Golgi-mediated transport of seed storage proteins

Seed Science Research

Volumn 9, Issue 4, 1999, Pages 267-283

  Robinson, David G ^a   Hinz, Giselbert ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Clathrin coated vesicles; Dense vesicles; Golgi apparatus; Pea cotyledons; Pre vacuolar compartment; Protein storage vacuole; Vacuolar sorting signals

Indexed keywords

EUKARYOTA; PISUM SATIVUM;

EID: 0033387444     PISSN: 09602585     EISSN: None     Source Type: Journal    
DOI: 10.1017/s0960258599000288     Document Type: Review

References (125)

1. Ahmed, S.U., Bar-Peled, M. and Raikhel, N.V. (1997) Cloning and subcellular location of an Arabidopsis receptor-like protein that shares common features with protein-sorting receptors of eukaryotic cells. Plant Phyioslogy 115, 311-312.
2. Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K. and Watson, J.D. (1994) The molecular biology of the cell. New York & London, Garland Publishing.
3. Allen, A.K., Desai, N.N. and Neuberger, A. (1976) The purification of the glycoprotein lectin from broad bean (Vicia faba) and a comparison of its properties with lectins of similar specificity. Biochemical Journal 155, 127-135.
4. Andreeva, A.V., Kutuzov, M.A., Evans, D.E. and Hawes, C.R. (1998) The structure and function of the Golgi apparatus: a hundred years of questions. Journal of Experimental Botany 49, 1281-1291.
5. Bagga, S., Adams, H., Kemp, J.D. and Sengupta-Gopalan, C. (1995) Accumuulation of 15-kilodalton zein in novel protein bodies in transgenic tobacco. Plant Physiology 107, 13-23.
6. Barr, F.A. and Warren, G. (1996) Disassembly and reassembly of the Golgi apparatus. Cell and Developmental Biology 7, 505-551.
7. Becherer, K.A., Rider, S.E., Emr, S.D. and Jones, E.W. (1996) Novel syntaxin homologue, PEP12p, required for the sorting of luminal hydrolases to the lysosome-like vacuole in yeast. Molecular Biology of the Cell 7, 579-594.
8. Beevers, L. and Raikhel, N.V. (1998) Transport to the vacuole: receptors and trans elements. Journal of Experimental Botany 49, 1271-1279.
9. Berger, E.G. (1997) The Golgi apparatus: from discovery to contemporary studies. pp. 1-35 in Berger, E.G.; Roth, J. (Eds) The Golgi apparatus. Basel, Switzerland, Birkhäuser Verlag.
10. Blanco-Labra, A., Sandoval-Cardoso, L., Mendiola-Olaya, E., Valdés-Rodríguez, S. and López, M.G. (1996) Purification and characterization of a glycoprotein α-amylase inhibitor from tepary bean (Phaseolus acutifolius A. Gray). Journal of Plant Physiology 149, 650-656.
11. Boevink, P., Oparka, K., Santa Cruz, S., Martin, B., Betteridge, A. and Hawes, C. (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. The Plant Journal 15, 441-447.
12. Boller, T. and Wiemken, A. (1987) Dynamics of vacuolar compartmentation. Annual Review of Plant Physiology 37, 137-164.
13. Bollini, R., Ceriotti, A., Daminati, M.G. and Vitale, A. (1985) Glycosylation is not needed for intracellular transport of phytohemagglutinin in developing Phaseolus vulgaris cotyledons and for maintenance of its biological activity. Physiologia Plantarum 65, 15-22.
14. Braulke, T. (1996) Origin of lysosomal proteins. pp. 15-49 in Lloyd, J.B.; Mason, R.W. (Eds) Biology of the lysosomes. Subcellular Biochemistry 27, New York, Plenum Press.
15. Chrispeels, M.J. (1983) The Golgi apparatus mediates the transport of phytohemagglutinin to the protein bodies in bean cotyledons. Planta 158, 140-151.
