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The Plant Endomembrane System—A Complex Network Supporting Plant Development and Physiology Miyo Terao Morita1,* and Tomoo Shimada2,* 1 Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya, 464-8601 Japan Department of Botany, Graduate School of Science, Kyoto University, Kyoto, 606-8502 Japan *Corresponding author: Miyo Terao Morita, E-mail, [email protected]; Fax, +81-52-789-4123; Tomoo Shimada, E-mail, [email protected]; Fax, +81-75-753-4141. 2 In eukaryotic cells, the endomembrane system is a functionally inter-related membrane system including the endoplasmic reticulum (ER), the nuclear envelope, the Golgi apparatus, vacuoles/lysosomes, endosomes, the plasma membrane (PM) and vesicles. The endomembrane system comprises a complex network of membrane trafficking, which is essential for transport and exchange of materials such as proteins and lipids. There is no doubt that membrane trafficking fulfills a fundamental function, supporting cell proliferation, maintenance of cellular homeostasis and specific demands for higher order function in multicellular organisms. The plant endomembrane system is mostly conserved amongst all eukaryotes, but also displays some highly complex and unique characteristics. Homology-based approaches, which have been greatly supported by the Arabidopsis genome project, have shaped our understanding of the conserved framework underlying the plant endomembrane system (Bassham et al. 2008). In addition, cumulative knowledge about the genes involved as well as the development of live cell imaging tools has led to an explosion of studies highlighting the many diverse plant-specific cellular and developmental processes, and whole plant-related phenomena that are supported by the endomembrane system. This Special Focus Issue presents a further two reviews and 12 research articles that enhance our understanding of endomembrane function and dynamics in plants. Current Trends in Plant Endomembrane Research Membrane trafficking pathways are essential for maintaining fundamental cellular functions as well as for responding to various environmental stimuli. Recently, the role of membrane trafficking in plant–microbe interactions has been highlighted. In the first of two reviews in this issue, Inada and Ueda (2014) comprehensively describe current understanding of the relationship between membrane trafficking and microbes for both pathogenic and mutualistic interactions. Together with superb illustrations, this review provides not only an update on progress but also valuable insight into future research goals in this field. Cell walls perform a number of essential functions in plant cells, such as providing shape, mechanical strength, an interface between adjacent cells and resistance under biotic and abiotic stress conditions. The second review by Kim and Brandizzi (2014) neatly describes specific key discoveries related to mechanisms and functions of the secretory pathway in cell wall biogenesis. Novel Features of the Plant Endomembrane System Live cell imaging using appropriate molecular markers has revealed a wealth of information regarding the dynamic nature of the plant endomembrane. The TGN (trans-Golgi network) functions as a sorting station that directs cargo proteins to a variety of destinations, including post-Golgi compartments and extracellular spaces. Recent studies have demonstrated that the TGN also functions as an early endosome (EE) in plant cells (Dettmer et al. 2006, Viotti et al. 2010). In this issue, Uemura et al. (2014) reveal the dynamic behavior of green fluorescent protein (GFP)–SYP43 (the ortholog of Tlg2/syntaxin 16)-labeled TGN. Using superresolution confocal live imaging microscopy developed by the authors, two independent types of TGN were identified in Arabidopsis root cells: the GA-TGN (Golgi-associated TGN), located on the trans-side of the Golgi apparatus, and the GITGN (Golgi-released independent TGN), located away from the Golgi apparatus. These results revealed dynamic features of the TGN in plant cells that differ from those of animal and yeast cells, and will form the basis of future studies targeted at uncovering further unique functions of the TGN in plant cells. The structural organization of the endomembrane system is important for proper membrane trafficking and is fundamental for plant physiology. To explore the mechanisms regulating membrane trafficking and endomembrane organization in plant cells, Uehara et al. (2014) screened Arabidopsis mutants defective in the localization of GFP–NIP5;1 (nodulin 26-like Plant Cell Physiol. 55(4): 667–671 (2014) doi:10.1093/pcp/pcu049, available online at www.pcp.oxfordjournals.org ! The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: [email protected] Plant Cell Physiol. 55(4): 667–671 (2014) doi:10.1093/pcp/pcu049 ! The Author 2014. 667 intrinsic protein). NIP5;1 is a PM-localized boric acid channel belonging to the major intrinsic protein (aquaporin) family (Takano et al. 2006). Fluorescence imaging-based screening led to the isolation of a mutant which accumulated abnormal intracellular aggregates labeled with GFP–NIP5;1. The responsible gene encodes UDP-glucose 4-epimerase 4 (UGE4), which is involved in D-galactose biosynthesis, and is required for the synthesis of the cell wall polysaccharide xyloglucan and arabinogalactan proteins (Seifert et al. 2002). Alleles of UGE4 were previously identified as root hair defective 1 (rhd1) and root epidermal bulgar 1 (reb1) mutants, which exhibit defective root hair development, root morphology and susceptibility to nematode infection (Schiefelbein and Somerville 1990, Baskin et al. 1992, Baum et al. 2000). These observations suggest that UGE4 activity in D-galactose synthesis is required for the structure of cell wall polysaccharides and endomembrane organization. Autophagy is a degradation pathway that recycles cell materials upon encountering stress conditions or during specific developmental processes (Klionsky 2007). The AuTophaGyrelated (ATG) genes that regulate the autophagic process were initially discovered in yeast (Xie and Klionsky 2007) and their homologs are well conserved in mammals and plants (Reumann et al. 2010, Tanida 2011). To better understand the physiological roles of autophagy in plants, Merkulova et al. (2014) carefully observed the autophagic process in planta using different monitoring methods in Arabidopsis roots. They identified a GFP–ATG8 fusion protein as an excellent tool for monitoring autophagy in plants. In contrast, acidotropic dyes such as monodansylcadaverine (MDC) and LysoTracker Red (LTR), which are often used for monitoring autophagy in mammals and yeast, did not work well in planta. Furthermore, assessment and optimization of autophagy monitoring methods in Arabidopsis roots provided some evidence for the direct fusion of autophagosomes with vacuoles (Merkulova et al. 2014). Ubiquitination is a post-translational protein modification that is well conserved among eukaryotic cells (Kerscher et al. 2006). A cascade of E1, E2 and E3 enzymes work together to conjugate ubiquitin to the target protein, and this modification can be reversed by the activity of deubiquitinating enzymes. Recent studies have shown that ubiquitination regulates endocytosis and the subsequent vacuolar degradation of PM proteins in plants (Abas et al. 2006, Gohre et al. 2008, Lee et al. 2009, Barberon et al. 2011, Kasai et al. 2011). In this issue, Katsiarimpa et al. (2014) show that ASSOCIATED MOLECULE WITH THE SH3 DOMAIN OF STAM 3 (AMSH3) is essential for degradation of ubiquitinated membrane proteins in Arabidopsis. AMSH3 is a deubiquitinating enzyme that interacts with the endosomal sorting complex required for transport (ESCRT)-III machinery (Isono et al., 2010). An enzymatic inactive AMSH3 variant inhibits the AvrPtoB-dependent endocytic degradation of CERK1 (CHITIN ELICITOR RECEPTOR KINASE 1), and interaction of AMSH3 with ESCRT-III is important for its function in planta. 