Protein Sorting and Protein Modification Along the Secretory Pathway in BY-2 Cells

  • Ken Matsuoka
Part of the Biotechnology in Agriculture and Forestry book series (AGRICULTURE, volume 53)


Many different compartments in the cell, which we call organelles, function as many respective specialized intracellular factories in the cell. Some organelles, such as chloroplast, mitochondria and peroxisomes, function relatively independently of other organelles. In contrast, the endoplasmic reticulum (ER), Golgi apparatus, endosome, prevacuolar compartments (PVC), secretory vesicles and vacuoles, consist of a highly sophisticated organelle network: these organelles are always communicating with each other and with the plasma membrane. The rough ER, the Golgi apparatus and the vacuoles can be easily distinguished morphologically from other organelles. However, others, such as the endosome and prevacuolar compartment cannot be easily distinguished morphologically from the smooth ER and secretory vesicles, at least in BY-2 cells, because these organelles may be defined only by their function.


Golgi Apparatus Secretory Pathway Vacuolar Protein Golgi Stack Cell Plate Formation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Ahmed S, Rojo E, Kovaleva V, Venkataraman S, Dombrowski J, Matsuoka K, Raikhel N (2000) The plant vacuolar sorting receptor AtELP is involved in transport of NH(2)-terminal propeptide-containing vacuolar proteins in Arabidopsis thaliana. J Cell Biol 149: 1335–1344PubMedCrossRefGoogle Scholar
  2. An G (1985) High-efficiency transformation of cultured tobacco cells. Plant Physiol 79: 568–570PubMedCrossRefGoogle Scholar
  3. Bednarek S, Raikhel N (1991) The barley lectin carboxyl-terminal propeptide is a vacuolar protein sorting determinant in plants. Plant Cell 3: 1195–1206PubMedGoogle Scholar
  4. Bednarek S, Wilkins T, Dombrowski J, Raikhel N (1990) A carboxyl-terminal propeptide is necessary for proper sorting of barley lectin to vacuoles of tobacco. Plant Cell 2: 1145–1155PubMedGoogle Scholar
  5. Bethke P, Jones R (2000) Vacuoles, prevacuolar compartments. Curr Opin Plant Biol 3: 469–475PubMedCrossRefGoogle Scholar
  6. Breyne P, Dreesen R, Vandepoele K, De Veylder L, Van Breusegem F, Callewaert L, Rombauts S, Raes J, Cannoot B, Engler G, Inze D, Zabeau M (2002) Transcriptome analysis during cell division in plants. Proc Natl Acad Sci USA 99: 14825–14830PubMedCrossRefGoogle Scholar
  7. Brodsky J (1998) Translocation of proteins across the endoplasmic reticulum membrane. Int Rev Cytol 178: 277–328PubMedCrossRefGoogle Scholar
  8. Cao X, Rogers S, Butler J, Beevers L, Rogers J (2000) Structural requirements for ligand binding by a probable plant vacuolar sorting receptor. Plant Cell 12: 493–506PubMedGoogle Scholar
  9. Czempinski K, Frachisse J, Maurel C, Barbier-Brygoo H, Mueller-Roeber B (2002) Vacuolar membrane localization of the Arabidopsis “two-pore” K+ channel KCO1. Plant J 29: 809–820PubMedCrossRefGoogle Scholar
  10. Denecke J, Goldman M, Demolder J, Seurinck J, Botterman J (1991) The tobacco luminal binding protein is encoded by a multigene family. Plant Cell 3: 1025–1035PubMedGoogle Scholar
  11. Denmat-Ouisse L, Faye L, Gomord V (1999) Post-translational maturation of natural, drug-induced missorted phytohemagglutinin. Plant Physiol Biochem 37: 849–858PubMedCrossRefGoogle Scholar
  12. Dixit R, Cyr R (2002) Golgi secretion is not required for marking the preprophase band site in cultured tobacco cells. Plant J 29: 99–108PubMedCrossRefGoogle Scholar
  13. Dombrowski J, Schroeder M, Bednarek S, Raikhel N (1993) Determination of the functional elements within the vacuolar targeting signal of barley lectin. Plant Cell 5: 587–596PubMedGoogle Scholar
  14. Emans N, Zimmermann S, Fischer R (2002) Uptake of a fluorescent marker in plant cells is sensitive to brefeldin A, wortmannin. Plant Cell 14: 71–86PubMedCrossRefGoogle Scholar
  15. Fu L, Sztul E (2003) Traffic-independent function of the Sar1p/COPII machinery in proteasomal sorting of the cystic fibrosis transmembrane conductance regulator. J Cell Biol 160: 157–163PubMedCrossRefGoogle Scholar
  16. Gomord V, Denmat L, Fitchette-Laine A, Satiat-Jeunemaitre B, Hawes C, Faye L (1997) The C-terminal HDEL sequence is sufficient for retention of secretory proteins in the endoplasmic reticulum (ER) but promotes vacuolar targeting of proteins that escape the ER. Plant J 11:313– 325Google Scholar
