PostGolgi Traffic in Plants - Wiley Online Library

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© 2009 John Wiley & Sons A/S doi: 10.1111/j.1600-0854.2009.00916.x

Review

Post-Golgi Traffic in Plants ¨ Sandra Richter, Ute Voß and Gerd Jurgens* ¨ Tubingen, ¨ ZMBP, Entwicklungsgenetik,Universitat Auf ¨ der Morgenstelle 3, D-72076 Tubingen, Germany ∗Corresponding author: Gerd Jurgens, ¨ [email protected] Secretory and endocytic traffic through the post-Golgi endomembrane system regulates the abundance of plasma-membrane proteins such as receptors, transporters and ion channels, modulating the ability of a cell to communicate with its neighbours and to adapt to a changing environment. The major post-Golgi compartments are numerous and appear to be similar to their counterparts in animals. However, endosomes are rather ill defined morphologically but seem to be involved in specific trafficking pathways. Many plasma-membrane proteins cycle constitutively via endosomal compartments. The trans -Golgi network (TGN) appears to be an early endosome where secretory and endocytic traffic meet. Endocytosed proteins that are to be degraded are targeted to the vacuole via the multivesiculate prevacuolar compartment (PVC) whereas cycling proteins pass through recycling endosomes. The trafficking machinery involves the same classes of proteins as in other eukaryotes. However, there are modifications that match the specifics of post-Golgi traffic in plants. Although plants lack epithelia, some plasma-membrane proteins are located on specific faces of the cell which reflects polarized traffic and influences the physiological performance of the tissue. Plants also differentiate highly polarized tip-growing cells in which post-Golgi traffic is adapted to very high rates of targeted exocytosis, endocytosis and recycling. Key words: Arabidopsis, endosome, trans-Golgi network, prevacuolar compartment, secretion, endocytosis, recycling, brefeldin A (BFA), ARF exchange factor Received 14 November 2008, revised and accepted for publication 13 March 2009, uncorrected manuscript published online 18 March 2009, published online 22 April 2009

Membrane traffic is essential to eukaryotic life, mediating physiological compartmentation, nutrient uptake as well as communication between cells and with the environment. Secretory traffic delivers newly synthesized proteins such as transporters and receptors from the endoplasmic reticulum (ER) via intermediate endomembrane compartments to the plasma membrane (PM) as well as secreted enzymes and peptide ligands to the extracellular space. Conversely, receptors and transporters are

endocytosed from the PM and either recycled or targeted to the lysosome/vacuole for degradation. Secretory and endocytic trafficking pathways intersect in post-Golgi compartments of the endomembrane system, and these compartments appear to be more diverse between plants and non-plant organisms than the ER and the Golgi apparatus of the early secretory pathway. The aim of this review is to summarize recent progress in the analysis of plant post-Golgi membrane trafficking. We will discuss the endomembrane compartments, the trafficking pathways and the molecular machinery involved. We will also give examples of how post-Golgi trafficking contributes to cell–cell communication and cellular differentiation in plant development as well as physiological adaptation of plant cells to their environment.

Post-Golgi Compartments The section of the endomembrane system through which both secretory and endocytic traffic pass is bounded by the Golgi apparatus, the PM and the vacuole (Figure 1). The plant Golgi apparatus comprises numerous Golgi stacks each comprising several cisternae. The number of stacks can vary between cell types, depending on their secretory activity, and also doubles before cell division as if to facilitate the inheritance of the Golgi apparatus by the daughter cells (1). The vesiculate transGolgi network (TGN) is often closely associated with the trans-face of the Golgi stack (1). Unlike their animal and yeast counterparts, plant TGNs are not only involved in secretory traffic but also serve as early endosomes (EE), as demonstrated by the very rapid labelling with the endocytic tracer FM4-64 (2). Plant cells contain multiple multivesicular bodies (MVBs) that serve as prevacuolar compartments (PVCs) and thus correspond to late endosomes (LE) of animal cells (3). The internal vesicles are presumed to originate by invagination of the surrounding membrane, although this has not been documented in plants. The plant vacuole is polymorphic, changing from several small vacuoles in proliferating cells to a large central vacuole in differentiated cells (4). In addition, there are two functionally distinct vacuoles, one involved in protein storage and another involved in protein degradation (4). These two types of vacuole were considered physically distinct, although able to fuse with one another. However, more recent evidence raises the possibility that there is physical continuity but changing function of the vacuole (4). The post-Golgi compartments discussed so far are morphologically distinct—TGN/EE, MVB/PVC/LE and vacuole (Figure 1). Plant cells may have www.traffic.dk

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Figure 1: Schematic overview of membrane traffic. Main trafficking routes between compartments are highlighted by white arrows in interphase cells and by yellow arrows in dividing cells. Some PM proteins are polar localized as indicated. For details see text.

additional endosomal compartments that are structurally difficult to identify. For example, the ADP ribosylation factor–GTP exchange factor (ARF–GEF) GNOM (Table 1) does not localize to the TGN or MVB suggesting the existence of a functionally distinct ‘recycling endosome’ (RE) (5). Alternatively, GNOM might define a recycling pathway from a maturing tubulovesicular endosome akin to what has been proposed for animal cells (6,7). Other putative endosomal compartments are labelled by specific markers such as δ-adaptin/epsin R2/TFL1, RAB-A2/A3 or RAB-A4 (8–11). An additional post-Golgi compartment named cell plate is formed in dividing cells. The cell plate develops into the partitioning PM between the daughter cells and is made from both secretory and endocytic materials (see the subsequent text).

