The endoplasmic reticulum is the main membrane source for biogenesis of the lytic vacuole in Arabidopsis

Plant Cell

Volumn 25, Issue 9, 2013, Pages 3434-3449

  Viotti, Corrado ^a,b   Krüger, Falco ^a   Krebs, Melanie ^a   Neubert, Christoph ^a   Fink, Fabian ^a   Lupanga, Upendo ^a   Scheuring, David ^a   Boutté, Yohann ^b,d   Frescatada Rosa, Márcia ^b   Wolfenstetter, Susanne ^c   Sauer, Norbert ^c   Hillmer, Stefan ^a   Greb, Markus ^b   Schumacher, Karin ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UMEÅ UNIVERSITY   (Sweden)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d University Victor Segalen   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ADENOSINE TRIPHOSPHATASE; ARABIDOPSIS PROTEIN; HYBRID PROTEIN; INORGANIC PYROPHOSPHATASE; STEROL;

ARABIDOPSIS; CELL VACUOLE; ENDOPLASMIC RETICULUM; ENZYMOLOGY; GENETICS; GOLGI COMPLEX; LIPID METABOLISM; MERISTEM; METABOLISM; PH; PHYSIOLOGY; PLANT ROOT; PROTEIN TRANSPORT; REPORTER GENE; TRANSGENIC PLANT; ULTRASTRUCTURE;

ADENOSINE TRIPHOSPHATASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ENDOPLASMIC RETICULUM; GENES, REPORTER; GOLGI APPARATUS; HYDROGEN-ION CONCENTRATION; INORGANIC PYROPHOSPHATASE; LIPID METABOLISM; MERISTEM; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; STEROLS; VACUOLES;

EID: 84886488441     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.114827     Document Type: Article

References (75)