668 The Endomembrane System and Plant Development The levels and distribution of the plant hormone auxin are critical in regulating multiple developmental processes in plants (Mockaitis and Estelle 2008, Vanneste and Friml 2009). Auxin transporters of the PIN-FORMED (PIN) family localize asymmetrically at the PM and mediate directional intercellular auxin transport (Tanaka et al. 2006, Vanneste and Friml 2009). The subcellular localization of PIN proteins, which is mainly regulated by vesicle trafficking, is a key determinant of polar auxin transport. Using a fluorescence imaging-based forward genetic approach, Tanaka et al. (2014) show that BFAVISUALIZED EXOCYTIC TRAFFICKING DEFECTIVE1 (BEX1) is required for recycling of PIN transporters and auxin-mediated development in Arabidopsis. BEX1 encodes a member of the ADP-ribosylation factor (ARF) small GTPases, ARF1A1C, which localizes to the TGN/EE and Golgi apparatus. While previous studies have shown that the ARF guanine nucleotide exchange factor (GEF), GNOM, plays a major role in localizing PIN1 predominantly to the basal side of the PM (Steinmann et al. 1999), this study provides new insight into the missing link between GNOM function and asymmetric PIN1 localization. Polar auxin transport by PIN1 is required for normal venation patterning (Mattsson et al. 1999, Koizumi et al. 2005). Similarly, VASCULAR NETWORK DEFECTIVE4 (VAN4) is required for venation development and cellular growth. In this issue, Naramoto et al (2014) further demonstrate that VAN4 encodes a putative TRS120 subunit of the TRAPPII complex protein that functions as a Rab-GEF and/or tethering factor (Jones et al. 2000, Sacher et al. 2008). Although the importance of VAN4 function in polar localization of PIN proteins is still ambiguous, VAN4 localizes to the TGN/EE where it appears to be involved in the recycling of PIN proteins. Previous reports also indicated that VAN3/SFC, ARF-GAP and VAN7/ GNOM ARF-GEF regulate venation pattern by controlling the activity of the ARF GTPase (Koizumi et al. 2000, Koizumi et al. 2005, Sieburth et al. 2006, Naramoto et al. 2009). Collectively, these studies provide robust evidence for the importance of vesicle transport in leaf vascular formation. Another link between endomembrane trafficking and plant development was revealed by the analysis of continuous vascular ring (cov1) mutants. Previously, the cov1 mutant was reported to exhibit ectopic differentiation of vascular cells in the Arabidopsis stem (Parker et al. 2003). In this issue, Shirakawa et al. (2014) show that COV1 is a TGN-localized membrane protein that is required for Golgi morphology and vacuolar protein trafficking. In addition to the vascular patterning, COV1 is also required for the development of myrosin cells in leaves (Shirakawa et al. 2014). These results highlight the important relationship between endomembrane trafficking and plant higher order function, particularly vascular patterning and myrosin cell development. Similar defects in vascular patterning and myrosin development have been reported in Arabidopsis syp2 mutants, which lack key components of the Plant Cell Physiol. 