The Role of RAB GTPases and SNARE Proteins in Plant Endocytosis and Post-Golgi Trafficking

Chapter

Abstract

Each membrane trafficking pathway involves several evolutionarily conserved key molecules, including RAB GTPases and SNARE proteins. Distinct sets of RAB and SNARE molecules regulate tethering and fusion of the carrier membrane to the target membrane for different trafficking pathways. These proteins are thought to control the specificity of directional targeting and membrane fusion to the correct target organelles. These molecules also exhibit distinctive subcellular localizations and are, therefore, regarded as earmarks for organelles. Several subgroups of RAB and SNARE are widely conserved among eukaryotic lineages, indicating ancient origins and conserved functions. In contrast, recent comparative genomics indicated RAB and SNARE members have expanded in a lineage-specific manner. This finding suggests novel trafficking routes, which are unique to each lineage, developed during evolution. Plant-unique sets of RAB and SNARE proteins have been identified and characterized in recent years. In this chapter, we summarize the conserved and unique features of plant RAB and SNARE proteins with a special focus on post-Golgi trafficking pathways, including the endocytic pathway.

Keywords

Vacuolar Membrane Endocytic Pathway Snare Complex Snare Protein Trafficking Pathway 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abbal P, Pradal M, Muniz L, Sauvage FX, Chatelet P, Ueda T, Tesniere C (2008) Molecular characterization and expression analysis of the Rab GTPase family in Vitis vinifera reveal the specific expression of a VvRabA protein. J Exp Bot 59(9):2403–2416. doi: 10.1093/jxb/ern132 PubMedCrossRefGoogle Scholar
  2. Assaad FF, Huet Y, Mayer U, Jurgens G (2001) The cytokinesis gene KEULE encodes a Sec1 protein that binds the syntaxin KNOLLE. J cell biol 152(3):531–543PubMedCrossRefGoogle Scholar
  3. 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 (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15(11):5118–5129. doi: 10.1091/mbc.E04-02-0140 PubMedCrossRefGoogle Scholar
  4. Benmerah A (2004) Endocytosis: signaling from endocytic membranes to the nucleus. Curr Biol 14(8):R314–R316PubMedCrossRefGoogle Scholar
  5. Bolte S, Brown S, Satiat-Jeunemaitre B (2004) The N-myristoylated Rab-GTPase m-Rabmc is involved in post-Golgi trafficking events to the lytic vacuole in plant cells. J Cell Sci 117(Pt 6):943–954PubMedCrossRefGoogle Scholar
  6. Bolte S, Schiene K, Dietz KJ (2000) Characterization of a small GTP-binding protein of the rab 5 family in Mesembryanthemum crystallinum with increased level of expression during early salt stress. Plant Mol Biol 42(6):923–936PubMedCrossRefGoogle Scholar
  7. Bottanelli F, Foresti O, Hanton S, Denecke J (2011) Vacuolar transport in tobacco leaf epidermis cells involves a single route for soluble cargo and multiple routes for membrane cargo. Plant Cell 23(8):3007–3025. doi: 10.1105/tpc.111.085480 PubMedCrossRefGoogle Scholar
  8. Bottanelli F, Gershlick DC, Denecke J (2012) Evidence for sequential action of Rab5 and Rab7 GTPases in prevacuolar organelle partitioning. Traffic 13(2):338-354PubMedCrossRefGoogle Scholar
  9. Cai H, Reinisch K, Ferro-Novick S (2007) Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 12(5):671–682PubMedCrossRefGoogle Scholar
  10. Camacho L, Smertenko AP, Perez-Gomez J, Hussey PJ, Moore I (2009) Arabidopsis Rab-E GTPases exhibit a novel interaction with a plasma-membrane phosphatidylinositol-4-phosphate 5-kinase. J Cell Sci 122(Pt 23):4383–4392. doi: 10.1242/jcs.053488 PubMedCrossRefGoogle Scholar