Trafficking Pathways Newly synthesized membrane or soluble cargo proteins are trafficked from the ER through the Golgi apparatus to the TGN for sorting. Secretory traffic moves on to the PM whereas vacuolar traffic passes through the MVB/PVC en route to the vacuole. The secretory route to the PM has not been mapped out in detail. It is thus unknown whether secretory carriers move from the TGN to the PM directly or/and indirectly via other 820

endosomal compartments. Furthermore, the transport carriers have not been structurally identified in plants and the machinery involved is largely unknown. Secretory green fluorescent protein (secGFP), which contains an N-terminal signal peptide for uptake into the ER, is secreted from the cell, suggesting that trafficking to the PM is a default pathway, at least for soluble cargo proteins. It is of interest to note that secretion of secGFP cannot be blocked by brefeldin A (BFA) treatment in wildtype Arabidopsis whereas gnl1 mutant seedling root cells accumulate secGFP intracellularly as a consequence of the inhibition of ER-Golgi traffic (12,13). Other soluble cargos include secreted enzymes such as cell-wall invertase or subtilisin-like protease Ara12 and peptide ligands such as CLV3 (14,15). Secretory membrane cargo includes receptors, transporters, ion channel, cell-wall enzymes, arabinogalactan proteins (AGPs) and t-SNARE proteins. For single-pass membrane proteins, targeting to the PM seems to depend, at least in part, on the length of the transmembrane domain (16). Secretory traffic to the PM seems to be the default pathway in interphase. In dividing cells, however, newly synthesized PM proteins such as syntaxin PEN1, aka SYP121, as well as secreted endoxyloglucan transferase (EXGT) fused to GFP are trafficked to the cell division plane/cell plate whereas the syntaxin PEP12, aka SYP21,

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Post-Golgi Traffic in Plants Table 1: Overview of Arabidopsis thaliana proteins used as compartment specific markers. Compartment

Marker

Protein class

Reference

Golgi

γ -COP GNL1 ST NAG TLG2a/SYP41 Vacuolar H+ ATPase subunit a1 SCAMP 1 RabA2, RabA3 GNOM FM4-64 ARA7/ RabF2b Rha1/RabF2a BP-80/VSR1 VPS4/SKD1

COPI subunit ARF-GEF Sialyl tranferase N -acetyl glucosaminyl transferase I SNARE H+ ATPase Secretory carrier membrane protein Rab GTPases ARF-GEF Styryl dye Rab GTPase Rab GTPase Vacuolar-sorting receptor Endosomal sorting complex required for transport (ESCRT) subunit Retromer subunits

(103) (12,13)) (29,104) (29) (79) (2) (43) (10) (5,30) (5) (65) (65) (105) (106)

Tonoplast intrisic proteins

(105)

Proteases

(105)

Putative auxin efflux carrier Brassinosteroid receptor Boron import carrier

(30) (100) (109,110)

Boron export carrier SNARE SNARE

(111) (70) (71)

TGN

Recycling endosome Endosome MVB/PVC

Tonoplast

Vacuole lumen

Plasma membrane

Cell plate

VPS5/SNX1 VPS26 VPS29 VPS35 γ -TIP α-TIP δ -TIP Aleurain Sporamin Lectin PIN BRI1 NIP5 NIP1 BOR1 PEN1 KNOLLE

is still targeted to the PVC/MVB (17,18). Thus, the default pathway changes from the PM to the cell plate during cell division. Traffic of newly synthesized proteins to the vacuole requires sorting at the TGN. For example, CLV3 fused to a C-terminal vacuolar-sorting signal (VSS) accumulates in the vacuole rather than the extracellular space (15). The VSS of soluble cargo such as hydrolases, peptidases or proteases is recognized by vacuolar-sorting receptors (VSRs), a family of seven proteins in Arabidopsis (19,20). Sorting requires recognition of the tyrosine motif YMPL in the cytosolic tail of the VSR by the μA-adaptin subunit of a TGN-associated adaptor protein (AP)-complex. Although this has not been demonstrated in vivo, μA-adaptin interacts with YMPL but not AMPA in vitro (21). The roles of the individual members of the VSR family have not been clarified. The vacuolar soluble cargo is released from VSR after fusion of the transport carriers with the outer membrane of the PVC/MVB, presumably because of the more acidic pH in the lumen of the PVC. Whereas the VSR is recycled to the TGN (see the subsequent text) the cargo proteins

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(107) (6,32, 108)

are passed on to the vacuole, presumably by fusion of the MVB/PVC with the vacuole (22). This final step of vacuolar trafficking involves the homotypic fusion and protein sorting complex/class C VPS protein complex (HOPS/C-VPS) complex and VAM3/SYP22 syntaxin. Mutational inactivation of the HOPS subunit VCL1/VPS16 results in embryo lethality as a result of vacuolar traffic inhibition (23). To identify the additional factors involved in vacuolar targeting, screens for missorting mutants were performed (20,8). Retrograde traffic from the MVB/PVC to the TGN is mediated by the retromer complex recycling VSR to the TGN (24,25). This process is essential for vacuolar traffic of soluble cargo and can be inhibited by the phosphatidylinositol 3-kinase inhibitor wortmannin (26). Wortmannin also alters the structure of MVBs, reducing the number of internal vesicles and causing MVBs to swell (3). Therefore, blocking retrograde traffic from the MVB/PVC to the TGN also entails inhibition of anterograde traffic from the TGN to the MVB/PVC, resulting in the secretion of vacuolar soluble cargo. This effect is similar to the BFA-induced inhibition of retrograde traffic from the 821

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Golgi to the ER, which entails inhibition of anterograde traffic from the ER to the Golgi as well (12). Endocytosis of PM proteins is the other major trafficking activity in the post-Golgi endomembrane system. Although endocytosis in plants was disputed for quite some time because of the turgor pressure, there is no doubt that endocytosis does occur in plants. The time course of FM4-64 internalization suggests that the TGN corresponds to the EE in plants, being labelled within a few minutes (2). The endocytic tracer FM4-64 then labels the MBV/PVC where endocytic and vacuolar traffic routes were proposed to merge (3). Surprisingly, most PM proteins undergo constitutive cycling between the PM and some endosomal compartment(s) (27,28) as demonstrated by fluorescence recovery after photobleaching (FRAP) analysis and live imaging (29) and entrapment of PM proteins in BFA compartments. If endocytosed PM proteins do not enter the recycling pathway, they are passed on to the vacuole for degradation. Constitutive cycling of PM proteins is blocked by BFA (30). Rendering the BFA target ARF-GEF GNOM resistant to BFA enables recycling of the auxin efflux carrier PINFORMED1 (PIN1) to the PM in the presence of BFA whereas other PM proteins are still partially or completely trapped in BFA compartments (5). Thus, there appears to be more than one recycling pathway from endosomes to the PM. Continued inhibition of basal recycling by BFA results not just in BFA compartments but in apical localization of PIN1, a phenomenon called transcytosis. Transcytosis does not occur in cells expressing BFAresistant GNOM, suggesting that apical targeting of PIN1 might only be an alternative if basal trafficking is blocked (31). In contrast snx1 or vps29 mutants had no effect, although the latter had been implicated in PIN1 recycling (32). It is conceivable that the effect of vps29 on PIN1 recycling is indirect by blocking anterograde traffic to the MVB/PVC, which might then affect GNOM-dependent recycling of PIN1 to the PM (33). It is currently unknown where in the post-Golgi endomembrane system endocytosed PM proteins are sorted for recycling versus degradation, although the SNX1-positive compartment has been proposed to be a sorting endosome (34). However, all the effects described for mutant cells might be rather indirect. Nonetheless, the effects on both endocytic and secretory traffic suggest that the SNX1-positive MVB/PVC might be involved in both trafficking routes. Endocytosed proteins that are targeted for degradation in the vacuole are likely ubiquitinated and interact with VPS23-related ELCH protein, which interacts with ubiquitin and endosomal sorting complex required for transport (ESCRT) I complex proteins and localizes to MVBs/PVCs (35). So far, no ubiquinated endocytosed plant protein has been identified as an ELCH substrate. Once proteins are sorted into internalized vesicles of MVBs they are passed on to the vacuole by fusion of MVBs with the vacuole, as suggested by the transient presence of 822

