Molecular and biochemical analysis of the first ARA6 homologue, a RAB5 GTPase, from green algae

Journal of Experimental Botany

Volumn 64, Issue 18, 2013, Pages 5553-5568

  Hoepflinger, Marion C ^a   Geretschlaeger, Anja ^a   Sommer, Aniela ^a   Hoeftberger, Margit ^a   Nishiyama, Tomoaki ^b   Sakayama, Hidetoshi ^c   Hammerl, Peter ^a   Tenhaken, Raimund ^a   Ueda, Takashi ^d   Foissner, Ilse ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

^b KANAZAWA UNIVERSITY   (Japan)

^c KOBE UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

ARA6; Chara australis; endosomal trafficking; multivesicular endosome; plant specific RAB5 GTPase; plasma membrane; trans Golgi network

Indexed keywords

ARA6 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; RAB PROTEIN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARA6; ARTICLE; CELL MEMBRANE; CHARA; CHARA AUSTRALIS; ENDOSOMAL TRAFFICKING; ENDOSOME; ENZYMOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MOUSE; MULTIVESICULAR BODY; MULTIVESICULAR ENDOSOME; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT EPIDERMIS; PLANT LEAF; PLANT-SPECIFIC RAB5 GTPASE; POINT MUTATION; SEQUENCE HOMOLOGY; TOBACCO; TRANS-GOLGI NETWORK.; TRANSGENIC PLANT;

ARA6; CHARA AUSTRALIS; ENDOSOMAL TRAFFICKING; MULTIVESICULAR ENDOSOME; PLANT-SPECIFIC RAB5 GTPASE; PLASMA MEMBRANE; TRANS-GOLGI NETWORK.;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS PROTEINS; CELL MEMBRANE; CHARA; ENDOSOMES; MICE; MOLECULAR SEQUENCE DATA; MULTIVESICULAR BODIES; PHYLOGENY; PLANT EPIDERMIS; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POINT MUTATION; RAB GTP-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TOBACCO;

EID: 84891543722     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert322     Document Type: Article

References (71)