  17. Hamasaki M, Noda T, Ohsumi Y (2003) The early secretory pathway contributes to autophagy in yeast. Cell Struct Funct 28: 49–54PubMedCrossRefGoogle Scholar
  18. Hong Z, Delauney A, Verma D (2001) A cell plate-specific callose synthase, its interaction with phragmoplastin. Plant Cell 13: 755–768PubMedGoogle Scholar
  19. Inaba T, Nagano Y, Nagasaki T, Sasaki Y (2002) Distinct localization of two closely related Ypt3/Rab11 proteins on the trafficking pathway in higher plants. J Biol Chem 277: 9183–9188PubMedCrossRefGoogle Scholar
  20. Jauh G, Phillips T, Rogers J (1999) Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell 11: 1867–1882PubMedGoogle Scholar
  21. Kawazu T, Kawano S, Kuroiwa T (1995) Distribution of Golgi apparatus in the mitosis of cultured tobacco cells as revealed by DiOC6 fluorescence microscopy. Protoplasma 186: 183–192CrossRefGoogle Scholar
  22. Kirsch T, Paris N, Butler J, Beevers L, Rogers J (1994) Purification, initial characterization of a potential plant vacuolar targeting receptor. Proc Natl Acad Sci USA 91: 3403–3407PubMedCrossRefGoogle Scholar
  23. Koide Y, Hirano H, Matsuoka K, Nakamura K (1997) The N-terminal propeptide of the precursor to sporamin acts as a vacuole-targeting signal even at the C terminus of the mature part in tobacco cells. Plant Physiol 114: 863–870PubMedCrossRefGoogle Scholar
  24. Koide Y, Matsuoka K, Ohto M, Nakamura K (1999) The N-terminal propeptide and the C terminus of the precursor to 20-kilo-dalton potato tuber protein can function as different types of vacuolar sorting signals. Plant Cell Physiol 40: 1152–1159PubMedCrossRefGoogle Scholar
  25. Kutsuna N, Hasezawa S (2002) Dynamic organization of vacuolar and microtubule structures during cell cycle progression in synchronized tobacco BY-2 cells. Plant Cell Physiol 43: 965–973PubMedCrossRefGoogle Scholar
  26. Lee J, Yoo B, Rojas M, Gomez-Ospina N, Staehelin L, Lucas W (2003) Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299: 392–396PubMedCrossRefGoogle Scholar
  27. Li Y, Rogers S, Tse Y, Lo S, Sun S, Jauh G, Jiang L (2002) BP-80 and homologs are concentrated on post-Golgi, probable lytic prevacuolar compartments. Plant Cell Physiol 726–742Google Scholar
  28. Matsuoka K, Nakamura K (1991) Propeptide of a precursor to a plant vacuolar protein required for vacuolar targeting. Proc Natl Acad Sci USA 88: 834–838PubMedCrossRefGoogle Scholar
  29. Matsuoka K, Nakamura K (1999) Large alkyl side-chains of isoleucine and leucine in the NPIRL region constitute the core of the vacuolar sorting determinant of sporamin precursor. Plant Mol Biol 41: 825–835PubMedCrossRefGoogle Scholar
  30. Matsuoka K, Neuhaus J-M (1999) cis-element of protein transport to the plant vacuoles J Exp Bot 50:165–173Google Scholar
  31. Matsuoka K, Bassham D, Raikhel N, Nakamura K (1995a) Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells. J Cell Biol 130: 1307–1318PubMedCrossRefGoogle Scholar
  32. Matsuoka K, Watanabe N, Nakamura K (1995b) O-glycosylation of a precursor to a sweet potato vacuolar protein, sporamin, expressed in tobacco cells. Plant J 8: 877–889PubMedCrossRefGoogle Scholar
  33. Matsuoka K, Higuchi T, Maeshima M, Nakamura K (1997) A vacuolar-type H+-ATPase in a nonvacuolar organelle is required for the sorting of soluble vacuolar protein precursors in tobacco cells. Plant Cell 9: 533–546PubMedGoogle Scholar
  34. Merigout P, Kepes F, Perret AM, Satiat-Jeunemaitre B, Moreau P (2002) Effects of brefeldin A and nordihydroguaiaretic acid on endomembrane dynamics and lipid synthesis in plant cells. FEBS Lett 518: 88–92PubMedCrossRefGoogle Scholar
  35. Moriyasu Y, Ohsumi Y (1996) Autophagy in tobacco suspension-cultured cells in response to sucrose starvation. Plant Physiol 111: 1233–1241PubMedGoogle Scholar
  36. Mullen R, Lisenbee C, Miernyk J, Trelease R (1999) Peroxisomal membrane ascorbate peroxidase is sorted to a membranous network that resembles a subdomain of the endoplasmic reticulum. Plant Cell 11: 2167–2185PubMedGoogle Scholar
  37. Nebenfuhr A, Frohlick J, Staehelin L (2000) Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol 124: 135–151PubMedCrossRefGoogle Scholar
  38. Pagny S, Denmat-Ouisse LA, Gomord V, Faye L (2003) Fusion with HDEL protects cell wall invertase from early degradation when N-glycosylation is inhibited. Plant Cell Physiol 44:173– 182Google Scholar
