SNARE VTI13 plays a unique role in endosomal trafficking pathways associated with the vacuole and is essential for cell wall organization and root hair growth in arabidopsis

Annals of Botany

Volumn 114, Issue 6, 2014, Pages 1147-1159

  Larson, Emily R ^a,c   Domozych, David S ^b   Tierney, Mary L ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b SKIDMORE COLLEGE   (United States)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Arabidopsis thaliana; early endosomes; endosomal trafficking pathway; membrane transport; plant cell wall; root hairs; SNARE proteins; tip growth; trans Golgi; vacuole; vesicle trafficking

Indexed keywords

CELL ORGANELLE; DICOTYLEDON; FUNCTIONAL ROLE; GENE EXPRESSION; GROWTH REGULATOR; MEMBRANE; PHYTOCHEMISTRY; ROOT SYSTEM; TRANSGENIC PLANT; TRICHOME;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; GREEN FLUORESCENT PROTEIN; SNARE PROTEIN; VTI13 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; CELL MEMBRANE; CELL VACUOLE; CELL WALL; ENDOSOME; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MULTIVESICULAR BODY; PHENOTYPE; PLANT ROOT; TRANS GOLGI NETWORK; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELL WALL; ENDOSOMES; GREEN FLUORESCENT PROTEINS; MULTIVESICULAR BODIES; PHENOTYPE; PLANT ROOTS; SNARE PROTEINS; TRANS-GOLGI NETWORK; VACUOLES;

EID: 84907948296     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcu041     Document Type: Article

References (59)