55(4): 667–671 (2014) doi:10.1093/pcp/pcu049 ! The Author 2014. vacuolar SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) (Ueda et al. 2006, Shirakawa et al. 2010). It is thus possible that trafficking pathways (the vacuolar trafficking pathway and/or the endocytic pathway) common to COV1 and SYP2 family proteins affect the development of myrosin cells. The Endomembrane System in Plant-Specific Processes The Arabidopsis stomatal complex is composed of a pair of guard cells and surrounding anisocytic subsidiary cells (Serna and Fenoll 2000). Although subsidiary cells, together with guard cells, are thought to cause stomatal movement via bulk water and ion flow (Raschke and Fellows 1971), the underlying molecular mechanism remains unclear. Higaki et al. (2014) studied the dynamic behavior and environmental responses of PROTON-ATPase TRANSLOCATION CONTROL 1 (PATROL1) on stomatal movement. PATROL1 is a translocation factor of the PM proton pump ATPase AHA1 in guard cells (Hashimoto-Sugimoto et al. 2013). Interestingly, subsidiary cells showed changes in localization of GFP–PATROL1 in response to environmental stimuli that contrasted with those in guard cells (Higaki et al. 2014). GFP–PATROL1 and red fluorescent protein (RFP)–AHA1 co-localized in hyperosmotic conditions, and a mutation in PATROL1 resulted in increased GFP–AHA1 internalization in subsidiary cells. These live-cell imaging results suggest that PATROL1-mediated membrane trafficking in subsidiary cells is important for stomatal movement. Over 60 genes in the Arabidopsis genome encode SNARE proteins (Uemura et al. 2004, Sanderfoot 2007), which contribute to various biological processes including growth, homeostasis, hormone and stress responses, and immunity against pathogens (Collins et al. 2003, Lipka et al. 2007, El Kasmi et al. 2013). To characterize SNARE protein networks in cells, Fujiwara et al. (2014) performed interactomics using immunoprecipitation and mass spectrometry as a powerful, highthroughput tool to identify the proteins that interact with 12 Arabidopsis Qa-SNAREs. Despite their redundant nature, nine Qa-SNARE molecules have been shown to localize to the PM (Uemura et al. 2004), implying that each PM Qa-SNARE molecule has a specialized physiological function, yet exhibits partially overlapping functions. Ichikawa et al. (2014) report that two different PM-localized Qa-SNAREs, SYP123 and SYP132, function coordinately in root hair elongation in Arabidopsis by forming SNARE complexes with a PM R-SNARE, VAMP721/722/724. BiP is an ER-localized molecular chaperone of the heat shock protein 70 (Hsp70) family and plays key roles in protein translocation, protein folding and quality control in the ER (Nishikawa et al. 2005, Bukau et al. 2006). Flowering plants have multiple BIP genes, in contrast to yeast and mammals. Among three BiP paralogs in Arabidopsis, two almost identical BiPs (BiP1 and BiP2) are ubiquitously expressed, while the less well conserved BiP3 is expressed only under ER stress conditions (Noh et al. 2003). Maruyama et al. (2014) demonstrate that BiP3 is expressed in pollen and pollen tubes without ER stress and has functions that are comparable with those of BiP1 and BiP2 in male gametogenesis and pollen tube growth. The study suggests that the multiple BiP proteins of flowering plants are important to meet the high cellular demands for protein secretion in actively growing cells such as the pollen tube. In mature plant cells, vacuolar membranes (VMs) display dynamic structures, which are formed by invagination and folding of VMs into the lumenal side and can gradually move and change shape (Saito et al. 2002, Oda et al. 2009). The dynamic nature of VMs is important for the whole-plant-related phenomenon, shoot gravitropism. Dynamic VM structures in gravity-sensing cells are required for statolith (amyloplast) sedimentation in gravity susception (Morita 2010). Hashiguchi et al. (2014) report on a novel HEAT-repeat protein, SHOOT GRAVITROPISM6 (SGR6), which affects amyloplast sedimentation via control of dynamic VM structures within shoot gravity-sensing cells. Live imaging analyses indicate that VM-associated SGR6 is involved in the formation and/or maintenance of invaginated VM