  39. Pelham H, Rothman J (2000) The debate about transport in the Golgi—two sides of the same coin? Cell 102: 713–719PubMedCrossRefGoogle Scholar
  40. Petrasek J, Cerna A, Schwarzerova K, Elckner M, Morris DA, Zazimalova E (2003) Do phytotropins inhibit auxin efflux by impairing vesicle traffic? Plant Physiol 131: 254–263PubMedCrossRefGoogle Scholar
  41. Ritzenthaler C, Laporte C, Gaire F, Dunoyer P, Schmitt C, Duval S, Piequet A, Loudes A, Rohfritsch O, Stussi-Garaud C, Pfeiffer P (2002a) Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. J Virol 76: 8808–8819PubMedCrossRefGoogle Scholar
  42. Ritzenthaler C, Nebenfuhr A, Movafeghi A, Stussi-Garaud C, Behnia L, Pimpl P, Staehelin L, Robinson D (2002b) 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 14: 237–261PubMedCrossRefGoogle Scholar
  43. Robinson D (ed) (2003) The Golgi apparatus and the plant secretory pathway. Annual Plant Reviews vol. 9, Blackwell Publishing, OxfordGoogle Scholar
  44. Saint-Jore C, Evins J, Batoko H, Brandizzi F, Moore I, Hawes C (2002) Redistribution of membrane proteins between the Golgi apparatus and endoplasmic reticulum in plants is reversible and not dependent on cytoskeletal networks. Plant J 29: 661–678PubMedCrossRefGoogle Scholar
  45. Saito T, Niwa Y, Ashida H, Tanaka K, Kawamukai M, Matsuda H, Nakagawa T (1999) Expression of a gene for cyclophilin which contains an amino-terminal endoplasmic reticulum-targeting signal. Plant Cell Physiol 40: 77–87PubMedCrossRefGoogle Scholar
  46. Samuels A, Giddings TJ, Staehelin L (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130: 1345–1357PubMedCrossRefGoogle Scholar
  47. Schekman R, Orci L (1996) Coat proteins and vesicle budding. Science 271: 1526–1533PubMedCrossRefGoogle Scholar
  48. Shpak E, Barbar E, Leykam J, Kieliszewski M (2001) Contiguous hydroxyproline residues direct hydroxyproline arabinosylation in Nicotiana tabacum. J Biol Chem 276: 11272–11278PubMedCrossRefGoogle Scholar
  49. Staehelin L (1997) The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J 11: 1151–1165PubMedCrossRefGoogle Scholar
  50. Takeuchi M, Tada M, Saito C, Yashiroda H, Nakano A (1998) Isolation of a tobacco cDNA encoding Sar1 GTPase and analysis of its dominant mutations in vesicular traffic using a yeast complementation system. Plant Cell Physiol 39: 590–599PubMedCrossRefGoogle Scholar
  51. Takeuchi M, Ueda T, Sato K, Abe H, Nagata T, A. N (2000) A dominant negative mutant of sar1 GTPase inhibits protein transport from the endoplasmic reticulum to the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J 23: 517–525PubMedCrossRefGoogle Scholar
  52. Takeuchi M, Ueda M, Yahara N, Nakano A (2002) Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J 31: 499–515PubMedCrossRefGoogle Scholar
  53. Toyooka K, Okamoto T, Minamikawa T (2000) Mass transport of proform of a KDEL-tailed cysteine proteinase (SH-EP) to protein storage vacuoles by endoplasmic reticulum-derived vesicle is involved in protein mobilization in germinating seeds. J Cell Biol 154: 973–982CrossRefGoogle Scholar
  54. Winicur Z, Zhang G, Staehelin L (1998) Auxin deprivation induces synchronous Golgi differentiation in suspension-cultured tobacco BY-2 cells. Plant Physiol 117: 501–513PubMedCrossRefGoogle Scholar
  55. Yasuhara H, Sonobe S, Shibaoka H (1995) Effects of brefeldin A on the formation of the cell plate in tobacco BY-2 cells. Eur J Cell Biol 66: 274–281PubMedGoogle Scholar
  56. Zhao Z, Tan L, Showalter A, Lamport D, Kieliszewski M (2002) Tomato LeAGP-1 arabinogalactanprotein purified from transgenic tobacco corroborates the Hyp contiguity hypothesis. Plant J 31: 431–444PubMedCrossRefGoogle Scholar
  57. Zheng H, von Mollard G, Kovaleva V, Stevens T, Raikhel N (1999) The plant vesicle-associated SNARE AtVTI1a likely mediates vesicle transport from the trans-Golgi network to the prevacuolar compartment. Mol Biol Cell 10: 2251–2264PubMedGoogle Scholar
  58. Zuo J, Niu Q, Nishizawa N, Wu Y, Kost B, Chua N (2000) KORRIGAN, an Arabidopsis endo-1,4-beta-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell 12: 1137–1152PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2004

Authors and Affiliations

  • Ken Matsuoka
    • 1
  1. 1.Plant Science Center RikenTsurumi-ku, YokohamaJapan

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