Mechanisms of Functional Specificity Among Plasma-Membrane Syntaxins in Arabidopsis

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Volumn 12, Issue 9, 2011, Pages 1269-1280

  Reichardt, Ilka ^a,b   Slane, Daniel ^a   El Kasmi, Farid ^a   Knöll, Christian ^a   Fuchs, Rene ^c,d   Mayer, Ulrike ^a   Lipka, Volker ^c,d   Jürgens, Gerd ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^c SAINSBURY LABORATORY   (United Kingdom)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Arabidopsis; Cell cycle; Cytokinesis; Innate immunity; Plasma membrane; Protein dynamics; Recycling; Syntaxin

Indexed keywords

KNOLLE PROTEIN; PEN1 PROTEIN; SYNTAXIN; SYP132 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARABIDOPSIS; ARTICLE; CELL MEMBRANE; CHIMERA; ENDOCYTOSIS; MEMBRANE FUSION; NONHUMAN; PLANT IMMUNITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCOMYCOTA; CELL MEMBRANE; ENDOSOMES; MEMBRANE FUSION; PLANTS, GENETICALLY MODIFIED; QA-SNARE PROTEINS; RECOMBINANT FUSION PROTEINS; SNARE PROTEINS;

EID: 80051669181     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01222.x     Document Type: Article

References (52)

