREE Full Text
  44. ↵
    Huber LA, Dupree P, Dotti CG (1995) A deficiency of the small GTPase rab8 inhibits membrane traffic in developing neurons. Mol Cell Biol 15: 918–924
    OpenUrlAbstract/FREE Full Text
  45. ↵
    Huber LA, Pimplikar S, Parton RG, Virta H, Zerial M, Simons K (1993b) Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J Cell Biol 123: 35–45
    OpenUrlAbstract/FREE Full Text
  46. ↵
    Inaba T, Nagano Y, Nagasaki T, Sasaki Y (2002) Distinct localization of two closely related Ypt3/Rab11 proteins on the trafficking pathway in higher plants. J Biol Chem 277: 9183–9188
    OpenUrlAbstract/FREE Full Text
  47. ↵
    Jaillais Y, Fobis-Loisy I, Miege C, Gaude T (2008) Evidence for a sorting endosome in Arabidopsis root cells. Plant J 53: 237–247
    OpenUrlCrossRefPubMed
  48. ↵
    Jedd G, Mulholland J, Segev N (1997) Two new Ypt GTPases are required for exit form the yeast trans-Golgi compartment. J Cell Biol 137: 563–580
    OpenUrlAbstract/FREE Full Text
  49. ↵
    Kahn RA, Gilman AG (1984) Purification of a protein cofactor required for ADP-ribosylation of the stimulatory regulatory component of adenylate cyclase by cholera toxin. J Biol Chem 259: 6228–6234
    OpenUrlAbstract/FREE Full Text
  50. ↵
    Kim WY, Cheong NE, Lee DC, Lee KO, Je DY, Bahk JD, Cho MJ, Lee SY (1996) Isolation of an additional soybean cDNA encoding Ypt/Rab-related small GTP-binding protein and its functional comparison to Sypt using a yeast ypt1-1 mutant. Plant Mol Biol 31: 783–792
    OpenUrlCrossRefPubMed
  51. ↵
    Koizumi K, Naramoto S, Sawa S, Yahara N, Ueda T, Nakano A, Sugiyama M, Fukuda H (2005) VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation. Development 132: 1699–1711
    OpenUrlAbstract/FREE Full Text
  52. ↵
    Koizumi K, Sugiyama M, Fukuda H (2000) A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question. Development 127: 3197–3204
    OpenUrlAbstract
  53. ↵
    Kotzer AM, Brandizzi F, Neumann U, Paris N, Moore I, Hawes C (2004) AtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells. J Cell Sci 117: 6377–6389
    OpenUrlAbstract/FREE Full Text
  54. ↵
    Ladinsky MS, Mastronarde DN, McIntosh JR, Howell KE, Staehelin LA (1999) Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J Cell Biol 144: 1135–1149
    OpenUrlAbstract/FREE Full Text
  55. ↵
    Lee GJ, Sohn EJ, Lee MH, Hwang I (2004) The Arabidopsis Rab5 homologs Rha1 and Ara7 localize to the prevacuolar compartment. Plant Cell Physiol 45: 1211–1220
    OpenUrlAbstract/FREE Full Text
  56. ↵
    Lee MH, Min MK, Lee YJ, Jin JB, Shin DH, Kim DH, Lee KH, Hwang I (2002) ADP-ribosylation factor 1 of Arabidopsis plays a critical role in intracellular trafficking and maintenance of endoplasmic reticulum morphology in Arabidopsis. Plant Physiol 129: 1507–1520
    OpenUrlAbstract/FREE Full Text
  57. ↵
    Lu C, Zainal Z, Tucker GA, Lycett GW (2001) Developmental abnormalities and reduced fruit softening in tomato plants expressing an antisense Rab11 GTPase gene. Plant Cell 13: 1819–1833
    OpenUrlAbstract/FREE Full Text
  58. ↵
    Matheson LA, Hanton SL, Brandizzi F (2006) Traffic between the plant endoplasmic reticulum and Golgi apparatus: to Golgi and beyond. Curr Opin Plant Biol 9: 601–609
    OpenUrlCrossRefPubMed
  59. ↵
    Matheson LA, Suri SS, Hanton SL, Chatre L, Brandizzi F (2008) Correct targeting of plant ARF GTPases relies on distinct protein domains. Traffic 9: 103–120
    OpenUrlCrossRefPubMed
  60. ↵