16. Colley, K.J. (1997) Golgi localization of glycosyltransferases: more questions than answers. Glycobiology 7, 1-13.
17. Conceicao, A. da Silva, Marty-Mazars, D., Bassham, D.C., Sanderfoot, A.A., Marty, F. and Raikhel, N.V. (1997) the syntaxin homolog AtPEP12p resides on a late post-Golgi compartment in plants. The Plant Cell 9, 571-582.
18. Cooper, A.A. and Stevens, T.H. (1996) VPS10p cycles between the late Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases. Journal of Cell Biology 133, 529-541.
19. Coulomb, S. and Coulomb, P. (1996) Endocytosis in Cucurbita pepo root meristems: coated vesicles, multivesicular bodies and vacuole relationship. Comptes Rendus des Séances de l'Académie des Sciences 319, 377-383.
20. Craig, S. (1988) Structural aspects of protein accumulation in developing legume seeds. Bichemie une Physiologie der Pflanzen 183, 159-171.
21. Craig, S. and Goodchild, D.J. (1984) Periodate-acid treatment of sections permits on-grid immunogold localization of pea seed vicilin in ER and Golgi. Protoplasma 122, 35-44.
22. Davey, R.A. and Dudman, W.F. (1979) The carbohydrate of storage glycoproteins from seeds of Pisum sativum: Characterization and distribution of component polypeptides. Australian Journal of Plant Physiology 6, 435-447.
23. Dhugga, K.S., Tiwari, S.C. and Ray, P.M. (1997) A reversibly glycosylvated peptide (RGP1) possibly involved in plant cell wall synthesis: purification, gene cloning, and trans Golgi localization. Proceedings of the National Academy of Science (USA) 94, 7679-7684.
24. Di Sansebastiano, G.P., Paris, N., Marc-Martin, S. and Neuhaus, J-M. (1998) Specific accumulation of GFP in a non-acidic vacuolar compartment via a C-terminal propeptide-mediated sorting pathway. The Plant Journal 15, 449-457.
25. Dittié, A.S., Hajibagheri, N. and Tooze, S.A. (1996) The AP-1 adaptor complex binds to immature secretory granules from PC12 cells, and is regulated by ADP-ribosylation factor. Journal of Cell Biology 132, 523-536.
26. Dittié, A.S., Thomas, L., Thomas, G. and Tooze, S.A. (1997) Interaction of furin in immature secretory granules from neuroendocrine cells with the AP-1 adaptor complex is modulated by casein kinase II phosphorylation. The EMBO Journal 16, 4859-4870.
27. Dombrowski, J.E., Schroeder, M.R., Bednarek, S.Y. and Raikhel, N.V. (1993) Determination of the functional elements within the vacuolar targeting signal of barley lectin. The Plant Cell 5, 587-596.
28. Draper, R.K., Goda, Y., Brodsky, F.M. and Pfeffer, S.R. (1990) Antibodies to clathrin inhibit endocytosis but not recycling to the trans-Golgi network in vitro. Science 248, 1539-1541.
29. Driouich, A. and Staehelin, A. (1997) The plant Golgi apparatus: structural organization and functional properties. pp. 275-301 in Berger, E.G.; Roth, J. (Eds) The Golgi apparatus. Basel, Switzerland, Birkhäuser Verlag.
30. Duden, R. and Schekman, R. (1997) Insights into Golgi function through mutants in yeast and animal cells. pp. 219-246 in Berger, E.G.; Roth, J. (Eds) The Golgi apparatus. Basel, Switzerland, Birkhäuser Verlag.
31. Duranti, M., Guerrieri, N., Cerletti, P. and Vecchio, G. (1992) The legumin precursor from white lupin seed. Identity of the subunits, assembly, and proteolysis. European Journal of Biochemistry 206, 941-947.
32. Duranti, M., Restani, P., Poniatowska, M. and Cerletti, P. (1981) The seed globulins of Lupinus albus. Phytochemistry 20, 2071-2075.