1. Altschul S, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research 25, 3389-3402
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215, 403-410
3. Aniento F, Robinson DG. 2005. Testing for endocytosis in plants. Protoplasma 226, 3-11
4. Banks JA, Nishiyama T, Hasebe M, et al. 2011. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332, 960-963
5. Bolte S, Brown S, Satiat-Jeunemaitre B. 2004. The N-myristoylated RAB-GTPase m-RAB(mc) is involved in post-Golgi trafficking events to the lytic vacuole in plant cells. Journal of Cell Science 117, 943-954
6. Bolte S, Schiene K, Dietz K-J. 2000. Characterization of a small GTP-binding protein of the RAB5 family in Mesembryanthemum crystallinum with increased level of expression during early salt stress. Plant Molecular Biology 42, 923-935
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, 3007-3025
8. Braun M, Foissner I, Lühring H, Schubert H, Thiel G. 2007. Characean algae: Still a valid model system to examine fundamental principles in plants. Progress in Botany 68, 193-220
9. Casanova MT. 2005. An overview of Chara L. in Australia (Characeae, Charophyta). Australian Systematic Botany 18, 25-39
10. Chau R, Bisson MA, Siegel A, Elkin G, Klim P, Straubinger RM. 1994. Distribution of charasomes in Chara-reestablishment and loss in darkness and correlation with banding and inorganic carbon uptake. Australian Journal of Plant Physiology 21, 113-123
11. Contento AL, Bassham DC. 2012. Structure and function of endosomes in plant cells. Journal of Cell Science 125, 3511-3518
12. Curtis M, Grossniklaus U. 2003. A gateway cloning vector set for high-Throughput functional analysis of genes in planta. Plant Physiology 133, 462-469
13. Derrien B, Baumberger N, Schepetilnikov M, Viotti C, De Cillia J, Ziegler-Graff V, Isono E, Schumacher K, Genschik P. 2012. Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proceedings of the National Academy of Sciences, USA 109, 15942-15946
14. Dhonukshe P, Baluska F, Schlicht M, Hlavacka A, Samaj J, Friml J, Gadella TWJ. 2006. Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Developmental Cell 10, 137-150
15. Ebine K, Fujimoto M, Okatani Y, et al. 2011. A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nature Cell Biology 13, 853-859
16. Ebine K, Miyakawa N, Fujimoto M, Uemura T, Nakano A, Ueda T. 2012. Endosomal trafficking pathway regulated by ARA6, a RAB5 GTPase unique to plants. Small GTPases 3, 23-27
17. Ebine K, Ueda T. 2009. Unique mechanism of plant endocytic/ vacuolar transport pathways. Journal of Plant Research 122, 21-30
18. Felsenstein J. 1985. Confidence limits on phylogenies-An approach using the bootstrap. Evolution 39, 783-791
19. Felsenstein J. 2005. PHYLIP (Phylogeny Inference Package) version 3.65. Department of Genome Sciences, University of Washington, Seattle, WA, USA
20. Finet C, Timme RE, Delwiche CF, Marletaz F. 2010. Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Current Biology 20, 2217-2222
21. Foissner I, Wasteneys GO. 2012. The characean internodal cell as a model system for studying wound healing. Journal of Microscopy 247, 10-22
22. Foresti O, Denecke J. 2008. Intermediate organelles of the plant secretory pathway: Identity and function. Traffic 9, 1599-1612
23. Fukuda M, Wen L, Satoh-Cruz M, et al. 2013. A guanine nucleotide exchange factor for Rab5 proteins is essential for intracellular transport of the proglutelin from the Golgi apparatus to the protein storage vacuole in rice endosperm. Plant Physiology 162, 663-674
24. Goh T, Uchida W, Arakawa S, Ito E, Dainobu T, Ebine K, Takeuchi M, Sato K, Ueda T, Nakano A. 2007. VPS9a, the common activator for two distinct types of RAB5 GTPases, is essential for the development of Arabidopsis thaliana. Plant Cell 19, 3504-3515
25. Graham LE, Cook ME, Busse JS. 2000. The origin of plants: Body plan changes contributing to a major evolutionary radiation. Proceedings of the National Academy of Sciences, USA 97, 4535-4540
26. Grebe M, Xu J, Mobius W, Ueda T, Nakano A, Geuze HJ, Rook MB, Scheres B. 2003. Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Current Biology 13, 1378-1387
27. Gunning BES, Pate JS. 1969. Transfer cells. Plant cells with wall ingrowths, specialized in relation to short distance transport of solutes-Their occurrence, structure, and development. Protoplasma 68, 107-133
28. 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 LYSTINTERACTING PROTEIN5. Plant Cell 19, 1295-1312
29. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences 8, 275-282
30. Karol KG, McCourt RM, Cimino MT, Delwiche CF. 2001. The closest living relatives of land plants. Science 294, 2351-2353
31. Kato S, Sakayama H, Morishima H, Sano S, Oomori Y, Kato N. 2010. Morphology and molecular phylogeny of Chara altaica (Charales, Charophyceae), a monoecious species of the section Desvauxia. Cytologia 75, 211-220
32. Katoh K, Kuma K-i, Toh H, Miyata T. 2005. MAFFT version 5: Improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511-518
33. Klima A, Foissner I. 2008. FM dyes label sterol-rich plasma membrane domains and are internalized independently of the cytoskeleton in characean internodal cells. Plant and Cell Physiology 49, 1508-1521
34. Klima A, Foissner I. 2011. Actin-dependent deposition of putative endosomes and endoplasmic reticulum during early stages of wound healing in characean internodal cells. Plant Biology 13, 590-601
35. Kotzer AM, Brandizzi F, Neumann U, Paris N, Moore I, Hawes C. 2004. AtRABF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells. Journal of Cell Science 117, 6377-6389