structures. Final Remarks The Nobel Prize in Physiology or Medicine 2013 was awarded jointly to James E. Rothman, Randy W. Schekman and Thomas C. Südhof for their discoveries of the machinery regulating vesicle trafficking. This reaffirms the importance and expansiveness of the endomembrane research field. As introduced above, plant endomembrane research is intimately associated with a wide variety of research areas. We expect that this Special Focus Issue will serve as a trigger to consider the relationship between your research topic and the plant endomembrane system. References Abas, L., Benjamins, R., Malenica, N., Paciorek, T., Wisniewska, J., Moulinier-Anzola, J.C. et al. (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8: 249–256. Barberon, M., Zelazny, E., Robert, S., Conejero, G., Curie, C., Friml, J. et al. (2011) Monoubiquitin-dependent endocytosis of the IRON-REGULATED TRANSPORTER 1 (IRT1) transporter controls iron uptake in plants. Proc. Natl Acad. Sci. USA 108: E450–E458. Baskin, T., Betzner, A., Hoggard, R., Cork, A. and Williamson, R.E. (1992) Root morphology mutants in Arabidopsis thaliana. Aust. J. Plant Physiol. 19: 427–437. Bassham, D.C., Brandizzi, F., Otegui, M.S. and Sanderfood, A.A. (2008) The secretory system of Arabidopsis. The Arabidopsis Book 6: e0116. Baum, T.J., Wubben, M.J.E., Hardy, Y.K.A., Su, H. and Rodermel, S.R. (2000) A screen for Arabidopsis thaliana mutants with altered susceptibility to Heterodera schachtii. J. Nematol. 32: 166–173. Bukau, B., Weissman, J.S. and Horwich, A.L. (2006) Molecular chaperones and protein quality control. Cell 125: 443–451. Plant Cell Physiol. 55(4): 667–671 (2014) doi:10.1093/pcp/pcu049 ! The Author 2014. 669 Collins, N.C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J.L. et al. (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425: 973–977. Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.D. and Schumacher, K. (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715–730. El Kasmi, F., Krause, C., Hiller, U., Stierhof, Y.D., Mayer, U., Conner, L. et al. (2013) SNARE complexes of different composition jointly mediate membrane fusion in Arabidopsis cytokinesis. Mol. Biol. Cell 24: 1593–1601. Fujiwara, M., Uemura, T., Ebine, K., Nishimori, Y., Ueda, T., Nakano, A. et al. (2014) Interactomics of Qa-SNARE in Arabidopsis thaliana. Plant Cell Physiol. 55: 781–789. Gohre, V., Spallek, T., Haweker, H., Mersmann, S., Mentzel, T., Boller, T. et al. (2008) Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18: 1824–1832. Hashiguchi, Y., Yano, D., Nagafusa, K., Kato, T., Saito, C., Uemura, T. et al. (2014) A unique HEAT repeat-containing protein SHOOT GRAVITROPISM6 is involved in vacuolar membrane dynamics in gravity sensing cells of Arabidopsis inflorescence stem. Plant Cell Physiol. 55: 811–822. Hashimoto-Sugimoto, M., Higaki, T., Yaeno, T., Nagami, A., Irie, M., Fujimi, M. et al. (2013) A Munc13-like protein in Arabidopsis mediates H+-ATPase translocation that is essential for stomatal responses. Nat. Commun. 4: 2215. Higaki, T., Hashimoto-Sugimoto, M., Akita, K., Iba, K. and Hasezawa, S. (2014) Dynamics and environmental responses of PATROL1 in Arabidopsis subsidiary cells. Plant Cell Physiol. 55: 773–780. Ichikawa, M., Hirano, T., Enami, K., Fuselier, T., Kato, N., Kwon, C. et al. (2014) Syntaxin of plant proteins SYP123 and SYP132 mediate root hair tip growth in Arabidopsis thaliana. Plant Cell Physiol. 55: 790–800. Inada, N. and Ueda, T. (2014) Membrane trafficking pathways and their roles in plant–microbe interactions. Plant Cell Physiol. 