1. Assaad FF, Qiu J-L, Youngs H, et al. 2004. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Molecular Biology of the Cell 15: 5118-5129.
2. Atmodjo MA, Sakuragi Y, Zhu X, et al. 2011. Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex. Proceedings of the National Academy Sciences of the USA 108: 20225-20230.
3. Baluska F, Hlavacka A, Samaj J, et al. 2002. F-actin-dependent endocytosis of cell wall pectins in meristematic root cells. insights from brefeldin A-induced compartments. Plant Physiology 130: 422-431.
4. Barberon M, Zelazny E, Robert S, et al. 2011. Monoubiquitin-dependent endo-cytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proceedings of the National Academy Sciences of the USA 108: E450-458.
5. Bassham DC, Sanderfoot AA, Kovaleva V, Zheng H, Raikhel NV 2000. At VPS45 complex formation at the trans-Golgi network. Molecular Biology of the Cell 11: 2251-2265.
6. Bechtold N, Pelletier G1998. Inplanta Agrobacterium-mediatedtransformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods in Molecular Biology 82: 259-266.
7. Bernhardt C, Tierney ML 2000. Expression of At PRP3, a proline-rich structural cell wall protein from Arabidopsis, is regulated by cell-type-specific developmental pathways involved in root hair formation. Plant Physiology 122: 705-714.
8. Campàs O, Mahadevan L 2009. Shape and dynamics of tip-growing cells. Current Biology 19: 2102-2107.
9. Cárdenas L 2009. New findings in the mechanisms regulating polar growth in root hair cells. Plant Signaling and Behavior 4: 4-8.
10. De Caroli M, Lenucci MS, Di Sansebastiano G-P, Dalessandro G, De Lorenzo G, Piro G 2011. Protein trafficking to the cell wall occurs through mechanisms distinguishable from default sorting in tobacco. Plant Journal 65: 295-308.
11. Dettmer J, Hong-Hermesdorf A, Stierhof Y-D, Schumacher K 2006. Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730.
12. Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD 2002. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. Journal of Biological Chemistry 277: 33105-33114.
13. Drakakaki G, vandeVen W, Pan S, et al. 2011. Isolation andproteomicanalysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Research 22: 413-424.
14. Earley KW, Haag JR, Pontes O, et al. 2006. Gateway-compatible vectors for plant functional genomics and proteomics. Plant Journal 45: 616-629.
15. Fischer von Mollard G, Stevens TH 1999. The Saccharomyces cerevisiae v-SNARE Vti1p is required for multiple membrane transport pathways to the vacuole. Molecular Biology of the Cell 10: 1719-1732.
16. Fischer-Parton S, Parton RM, Hickey PC, Dijksterhuis J, Atkinson HA, Read ND 2000. Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. Journal of Microscopy 198: 246-259.
17. Geldner N, Anders N, Wolters H, et al. 2003. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin dependent growth. Cell 112: 219-230.
18. Grebe M, Xu J, Mobius W, et al. 2003. Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Current Biology 13: 1378-1387.
19. Grefen C, Blatt MR2008. SNAREs-molecular governorsinsignalling andde-velopment. Current Opinion in Plant Biology 11: 600-609.
20. Guo F, McCubbin AG 2012. The pollen-specific R-SNARE/longin Pi VAMP726 mediates fusion of endo-and exocytic compartments in pollen tube tip growth. Journal of Experimental Botany 63: 3083-3095.
21. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AMC, Ehrhardt DW2009. Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nature Cell Biology 11: 797-806.
22. Hanaoka H, Noda T, Shirano Y, et al. 2002. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiology 129: 1181-1193.
23. Heese M, Gansel X, Sticher L, et al. 2001. Functional characterization of the KNOLLE-interacting t-SNAREAt SNAP33 anditsroleinplantcytokinesis. Journal of Cell Biology 155: 239-250.
24. Hicks GR, Raikhel N 2010. Advances in dissecting endomembrane trafficking with small molecules. Current Opinion in Plant Biology 13: 706-713.
25. Kato T, Morita MT, Fukaki H, et al. 2002. SGR2, aphospholipase-like protein, and ZIG/SGR4, a SNARE, are involved in the shoot gravitropism of Arabidopsis. Plant Cell 14: 33-46.
26. Ketelaar T, Galway ME, Mulder BM, Emons AMC2008. Ratesofexocytosis and endocytosis in Arabidopsis root hairs and pollen tubes. Journal of Microscopy 231: 265-273.
27. Kim S-J, Bassham DC 2011. TNO1 is involved in salt tolerance and vacuolar trafficking in Arabidopsis. Plant Physiology 156: 514-526.
28. Kroeger JH, Zerzour R, Geitmann A2011. Regulatorordrivingforce? Therole of turgor pressure in oscillatory plant cell growth. PLoS One 6: e18549.
29. Lam SK, Cai Y, Tse YC, et al. 2009. BFA-inducedcompartments from theGolgi apparatus and trans-Golgi network/early endosome are distinct in plant cells. Plant Journal 60: 865-881.
