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Plant Physiology 147:1516-1526 (2008) © 2008 American Society of Plant Biologists The Regulatory RAB and ARF GTPases for Vesicular Trafficking1,[W]Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48109 (E.N.); Department of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, Massachusetts 01003 (A.Y.C.); and Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7–3–1 Hongo, Bunkyo-ku, Tokyo 113–0033, Japan (T.U.)
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
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.
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.
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
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
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
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 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.
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.
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
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
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
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
RAB5F1 and RAB5F2 localize on different populations of multivesiculated endosomes/prevacuolar compartments with considerable overlap (Ueda et al., 2004
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.
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
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
ARF was first identified as a cofactor required in the ADP-ribosylation of G
Plants express a conserved family of ARF proteins consisting of ARF and ARL subgroups (Vernoud et al., 2003
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
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
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
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.
The following materials are available in the online version of this article.
Received April 22, 2008; accepted May 23, 2008; published August 6, 2008.
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.).  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).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.108.121798 * Corresponding author; e-mail acheung{at}biochem.umass.edu.
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NOMENCLATURE AND THE RESEARCH...
RAB1/RABD AND RAB2/RABB
s by cholera toxin (Enomoto and Gill, 1980