    Matsuzaki M, Misumi O, Shin IT, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Yoshida Y, et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428: 653–657
    OpenUrlCrossRefPubMed
  61. ↵
    Mazel A, Leshem Y, Tiwari BS, Levine A (2004) Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7 (AtRabG3e). Plant Physiol 134: 118–128
    OpenUrlAbstract/FREE Full Text
  62. ↵
    McElver J, Patton D, Rumbaugh M, Liu C, Yang LJ, Meinke D (2000) The TITAN5 gene of Arabidopsis encodes a protein related to the ADP ribosylation factor family of GTP binding proteins. Plant Cell 12: 1379–1392
    OpenUrlAbstract/FREE Full Text
  63. ↵
    Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B, Wilm M, Parton RG, Zerial M (2004) APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116: 445–456
    OpenUrlCrossRefPubMed
  64. ↵
    Miaczynska M, Zerial M (2002) Mosaic organization of the endocytic pathway. Exp Cell Res 272: 8–14
    OpenUrlCrossRefPubMed
  65. ↵
    Moshkov IE, Mur LA, Novikova GV, Smith AR, Hall MA (2003) Ethylene regulates monomeric GTP-binding protein gene expression and activity in Arabidopsis. Plant Physiol 131: 1705–1717
    OpenUrlAbstract/FREE Full Text
  66. ↵
    Moyer BD, Allan BB, Balch WE (2001) Rab1 interaction with a GM130 effector complex regulates COPII vesicle cis-Golgi tethering. Traffic 2: 268–276
    OpenUrlCrossRefPubMed
  67. ↵
    Nachury MA, Loktev AV, Zhang Q, Westlake CJ, Peranen J, Merdes A, Slusarski DC, Scheller RH, Bazen JF, Sheffield VC, et al (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promoter cilia membrane biogenesis. Cell 129: 1201–1213
    OpenUrlCrossRefPubMed
  68. ↵
    Nakano A, Muramatsu M (1989) A novel GTP-binding protein, Sar1p, is involved in transport from the endoplasmic reticulum to the Golgi apparatus. J Cell Biol 109: 2677–2691
    OpenUrlAbstract/FREE Full Text
  69. ↵
    Nielsen E, Christoforidis S, Uttenweiler-Joseph S, Miaczynska M, Dewitte F, Wilm M, Hoflack B, Zerial M (2000) Rebenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J Cell Biol 151: 601–612
    OpenUrlAbstract/FREE Full Text
  70. ↵
    Nielsen E, Severin F, Backer JM, Hyman AA, Zerial M (1999) Rab5 regulates motility of early endosomes on microtubules. Nat Cell Biol 1: 376–382
    OpenUrlCrossRefPubMed
  71. ↵
    Novick P, Brennwald P (1993) Friends and family: the role of the Rab GTPases in vesicular traffic. Cell 75: 597–601
    OpenUrlCrossRefPubMed
  72. ↵
    Ortiz D, Novick PJ (2006) Ypt32p regulates the translocation of Chs3p from an internal pool to the plasma membrane. Eur J Cell Biol 85: 107–116
    OpenUrlCrossRefPubMed
  73. ↵
    Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jurgens G, Geldner N, et al (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435: 1251–1256
    OpenUrlCrossRefPubMed
  74. ↵
    Park YS, Song OK, Kwak JM, Hong SW, Lee HH, Nam HG (1997) Functional complementation of a yeast vesicular transport mutation ypt1-1 by a Brassica napus cDNA clone encoding a small GTP-binding protein. Plant Mol Biol 26: 1725–1735
    OpenUrlCrossRef
  75. ↵
    Parton RM, Fischer-Parton S, Watahiki MK, Trewavas AJ (2001) Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes. J Cell Sci 114: 2685–2695
    OpenUrlPubMed
  76. ↵
    Pelissier A, Chauvin JP, Lecuit T (2003) Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr Biol 13: 1848–1857
    OpenUrlCrossRefPubMed
  77. ↵
    Peranen J, Auvinen P, Virta H, Wepf R, Simons K (1996) Rab8 promotes polarized membrane transport through reorganization of actin and microtubules in fibroblasts. J Cell Biol 135: 153–167