cytokinesis-specific syntaxin KNOLLE in internal vesicles of the MVBs and in the vacuole after the completion of cytokinesis (17). If the EE does not perform a sorting function in plants, in contrast to the situation in animals, it is conceivable that sorting occurs on the maturing MVB from which all recycling proteins are removed by retrograde traffic to the TGN or recycling to the PM before the MVB fuses with the vacuole, delivering the proteins to be degraded.

Molecular machinery of post-Golgi traffic Trafficking pathways in the post-Golgi endomembrane system are presumed to involve transport vesicles that are coated with clathrin and adaptor protein (AP) complexes. However, supporting evidence is rather limited in plants. Clathrin and clathrin-coated pits have been detected at the PM and the cell plate, and the expression of dominant-negative (DN) variants of clathrin heavy chain interfered with endocytosis of the auxin efflux carriers PIN1 and PIN2 (36,37). Clathrin-interacting proteins epsin 1 or epsin R2 might play roles in vacuolar trafficking from the TGN or some ill-defined endosomal compartment (38,9). Membrane-constricting or severing dynaminrelated proteins (DRPs) have been localized to the PM, cell plate and trans-Golgi (39–42). Although Arabidopsis encodes subunits of four different AP complexes, their precise roles in trafficking have not been elucidated. AP-1 subunit γ -adaptin might localize to the transGolgi (38,43), AP-3 subunit δ-adaptin to an unidentified endosomal compartment (9) whereas αC-adaptin is a candidate subunit of the endocytic AP-2 complex (44). However, medium-sized μ-subunits that interact with tyrosine-based sorting motifs of cargo proteins have not been localized or functionally characterized, with the possible exception of μA-adaptin to the trans-Golgi (21). Interestingly, the tyrosine analogue tyrphostin A23 that is thought to interfere with cargo recruitment by μ-adaptin has been reported to block clathrin-mediated endocytosis (45,37). However, interference of other clathrin-mediated trafficking processes has not been studied. Recruitment of coat proteins to the forming membrane vesicle requires activation of ARF GTPases, or SAR1 GTPase at the ER. Arabidopsis encodes approximately one dozen each of ARF GTPases and ARF GTPase-activating proteins (ARFGAPs) as well as eight ARF-GEFs (46). ARF1 seems to act at several endomembrane compartments such as cis-Golgi and BFA-sensitive endosomes, interacting with different effectors (47,48), whereas the plant-specific ARFB associates with the PM, with targeting specificity depending on multiple protein domains (49). The membrane targeting of ARF GTPases might be mediated by ARF-GEFs. However, their substrate specificities are not known. Although BIG3 has been shown to mediate GDP–GTP exchange on ARF1 in a BFA-resistant manner, its subcellular localization has not been determined (50). Conversely, GNOM and GNL1 have been localized but their substrate specificity is not known (5,13,12). Similarly, ARF-GAPs have been either localized or characterized for

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their substrate specificity but not both [Arabidopsis ARFGAP DOMAIN-CONTAINING PROTEIN 1 (AGD1): (51); AGD7: (52); rice OsGAP: (53); Arabidopsis ROOT AND POLLEN ARF-GAP (RPA): (38); Arabidopsis protein SCARFACE (SCF): (54); Arabidopsis VASCULAR NETWORK 3 (VAN3): (55)]. Several ARF-GAPs appear to be involved in PIN localization or auxin physiology and might thus be associated with recycling traffic to the PM. Tethering, docking and fusion of membrane vesicles with their target membranes involve RAB GTPases, their regulators and effectors as well as the SNARE fusion machinery and their regulators. In Arabidopsis, both RABs and SNAREs are large protein families whose members have been analysed by sequence alignment and/or subcellular localization, whereas only a limited number of functional studies have been performed (56–59). Of the 5 RAB groups involved in post-Golgi traffic, RAB-E1 GTPase related to yeast Sec4 localizes to the Golgi and plays a role in secretory traffic to the PM (60). RAB-A2 and RAB-A3 related to Rab11 or Rab25 label a TGN-related compartment, overlapping with the TGN-localized Arabidopsis VACUOLAR H+ ATPASE SUBUNIT a1 (VHA-a1), and also label the cell plate during cytokinesis, suggesting that these RABs identify a secretory compartment (10). The RAB-F group GTPases related to endosomal Rab5 in animals play prominent roles in endocytosis and have been used as markers in trafficking studies. Two conventional Rab5-type GTPases, RAB-F2a/RHA1 and RAB-F2b/ARA7, and the plant-specific, N-terminally myristoylated RAB-F1/ARA6 localize to the MVB/PVC (61–64,17). Although the two Rab GTPases, RAB-F1/ARA6 and RAB-F2b/ARA7, localize to nearly the same endomembrane compartment and are activated by the same RAB-GEF VPS9a, they are functionally distinct and might act in different trafficking pathways (65). RAB-G group GTPases act in vacuolar trafficking, as suggested by their similarity to animal Rab7 GTPases (66). Rice Rab7 localizes to the vacuolar membrane, suggesting it might interact with the HOPS/CVPS complex. Finally, the RAB-H group GTPases are related to animal Rab6 and might thus be involved in MVB/PVC retrograde traffic to the TGN but have not been studied experimentally (57). PVC-derived vesicles are tethered to the Golgi or TGN by the Golgi-associated retrograde protein (GARP) complex whose subunit POKY POLLEN TUBE (POK) related to yeast VPS52p is essential for pollen function (67,68). It is also interesting to note that plants lack counterparts to Rab4 involved in recycling from endosomes to the PM, which may reflect the postulated evolutionary divergence of the plant and animal organization of the post-Golgi endomembrane traffic (28). Non-host resistance against fungal pathogens is mediated by a specific SNARE complex that has been identified and functionally characterized (69). The syntaxin involved named PEN1/SYP121 localizes to the penetration site and is essential for non-host resistance, whereas it acts