  11. Catalano CM, Czymmek KJ, Gann JG, Sherrier DJ (2007) Medicago truncatula syntaxin SYP132 defines the symbiosome membrane and infection droplet membrane in root nodules. Planta 225(3):541–550. doi: 10.1007/s00425-006-0369-y PubMedCrossRefGoogle Scholar
  12. Chen Y, Shin YK, Bassham DC (2005) YKT6 is a core constituent of membrane fusion machineries at the Arabidopsis trans-Golgi network. J Mol Biol 350(1):92–101. doi: 10.1016/j.jmb.2005.04.061 PubMedCrossRefGoogle Scholar
  13. Chow CM, Neto H, Foucart C, Moore I (2008) Rab-A2 and Rab-A3 GTPases define a trans-Golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. Plant Cell 20(1):101–123PubMedCrossRefGoogle Scholar
  14. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425(6961):973–977. doi: 10.1038/nature02076 PubMedCrossRefGoogle Scholar
  15. Dacks JB, Field MC (2007) Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J Cell Sci 120(Pt 17):2977–2985PubMedCrossRefGoogle Scholar
  16. de Graaf BH, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, Wu HM (2005) Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 17(9):2564–2579PubMedCrossRefGoogle Scholar
  17. Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18(3):715–730. doi: 10.1105/tpc.105.037978 PubMedCrossRefGoogle Scholar
  18. Drakakaki G, van de Ven W, Pan S, Miao Y, Wang J, Keinath NF, Weatherly B, Jiang L, Schumacher K, Hicks G, Raikhel N (2012) Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res 22(2):413–424. doi: 10.1038/cr.2011.129 PubMedCrossRefGoogle Scholar
  19. Ebine K, Fujimoto M, Okatani Y, Nishiyama T, Goh T, Ito E, Dainobu T, Nishitani A, Uemura T, Sato MH, Thordal-Christensen H, Tsutsumi N, Nakano A, Ueda T (2011) A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat Cell Biol 13(7):853–859. doi: 10.1038/ncb2270 PubMedCrossRefGoogle Scholar
  20. Ebine K, Miyakawa N, Fujimoto M, Uemura T, Nakano A, Ueda T (2012a) An endosomal trafficking pathway regulated by the plant-unique RAB5, ARA6. Small GTPases 3(1):1–5. doi: 10.1038/ncb2270 CrossRefGoogle Scholar
  21. Ebine K, Uemura T, Nakano A, Ueda T (2012b) Flowering time modulation by a vacuolar SNARE via FLOWERING LOCUS C in Arabidopsis thaliana. PLoS ONE 7(7):e42239Google Scholar
  22. Ebine K, Okatani Y, Uemura T, Goh T, Shoda K, Niihama M, Morita MT, Spitzer C, Otegui MS, Nakano A, Ueda T (2008) A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. Plant Cell 20(11):3006–3021. doi: 10.1105/tpc.107.057711 PubMedCrossRefGoogle Scholar
  23. Ebine K, Ueda T (2009) Unique mechanism of plant endocytic/vacuolar transport pathways. J Plant Res 122(1):21–30. doi: 10.1007/s10265-008-0200-x PubMedCrossRefGoogle Scholar
  24. Enami K, Ichikawa M, Uemura T, Kutsuna N, Hasezawa S, Nakagawa T, Nakano A, Sato MH (2009) Differential expression control and polarized distribution of plasma membrane-resident SYP1 SNAREs in Arabidopsis thaliana. Plant Cell Physiol 50(2):280–289. doi: 10.1093/pcp/pcn197 PubMedCrossRefGoogle Scholar
  25. Epp N, Rethmeier R, Kramer L, Ungermann C (2011) Membrane dynamics and fusion at late endosomes and vacuoles–Rab regulation, multisubunit tethering complexes and SNAREs. Eur J Cell Biol 90(9):779–785. doi: 10.1016/j.ejcb.2011.04.007 PubMedCrossRefGoogle Scholar
  26. Foresti O, daSilva LL, Denecke J (2006) Overexpression of the Arabidopsis syntaxin PEP12/SYP21 inhibits transport from the prevacuolar compartment to the lytic vacuole in vivo. Plant Cell 18(9):2275–2293. doi: 10.1105/tpc.105.040279 PubMedCrossRefGoogle Scholar
  27. Geelen D, Leyman B, Batoko H, Di Sansebastiano GP, Moore I, Blatt MR (2002) The abscisic acid-related SNARE homolog NtSyr1 contributes to secretion and growth: evidence from competition with its cytosolic domain. Plant Cell 14(2):387–406PubMedCrossRefGoogle Scholar