    OpenUrlAbstract/FREE Full Text
  78. ↵
    Pereira-Leal JB, Seabra MC (2001) Evolution of the Rab Family of small GTP-binding proteins. J Mol Biol 313: 889–901
    OpenUrlCrossRefPubMed
  79. ↵
    Pfeffer SR (2007) Unsolved mysteries in membrane traffic. Annu Rev Biochem 76: 629–645
    OpenUrlCrossRefPubMed
  80. ↵
    Pimpl P, Hanton SL, Taylor JP, Pinto-daSilva LL, Denecke J (2003) The GTPase ARF1p controls the sequence-specific vacuolar sorting route to the lytic vacuole. Plant Cell 15: 1242–1256
    OpenUrlAbstract/FREE Full Text
  81. ↵
    Preuss D, Mulholland J, Franzusoff A, Segev N, Botstein D (1992) Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy. Mol Biol Cell 3: 789–803
    OpenUrlAbstract/FREE Full Text
  82. ↵
    Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kinase-β1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172: 991–998
    OpenUrlAbstract/FREE Full Text
  83. ↵
    Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E (2004) The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16: 1589–1603
    OpenUrlAbstract/FREE Full Text
  84. ↵
    Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20: 537–542
    OpenUrlAbstract/FREE Full Text
  85. ↵
    Richter S, Geldner N, Schrader J, Wolters H, Stierhof YD, Rios G, Koncz C, Robinson DG, Jurgens G (2007) Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448: 488–492
    OpenUrlCrossRefPubMed
  86. ↵
    Riggs B, Rothwell W, Mische S, Hickson GR, Matheson J, Hays TS, Gould GW, Sullivan W (2003) Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components nuclear-fallout and Rab11. J Cell Biol 163: 143–154
    OpenUrlAbstract/FREE Full Text
  87. ↵
    Rojo E, Gillmor CS, Kovaleva V, Somerville CR, Raikhel NV (2001) VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev Cell 1: 303–310
    OpenUrlCrossRefPubMed
  88. ↵
    Rutherford S, Moore I (2002) The Arabidopsis Rab GTPase family: another enigma variation. Curr Opin Plant Biol 5: 518–528
    OpenUrlCrossRefPubMed
  89. ↵
    Saito C, Ueda T, Abe H, Wada Y, Kuroiwa T, Hisada A, Furuya M, Nakano A (2002) A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J 29: 245–255
    OpenUrlCrossRefPubMed
  90. ↵
    Salminen A, Novick PJ (1987) A ras-like protein is required for a post-Golgi event in yeast secretion. Cell 49: 527–538
    OpenUrlCrossRefPubMed
  91. ↵
    Sato K, Nakano A (2007) Mechanisms of COPII vesicle formation and protein sorting. FEBS Lett 581: 2076–2082
    OpenUrlCrossRefPubMed
  92. ↵
    Sato T, Mushiake S, Kato Y, Sato K, Sato M, Takeda N, Ozono K, Miki K, Kubo Y, Tsuji A, et al (2007) The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448: 366–369
    OpenUrlCrossRefPubMed
  93. ↵
    Segev N, Mulholland J, Botstein D (1988) The yeast GTP-binding protein and a mammalian counterpart are associated with the secretion machinery. Cell 52: 912–924
    OpenUrl
  94. ↵
    Sieburth LE, Muday GK, King EJ, Benton G, Kim S, Metcalf KE, Meyers L, Seamen E, Van Norman JM (2006) SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. Plant Cell 18: 1396–1411
    OpenUrlAbstract/FREE Full Text
  95. ↵
    Simonsen A, Lippe R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394: 494–498
    OpenUrlCrossRefPubMed
  96. ↵
    Sivars U, Aivazian D, Pfeffer SR (2003) Yip3 catalyses the dissociation of endosomal Rab-GDI complexes. Nature 425: 856–859
    OpenUrlCrossRefPubMed
  97. ↵