36. Laurin-Lemay S, Brinkmann H, Philippe H. 2012. Origin of land plants revisited in the light of sequence contamination and missing data. Current Biology 22, R593-R594
37. Littlejohn GR, Gouveia JD, Edner C, Smirnoff N, Love J. 2010. Perfluorodecalin enhances in vivo confocal microscopy resolution of Arabidopsis thaliana mesophyll. New Phytologist 186, 1018-1025
38. Lucas WJ, Franceschi VR. 1981. Characean charasome-complex and plasmalemma vesicle development. Protoplasma 107, 255-267
39. Maddison D, Maddison W. 2000. MacClade 4: Analysis of phylogeny and character evolution. Massachusetts: Sinauer Associates, Inc
40. Mattox KR, Stewart KD. 1984. Classification of the green algae: A concept based on comparative cytology. In: Irvine DEG, John DM, eds. Systematics of the green algae. London: Academic Press, 29-120
41. McCourt RM, Delwiche CF, Karol KG. 2004. Charophyte algae and land plant origins. Trends in Ecology and Evolution 19, 661-666
42. Meckel T, Hurst AC, Thiel G, Homann U. 2004. Endocytosis against high turgor: Intact guard cells of Vicia faba constitutively endocytose fluorescently labelled plasma membrane and GFP-Tagged K+-channel KAT1. The Plant Journal 39, 182-193
43. Murphy AS, Bandyopadhyay A, Holstein SE, Peer WA. 2005. Endocytotic cycling of plasma membrane proteins. Annual Review of Plant Biology 56, 221-251
44. Nelson BK, Cai X, Nebenfuhr A. 2007. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. The Plant Journal 51, 1126-1136
45. Nishiyama T. 2007. Evolutionary developmental biology of nonflowering land plants. International Journal of Plant Sciences 168, 37-47
46. Norris SR, Meyer SE, Callis J. 1993. The intron of Arabidopsis thaliana polyubiquitin genes is conserved in location and is a quantitative determinant of chimeric gene expression. Plant Molecular Biology 21, 895-906
47. Offler CE, McCurdy DW, Patrick JW, Talbot MJ. 2003. Transfer cells: Cells specialized for a special purpose. Annual Review of Plant Biology 54, 431-454
48. Park M, Jürgens G. 2012. Membrane traffic and fusion at post-Golgi compartments. Frontiers in Plant Science 2, article 111
49. Reyes FC, Buono R, Otegui MS. 2011. Plant endosomal trafficking pathways. Current Opinion in Plant Biology 14, 666-673
50. Richter S, Voss U, Jürgens G. 2009. Post-Golgi traffic in plants. Traffic 10, 819-828
51. Roberts RL, Barbieri MA, Pryse KM, Chua M, Morisaki JH, Stahl PD. 1999. Endosome fusion in living cells overexpressing GFP-RAB5. Journal of Cell Science 112, 3667-3675
52. Saito C, Ueda T. 2009. Functions of RAB and SNARE Proteins in Plant Life. In: Kwang WJ, ed. International Review of Cell and Molecular Biology , Vol. 274. Academic Press, 183-233
53. Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406-425
54. Sakayama H, Kasai F, Nozaki H, Watanabe MM, Kawachi M, Shigyo M, Nishihiro J, Washitani I, Krienitz L, Ito, Motomi. 2009. Taxonomic reexamination of Chara globularis (Charales, Charophyceae) from Japan based on oospore morphology and rbcL gene sequences, and the description of C. leptospora sp. nov. Journal of Phycology 45, 917-927
55. Scheuring D, Viotti C, Krüger F, Künzl F, Sturm S, Bubeck J, Hillmer S, Frigerio L, Robinson DG, Pimpl P, Schumacher K. 2011. Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23, 3463-3481
56. Schmölzer PM, Höftberger M, Foissner I. 2011. Plasma membrane domains participate in pH banding of Chara internodal cells. Plant and Cell Physiology 52, 1274-1288
57. Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A. 2007. RAB GTPases at a glance. Journal of Cell Science 120, 3905-3910
58. Sohn EJ, Kim ES, Zhao M, Kim SJ, Kim H, Kim Y-W, 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, 1057-1070
59. Stenmark H, Parton RG, Steele-Mortimer O, Lütcke A, Gruenberg J, Zerial M. 1994. Inhibition of RAB5 GTPase activity stimulates membrane fusion in endocytosis. EMBO Journal 14, 1287-1296
60. Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani M, Henschel K, Münster T, Theissen G, Nozaki H, Ito M. 2005. Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proceedings of the National Academy of Sciences, USA 102, 2436-2441
61. Tazawa M, Shimmen T. 2001. How characean cells have contributed to the progress of plant membrane biophysics. Australian Journal of Plant Physiology 28, 523-539
62. Timme RE, Bachvaroff TR, Delwiche CF. 2012. Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE 7, e29696
63. Turmel M, Pombert JF, Charlebois P, Otis C, Lemieux C. 2007. The green algal ancestry of land plants as revealed by the chloroplast genome. International Journal of Plant Sciences 168, 679-689
64. Ueda T, Uemura T, Sato MH, Nakano A. 2004. Functional differentiation of endosomes in Arabidopsis cells. The Plant Journal 40, 783-789
65. 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 Journal 20, 4730-4741
66. Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH. 2004. Systematic analysis of SNARE molecules in Arabidopsis: Dissection of the post-Golgi network in plant cells. Cell Structure and Function 29, 49-65
67. Viotti C, Bubeck J, Stierhof YD, 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
68. Wang JQ, Cai Y, Miao YS, Lam SK, Jiang LW. 2009. Wortmannin induces homotypic fusion of plant prevacuolar compartments. Journal of Experimental Botany 60, 3075-3083
69. Weigel D, Glazebrook J. 2002. Arabidopsis: A laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press
70. Wodniok S, Brinkmann H, Glockner G, Heidel A, Philippe H, Melkonian M, Becker B. 2011. Origin of land plants: Do conjugating green algae hold the key? BMC Evolutionary Biology 11, 104
71. Wood RD, Imahori K. 1965. A revision of the Characeae, Vol. I. Monograph of the Characeae. Weinheim: J. Cramer, i-xxiv, 1-904