33. Farquhax, M.G. and Hauri, H-P. (1997) Protein sorting and vesicular traffic in the Golgi apparatus. pp. 63-129 in Berger, E.G.; Roth, J. (Eds) The Golgi apparatus. Basel, Switzerland, Birkhäuser Verlag.
34. Frigerio, L., de Virgilio, M., Prada, A., Faoro, F. and Vitale, A. (1998) Sorting of phaseolin to the vacuole is saturable and requires a short C-terminal peptide. The Plant Cell 10, 1031-1042.
35. Füllekrug, J. and Nilsson, T. (1998) Protein sorting in the Golgi complex. Biochimica et Biophysica Acta 1404, 77-84.
36. Futter, C.E., Pearse, A., Hewlett, L.J. and Hopkins, C.R. (1996) Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. Journal of Cell Biology 132, 1011-1023.
37. Galili, G. (1997) The prolamin storage proteins of wheat and its relatives. pp. 221-242 in Larkins, B.A.; Vasil, I.K. (Eds) Cellular and molecular biology of plant seed development. Dordrecht (Netherlands), Kluwer Academic Publishers.
38. Galili, G., Altschuler, Y. and Levanony, H. (1993) Assembly and transport of seed storage proteins. Trends in Cell Biology 3, 437-442.
39. Galili, G., Sengupta-Gopalan, C. and Ceriotti, A. (1998) The endoplasmic reticulum of plant cells and its role in protein maturation and biogenesis of oil bodies. Plant Molecular Biology 38, 1-29.
40. Galway, M.E., Rennie, P.J. and Fowke, L.C. (1993) Ultrastructure of the endocytotic pathway in glutaraldehyde-fixed and high-pressure frozen/freeze-substituted protoplasts of white spruce (Picea glauca). Journal of Cell Science 106, 847-858.
41. Glick, B.S. and Malhotra, V. (1998) The curious status of the Golgi apparatus. Cell 95, 883-889.
42. Gomez, L. and Chrispeels, M.J. (1993) Tonoplast and soluble vacuolar proteins are targeted by different mechanisms. The Plant Cell 5, 1113-1124.
43. Griffing, L.R. (1991) Comparisons of Golgi structure and dynamics in plant and animal cells. Journal of Electron Microscopic Techniques 17, 179-199.
44. Hara-Nishimura, I., Shimada, T., Hatano, K., Takeuchi, Y. and Nishimura, M. (1998) Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. The Plant Cell 10, 825-836.
45. Harris, N., Grindley, H., Mulchrone, J. and Croy, J.D. (1989) Correlated in situ hybridization and immunochemical studies of legumin storage protein deposition in pea (Pisum sativum L.). Cell Biology International Reports 13, 23-35.
46. Hawes, C. and Satiat-Jeunemaitre, B. (1996) Stacks of questions - How does the plant Golgi work? Trends in Plant Science 1, 395-401.
47. Herman, E.H. (1994) Multiple origins of intravacuolar protein accumulation in plant cells. Advances in Structural Biology 3, 243-283.
48. Higgins, T.J.V., Chandler, P.M., Zurawski, G., Button, S.C. and Spencer, D. (1983) The biosynthesis and primary structure of pea seed lectin. Journal of Biological Chemistry 258, 9544-9549.
49. Hinz, G., Hoh, B., Hohl, I. and Robinson, D.G. (1995) Stratification of storage proteins in the protein storage vacuole of developing cotyledons of Pisum sativum L. Journal of Plant Physiology 145, 437-442.
50. Hinz, G., Menze, A., Hohl, I. and Vaux, U. (1997) Isolation of prolegumin from developing pea seeds: its binding to endomembranes and assembly into prolegumin hexamers in the protein storage vacuole. Journal of Experimental Botany 48, 139-149.
51. Hinz, G., Hillmer, S., Bäumer, M. and Hohl, I. (1999) Vacuolar storage proteins and the putative sorting receptor BP-80 exit the Golgi apparatus of developing pea cotyledons in different transport vesicles. The Plant Cell 11, 1509-1524.