55: 672–686. Isono, E., Katsiarimpa, A., Muller, I.K., Anzenberger, F., Stierhof, Y.D., Geldner, N. et al. (2010) The deubiquitinating enzyme AMSH3 is required for intracellular trafficking and vacuole biogenesis in Arabidopsis thaliana. Plant Cell 22: 1826–1837. Jones, S., Newman, C., Liu, F. and Segev, N. (2000) The TRAPP complex is a nucleotide exchanger for Ypt1 and Ypt31/32. Mol. Biol. Cell 11: 4403–4411. Kasai, K., Takano, J., Miwa, K., Toyoda, A. and Fujiwara, T. (2011) High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J. Biol. Chem. 286: 6175–6183. Katsiarimpa, A., Muñoz, A., Kalinowska, K., Uemura, T., Rojo, E. and Isono, E. (2014) The ESCRT-III-interacting deubiquitinating enzyme AMSH3 is essential for degradation of ubiquitinated membrane proteins in Arabidopsis thaliana. Plant Cell Physiol. 55: 727–736. Kerscher, O., Felberbaum, R. and Hochstrasser, M. (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22: 159–180. Kim, S.-J. and Brandizzi, F. (2014) The plant secretory pathway: an essential factory for building the plant cell wall. Plant Cell Physiol. 55: 687–693. Klionsky, D.J. (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nature Rev. Mol. Cell Biol. 8: 931–937. 670 Koizumi, K., Sugiyama, M. and 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. Koizumi, K., Naramoto, S., Sawa, S., Yahara, N., Ueda, T., Nakano, A. et al. (2005) VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation. Development 132: 1699–1711. Lee, H.K., Cho, S.K., Son, O., Xu, Z., Hwang, I. and Kim, W.T. (2009) Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 21: 622–641. Lipka, V., Kwon, C. and Panstruga, R. (2007) SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu. Rev. Cell Dev. Biol. 23: 147–174. Maruyama, D., Sugiyama, T., Endo, T. and Nishikawa, S.-i. (2014) Multiple BiP genes of Arabidopsis thaliana are required for male gametogenesis and pollen competitiveness. Plant Cell Physiol. 55: 801–810. Mattsson, J., Sung, Z. and Berleth, T. (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126: 2979–2991. Merkulova, E.A., Guiboileau, A., Naya, L., Masclaux-Daubresse, C. and Yoshimoto, K. (2014) Assessment and optimization of autophagy monitoring methods in Arabidopsis roots indicate direct fusion of autophagosomes with vacuoles. Plant Cell Physiol. 55: 715–726. Mockaitis, K. and Estelle, M. (2008) Auxin receptors and plant development: a new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24: 55–80. Morita, M.T. (2010) Directional gravity sensing in gravitropism. Annu. Rev. Plant Biol. 61: 706–720. Naramoto, S., Sawa, S., Koizumi, K., Uemura, T., Ueda, T., Friml, J. et al. (2009) Phosphoinositide-dependent regulation of VAN3 ARF-GAP localization and activity essential for vascular tissue continuity in plants. Development 136: 1529–1538. Naramoto, S., Nodzyński, T., Dainobu, T., Takatsuka, H., Okada, T. et al. (2014) VAN4 encodes a putative TRS120 that is required for normal cell growth and vein development in Arabidopsis. Plant Cell Physiol. 55: 750–763. Nishikawa, S., Brodsky, J.L. and Nakatsukasa, K. (2005) Roles of molecular chaperones in endoplasmic reticulum (ER) quality control and ER-associated degradation (ERAD). J. Biochem. 137: 20 551–555. Noh, S.J., Kwon, C.S., Oh, D.H., Moon, J.S. and Chung, W.I. (2003) Expression of an evolutionarily distinct novel BiP gene during the unfolded protein response in Arabidopsis thaliana. Gene 311: 81–91. Oda, Y., Higaki, T., Hasezawa, S. and Kutsuna, N. (2009) New insights into plant vacuolar structure and dynamics. Int. Rev. Cell Mol. Biol. 277: 103–135. Parker, G., Schofield, R., Sundberg, B. and Turner, S. (2003) Isolation of COV1, a gene involved in the regulation of vascular patterning in the stem of Arabidopsis. Development 130: 2139–2148. Raschke, K. and Fellows, M.P. (1971) Stomatal movement in Zea mays: shuttle of potassium and chloride between guard cells and subsidiary cells. Planta 101: 296–316. Reumann, S., Voitsekhovskaja, O. and Lillo, C. (2010) From signal transduction to autophagy plant cell organelles: lessons from yeast and mammals and plant-specific features. Protoplasma 247: 233–256. Sacher, M., Kim, Y., Lavie, A., Oh, B. and Segev, N. (2008) The TRAPP complex: insights into its architecture and function. Traffic 9: 2032–2042. Saito, C., Ueda, T., Abe, H., Wada, Y., Kuroiwa, T., Hisada, A. et al. (2002) A complex and mobile structure forms a distinct subregion Plant Cell Physiol. 