1. Amelunxen, F., and Heinze, U. (1984). Zur entwicklung der vacuole in testa-zellen des leinsamens. Eur. J. Cell Biol. 35: 343-354.
2. Bassham, D.C., Sanderfoot, A.A., Kovaleva, V., Zheng, H., and Raikhel, N.V. (2000). AtVPS45 complex formation at the trans-Golgi network. Mol. Biol. Cell 11: 2251-2265.
3. Berjak, P. (1972). Lysosomal compartmentation: Ultrastructural aspects of the origin, development, and function of vacuoles in root cells of Lepidium sativum. Ann. Bot. (Lond.) 36: 73-81.
4. Boutté, Y., Frescatada-Rosa, M., Men, S., Chow, C.-M., Ebine, K., Gustavsson, A., Johansson, L., Ueda, T., Moore, I., Jürgens, G., and Grebe, M. (2010). Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO J. 29: 546-558.
5. Boutté, Y., and Grebe, M. (2009). Cellular processes relying on sterol function in plants. Curr. Opin. Plant Biol. 12: 705-713.
6. Boutté, Y., Men, S., and Grebe, M. (2011). Fluorescent in situ visualization of sterols in Arabidopsis roots. Nat. Protoc. 6: 446-456.
7. Brüx, A., Liu, T.-Y., Krebs, M., Stierhof, Y.-D., Lohmann, J.U., Miersch, O., Wasternack, C., and Schumacher, K. (2008). Reduced V-ATPase activity in the trans-Golgi network causes oxylipindependent hypocotyl growth Inhibition in Arabidopsis. Plant Cell 20: 1088-1100.
8. Bryant, N.J., and Stevens, T.H. (1998). Vacuole biogenesis in Saccharomyces cerevisiae: Protein transport pathways to the yeast vacuole. Microbiol. Mol. Biol. Rev. 62: 230-247.
9. Campbell, R.E., Tour, O., Palmer, A.E., Steinbach, P.A., Baird, G.S., Zacharias, D.A., and Tsien, R.Y. (2002). A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99: 7877-7882.
10. Carter, C., Pan, S., Zouhar, J., Avila, E.L., Girke, T., and Raikhel, N.V. (2004). The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16: 3285-3303.
11. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
12. +-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730.
13. Feraru, E., Paciorek, T., Feraru, M.I., Zwiewka, M., De Groodt, R., De Rycke, R., Kleine-Vehn, J., and Friml, J. (2010). The AP-3 β adaptin mediates the biogenesis and function of lytic vacuoles in Arabidopsis. Plant Cell 22: 2812-2824.
14. Ferjani, A., Segami, S., Horiguchi, G., Muto, Y., Maeshima, M., and Tsukaya, H. (2011). Keep an eye on PPi: The vacuolar-type H+-pyrophosphatase regulates postgerminative development in Arabidopsis. Plant Cell 23: 2895-2908.
15. Finnigan, G.C., Cronan, G.E., Park, H.J., Srinivasan, S., Quiocho, F.A., and Stevens, T.H. (2012). Sorting of the yeast V-ATPase: Identification of a necessary and sufficient Golgi/endosomal retention signal in Stv1p. J. Biol. Chem. 287: 19487-19500.
16. Gaxiola, R.A., Palmgren, M.G., and Schumacher, K. (2007). Plant proton pumps. FEBS Lett. 581: 2204-2214.
17. Gomez, L., and Chrispeels, M.J. (1993). Tonoplast and soluble vacuolar proteins are targeted by different mechanisms. Plant Cell 5: 1113-1124.
18. Graham, L.A., Flannery, A.R., and Stevens, T.H. (2003). Structure and assembly of the yeast V-ATPase. J. Bioenerg. Biomembr. 35: 301-312.
19. Hanton, S.L., Matheson, L.A., and Brandizzi, F. (2006). Seeking a way out: Export of proteins from the plant endoplasmic reticulum. Trends Plant Sci. 11: 335-343.
20. Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T., and Yamamoto, A. (2009). A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 11: 1433-1437.
21. Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T., and Yamamoto, A. (2010). Electron tomography reveals the endoplasmic reticulum as a membrane source for autophagosome formation. Autophagy 6: 301-303.
22. Herman, E.M., Li, X., Su, R.T., Larsen, P., Hsu, H., and Sze, H. (1994). Vacuolar-type H+-ATPases are associated with the endoplasmic reticulum and provacuoles of root tip cells. Plant Physiol. 106: 1313-1324.
23. Hilling, B., and Amelunxen, F. (1985). On the development of the vacuole. II: Further evidence for endoplasmic reticulum origin. Eur. J. Cell Biol. 38: 195-200.
24. Hillmer, S., Viotti, C., and Robinson, D.G. (2012). An improved procedure for low-temperature embedding of high-pressure frozen and freeze-substituted plant tissues resulting in excellent structural preservation and contrast. J. Microsc. 247: 43-47.
25. Hofius, D., Schultz-Larsen, T., Joensen, J., Tsitsigiannis, D.I., Petersen, N.H.T., Mattsson, O., Jørgensen, L.B., Jones, J.D.G., Mundy, J., and Petersen, M. (2009). Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137: 773-783.