30. Langhans M, Förster S, Helmchen G, Robinson DG 2011. Differential effects of the brefeldin A analogue (6R)-hydroxy-BFA in tobacco and Arabidopsis. Journal of Experimental Botany 62: 2949-2957.
31. Lew RR 1996. Pressure regulation of the electrical properties of growing Arabidopsis thaliana L. root hairs. Plant Physiology 112: 1089-1100.
32. Lukowitz W, Mayer U, JürgensG1996. Cytokinesisinthe Arabidopsisembryo involves the syntaxin-related KNOLLE gene product. Cell 84: 61-71.
33. Marcus SE, Verhertbruggen Y, Hervé C, et al. 2008. Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biology 8: 60.
34. Messerli MA, Danuser G, Robinson KR 1999. Pulsatile influxes of H+, K+ and Ca2+ lag growth pulses of Lilium longiflorum pollen tubes. Journal of Cell Science 112: 1497-1509.
35. Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S 2007. Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proceedings of the National Academy of Sciences of the USA 104: 20996-21001.
36. Monshausen GB, Messerli MA, Gilroy S 2008. Imaging of the Yellow Cameleon 3. 6 indicator revealsthat elevationsincytosolic Ca2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiology 147: 1690-1698.
37. Müller O, Sattler T, Flötenmeyer M, Schwarz H, Plattner H, Mayer A 2000. Autophagic tubes: vacuolar invaginations involved in lateral membrane sorting and inverse vesicle budding. Journalof Cell Biology 151: 519-528.
38. Nelson BK, Cai X, Nebenführ A 2007. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant Journal 51: 1126-1136.
39. Niihama M, Uemura T, Saito C, et al. 2005. Conversionoffunctionalspecificity in Qb-SNARE VTI1 homologues of Arabidopsis. Current Biology 15: 555-560.
40. Niihama M, Takemoto N, Hashiguchi Y, Tasaka M, Morita MT 2009. ZIP genes encode proteins involved in membrane trafficking of the TGN-PVC/vacuoles. Plant and Cell Physiology 50: 2057-2068.
41. Park S, Szumlanski AL, Gu F, Guo F, Nielsen E2011. Arolefor CSLD3during cell-wall synthesis in apical plasma membranes of tip-growing root-hair cells. Nature Cell Biology 13: 973-980.
42. Peyroche A, Antonny B, Robineau S, Acker J, Cherfils J, Jackson CL 1999. Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: involvement of specific residues of the sec7 domain. Molecular Cell 3: 275-285.
43. Richter S, Geldner N, Schrader J, et al. 2007. Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448: 488-492.
44. Richter S, Müller LM, Stierhof Y-D, et al. 2012. Polarized cell growth in Arabidopsis requires endosomal recycling mediated by GBF1-related ARF exchange factors. Nature Cell Biology 14: 80-86.
45. Robinson DG, Jiang L, Schumacher K 2008. The endosomal system of plants: charting new and familiar territories. Plant Physiology 147: 1482-1492.
46. Saito C 2003. A 'bulb' subregion in the vacuolar membrane. Plant Morphology 15: 60-67.
47. Saito C, Ueda T, Abe H, et al. 2002. A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane inyoung cotyledons of Arabidopsis. Plant Journal 29: 245-255.
48. Saito C, Uemura T, Awai C, Ueda T, Abe H, Nakano A 2011. Qualitative difference between 'bulb' membranes and other vacuolar membranes. Plant Signaling and Behavior 6: 1914-1917.
49. 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. Molecular Biology of the Cell 12: 3733-3743.
50. Sanderfoot AA, Pilgrim M, Adam L, Raikhel NV 2001b. Disruption of indi-vidualmembersofArabidopsissyntaxingene familiesindicateseach has essential functions. Plant Cell 13: 659-666.
51. Sanmartín M, Ordóñez A, Sohn EJ, et al. 2007. Divergent functions of VTI12 and VTI11 in trafficking to storage and lytic vacuoles in Arabidopsis. Proceedings of the National Academy Sciences of the USA 104: 3645-3650.
52. Shin R, Berg RH, Schachtman DP2005. Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant and Cell Physiology 46: 1350-1357.
53. Silva PA, Ul-Rehman R, Rato C, Di Sansebastiano G-P, Malhó R 2010. Asymmetric localization of Arabidopsis SYP124 syntaxin at the pollen tube apical and sub-apical zones is involved in tip growth. BMC Plant Biology 10: 179.
54. Surpin M, Zheng H, Morita MT, et al. 2003. The VTI family of SNARE proteins is necessary for plant viability and mediates different protein transport pathways. Plant Cell 15: 2885-2899.
55. 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.
56. Viotti C, Bubeck J, Stierhof Y-D, 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.
57. Volgger M, Lang I, Ovecka M, Lichtscheidl I 2010. Plasmolysis and cell wall deposition in wheat root hairs under osmotic stress. Protoplasma 243: 51-62.
58. Zhang X, Henriques R, Lin S-S, Niu Q-W, Chua N-H 2006. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature Protocols 1: 641-646.
59. Zheng H, von Mollard GF, Kovaleva V, Stevens TH, Raikhel NV 1999. The plant vesicle-associated SNARE At VTI1a likely mediates vesicle transport from the trans-Golgi network to the prevacuolar compartment. Molecular Biology of the Cell 10: 2251-2264.