52. Hoh, B., Hinz, G., Jeong, B-K. and Robinson, D.G. (1995) Protein storage vacuoles form de novo during pea cotyledon development. Journal of Cell Science 108, 299-310.
53. Hohl, I., Robinson, D.G., Chrispeels, M.J. and Hinz, G. (1996) Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat. Journal of Cell Science 109, 2539-2550.
54. Horazdovsky, B.F., DeWald, D.B. and Emr, S.D. (1995) Protein transport to the yeast vacuole. Current Opinion in Cell Biology 7, 544-551.
55. Jiang, L. and Rogers, J.C. (1998) Integral membrane protein sorting to vacuoles in plant cells: Evidence for two pathways. Journal of Cell Biology 143, 1183-1199.
56. Johnson, K.D. and Chrispeels, M.J. (1987) Substrace specificities of N-acetylglucosaminyl-, fucosyl-, and xylosyltransferases that modify glycoproteins in the Golgi apparatus of bean cotyledons. Plant Physiology 84, 1301-1308.
57. Kim, W.T., Franceschi, V.R., Krishnan, H.B. and Okita, T.W. (1988) Formation of wheat protein bodies: involvement of the Golgi apparatus in gliadin transport. Planta 176, 173-182.
58. Kirsch, T., Paris, N., Butler, J.M., Beevers, L. and Rogers, J.C. 91994) Purification and initial characterization of a potential plant vacuolar targeting receptor. Proceedings of the National Academy of Science (USA) 91, 3403-3407.
59. Kirsch, T., Saalbach, G., Raikhel, N.V. and Beevers, L. (1996) Interaction of a potential vacuolar targeting receptor with amino- and carboxyl-terminal targeting determinants. Plant Physiology 111, 469-474.
60. Klauer, S.F. and Franceschi, V.R. (1997) Mechanism of transport of vegetative storage proteins to the vacuole of the paraveinal mesophyll of soybean leaf. Protoplasma 200, 174-185.
61. Kleene, R., Dartsch, H. and Kern, H-F. (1999) The secretory lectin ZG16p mediates sorting of enzyme proteins to the zymogen granule membrane in pancreatic acinar cells. European Journal of Cell Biology 78, 79-90.
62. Kreis, T.E., Goodson, H.V., Perez, F. and Rönnholm, R. (1997) Golgi apparatus-cytoskeleton interactions. pp. 179-193 in Berger, E.G.; Roth, J. (Eds) The Golgi apparatus. Basel, Switzerland, Birkhäuser Verlag.
63. Krishnan, H.B., Franceschi, V.R. and Okita, T.W. (1986) Immunochemical studies on the role of the Golgi complex in protein body formation in rice cells. Planta 169, 471-480.
64. Kuliawat, R., Klumperman, J., Ludwig, P. and Arvan, P. (1997) Differential sorting of lysosomal enzymes out of the regulated secretory pathway in pancreatic β-cells. Journal of Cell Biology 37, 595-608.
65. Kummer, H. and Rüdiger, H. (1988) Characterization of a lectin-binding storage protein from pea (Pisum sativum). Biological Chemistry Hoppe-Seyler 369, 639-646.
66. Lending, C.R. and Larkins, B.A. (1989) Changes in the zein composition of protein bodies during maize endosperm development. The Plant Cell 1, 1011-1023.
67. Lerouge, P., Cananes-Macheteau, M., Rayon, C., Fischette-Lainé, A.C., Gomord, V. and Faye, L. (1998) N-glycoprotein biosynthesis in plants: recent developments and future trends. Plant Molecular Biology 38, 31-48.
68. Li, X., Wu, Y., Zhang, D-Z., Gillikin, J.W., Boston, R.S., Francheschi, V.R. and Okita, T. (1993) Rice prolamine protein body biogenesis: a BiP-mediated process. Science 262, 1054-1056.