26. Inoue, Y., Suzuki, T., Hattori, M., Yoshimoto, K., Ohsumi, Y., and Moriyasu, Y. (2006). AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells. Plant Cell Physiol. 47: 1641-1652.
27. Isono, E., Katsiarimpa, A., Müller, I.K., Anzenberger, F., Stierhof, Y.-D., Geldner, N., Chory, J., and Schwechheimer, C. (2010). The deubiquitinating enzyme AMSH3 is required for intracellular trafficking and vacuole biogenesis in Arabidopsis thaliana. Plant Cell 22: 1826-1837.
28. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J., and Bourguignon, J. (2007). A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cell. Proteomics 6: 394-412.
29. Jiang, L., Phillips, T.E., Rogers, S.W., and Rogers, J.C. (2000). Biogenesis of the protein storage vacuole crystalloid. J. Cell Biol. 150: 755-770.
30. Jiang, L., and Rogers, J.C. (1998). Integral membrane protein sorting to vacuoles in plant cells: Evidence for two pathways. J. Cell Biol. 143: 1183-1199.
31. Kartner, N., Yao, Y., Bhargava, A., and Manolson, M.F. (2013). Topology, glycosylation and conformational changes in the membrane domain of the vacuolar H+-ATPase a subunit. J. Cell. Biochem. 114: 1474-1487.
32. Keinath, N.F., Kierszniowska, S., Lorek, J., Bourdais, G., Kessler, S.A., Shimosato-Asano, H., Grossniklaus, U., Schulze, W.X., Robatzek, S., and Panstruga, R. (2010). PAMP (pathogenassociated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J. Biol. Chem. 285: 39140-39149.
33. Iizuka, R., Yamagishi-Shirasaki, M., and Funatsu, T. (2011). Kinetic study of de novo chromophore maturation of fluorescent proteins. Anal. Biochem. 414: 173-178.
34. Klemm, R.W., Ejsing, C.S., Surma, M.A., Kaiser, H.-J., Gerl, M.J., Sampaio, J.L., de Robillard, Q., Ferguson, C., Proszynski, T.J., Shevchenko, A., and Simons, K. (2009). Segregation of sphingolipids and sterols during formation of secretory vesicles at the trans-Golgi network. J. Cell Biol. 185: 601-612.
35. Klionsky, D.J., et al. (2008). Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4: 151-175.
36. Knorr, R.L., Dimova, R., and Lipowsky, R. (2012). Curvature of double-membrane organelles generated by changes in membrane size and composition. PLoS ONE 7: e32753.
37. Kobae, Y., Mizutani, M., Segami, S., and Maeshima, M. (2006). Immunochemical analysis of aquaporin isoforms in Arabidopsis suspension-cultured cells. Biosci. Biotechnol. Biochem. 70: 980-987.
38. Krebs, M., Beyhl, D., Görlich, E., Al-Rasheid, K.A.S., Marten, I., Stierhof, Y.-D., Hedrich, R., and Schumacher, K. (2010). Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc. Natl. Acad. Sci. USA 107: 3251-3256.
39. Lauber, M.H., Waizenegger, I., Steinmann, T., Schwarz, H., Mayer, U., Hwang, I., Lukowitz, W., and Jürgens, G. (1997). The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139: 1485-1493.
40. Lynes, E.M., and Simmen, T. (2011). Urban planning of the endoplasmic reticulum (ER): How diverse mechanisms segregate the many functions of the ER. Biochim. Biophys. Acta 1813: 1893-1905.
41. Maeshima, M. (2001). TONOPLAST TRANSPORTERS: Organization and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 469-497.
42. Martinoia, E., Maeshima, M., and Neuhaus, H.E. (2007). Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 58: 83-102.
43. Marty, F. (1978). Cytochemical studies on GERL, provacuoles, and vacuoles in root meristematic cells of Euphorbia. Proc. Natl. Acad. Sci. USA 75: 852-856.
44. Marty, F. (1999). Plant vacuoles. Plant Cell 11: 587-600.
45. Matile, P. (1978). Biochemistry and function of vacuoles. Annu. Rev. Plant Physiol. 29: 193-213.
46. Matile, P., andMoor, H. (1968). Vacuolation: Origin and development of the lysosomal apparatus in root-tip cells. Planta 80: 159-175.
47. Mesquita, J.F. (1969). Electron microscope study of the origin and development of the vacuoles in root-tip cells of Lupinus albus L. J. Ultrastruct. Res. 26: 242-250.
48. Nebenführ, A., Ritzenthaler, C., and Robinson, D.G. (2002). Brefeldin A: Deciphering an enigmatic inhibitor of secretion. Plant Physiol. 130: 1102-1108.
49. Neubert, C., Graham, L.A., Black-Maier, E.W., Coonrod, E.M., Liu, T.-Y., Stierhof, Y.-D., Seidel, T., Stevens, T.H., and Schumacher, K. (2008). Arabidopsis has two functional orthologs of the yeast V-ATPase assembly factor Vma21p. Traffic 9: 1618-1628.
50. Ozolina, N.V., Nesterkina, I.S., Kolesnikova, E.V., Salyaev, R.K., Nurminsky, V.N., Rakevich, A.L., Martynovich, E.F., and Chernyshov, M.Y. (2012). Tonoplast of Beta vulgaris L. contains detergent-resistant membrane microdomains. Planta 237: 859-871.