  28. Goh T, Uchida W, Arakawa S, Ito E, Dainobu T, Ebine K, Takeuchi M, Sato K, Ueda T, Nakano A (2007) VPS9a, the common activator for two distinct types of Rab5 GTPases, is essential for the development of Arabidopsis thaliana. Plant Cell 19(11):3504–3515. doi: 10.1105/tpc.107.053876 PubMedCrossRefGoogle Scholar
  29. Grefen C, Chen Z, Honsbein A, Donald N, Hills A, Blatt MR (2010) A novel motif essential for SNARE interaction with the K(+) channel KC1 and channel gating in Arabidopsis. Plant Cell 22(9):3076–3092. doi: 10.1105/tpc.110.077768 PubMedCrossRefGoogle Scholar
  30. Haas TJ, Sliwinski MK, Martinez DE, Preuss M, Ebine K, Ueda T, Nielsen E, Odorizzi G, Otegui MS (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19(4):1295–1312. doi: 10.1105/tpc.106.049346 PubMedCrossRefGoogle Scholar
  31. Heese M, Gansel X, Sticher L, Wick P, Grebe M, Granier F, Jurgens G (2001) Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J Cell Biol 155(2):239–249. doi: 10.1083/jcb.200107126 PubMedCrossRefGoogle Scholar
  32. Honsbein A, Sokolovski S, Grefen C, Campanoni P, Pratelli R, Paneque M, Chen Z, Johansson I, Blatt MR (2009) A tripartite SNARE-K+ channel complex mediates in channel-dependent K+ nutrition in Arabidopsis. Plant Cell 21(9):2859–2877. doi: 10.1105/tpc.109.066118 PubMedCrossRefGoogle Scholar
  33. Ishikawa T, Machida C, Yoshioka Y, Ueda T, Nakano A, Machida Y (2008) EMBRYO YELLOW gene, encoding a subunit of the conserved oligomeric Golgi complex, is required for appropriate cell expansion and meristem organization in Arabidopsis thaliana. Genes to cells: devoted to molecular and cellular mechanisms 13 (6):521–535. doi: 10.1111/j.1365-2443.2008.01186.x
  34. Jahn R, Scheller RH (2006) SNAREs–engines for membrane fusion. Nat Rev Mol Cell Biol 7(9):631–643PubMedCrossRefGoogle Scholar
  35. Kalde M, Nuhse TS, Findlay K, Peck SC (2007) The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc Nat Acad Sci USA 104(28):11850–11855. doi: 10.1073/pnas.0701083104 PubMedCrossRefGoogle Scholar
  36. 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, Schulze-Lefert P (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451(7180):835–840. doi: 10.1038/nature06545 PubMedCrossRefGoogle Scholar
  37. Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U, Hwang I, Lukowitz W, Jurgens G (1997) The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J cell biol 139(6):1485–1493PubMedCrossRefGoogle Scholar
  38. Leshem Y, Melamed-Book N, Cagnac O, Ronen G, Nishri Y, Solomon M, Cohen G, Levine A (2006) Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. Proc Nat Acad Sci U S A 103(47):18008–18013. doi: 10.1073/pnas.0604421103 CrossRefGoogle Scholar
  39. Leyman B, Geelen D, Blatt MR (2000) Localization and control of expression of Nt-Syr1, a tobacco SNARE protein. Plant J 24(3):369–381PubMedCrossRefGoogle Scholar
  40. Leyman B, Geelen D, Quintero FJ, Blatt MR (1999) A tobacco syntaxin with a role in hormonal control of guard cell ion channels. Science 283(5401):537–540PubMedCrossRefGoogle Scholar
  41. Limpens E, Ivanov S, van Esse W, Voets G, Fedorova E, Bisseling T (2009) Medicago N2-fixing symbiosomes acquire the endocytic identity marker Rab7 but delay the acquisition of vacuolar identity. Plant Cell 21(9):2811–2828. doi: 10.1105/tpc.108.064410 PubMedCrossRefGoogle Scholar
  42. Lu C, Zainal Z, Tucker GA, Lycett GW (2001) Developmental abnormalities and reduced fruit softening in tomato plants expressing an antisense Rab11 GTPase gene. Plant Cell 13(8):1819–1833PubMedGoogle Scholar
  43. Lukowitz W, Mayer U, Jurgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84(1):61–71PubMedCrossRefGoogle Scholar