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redundantly with its closest homologue, SYP122, in development (70). The SYP1 group of PM syntaxins comprises another seven members of which KNOLLE/SYP111 is specifically required for vesicle fusion during cell-plate formation whereas its closest homologue, SYP112, has no obvious role (71). Three other members (SYP124, SYP125, SYP131) are exclusively expressed in pollen, and SYP132 is involved in nodule symbiosis in Medicago (72,73). DN fragments of several syntaxins were assayed for their effects on the trafficking of specific cargo molecules, and the results suggest that specifically PEN1/SYP121 and SYP122 are involved in trafficking to the PM whereas PEP12/SYP21 mediates traffic to the vacuolar membrane (74). PEP12/SYP21 overexpression was also shown to inhibit traffic from the MVB/PVC to the vacuole and retrograde traffic to the Golgi apparatus, without affecting traffic from the Golgi apparatus to the PM (75). In contrast to the specific roles of syntaxins, the interacting Qb,c-SNARE SNAP33 appears to be more promiscuous, participating in SNARE complexes at both the PM and the cell plate (76,69). Most vesicle-associated R-SNAREs of Arabidopsis are related to animal VAMP7 and have an N-terminal extension relative to synaptobrevins that mediates their subcellular targeting (77). Incomplete SNARE complexes have been described for the TGN and PVC (78,79). In addition, SNARE-interacting SM (Sec1/Munc18) proteins KEULE and VPS45 have been implicated in cell-plate formation and membrane fusion at the TGN, respectively, whereas VPS33 has been identified as part of the vacuolar RAB effector complex HOPS/VPS-C and localized to the PVC and vacuolar membrane (80,81).

Polarized traffic to the PM Many but not all PM proteins are distributed over the entire surface of the cell. Auxin efflux carriers of the PIN family were the first proteins shown to localize to specific faces of the cell, for example PIN1 accumulating at the basal end of vascular cells but at the apical end of epidermal cells in the shoot. Similarly, PIN2 is located basally in cortex and endodermis cells but apically in the root epidermis. During cell division in the root, both PIN1 and PIN2 localize to the cell plate and thus to the ‘wrong’ end in one of the daughter cells, which normally is corrected immediately after cell division. However, mutations eliminating the ERlocalized cyclopropylsterol isomerase 1 (CPI1) required for the correct membrane sterol composition appear to slow down endocytosis after cytokinesis such that PIN2 was observed both apically and basally in the same interphase cell (82). PIN proteins continually cycle between the PM and endosomes. In contrast to PIN1 basal recycling PIN2 apical recycling is GNOM independent, but the mechanism is unknown. Interestingly, apical localization of PIN1 requires its phosphorylation by the Ser/Thr kinase PINOID (PID) whereas its dephosphorylation by three redundant protein phosphatase 2A (PP2A) subunits favours basal localization of PIN1 (83). However, the polar localization of PIN2 does not depend on the PP2A-PID phosphorylation system. 823

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Specific cell types display marked mediolateral polarity. For example, the endodermis in dicots, and endodermis and exodermis in monocots are partitioned by an extracellular band of suberin (‘Casparian strip’) into a medial (or inner) and a lateral (or outer) surface area. The suberin band prevents extracellular passage of nutrient and ions from the outer root tissue layers to the central vascular cylinder. Thus, specific importers are localized in the lateral PM whereas the corresponding exporters reside in the medial PM, as was shown for Arabidopsis and rice transporters such as boron importers NIP5;1 and OsNIP3;1 as well as silicon importer Lsi1 (= OsNIP2;1), and boron exporters BOR1 and OsBOR1 as well as silicon exporter Lsi2 (84–86). These transporters also seem to cycle continually between the PM and endosomes as revealed by BFA inhibition of recycling. BOR1 cycling occurs when the external concentration of boron is low. However, when the cell experiences a high, toxic level of boron BOR1 is internalized from the PM and targeted to the vacuole for degradation (84). Another cell type displaying a distinct mediolateral polarity is the epidermis. In the shoot, epidermal cells form a cuticle on their outer surface to protect against water loss. Cuticle formation is a complex process that requires the transport of cutin monomers across the outer PM. This transport is mediated by WHITE-BROWN COMPLEX 11 (WBC11)/DESPERADO (DSO), an ABC transporter that is specifically located in the outer PM (87,88).

Post-Golgi traffic in polarized tip-growing cells Root hairs and pollen tubes are highly specialized tipgrowing cells involved in nutrient uptake and delivery of the male gametes to the ovules, respectively. Despite their different roles, these cell types display a quite similar architecture and rapid growth from one end known as polar tip growth (Figure 2). The actin cytoskeleton supports membrane traffic to the growing tip, and endomembrane compartments are concentrated near the tip. In pollen tubes, secretory vesicles accumulate in the socalled clear zone at the growing tip, before fusing with the PM to deliver both membrane and cell-wall material (89). To meet the large demand of cell-wall components, about five times more secretory vesicles have to fuse with the apical membrane than are needed for PM expansion (90,91). The excess membrane material has to be removed by endocytosis, which was thought to occur in the subapical region (90). However, successive treatment with two endocytic tracers, FM1-43 and FM4-64, as well as FRAP experiments suggest that endocytosis occurs mainly in the apex (92,91). In addition, very high turnover rates of vesicles as compared to calculated values support the idea that many secretory vesicles attempt repeatedly to fuse with the PM before they succeed (91). A similar mechanism appears to operate in growing root hairs. The endocytic tracer FM1-43 initially labels the PM, then tiny fluorescent endocytotic vesicles in the clear zone and few minutes later, larger putative EE appear in the subapical 824