55(4): 667–671 (2014) doi:10.1093/pcp/pcu049 ! The Author 2014. within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J. 29: 245–255. Sanderfoot, A. (2007) Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol. 144: 6–17. Schiefelbein, J. and Somerville, C. (1990) Genetic control of root hair development in Arabidopsis thaliana. Plant Cell 2: 235–243. Seifert, G.J., Barber, C., Wells, B., Dolan, L. and Roberts, K. (2002) Galactose biosynthesis in Arabidopsis: genetic evidence for substrate channeling from UDP-D-galactose into cell wall polymers. Curr. Biol. 12: 1840–1845. Serna, L. and Fenoll, C. (2000) Stomatal development and patterning in Arabidopsis leaves. Physiol. Plant. 109: 351–358. Shirakawa, M., Ueda, H., Shimada, T., Koumoto, Y., Shimada, T.L., Kondo, M. et al. (2010) Arabidopsis Qa-SNARE SYP2 proteins localized to different subcellular regions function redundantly in vacuolar protein sorting and plant development. Plant J. 64: 924–935. Shirakawa, M., Ueda, H., Koumoto, Y., Fuji, K., Nishiyama, C., Kohchi, T. et al. (2014) CONTINUOUS VASCULAR RING (COV1) is a transGolgi network-localized membrane protein required for Golgi morphology and vacuolar protein sorting. Plant Cell Physiol. 55: 764–772. Sieburth, L., Muday, G., King, E., Benton, G., Kim, S., Metcalf, K. et al. (2006) SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. Plant Cell 18: 1396–1411. Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C.L., Paris, S. et al. (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286: 316–318. Takano, J., Wada, M., Ludewig, U., Schaaf, G., von Wiren, N. and Fujiwara, T. (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18: 1498–1509. Tanaka, H., Dhonukshe, P., Brewer, P.B. and Friml, J. (2006) Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development. Cell. Mol. Life Sci. 63: 2738–2754. Tanaka, H., Nodzyński, T., Kitakura, S., Feraru, M.I., Sasabe, M., Ishikawa, T. et al. (2014) BEX1/ARF1A1C is required for BFA-sensitive recycling of PIN auxin transporters and auxin-mediated development in Arabidopsis. Plant Cell Physiol. 55: 737–749. Tanida, I. (2011) Autophagosome formation and molecular mechanism of autophagy. Antioxid. Redox Signal. 14: 2201–2214. Ueda, H., Nishiyama, C., Shimada, T., Koumoto, Y., Hayashi, Y., Kondo, M. et al. (2006) AtVAM3 is required for normal specification of idioblasts, myrosin cells. Plant Cell Physiol. 47: 164–175. Uehara, M., Wang, S., Kamiya, T., Shigenobu, S., Yamaguchi, K., Fujiwara, T. et al. (2014) Identification and characterization of an Arabidopsis mutant with altered localization of NIP5;1, a plasma membrane boric acid channel, reveals the requirement for D-galactose in endomembrane organization. Plant Cell Physiol. 55: 704–714. Uemura, T., Suda, Y., Ueda, T. and Nakano, A. (2014) Dynamic behavior of the trans-Golgi network in root tissues of Arabidopsis revealed by super-resolution live imaging. Plant Cell Physiol. 55: 694–703. Uemura, T., Ueda, T., Ohniwa, R.L., Nakano, A., Takeyasu, K. and Sato, M.H. (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct. Funct. 29: 49–65. Vanneste, S. and Friml, J. (2009) Auxin: a trigger for change in plant development. Cell 136: 1005–1016. Viotti, C., Bubeck, J., Stierhof, Y.D., Krebs, M., Langhans, M., van den Berg, W. et al. (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22: 1344–1357. Xie, Z. and Klionsky, D.J. (2007) Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9: 1102–1109. Plant Cell Physiol. 55(4): 667–671 (2014) doi:10.1093/pcp/pcu049 ! The Author 2014. 671