69. Lis, H., Sharon, N. and Katchalski, E. (1966) Soybean hemagglutinin, a plant glycoprotein. I. Isolation of a glycopeptide. Journal of Biological Chemistry 241, 684-689.
70. Matsuoka, K. and Neuhaus, J-M. (1999) Cis-elements of protein transport to the plant vacuoles. Journal of Experimental Botany 50, 165-174.
71. Matsuoka, K., Bassham, D.C., Raikhel, N.V. and Nakamura, K. (1995) Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells. Journal of Cell Biology 130, 1307-1318.
72. +-ATPase in a non-vacuolar organelle is required for the sorting of soluble vacuolar protein precursors in tobacco cells. The Plant Cell 9, 533-546.
73. Mollenhauer, H.H., Morré, D.J. and Rowe, L.D. (1990) Alteration of intracellular traffic by monensin: mechanism, specificity and relationship to toxicity. Biochimica et Biophysica Acta 1031, 225-246.
74. Moreno, J., Altabella, T. and Chrispeels, M.J. (1990) Characterization of α-amylase inhibitor, a lectin-like protein in the seeds of Phaseolus vulgaris. Plant Physiology 92, 703-709.
75. Müntz, K. (1996) Proteases and proteolytic cleavage of storage proteins in developing and germinating dicotyledenous seeds. Journal of Experimental Botany 47, 605-622.
76. Müntz, K. (1998) Deposition of storage proteins. Plant Molecular Biology 38, 77-99.
77. Nelson, N. (1992) Structure and function of V-ATPases in endocytic and secretory organelles. Journal of Experimental Biology 172, 149-153.
78. Neuhaus, J-M. and Rogers, J.C. (1998) Sorting of proteins to vacuoles in plant cells. Plant Molecular Biology 38, 127-144.
79. Oprins, A., Duden, R., Kreis, T.E., Geuze, H.J. and Slot, J.W. (1993) β-COP localizes mainly to the cis-Golgi side in exocrine pancreas. Journal of Cell Biology 121, 49-59.
80. Orci, L., Stamnes, M., Ravazzola, M., Amherst, M., Perrelet, A., Söllner, T.H. and Rothman, J.E. (1997) Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90, 335-349.
81. 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.
82. Paris, N., Rogers, S.W., Jiang, L., Kirsch, T., Beevers, L., Phillips, T.E. and Rogers, J.C. (1997) Molecular cloning and further characterization of a probable plant vacuolar sorting receptor. Plant Physiology 115, 29-39.
83. Pedrazzini, E., Giovanazzo, G., Bielli, A., de Virgilio, M., Frigerio, L., Pesca, M., Faoro, M., Bollini, R., Ceriotti, A. and Vitale, A. (1997) Protein quality control along the route to the plant vacuole. The Plant Cell 9, 1869-1880.
84. Rambourg, A. and Clermont, Y. (1997) Three-dimensional structure of the Golgi apparatus in mammalian cells. pp. 37-61 in Berger, E.G.; Roth, J. (Eds) The Golgi apparatus. Basel, Switzerland, Birkhäuser Verlag.
85. Raymond, C.K., Howald-Stevenson, I., Vater, C.A. and Stevens, T.H. (1992) Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Molecular Biology of the Cell 3, 1389-1402.
86. Rayon, C., Lerouge, P. and Faye, L. (1998) The protein N-glycosylation in plants. Journal of Experimental Biology 49, 1463-1472.
87. Record, R.D. and Griffing, L.R. (1988) Convergence of the endocyric and lysosomal pathways in soybean protoplasts. Planta 176, 425-432.
88. Robinson, D.G. (1985) Plant membranes: endo- and plasma membranes of plant cells. New York, Wiley.
89. Robinson, D.G. and Hillmer, S. (1990) Coated pits. pp. 233-255 in Larsson, C.; Möller, I.M. (Eds) The plant plasma membrane. Heidelberg, Germany, Springer Verlag.