region (93). However, the details of secretory, endocytic and recycling traffic are unknown. The trafficking machinery should be essentially very similar in all cells. However, two members of the RAB-A group of GTPases related to animal recycling Rab11 appear to be specifically involved in polar tip growth. Nicotiana tabacum NtRab11b localizes to the clear zone of pollen tubes. Interference with NtRab11b affects pollen tube growth and reduces plant fertility (94). NtRab11b appears to mediate traffic from the Golgi to the apical PM, as its DN and its constitutive active (CA) form localize at the Golgi and the PM, respectively (94). In addition, these GDP- or GTP-locked forms inhibited secretion of secGFP as well as the pollen tube wall-located invertase, suggesting a role of NtRab11b in exocytosis required for tobacco pollen tube growth. The Arabidopsis RAB-A4b appears to play a comparable role in root hairs. RAB-A4b labels a novel postGolgi compartment that might be specifically involved in polarized secretion during root hair tip growth (11). Another family of small GTPases named Rho of Plants (ROP) are mainly regulators of cytoskeleton reorganization and support polar tip growth, localizing in the apex of pollen tubes and root hairs. CA ROP causes isotropic growth and bulbous pollen tubes and root hairs whereas the DN variants inhibit growth. Actin reorganization was attributed to the two ROP interactors RIC3 and RIC4 (ROP-interactive Cdc42/Rac interactive binding (CRIB) motif containing proteins) (95). ROPs also interact with the exocyst subunit SEC3 via the scaffold protein ICR1 (96). Mutant analysis suggests that the exocyst complex mediates tethering and targeting of secretory vesicles to the PM in growing pollen tubes (97). ROPs are also linked to vesicle trafficking as shown by the loss of early polarization of ROPs by the ARF-GEF inhibitor BFA, suggesting that an ARF is involved in this process. In support, BFA and weak mutant alleles of ARF-GEF GNOM play a role in root hair positioning and polar localization of ROP2 (98). However, the effect of ARF1 on ROP2 is most likely indirect (48).

Implications for physiology and development Post-Golgi traffic profoundly influences physiology and development by modulating the availability of transporters and receptors at the PM. For example, the PM-localized Ser/Thr kinase FLS2 acts as a receptor for pathogenassociated molecular patterns (PAMPs) by specifically binding the bacterial flagellin peptide Flg22. FLS2 cycles, constitutively, like other PM proteins. However, Flg22 binding causes endocytosis and targeting to the vacuole for degradation (99). Another interesting finding is the observation that internalization of the brassinosteroid receptor BRI1 from the PM enhances downstream signalling output, suggesting that this plant receptor is activated by ligand binding but requires some additional endosome-associated factor for effective signalling (100). Finally, there is a large host of PM-localized receptor-like Traffic 2009; 10: 819–828

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Figure 2: Simplified presentation of post-Golgi system of tip-growing cells. Membrane and vesicle compartments are enriched in apical and subapical regions as indicated in this pollen tube. For details see text.

Ser/Thr protein kinases (e.g. S-LOCUS RECEPTOR-LIKE KINASE (SRK), SOMATIC EMBRYOGENESIS RECEPTORLIKE KINASE 1 (SERK1), Arabidopsis CLAVATA 1 (CLV1) receptor kinase, PHYTOSULFOKINE RECEPTOR 1 (AtPSKR1), which are often orphaned but for some of them, the secreted peptide ligands S-LOCUS CYSTEIN-RICH PEPTIDE (SCR), CLAVATA 3 (CLV3), and PHYTOSULFOKINE (PSK) are known. These receptors and their ligands play roles in diverse cell–cell communication processes including self-incompatibility, initiation of somatic embryogenesis and size regulation of the shoot meristem (101). Unfortunately, there is limited information on endocytosis of these receptors apart from SERK1 (102). There is even less information about the processing and exocytosis of the peptide ligands.

Conclusion Remarkable progress has been made in the analysis of plant post-Golgi membrane traffic in recent years. Although the basic organization of compartments and traffic routes has been worked out, there are still a number of unresolved problems. For example, the different endosomal compartments and their roles in secretion and recycling to the PM need to be clarified. In addition, the regulation of trafficking pathways is still unknown. Furthermore, it will be important to determine the role of

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endocytosis in cell–cell communication and adaptation to environmental conditions.

References 1. Segui-Simarro JM, Staehelin LA. Cell cycle-dependent changes in Golgi stacks, vacuoles, clathrin-coated vesicles and multivesicular bodies in meristematic cells of Arabidopsis thaliana: a quantitative and spatial analysis. Planta 2006;223(2):223–236. 2. Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K. Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 2006;18(3):715–730. 3. Tse YC, Mo B, Hillmer S, Zhao M, Lo SW, Robinson DG, Jiang L. Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 2004;16(3):672–693. 4. Frigerio L, Hinz G, Robinson DG. Multiple vacuoles in plant cells: rule or exception? Traffic 2008;9(10):1564–1570. 5. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jurgens G. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 2003;112(2):219–230. 6. Bonifacino JS, Rojas R. Retrograde transport from endosomes to the trans-Golgi network. Nat Rev Mol Cell Biol 2006;7(8):568–579. 7. Woodman PG, Futter CE. Multivesicular bodies: co-ordinated progression to maturity. Current Opin Cell Biology 2008;20(4):408–414. 8. Sohn EJ, Rojas-Pierce M, Pan S, Carter C, Serrano-Mislata A, Madueno F, Rojo E, Surpin M, Raikhel NV. The shoot meristem identity gene TFL1 is involved in flower development and trafficking to the protein storage vacuole. Proc Natl Acad Sci U S A 2007;104(47):18801–18806.