  44. Lycett G (2008) The role of Rab GTPases in cell wall metabolism. J Exp Bot 59(15):4061–4074. doi: 10.1093/jxb/ern255 PubMedCrossRefGoogle Scholar
  45. Markgraf DF, Peplowska K, Ungermann C (2007) Rab cascades and tethering factors in the endomembrane system. FEBS Lett 581(11):2125–2130PubMedCrossRefGoogle Scholar
  46. Matsuzaki M, Misumi O, Shin IT, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428(6983):653–657. doi: 10.1038/nature02398 PubMedCrossRefGoogle Scholar
  47. Morita MT, Kato T, Nagafusa K, Saito C, Ueda T, Nakano A, Tasaka M (2002) Involvement of the vacuoles of the endodermis in the early process of shoot gravitropism in Arabidopsis. Plant Cell 14(1):47–56PubMedCrossRefGoogle Scholar
  48. Nielsen E, Cheung AY, Ueda T (2008) The regulatory RAB and ARF GTPases for vesicular trafficking. Plant Physiol 147(4):1516–1526. doi: 10.1104/pp.108.121798 PubMedCrossRefGoogle Scholar
  49. Novick P, Medkova M, Dong G, Hutagalung A, Reinisch K, Grosshans B (2006) Interactions between Rabs, tethers, SNAREs and their regulators in exocytosis. Biochem Soc Trans 34(Pt 5):683–686. doi: 10.1042/BST0340683 PubMedGoogle Scholar
  50. Ohtomo I, Ueda H, Shimada T, Nishiyama C, Komoto Y, Hara-Nishimura I, Takahashi T (2005) Identification of an allele of VAM3/SYP22 that confers a semi-dwarf phenotype in Arabidopsis thaliana. Plant Cell Physiol 46(8):1358–1365. doi: 10.1093/pcp/pci146 PubMedCrossRefGoogle Scholar
  51. Ovečka M, Berson T, Beck M, Derksen J, Šamaj J, Baluška F, Lichtscheidl IK (2010) Structural sterols are involved in both the initiation and tip growth of root hairs in Arabidopsis thaliana. Plant Cell 22(9):2999–3019. doi: 10.1105/tpc.109.069880 PubMedCrossRefGoogle Scholar
  52. Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172(7):991–998PubMedCrossRefGoogle Scholar
  53. Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E (2004) The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16(6):1589–1603. doi: 10.1105/tpc.021634 PubMedCrossRefGoogle Scholar
  54. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin IT, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319(5859):64–69. doi: 10.1126/science.1150646 PubMedCrossRefGoogle Scholar
  55. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122(5):735–749. doi: 10.1016/j.cell.2005.06.043 PubMedCrossRefGoogle Scholar
  56. Rojo E, Gillmor CS, Kovaleva V, Somerville CR, Raikhel NV (2001) VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev Cell 1(2):303–310PubMedCrossRefGoogle Scholar
  57. Rutherford S, Moore I (2002) The Arabidopsis Rab GTPase family: another enigma variation. Curr Opin Plant Biol 5(6):518–528PubMedCrossRefGoogle Scholar
  58. Saito C, Ueda T (2009) Functions of RAB and SNARE proteins in plant life. Int rev cell mol biol 274:183–233. doi: 10.1016/S1937-6448(08)02004-2 PubMedCrossRefGoogle Scholar
  59. Saito C, Ueda T, Abe H, Wada Y, Kuroiwa T, Hisada A, Furuya M, Nakano A (2002) A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J 29(3):245–255PubMedCrossRefGoogle Scholar
  60. Sanderfoot A (2007) Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol 144(1):6–17. doi: 10.1104/pp.106.092973 PubMedCrossRefGoogle Scholar
  61. Sanderfoot AA, Kovaleva V, Bassham DC, Raikhel NV (2001a) Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol Biol Cell 12(12):3733–3743PubMedGoogle Scholar
  62. Sanderfoot AA, Pilgrim M, Adam L, Raikhel NV (2001b) Disruption of individual members of Arabidopsis syntaxin gene families indicates each has essential functions. Plant Cell 13(3):659–666PubMedGoogle Scholar
  63. Shirakawa M, Ueda H, Shimada T, Koumoto Y, Shimada TL, Kondo M, Takahashi T, Okuyama Y, Nishimura M, Hara-Nishimura I (2010) Arabidopsis Qa-SNARE SYP2 proteins localized to different subcellular regions function redundantly in vacuolar protein sorting and plant development. Plant J 64(6):924–935. doi: 10.1111/j.1365-313X.2010.04394.x PubMedCrossRefGoogle Scholar