    Sohn EJ, Kim ES, Zhao M, Kim SJ, Kim H, Kim YW, Lee YJ, Hillmer S, Sohn U, Jiang L, et al (2003) Rha1, an Arabidopsis Rab5 homolog, plays a critical role in the vacuolar trafficking of soluble cargo proteins. Plant Cell 15: 1057–1070
    OpenUrlAbstract/FREE Full Text
  98. ↵
    Song XF, Yang CY, Liu J, Yang WC (2006) RPA, a class II ARFGAP protein, activates ARF1 and U5 and plays a role in root hair development in Arabidopsis. Plant Physiol 141: 966–976
    OpenUrlAbstract/FREE Full Text
  99. ↵
    Stefano G, Renna L, Hanton SL, Chatre L, Haas TA, Brandizzi F (2006) ARL1 plays a role in the binding of the GRIP domain of a peripheral matrix protein to the Golgi apparatus in plant cells. Plant Mol Biol 61: 431–449
    OpenUrlCrossRefPubMed
  100. ↵
    Steinborn K, Maulbetsch C, Priester B, Trautmann S, Pacher T, Geiges B, Kuttner F, Lepiniec L, Stierhof YD, Schwarz H, et al (2002) The Arabidopsis PILZ group genes encode tubulin-folding cofactor orthologs required for cell division but not cell growth. Genes Dev 16: 959–971
    OpenUrlAbstract/FREE Full Text
  101. ↵
    Steinmann T, Geldner N, Brebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jurgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286: 316–318
    OpenUrlAbstract/FREE Full Text
  102. ↵
    Stenmark H, Olkkonen VM (2001) The Rab GTPase family. Genome Biol 2: REVIEWS3007
  103. ↵
    Takano J, Miwa K, Yuan L, von Wiren N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci USA 102: 12276–12281
    OpenUrlAbstract/FREE Full Text
  104. ↵
    Takeuchi M, Tada M, Saito C, Yashiroda H, Nakano A (1998) Isolation of a tobacco cDNA encoding Sar1 GTPase and analysis of its dominant mutations in vesicular traffic using a yeast complementation system. Plant Cell Physiol 39: 590–599
    OpenUrlAbstract/FREE Full Text
  105. ↵
    Takeuchi M, Ueda T, Yahara N, Nakano A (2002) Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J 31: 499–515
    OpenUrlCrossRefPubMed
  106. ↵
    Tall GG, Hama H, DeWald DB, Horazdovsky BF (1999) The phosphatidylinositol homologue to facilitate vesicle-mediated vacuolar protein sorting. Mol Biol Cell 10: 1873–1889
    OpenUrlAbstract/FREE Full Text
  107. ↵
    Teh OK, Moore I (2007) An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448: 493–496
    OpenUrlCrossRefPubMed
  108. ↵
    Terryn N, Anuntalabhochai S, Van Montagu M, Inze D (1992) Analysis of a Nicotiana plumbaginifolia cDNA encoding a novel small GTP-binding protein. FEBS Lett 299: 287–290
    OpenUrlCrossRefPubMed
  109. ↵
    Ueda T, Matsuda N, Anai T, Tsukaya H, Uchimiya H, Nakano A (1996) An Arabidopsis gene isolated by a novel method for detecting genetic interaction in yeast encodes the GDP dissociation inhibitor of Ara4 GTPase. Plant Cell 8: 2079–2091
    OpenUrlAbstract/FREE Full Text
  110. ↵
    Ueda T, Uemura T, Sato MH, Nakano A (2004) Functional differentiation of endosomes in Arabidopsis cells. Plant J 40: 783–789
    OpenUrlCrossRefPubMed
  111. ↵
    Ueda T, Yamaguchi M, Uchimiya H, Nakano A (2001) Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J 20: 4730–4741
    OpenUrlAbstract
  112. ↵
    Ueda T, Yoshizumi T, Anai T, Matsui M, Uchimiya H, Nakano A (1998) AtGDI2, a novel Arabidopsis gene encoding a Rab GDP dissociation inhibitor. Gene 206: 137–143
    OpenUrlCrossRefPubMed
  113. ↵
    Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135: 913–914
    OpenUrlAbstract/FREE Full Text
  114. ↵
    Vernoud V, Horton AC, Yang Z, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 131: 1191–1208