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Richter et al. 9. Lee GJ, Kim H, Kang H, Jang M, Lee DW, Lee S, Hwang I. EpsinR2 interacts with clathrin, adaptor protein-3, AtVTI12, and phosphatidylinositol-3-phosphate. Implications for EpsinR2 function in protein trafficking in plant cells. Plant Physiol 2007;143(4):1561–1575. 10. Chow CM, Neto H, Foucart C, Moore I. Rab-A2 and Rab-A3 GTPases define a trans-golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. Plant Cell 2008;20(1):101–123. 11. Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E. The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 2004;16(6):1589–1603. 12. Teh OK, Moore I. An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 2007;448(7152):493–496. 13. Richter S, Geldner N, Schrader J, Wolters H, Stierhof YD, Rios G, Koncz C, Robinson DG, Jurgens G. Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 2007;448(7152):488–492. 14. Hamilton JM, Simpson DJ, Hyman SC, Ndimba BK, Slabas AR. Ara12 subtilisin-like protease from Arabidopsis thaliana: purification, substrate specificity and tissue localization. Biochem J 2003;370(Pt 1):57–67. 15. Rojo E, Sharma VK, Kovaleva V, Raikhel NV, Fletcher JC. CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 2002;14(5):969–977. 16. Brandizzi F, Frangne N, Marc-Martin S, Hawes C, Neuhaus JM, Paris N. The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell 2002;14(5):1077–1092. 17. Reichardt I, Stierhof YD, Mayer U, Richter S, Schwarz H, Schumacher K, Jurgens G. Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr Biol 2007;17(23):2047–2053. 18. Yokoyama R, Nishitani K. Endoxyloglucan transferase is localized both in the cell plate and in the secretory pathway destined for the apoplast in tobacco cells. Plant Cell Physiol 2001;42(3):292–300. 19. Craddock CP, Hunter PR, Szakacs E, Hinz G, Robinson DG, Frigerio L. Lack of a vacuolar sorting receptor leads to non-specific missorting of soluble vacuolar proteins in Arabidopsis seeds. Traffic 2008;9(3):408–416. 20. Fuji K, Shimada T, Takahashi H, Tamura K, Koumoto Y, Utsumi S, Nishizawa K, Maruyama N, Hara-Nishimura I. Arabidopsis vacuolar sorting mutants (green fluorescent seed) can be identified efficiently by secretion of vacuole-targeted green fluorescent protein in their seeds. Plant Cell 2007;19(2):597–609. 21. Happel N, Honing S, Neuhaus JM, Paris N, Robinson DG, Holstein SE. Arabidopsis mu A-adaptin interacts with the tyrosine motif of the vacuolar sorting receptor VSR-PS1. Plant J 2004;37(5):678–693. 22. Yamada K, Fuji K, Shimada T, Nishimura M, Hara-Nishimura I. Endosomal proteases facilitate the fusion of endosomes with vacuoles at the final step of the endocytotic pathway. Plant J 2005;41(6):888–898. 23. Rojo E, Gillmor CS, Kovaleva V, Somerville CR, Raikhel NV. VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev Cell 2001;1(2):303–310. 24. Oliviusson P, Heinzerling O, Hillmer S, Hinz G, Tse YC, Jiang L, Robinson DG. Plant retromer, localized to the prevacuolar compartment and microvesicles in Arabidopsis, may interact with vacuolar sorting receptors. Plant Cell 2006;18(5):1239–1252. 25. Collins BM. The structure and function of the Retromer protein complex. Traffic 2008;9(11):1811–1822. 26. daSilva LL, Taylor JP, Hadlington JL, Hanton SL, Snowden CJ, Fox SJ, Foresti O, Brandizzi F, Denecke J. Receptor salvage from the

826

27.

28. 29.

30.

31.

32.

33. 34. 35.

36.

37.

38.

39.

40.

41.

42.

43.

44.

45.

prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 2005;17(1):132–148. Geldner N. The plant endosomal system—its structure and role in signal transduction and plant development. Planta 2004;219(4):547–560. Geldner N, Jurgens G. Endocytosis in signalling and development. Curr Opin Plant Biol 2006;9(6):589–594. Grebe M, Xu J, Mobius W, Ueda T, Nakano A, Geuze HJ, Rook MB, Scheres B. Arabidopsis sterol endocytosis involves actinmediated trafficking via ARA6-positive early endosomes. Curr Biol 2003;13(16):1378–1387. Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 2001;413(6854):425–428. Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer PB, Wisniewska J, Paciorek T, Benkova E, Friml J. ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol 2008;18(7):526–531. Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miege C, Gaude T. The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell 2007;130(6):1057–1070. Jurgens G, Geldner N. The high road and the low road: trafficking choices in plants. Cell 2007;130(6):977–979. Jaillais Y, Fobis-Loisy I, Miege C, Gaude T. Evidence for a sorting endosome in Arabidopsis root cells. Plant J 2008;53(2):237–247. Spitzer C, Schellmann S, Sabovljevic A, Shahriari M, Keshavaiah C, Bechtold N, Herzog M, Muller S, Hanisch FG, Hulskamp M. The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development (Cambridge, England) 2006;133(23):4679–4689. Hinz G, Colanesi S, Hillmer S, Rogers JC, Robinson DG. Localization of vacuolar transport receptors and cargo proteins in the Golgi apparatus of developing Arabidopsis embryos. Traffic 2007;8(10):1452–1464. Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof YD, Friml J. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 2007;17(6):520–527. Song XF, Yang CY, Liu Y, Yang, WC. RPA, a class II ARFGAP protein, activates ARF1 and U5 and plays a role in root hair development in Arabidopsis. Plant Physiol. 2006;141(3):966–976. Konopka CA, Bednarek SY. Comparison of the dynamics and functional redundancy of the Arabidopsis dynamin-related isoforms, DRP1A and DRP1C, during plant development. Plant Physiology 2008;147(4):1590–1602. Otegui MS, Staehelin LA. Electron tomographic analysis of postmeiotic cytokinesis during pollen development in Arabidopsis thaliana. Planta 2004;218(4):501–515. Jin JB, Kim YA, Kim SJ, Lee SH, Kim DH, Cheong GW, Hwang I. A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 2001;13(7):1511–1526. Hong Z, Geisler-Lee CJ, Zhang Z, Verma DP. Phragmoplastin dynamics: multiple forms, microtubule association and their roles in cell plate formation in plants. Plant Mol Biol 2003;53(3):297–312. Lam SK, Siu CL, Hillmer S, Jang S, An G, Robinson DG, Jiang L. Rice SCAMP1 defines clathrin-coated, trans-golgi-located tubularvesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell 2007;19(1):296–319. Barth M, Holstein SE. Identification and functional characterization of Arabidopsis AP180, a binding partner of plant alphaC-adaptin. J Cell Sci 2004;117(Pt 10):2051–2062. Ortiz-Zapater E, Soriano-Ortega E, Marcote MJ, Ortiz-Masia D, Aniento F. Trafficking of the human transferrin receptor in plant cells: effects of tyrphostin A23 and brefeldin A. Plant J 2006;48(5):757–770.