90. Robinson, D.G. and Hinz, G. (1997) Vacuole biogenesis and protein transport to the plant vacuole: a comparison with the yeast vacuole and the mammalian lysosome. Protoplasma 197, 1-25.
91. Robinson, D.G., Hoh, B., Hinz, G. and Jeong, B-K. (1995) One vacuole or two vacuoles: do protein storage vacuoles arise de novo during pea cotyledon development? Journal of Plant Physiology 45, 654-664.
92. Robinson, D.G., Bäumer, M., Hinz, G. and Hohl, I. (1997) Ultrastructure of the pea cotyledon Golgi apparatus: origin of dense vesicles and the action of brefeldin A. Protoplasma 200, 198-209.
93. Robinson, D.G., Bäumer, M., Hinz, G. and Hohl, I. (1998a) Vesicle transfer of storage proteins to the vacuole: the role of the Golgi apparatus and multivesicular bodies. Journal of Plant Physiology 152, 650-667.
94. Robinson, D.G., Hinz, G. and Holstein, S.E.H. (1998b) The molecular characterization of transport vesicles. Plant Molecular Biology 38, 49-76.
95. Saalbach, G., Jung, R., Kunze, G., Saalbach, I., Adler, K. and Müntz, K. (1991) Different legumin protein domains act as vacuolar targeting signals. The Plant Cell 3, 695-708.
96. Sanderfoot, A.A., Ahmed, S.U., Marty-Mazars, D., Rapoport, I., Kirchhausen, T., Marty, F. and Raikhel, N.V. (1998) A putative vacuolar cargo receptor partially colocalizes with AtPEP12p on a prevacuolar compartment in Arabidopsis roots. Proceedings of the National Academy of Science USA 95, 9920-9925.
97. Satiat-Jeunemaitre, B., Steele, C. and Hawes, C. (1996) Golgi-membrane dynamics are cytoskeleton dependent. A study on Golgi stack movement induced by brefeldin A. Protoplasma 191, 21-33.
98. Sato, M.H., Nakamura, N., Ohsumi, Y., Kouchi, H., Kondo, M., Hara-Nishimura, I., Nishimura, M. and Wada, Y. (1997) the AtVAM3 encodes a syntaxin-related molecule implicated in the vacuolar assembly in Arabidopsis thaliana. Journal of Biological Chemistry 272, 24530-24535.
99. Shewry, P.R. (1995) Plant storage proteins. Biological Review 70, 375-426.
100. Shimada, T., Kuroyanagi, M., Nishimura, M. and Hara-Nishimura, I. (1997) A pumpkin 72 kDa membrane protein of precursor-accumulating vesicles has characteristics of a vacuolar sorting receptor. Plant and Cell Physiology 38, 1414-1420.
101. Simpson, F., Peden, A.A., Christopoulou, L. and Robinson, M.S. (1997) Characterization of the adaptor-related protein complex, AP-3. Journal of Cell Biology 137, 835-845.
102. Söllner, T., Whiteheart, S.W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P. and Rothman, J.E. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
103. Sonnewald, U., Sturm, A., Chrispeels, M.J. and Willmitzer, L. (1989) Targeting and glycosylation of patatin, the major potato tuber protein in leaves of transgenic tobacco. Planta 179, 174-180.
104. Staehelin, A. and Hepler, P.K. (1996) Cytokinesis in higher plants. Cell 84, 821-824.
105. Staehelin, A. and Moore, I. (1995) The plant Golgi apparatus: structure, functional organization and trafficking mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 46, 261-288.
106. Storrie, B. and Yang, W. (1998) Dynamics of the interphase mammalian Golgi complex as revealed through drugs producing reversible Golgi disassembly. Biochimica et Biophysica Acta 1404, 127-137.
107. Sturm, A., Johnson, K.D., Szumilo, T., Elbein, A.D. and Chrispeels, M.J. (1987a) Subcellular localization of glycosidases and glycosyltransferases involved in the processing of N-linked oligosaccharides. Plant Physiology 85, 741-745.