    OpenUrlAbstract/FREE Full Text
  115. ↵
    Voigt B, Timmers AC, Samaj J, Hlavacka A, Ueda T, Preuss M, Nielsen E, Mathur J, Emans N, Stenmark H, et al (2005) Actin-based motility of endosome is linked to the polar tip growth of root hairs. Eur J Cell Biol 84: 609–621
    OpenUrlCrossRefPubMed
  116. ↵
    Wagner W, Bielli P, Wacha S, Ragnini-Wilson A (2002) Mlc1p promotes septum closure during cytokinesis via he IQ motifs of he vesicle motor Myo2p. EMBO J 21: 6397–6408
    OpenUrlAbstract
  117. ↵
    Wu SK, Luan P, Matteson J, Zeng K, Nishimura N, Balch WE (1998) Molecular role for the Rab binding platform of guanine nucleotide dissociation inhibitor in endoplasmic reticulum to Golgi transport. J Biol Chem 273: 26931–26938
    OpenUrlAbstract/FREE Full Text
  118. ↵
    Xu J, Scheres B (2005) Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17: 525–536
    OpenUrlAbstract/FREE Full Text
  119. ↵
    Yang YD, Elamawi R, Bubeck J, Pepperkok R, Ritzenthaler C, Robinson DG (2005) Dynamics of COPII vesicles and the Golgi apparatus in cultured Nicotiana tabacum BY2 cells provides evidence for transient association of Golgi stacks with endoplasmic exit sites. Plant Cell 17: 1513–1531
    OpenUrlAbstract/FREE Full Text
  120. ↵
    Zarsky V, Cvrckova F, Bischoff F, Palme K (1997) At-GDI1 from Arabidopsis thaliana encodes a rab-specific GDP dissociation inhibitor that complements the sec19 mutation of Saccharomyces cerevisiae. FEBS Lett 403: 303–308
    OpenUrlCrossRefPubMed
  121. ↵
    Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107–117
    OpenUrlCrossRefPubMed
  122. ↵
    Zhang J, Hill DR, Sylvester AW (2007) Diversification of the RAB guanosine triphosphatase family in dicots and monocots. J Integr Plant Biol 49: 1129–1141
    OpenUrlCrossRef
  123. ↵
    Zheng H, Camacho L, Wee E, Batoko H, Legen J, Leaver CJ, Malho R, Hussey PJ, Moore I (2005) A Rab-E GTPase mutant acts downstream of the Rab-D subclass in biosynthetic membrane traffic to the plasmamembrane in tobacco leaf epidermis. Plant Cell 17: 2020–2036
    OpenUrlAbstract/FREE Full Text
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The Regulatory RAB and ARF GTPases for Vesicular Trafficking
Erik Nielsen, Alice Y. Cheung, Takashi Ueda
Plant Physiology Aug 2008, 147 (4) 1516-1526; DOI: 10.1104/pp.108.121798

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The Regulatory RAB and ARF GTPases for Vesicular Trafficking
Erik Nielsen, Alice Y. Cheung, Takashi Ueda
Plant Physiology Aug 2008, 147 (4) 1516-1526; DOI: 10.1104/pp.108.121798
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  • Article
    • NOMENCLATURE AND THE RESEARCH TOOL BOX
    • RAB1/RABD AND RAB2/RABB
    • RAB11/RABA
    • RAB8/RABE
    • RAB5/RABF
    • RAB7/RABG
    • SAR AND ARF GTPASES
    • THE GTPASE CYCLE IS THE ENGINE THAT DRIVES VECTORIAL TRANSPORT
    • EFFECTORS AND DOWNSTREAM FUNCTION
    • PROSPECTUS
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    • LITERATURE CITED
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Plant Physiology: 147 (4)
Plant Physiology
Vol. 147, Issue 4
August 2008
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  • Plant Cyclic Nucleotide-Gated Channels: New Insights on Their Functions and Regulation
  • Plant Genome Editing and the Relevance of Off-Target Changes
  • Organellar and Secretory Ribonucleases: Major Players in Plant RNA Homeostasis
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