Traffic 2009; 10: 819–828

Post-Golgi Traffic in Plants 46. Jurgens G, Geldner N. Protein secretion in plants: from the transGolgi network to the outer space. Traffic 2002;3(9):605–613. 47. Matheson LA, Hanton SL, Rossi M, Latijnhouwers M, Stefano G, Renna L, Brandizzi F. Multiple roles of ADP-ribosylation factor 1 in plant cells include spatially regulated recruitment of coatomer and elements of the Golgi matrix. Plant Physiol 2007;143(4):1615–1627. 48. Xu J, Scheres B. Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 2005;17(2):525–536. 49. Matheson LA, Suri SS, Hanton SL, Chatre L, Brandizzi F. Correct targeting of plant ARF GTPases relies on distinct protein domains. Traffic 2008;9(1):103–120. 50. Nielsen M, Albrethsen J, Larsen F, Skriver K. The Arabidopsis ADPribosylation factor (ARF) and ARF-like (ARL) system and its regulation by BIG2, a large ARF-GEF. Plant Sci 2006;171:707–717. 51. Yoo CM, Wen J, Motes CM, Sparks JA, Blancaflor EB. A class one ADP-ribosylation factor GTPase-activating protein is critical for maintaining directional root hair growth in Arabidopsis thaliana. Plant Physiol 2008;147(4):1659–1674. 52. Min MK, Kim SJ, Miao Y, Shin J, Jiang L, Hwang I. Overexpression of Arabidopsis AGD7 causes relocation of Golgi-localized proteins to the endoplasmic reticulum and inhibits protein trafficking in plant cells. Plant Physiol 2007;143(4):1601–1614. 53. Zhuang X, Jiang J, Li J, Ma Q, Xu Y, Xue Y, Xu Z, Chong K. Over-expression of OsAGAP, an ARF-GAP, interferes with auxin influx, vesicle trafficking and root development. Plant J 2006;48(4):581–591. 54. Sieburth LE, Muday GK, King EJ, Benton G, Kim S, Metcalf KE, Meyers L, Seamen E, Van Norman JM. SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. Plant Cell 2006;18(6):1396–1411. 55. Koizumi K, Naramoto S, Sawa S, Yahara N, Ueda T, Nakano A, Sugiyama M, Fukuda H. VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation. Development (Cambridge, England) 2005;132(7):1699–1711. 56. Vernoud V, Horton AC, Yang Z, Nielsen E. Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 2003;131(3):1191–1208. 57. Rutherford S, Moore I. The Arabidopsis Rab GTPase family: another enigma variation. Curr Opin Plant Biol 2002;5(6):518–528. 58. Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH. Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct Funct 2004;29(2):49–65. 59. Sanderfoot A. Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol 2007;144(1):6–17. 60. Zheng H, Camacho L, Wee E, Batoko H, Legen J, Leaver CJ, Malho R, Hussey PJ, Moore I. A Rab-E GTPase mutant acts downstream of the Rab-D subclass in biosynthetic membrane traffic to the plasma membrane in tobacco leaf epidermis. Plant Cell 2005;17(7):2020–2036. 61. Kotzer AM, Brandizzi F, Neumann U, Paris N, Moore I, Hawes C. AtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells. J Cell Sci 2004;117(Pt 26):6377–6389. 62. Bolte S, Brown S, Satiat-Jeunemaitre B. The N-myristoylated RabGTPase m-Rabmc is involved in post-Golgi trafficking events to the lytic vacuole in plant cells. J Cell Sci 2004;117(Pt 6):943–954. 63. Ueda T, Uemura T, Sato MH, Nakano A. Functional differentiation of endosomes in Arabidopsis cells. Plant J 2004;40(5):783–789. 64. Lee GJ, Sohn EJ, Lee MH, Hwang I. The Arabidopsis rab5 homologs rha1 and ara7 localize to the prevacuolar compartment. Plant Cell Physiol 2004;45(9):1211–1220. 65. Goh T, Uchida W, Arakawa S, Ito E, Dainobu T, Ebine K, Takeuchi M, Sato K, Ueda T, Nakano A. VPS9a, the common activator for two

Traffic 2009; 10: 819–828

66.

67.

68.

69.

70.

71.

72. 73.

74.

75.

76.

77.

78.

79.

80. 81.

82.

distinct types of Rab5 GTPases, is essential for the development of Arabidopsis thaliana. Plant Cell 2007;19(11):3504–3515. Nahm MY, Kim SW, Yun D, Lee SY, Cho MJ, Bahk JD. Molecular and biochemical analyses of OsRab7, a rice Rab7 homolog. Plant Cell Physiol 2003;44(12):1341–1349. Lobstein E, Guyon A, Ferault M, Twell D, Pelletier G, Bonhomme S. The putative Arabidopsis homolog of yeast vps52p is required for pollen tube elongation, localizes to Golgi, and might be involved in vesicle trafficking. Plant Physiol 2004;135(3):1480–1490. Guermonprez H, Smertenko A, Crosnier MT, Durandet M, Vrielynck N, Guerche P, Hussey PJ, Satiat-Jeunemaitre B, Bonhomme S. The POK/AtVPS52 protein localizes to several distinct post-Golgi compartments in sporophytic and gametophytic cells. J Exp Bot 2008;59(11):3087–3098. Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, El Kasmi F, Jurgens G, Parker J, Panstruga R, Lipka V, et al. Co-option of a default secretory pathway for plant immune responses. Nature 2008;451(7180):835–840. Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, Somerville CR, Thordal-Christensen H. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 2004;15(11):5118–5129. Muller I, Wagner W, Volker A, Schellmann S, Nacry P, Kuttner F, Schwarz-Sommer Z, Mayer U, Jurgens G. Syntaxin specificity of cytokinesis in Arabidopsis. Nat Cell Biol 2003;5(6):531–534. Honys D, Twell D. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 2004;5(11):R85. Catalano CM, Czymmek KJ, Gann JG, Sherrier DJ. Medicago truncatula syntaxin SYP132 defines the symbiosome membrane and infection droplet membrane in root nodules. Planta 2007;225(3):541–550. Tyrrell M, Campanoni P, Sutter JU, Pratelli R, Paneque M, Sokolovski S, Blatt MR. Selective targeting of plasma membrane and tonoplast traffic by inhibitory (dominant-negative) SNARE fragments. Plant J 2007;51(6):1099–1115. Foresti O, daSilva LL, Denecke J. Overexpression of the Arabidopsis syntaxin PEP12/SYP21 inhibits transport from the prevacuolar compartment to the lytic vacuole in vivo. Plant Cell 2006;18(9):2275–2293. Heese M, Gansel X, Sticher L, Wick P, Grebe M, Granier F, Jurgens G. Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J Cell Biol 2001;155(2):239–249. Uemura T, Sato MH, Takeyasu K. The longin domain regulates subcellular targeting of VAMP7 in Arabidopsis thaliana. FEBS Lett 2005;579(13):2842–2846. Chen X, Matsumoto H, Hinck CS, Al-Hasani H, St-Denis JF, Whiteheart SW, Cushman SW. Demonstration of differential quantitative requirements for NSF among multiple vesicle fusion pathways of GLUT4 using a dominant-negative ATPase-deficient NSF. Biochem Biophys Res Commun 2005;333(1):28–34. Sanderfoot AA, Kovaleva V, Bassham DC, Raikhel NV. Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol Biology Cell 2001;12(12):3733–3743. Assaad FF. Plant cytokinesis. Exploring the links. Plant Physiol 2001;126(2):509–516. Bassham DC, Sanderfoot AA, Kovaleva V, Zheng H, Raikhel NV. AtVPS45 complex formation at the trans-Golgi network. Mol Biol Cell 2000;11(7):2251–2265. Men S, Boutte Y, Ikeda Y, Li X, Palme K, Stierhof YD, Hartmann MA, Moritz T, Grebe M. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 2008;10(2):237–244.