  64. Silva PA, Ul-Rehman R, Rato C, Di Sansebastiano GP, Malho R (2010) Asymmetric localization of Arabidopsis SYP124 syntaxin at the pollen tube apical and sub-apical zones is involved in tip growth. BMC Plant Biol 10:179. doi: 10.1186/1471-2229-10-179 PubMedCrossRefGoogle Scholar
  65. Sohn EJ, Kim ES, Zhao M, Kim SJ, Kim H, Kim YW, Lee YJ, Hillmer S, Sohn U, Jiang L, Hwang I (2003) Rha1, an Arabidopsis Rab5 homolog, plays a critical role in the vacuolar trafficking of soluble cargo proteins. Plant Cell 15(5):1057–1070PubMedCrossRefGoogle Scholar
  66. Somsel Rodman J, Wandinger-Ness A (2000) Rab GTPases coordinate endocytosis. J Cell Sci 113(Pt 2):183–192PubMedGoogle Scholar
  67. Surpin M, Zheng H, Morita MT, Saito C, Avila E, Blakeslee JJ, Bandyopadhyay A, Kovaleva V, Carter D, Murphy A, Tasaka M, Raikhel N (2003) The VTI family of SNARE proteins is necessary for plant viability and mediates different protein transport pathways. Plant Cell 15(12):2885–2899. doi: 10.1105/tpc.016121 PubMedCrossRefGoogle Scholar
  68. Sutter JU, Campanoni P, Tyrrell M, Blatt MR (2006) Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell 18(4):935–954. doi: 10.1105/tpc.105.038950 PubMedCrossRefGoogle Scholar
  69. Szumlanski AL, Nielsen E (2009) The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell 21(2):526–544. doi: 10.1105/tpc.108.060277 PubMedCrossRefGoogle Scholar
  70. Takáč T, Pechan T, Richter H, Muller J, Eck C, Bohm N, Obert B, Ren H, Niehaus K, Šamaj J (2011) Proteomics on brefeldin A-treated Arabidopsis roots reveals profilin 2 as a new protein involved in the cross-talk between vesicular trafficking and the actin cytoskeleton. J Proteome Res 10(2):488–501. doi: 10.1021/pr100690f PubMedCrossRefGoogle Scholar
  71. Takáč T, Pechan T, Šamajová O, Ovečka M, Richter H, Eck C, Niehaus K, Šamaj J (2012) Wortmannin treatment induces changes in Arabidopsis root proteome and post-Golgi compartments. J Proteome Res. doi: 10.1021/pr201111n PubMedGoogle Scholar
  72. Takano J, Miwa K, Yuan L, von Wiren N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Nat Acad Sci U S A 102(34):12276–12281CrossRefGoogle Scholar
  73. Touihri S, Knoll C, Stierhof YD, Muller I, Mayer U, Jurgens G (2011) Functional anatomy of the Arabidopsis cytokinesis-specific syntaxin KNOLLE. Plant J 68(5):755–764. doi: 10.1111/j.1365-313X.2011.04736.x PubMedCrossRefGoogle Scholar
  74. Ueda H, Nishiyama C, Shimada T, Koumoto Y, Hayashi Y, Kondo M, Takahashi T, Ohtomo I, Nishimura M, Hara-Nishimura I (2006) AtVAM3 is required for normal specification of idioblasts, myrosin cells. Plant Cell Physiol 47(1):164–175PubMedCrossRefGoogle Scholar
  75. Ueda T, Anai T, Tsukaya H, Hirata A, Uchimiya H (1996) Characterization and subcellular localization of a small GTP-binding protein (Ara-4) from Arabidopsis: conditional expression under control of the promoter of the gene for heat-shock protein HSP81-1. Mol Gen Genet 250(5):533–539PubMedGoogle Scholar
  76. Ueda T, Uemura T, Sato MH, Nakano A (2004) Functional differentiation of endosomes in Arabidopsis cells. Plant J 40(5):783–789. doi: 10.1111/j.1365-313X.2004.02249.x PubMedCrossRefGoogle Scholar
  77. Ueda T, Yamaguchi M, Uchimiya H, Nakano A (2001) Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J 20(17):4730–4741PubMedCrossRefGoogle Scholar
  78. Uemura T, Kim H, Saito C, Ebine K, Ueda T, Schulze-Lefert P, Nakano A (2012) Qa-SNAREs localized to the trans-Golgi network regulate multiple transport pathways and extracellular disease resistance in plants. Proc Nat Acad Sci U S A 109(5):1784–1789. doi: 10.1073/pnas.1115146109 CrossRefGoogle Scholar