108. Sturm, A., Van-Kuik, J.A., Vliegenthart, J.F. and Chrispeels, M.J. (1987b) Structure, position, and biosynthesis of the high mannose and the complex oligosaccharide side chains of the bean storage protein phaseollin. Journal of Biological Chemistry 262, 13392-13403.
109. Sturm, A., Voelker, T.A., Herman, E.H. and Chrispeels, M.J. (1988) Correct glycosylation, Golgi-processing, and targeting to protein bodies of the vacuolar protein phytohemagglutinin in transgenic tobacco. Planta 175, 170-183.
110. Tanchak, M.A. and Chrispeels, M.J. (1989) Crosslinking of microsomal proteins identifies P-9000, a protein that is co-transported with phaseolin and phytohemagglutinin in bean cotyledons. Planta 179, 495-505.
111. Tanchak, M.A. and Fowke, L.C. (1987) The morphology of multivesicular bodies in soybean protoplasts and their role in endocytosis. Protoplasma 138, 173-182.
112. Thiele, C., Gerdes, H-H. and Huttner, W.B. (1997) Protein secretion: puzzling receptors. Current Biology 7, R496-R500.
113. Tooze, S.A. (1998) Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochimica et Biophysica Acta 1404, 231-244.
114. Tooze, J. and Tooze, S.A. (1986) Clathrin-coated vesicular transport of secretory proteins during the formation of ACTH-containing secretory granules in AtT20 cells. Journal of Cell Biology 103, 839-850.
115. van Deurs, B., Holm, P.K., Kayser, L., Sandvig, K. and Hansen, S.H. (1993) Multivesicular bodies in Hep-2 cells are maturing endosomes. European Journal of Cell Biology 61, 208-224.
116. Vitale, A. and Chrispeels, M.J. (1992) Sorting of proteins to the vacuoles of plant cells. Bioessays 14, 151-160.
117. Vitale, A. and Denecke, J. (1999) The endoplasmic reticulum, gateway to the secretory pathway. The Plant Cell 11, 615-628.
118. Vitale, A. and Raikhel, N.V. (1999) What do proteins need to reach different vacuoles? Trends in Plant Science 4, 149-155.
119. Vitale, A., Warner, T.G. and Chrispeels, M.J. (1984) Phaseolus vulgaris phytohemagglutinin contains high-mannose and modified oligosaccharide chains. Planta 160, 256-263.
120. von Mollard, G.F., Nothwehr, S.F. and Stevens, T.H. (1997) The yeast v-SNARE Vti1p mediates two vesicle transport pathways through interactions with the t-SNAREs Sed5p and Pep12p. Journal of Cell Biology 137, 1511-1524.
121. Wee, E.G., Sherrier, D.J., Prime, T.A. and Dupree, P. (1998) Targeting of active sialytransferase to the plant Golgi apparatus. The Plant Cell 10, 1759-1768.
122. Wenzel, M., Gers-Barlag, H., Schimpl, A. and Rüdiger, H. (1993) Time-course of lectin and storage protein biosynthesis in developing pea (Pisum sativum) seeds. Biological Chemistry Hoppe-Seyler 374, 887-894.
123. Zheng, H., von Mollard, G.E., Kovaleva, V., Stevens, T.H. and Raikhel, N.V. (1999) The plant v-SNARE AtVT11a likely mediates vesicle transport from the TGN to the prevacuole. Molecular Biology of the Cell 10, 2251-2264.
124. Zheng, Z., Sumi, K., Tanaka, K. and Murai, N. (1995) The bean storage protein β-phaseolin is synthesized, processed, and accumulated in the vacuolar type-II protein bodies of transgenic rice endosperm. Plant Physiology 109, 777-786.
125. zur Nieden, U., Manteuffel, R., Weber, E. and Neumann, D. (1984) Dictyosomes participate in the intracellular pathway of storage proteins in developing Vicia faba cotyledons. European Journal of Cell Biology 34, 9-17.