827

Richter et al. 83. Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, etal. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 2007;130(6):1044–1056. 84. Takano J, Miwa K, Fujiwara T. Boron transport mechanisms: collaboration of channels and transporters. Trends Plant Sci 2008;13(8):451–457. 85. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M. A silicon transporter in rice. Nature 2006;440(7084):688–691. 86. Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, Katsuhara M, Yano M. An efflux transporter of silicon in rice. Nature 2007;448(7150):209–212. 87. Panikashvili D, Savaldi-Goldstein S, Mandel T, Yifhar T, Franke RB, Hofer R, Schreiber L, Chory J, Aharoni A. The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol 2007;145(4):1345–1360. 88. Bird D, Beisson F, Brigham A, Shin J, Greer S, Jetter R, Kunst L, Wu X, Yephremov A, Samuels L. Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 2007;52(3):485–498. 89. Lancelle SA, Hepler PK. Ultrastructure of freezesubstituted pollen tubes of Lilium longiflorum. Protoplasma 1992;167:215–230. 90. Derksen J, Rutten T, Lichtscheidl I, de Win K. AHN, Pierson ES, Rongen G. Quantitative analysis of the distribution of organelles in tobacco pollen tubes: implications for exocytosis and endocytosis. Protoplasma 1995;188(3–4):267–276. 91. Bove J, Vaillancourt B, Kroeger J, Hepler PK, Wiseman PW, Geitmann A. Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy (STICS) and fluorescence recovery after photobleaching (FRAP). Plant Physiology 2008;147(4):1646–1658. 92. Zonia L, Munnik T. Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. J Exp Bot 2008;59(4):861–873. 93. Ovecka M, Lang I, Baluska F, Ismail A, Illes P, Lichtscheidl IK. Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 2005;226(1–2):39–54. 94. de Graaf BH, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, Wu HM. Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 2005;17(9):2564–2579. 95. Gu Y, Fu Y, Dowd P, Li S, Vernoud V, Gilroy S, Yang Z. A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol 2005;169(1):127–138. 96. Lavy M, Bloch D, Hazak O, Gutman I, Poraty L, Sorek N, Sternberg H, Yalovsky S. A Novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr Biol 2007;17(11):947–952. 97. Hala M, Cole R, Synek L, Drdova E, Pecenkova T, Nordheim A, Lamkemeyer T, Madlung J, Hochholdinger F, Fowler JE, Zarsky V.

828

98.

99.

100.

101. 102.

103.

104.

105.

106.

107.

108. 109.

110.

111.

An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 2008;20(5):1330–1345. Fischer U, Ikeda Y, Ljung K, Serralbo O, Singh M, Heidstra R, Palme K, Scheres B, Grebe M. Vectorial information for Arabidopsis planar polarity is mediated by combined AUX1, EIN2, and GNOM activity. Curr Biol 2006;16(21):2143–2149. Robatzek S, Bittel P, Chinchilla D, Kochner P, Felix G, Shiu SH, Boller T. Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol Biol 2007;64(5):539–547. Geldner N, Hyman DL, Wang X, Schumacher K, Chory J. Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 2007;21(13):1598–1602. McCarty DR, Chory J. Conservation and innovation in plant signaling pathways. Cell 2000;103(2):201–209. Kwaaitaal MA, de Vries SC, Russinova E. Arabidopsis thaliana somatic embryogenesis receptor kinase 1 protein is present in sporophytic and gametophytic cells and undergoes endocytosis. Protoplasma 2005;226(1–2):55–65. Ritzenthaler C, Nebenfuhr A, Movafeghi A, Stussi-Garaud C, Behnia L, Pimpl P, Staehelin LA, Robinson DG. Reevaluation of the effects of brefeldin A on plant cells using tobacco Bright Yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. Plant Cell 2002;14(1):237–261. Wee EG, Sherrier DJ, Prime TA, Dupree P. Targeting of active sialyltransferase to the plant Golgi apparatus. Plant Cell 1998;10(10):1759–1768. Robinson DG, Oliviusson P, Hinz G. Protein sorting to the storage vacuoles of plants: a critical appraisal. Traffic 2005;6(8):615–625. Haas TJ, Sliwinski MK, Martinez DE, Preuss M, Ebine K, Ueda T, Nielsen E, Odorizzi G, Otegui MS. The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 2007;19(4):1295–1312. Jaillais Y, Fobis-Loisy I, Miege C, Rollin C, Gaude T. AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 2006;443(7107):106–109. Bonifacino JS, Hurley JH. Retromer. Curr Opin Cell Biol 2008;20(4):427–436. Takano J, Noguchi K, Yasumori M, Kobayashi M, Gajdos Z, Miwa K, Hayashi H, Yoneyama T, Fujiwara T. Arabidopsis boron transporter for xylem loading. Nature 2002;420(6913):337–340. Takano J, Wada M, Ludewig U, Schaaf G, von Wiren N, Fujiwara T. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 2006;18(6):1498–1509. Takano J, Miwa K, Yuan L, von Wiren N, Fujiwara T. Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci USA 2005;102(34):12276–12281.

Traffic 2009; 10: 819–828