51. Paez-Valencia, J., Patron-Soberano, A., Rodriguez-Leviz, A., Sanchez-Lares, J., Sanchez-Gomez, C., Valencia-Mayoral, P., Diaz-Rosas, G., and Gaxiola, R. (2011). Plasma membrane localization of the type I H(+)-PPase AVP1 in sieve elementcompanion cell complexes from Arabidopsis thaliana. Plant Sci. 181: 23-30.
52. Paris, N., Stanley, C.M., Jones, R.L., and Rogers, J.C. (1996). Plant cells contain two functionally distinct vacuolar compartments. Cell 85: 563-572.
53. Pedrazzini, E., Komarova, N.Y., Rentsch, D., and Vitale, A. (2013). Traffic routes and signals for the tonoplast. Traffic 14: 622-628.
54. Ratajczak, R., Hinz, G., and Robinson, D.G. (1999). Localization of pyrophosphatase in membranes of cauliflower inflorescence cells. Planta 208: 205-211.
55. Richter, S., Geldner, N., Schrader, J., Wolters, H., Stierhof, Y.-D., Rios, G., Koncz, C., Robinson, D.G., and Jürgens, G. (2007). Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448: 488-492.
56. Rojo, E., Gillmor, C.S., Kovaleva, V., Somerville, C.R., and Raikhel, N.V. (2001). VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev. Cell 1: 303-310.
57. Saftig, P., and Klumperman, J. (2009). Lysosome biogenesis and lysosomal membrane proteins: Trafficking meets function. Nat. Rev. Mol. Cell Biol. 10: 623-635.
58. Scheuring, D., Viotti, C., Krüger, F., Künzl, F., Sturm, S., Bubeck, J., Hillmer, S., Frigerio, L., Robinson, D.G., Pimpl, P., and Schumacher, K. (2011). Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23: 3463-3481.
59. Schulze, W.X., Schneider, T., Starck, S., Martinoia, E., and Trentmann, O. (2012). Cold acclimation induces changes in Arabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. Plant J. 69: 529-541.
60. Segami, S., Nakanishi, Y., Sato, M.H., and Maeshima, M. (2010). Quantification, organ-specific accumulation and intracellular localization of type II H(+)-pyrophosphatase in Arabidopsis thaliana. Plant Cell Physiol. 51: 1350-1360.
61. Seguí-Simarro, J.M., and Staehelin, L.A. (2006). Cell cycledependent changes in Golgi stacks, vacuoles, clathrin-coated vesicles and multivesicular bodies in meristematic cells of Arabidopsis thaliana: A quantitative and spatial analysis. Planta 223: 223-236.
62. Seidel, T., Schnitzer, D., Golldack, D., Sauer, M., and Dietz, K.-J. (2008). Organelle-specific isoenzymes of plant V-ATPase as revealed by in vivo-FRET analysis. BMC Cell Biol. 9: 28.
63. Staehelin, L.A. (1997). The plant ER: A dynamic organelle composed of a large number of discrete functional domains. Plant J. 11: 1151-1165.
64. Swanson, S.J., and Jones, R.L. (1996). Gibberellic acid induces vacuolar acidification in barley aleurone. Plant Cell 8: 2211-2221.
65. Sze, H., Schumacher, K., Müller, M.L., Padmanaban, S., and Taiz, L. (2002). A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H(+)-ATPase. Trends Plant Sci. 7: 157-161.
66. Taiz, L. (1992). The plant vacuole. J. Exp. Biol. 172: 113-122.
67. Teh, O.-K., and Moore, I. (2007). An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448: 493-496.
68. Thompson, A.R., Doelling, J.H., Suttangkakul, A., and Vierstra, R.D. (2005). Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 138: 2097-2110.
69. Tooze, S.A., and Yoshimori, T. (2010). The origin of the autophagosomal membrane. Nat. Cell Biol. 12: 831-835.
70. Viotti, C., 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.
71. Wolfenstetter, S., Wirsching, P., Dotzauer, D., Schneider, S., and Sauer, N. (2012). Routes to the tonoplast: The sorting of tonoplast transporters in Arabidopsis mesophyll protoplasts. Plant Cell 24: 215-232.
72. Xie, Z., and Klionsky, D.J. (2007). Autophagosome formation: Core machinery and adaptations. Nat. Cell Biol. 9: 1102-1109.
73. Yoshida, S., and Uemura, M. (1986). Lipid composition of plasma membranes and tonoplasts isolated from etiolated seedlings of mung bean (Vigna radiata L.). Plant Physiol. 82: 807-812.
74. Zheng, H., and Staehelin, L.A. (2011). Protein storage vacuoles are transformed into lytic vacuoles in root meristematic cells of germinating seedlings by multiple, cell type-specific mechanisms. Plant Physiol. 155: 2023-2035.
75. Zouhar, J., Rojo, E., and Bassham, D.C. (2009). AtVPS45 is a positive regulator of the SYP41/SYP61/VTI12 SNARE complex involved in trafficking of vacuolar cargo. Plant Physiol. 149: 1668-1678.