  79. Uemura T, Morita MT, Ebine K, Okatani Y, Yano D, Saito C, Ueda T, Nakano A (2010) Vacuolar/pre-vacuolar compartment Qa-SNAREs VAM3/SYP22 and PEP12/SYP21 have interchangeable functions in Arabidopsis. Plant J 64(5):864–873. doi: 10.1111/j.1365-313X.2010.04372.x PubMedCrossRefGoogle Scholar
  80. Ul-Rehman R, Silva PA, Malho R (2011) Localization of Arabidopsis SYP125 syntaxin in the plasma membrane sub-apical and distal zones of growing pollen tubes. Plant Sign Behav 6(5):665–670CrossRefGoogle Scholar
  81. Vedovato M, Rossi V, Dacks JB, Filippini F (2009) Comparative analysis of plant genomes allows the definition of the “Phytolongins”: a novel non-SNARE longin domain protein family. BMC Genomics 10:510. doi: 10.1186/1471-2164-10-510 PubMedCrossRefGoogle Scholar
  82. Vernoud V, Horton AC, Yang Z, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 131(3):1191–1208. doi: 10.1104/pp.013052 PubMedCrossRefGoogle Scholar
  83. Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M, van den Berg W, van Dongen W, Richter S, Geldner N, Takano J, Jurgens G, de Vries SC, Robinson DG, Schumacher K (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22(4):1344–1357. doi: 10.1105/tpc.109.072637 PubMedCrossRefGoogle Scholar
  84. Volker A, Stierhof YD, Jurgens G (2001) Cell cycle-independent expression of the Arabidopsis cytokinesis-specific syntaxin KNOLLE results in mistargeting to the plasma membrane and is not sufficient for cytokinesis. J Cell Sci 114(Pt 16):3001–3012PubMedGoogle Scholar
  85. Wang T, Ming Z, Xiaochun W, Hong W (2011) Rab7: role of its protein interaction cascades in endo-lysosomal traffic. Cell Signal 23(3):516–521. doi: 10.1016/j.cellsig.2010.09.012 PubMedCrossRefGoogle Scholar
  86. Warren G, Mellman I (2006) Protein trafficking between membranes. In: Lewin B (ed) Cell, 1st edn. Jones & Bartlett Pub, Sudbury, pp 153–204Google Scholar
  87. Wickner W, Schekman R (2008) Membrane fusion. Nat Struct Mol Biol 15(7):658–664PubMedCrossRefGoogle Scholar
  88. Woollard AA, Moore I (2008) The functions of Rab GTPases in plant membrane traffic. Curr Opin Plant Biol 11(6):610–619. doi: 10.1016/j.pbi.2008.09.010 PubMedCrossRefGoogle Scholar
  89. Yano D, Sato M, Saito C, Sato MH, Morita MT, Tasaka M (2003) A SNARE complex containing SGR3/AtVAM3 and ZIG/VTI11 in gravity-sensing cells is important for Arabidopsis shoot gravitropism. Proc Nat Acad Sci U S A 100(14):8589–8594. doi: 10.1073/pnas.1430749100 CrossRefGoogle Scholar
  90. Zainal Z, Tucker GA, Lycett GW (1996) A rab11-like gene is developmentally regulated in ripening mango (Mangifera indica L.) fruit. Biochim Biophys Acta 1314(3):187–190PubMedCrossRefGoogle Scholar
  91. Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149(2):916–928PubMedCrossRefGoogle Scholar
  92. Zhang L, Zhang H, Liu P, Hao H, Jin JB, Lin J (2011) Arabidopsis R-SNARE proteins VAMP721 and VAMP722 are required for cell plate formation. PLoS One 6(10):e26129. doi: 10.1371/journal.pone.0026129 PubMedCrossRefGoogle Scholar
  93. Zhu J, Gong Z, Zhang C, Song CP, Damsz B, Inan G, Koiwa H, Zhu JK, Hasegawa PM, Bressan RA (2002) OSM1/SYP61: a syntaxin protein in Arabidopsis controls abscisic acid-mediated and non-abscisic acid-mediated responses to abiotic stress. Plant Cell 14(12):3009–3028PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Biological Sciences, Graduate School of SciencesUniversity of TokyoBunkyo-ku TokyoJapan
  2. 2.Japan Science and Technology Agency (JST), PRESTOSaitamaJapan
  3. 3.Graduate School of Life and Environmental SciencesKyoto Prefectural UniversitySakyo-ku, KyotoJapan

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