1. Jahn R, Scheller RH. SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 2006;7:631-643.
2. Fasshauer D, Sutton RB, Brunger AT, Jahn R. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci U S A 1998;95:15781-15786.
3. Dacks JB, Doolittle WF. Novel syntaxin gene sequences from Giardia, Trypanosoma and algae: implications for the ancient evolution of the eukaryotic endomembrane system. J Cell Sci 2002;115: 1635-1642.
4. Bock JB, Matern HT, Peden AA, Scheller RH. A genomic perspective on membrane compartment organization. Nature 2001;409:839-841.
5. Lipka V, Kwon C, Panstruga R. SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu Rev Cell Dev Biol 2007;23:147-174.
6. Sanderfoot A. Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol 2007;144:6-17.
7. 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;29:49-65.
8. Enami K, Ichikawa M, Uemura T, Kutsuna N, Hasezawa S, Nakagawa T, Nakano A, Sato MH. Differential expression control and polarized distribution of plasma membrane-resident SYP1 SNAREs in Arabidopsis thaliana. Plant Cell Phys 2009;50:280-289.
9. Lukowitz W, Mayer U, Jürgens G. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 1996;84:61-71.
10. Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U, Hwang I, Lukowitz W, Jürgens G. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J Cell Biol 1997;139:1485-1493.
11. Leyman B, Geelen D, Quintero FJ, Blatt MR. A tobacco syntaxin with a role in hormonal control of guard cell ion channels. Science 1999;283:537-540.
12. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P. SNARE-protein mediated disease resistance at the plant cell wall. Nature 2003;425:973-977.
13. Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, El Kasmi F, Jürgens G, Parker J, Panstruga R, Lipka V, et al. Co-option of a default secretory pathway for plant immune responses. Nature 2008;451:835-840.
14. Grefen C, Donald N, Hashimoto K, Kudla J, Schumacher K, Blatt MR. A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J 2010;64:355-365.
15. Haga N, Kato K, Murase M, Araki S, Kubo M, Demura T, Suzuki K, Müller I, Voss U, Jürgens G, Ito M. R1R2R3-Myb proteins positively regulate cytokinesis through activation of KNOLLE transcription in Arabidopsis thaliana. Development 2007;134:1101-1110.
16. Reichardt I, Stierhof YD, Mayer U, Richter S, Schwarz H, Schumacher K, Jürgens G. Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr Biol 2007;17:2047-2053.
17. Sutter JU, Campanoni P, Tyrrell M, Blatt MR. Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell 2006;18:935-954.
18. Honsbein A, Sokolovski S, Grefen C, Campanoni P, Pratelli R, Paneque M, Chen Z, Johansson I, Blatt MR. A tripartite SNARE-K+ channel complex mediates in channel-dependent K+ nutrition in Arabidopsis. Plant Cell 2009;21:2859-2877.
19. Pajonk S, Kwon C, Clemens N, Panstruga R, Schulze-Lefert P. Activity determinents and functional specialisation of Arabidopsis PEN1 syntaxin in innate immunity. J Biol Chem 2008;283:26974-26984.
20. Kalde M, Nühse TS, Findlay K, Peck SC. The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc Natl Acad Sci U S A 2007;104:11850-11855.
21. 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;225:541-550.
22. Müller I, Wagner W, Völker A, Schellmann S, Nacry P, Küttner F, Schwarz-Sommer Z, Mayer U, Jürgens G. Syntaxin specificity of cytokinesis in Arabidopsis. Nat Cell Biol 2003;5:531-534.
23. Stierhof YD, El Kasmi F. Strategies to improve the antigenicity, ultrastructure preservation and visibility of trafficking compartments in Arabidopsis tissue. Eur J Cell Biol 2010;89:285-297.
24. 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;15:5118-5129.
25. Norris SR, Meyer SE, Callis J. The intron of Arabidopsis thaliana polyubiquitin genes is conserved in location and is a quantitative determinant of chimeric gene expression. Plant Mol Biol 1993;21: 895-906.
26. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 2005;310:1180-1183.
27. Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R. Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Natl Acad Sci U S A 2005;102:3135-3140.
28. Ritzenthaler C, Nebenführ 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;14:237-261.
29. Grebe M, Xu J, Möbius W, Ueda T, Nakano A, Geuze HJ, Rook MB, Scheres B. Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr Biol 2003;13:1378-1387.
30. +-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 2006;18:715-730.
31. Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M, van den Berg W, van Dongen W, Richter S, Geldner N, Takano J, Jürgens G, de Vries SC, Robinson DG, Schumacher K. Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 2010;22:1344-1357.
32. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 2003;112:219-230.
33. Cherfils J, Melancon P. On the action of Brefeldin A on Sec7-stimulated membrane-recruitment and GDP/GTP exchange of Arf proteins. Biochem Soc Trans 2005;33:635-638.
34. Teh OK, Moore I. An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 2007;448:493-496.
35. Richter S, Geldner N, Schrader J, Wolters H, Stierhof YD, Rios G, Koncz C, Robinson DG, Jürgens G. Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 2007;448:488-492.
36. Robinson DG, Jiang L, Schumacher K. The endosomal system of plants: charting new and familiar territories. Plant Physiol 2008;147:1482-1492.
37. Reichheld JP, Sonobe S, Clément B, Chaubet N, Gigot C. Cell cycle-regulated histone gene expression in synchronized plant cells. Plant J 1995;7:245-252.
38. Shaul O, Mironov V, Burssens S, Van Montagu M, Inze D. Two Arabidopsis cyclin promoters mediate distinctive transcriptional oscillation in synchronized tobacco BY-2 cells. Proc Natl Acad Sci U S A 1996;93:4868-4872.
39. Bennett MK, García-Arrarás JE, Elferink LA, Peterson K, Fleming AM, Hazuka CD, Scheller RH. The syntaxin family of vesicular transport receptors. Cell 1993;74:863-873.
40. Protopopov V, Govindan B, Novick P, Gerst JE. Homologs of the synaptobrevin/VAMP family of synaptic vesicle proteins function on the late secretory pathway in S. cerevisiae. Cell 1993;74:855-861.
41. Pevsner J, Hsu SC, Braun JE, Calakos N, Ting AE, Bennett MK, Scheller RH. Specificity and regulation of a synaptic vesicle docking complex. Neuron 1994;13:353-361.
42. Søgaard M, Tani K, Ye RR, Geromanos S, Tempst P, Kirchhausen T, Rothman JE, Söllner T. A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles. Cell 1994;78:937-948.
43. McNew JA, Parlati F, Fukuda R, Johnston RJ, Paz K, Paumet F, Sollner TH, Rothman JE. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 2000;407:153-159.
44. Heese M, Gansel X, Sticher L, Wick P, Grebe M, Granier F, Jürgens G. Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J Cell Biol 2001;155:239-249.
45. Völker A, Stierhof YD, Jürgens G. 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 2001;114:3001-3012.
46. Men S, Boutté 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;10:237-244.
47. Dhonukshe P, Tanaka H, Goh T, Ebine K, Mähönen AP, Prasad K, Blilou I, Geldner N, Xu J, Uemura T, Chory J, Ueda T, Nakano A, Scheres B, Friml J. Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 2008;456:962-966.
48. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998;16: 735-743.
49. Grebe M, Gadea J, Steinmann T, Kientz M, Rahfeld JU, Salchert K, Koncz C, Jürgens G. A conserved domain of the Arabidopsis GNOM protein mediates subunit interaction and cyclophilin 5 binding. Plant Cell 2000;12:343-356.
50. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1998.
51. Chomczynski P. Reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 1993;15:532-534, 536, 537.
52. Pimpl P, Movafeghi A, Coughlan S, Denecke J, Hillmer S, Robinson DG. In situ localization and in vitro induction of plant COPI-coated vesicles. Plant Cell 2000;12:2219-2236.