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The ER Folding Helpers: A Connection Between Protein Maturation, Stress Responses and Plant Development

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The Plant Endoplasmic Reticulum

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 4))

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Abstract

The main resident proteins of the endoplasmic reticulum (ER) collaborate to ensure that newlysynthesized secretory proteins acquire their correct conformation. Most ER residents are therefore,directly or indirectly, folding helpers and controllers of the quality of newly synthesized secretorypolypeptides. Genetic approaches have revealed that these helpers are necessary for virtually anymajor aspect of plant life, from differentiation to reproduction to interactions with the environment.Detailed biochemical analysis on the protein–protein interactions that occur during foldingin the ER has been performed on a number of model secretory proteins, and the integration betweengenetics and biochemistry is a major future goal of this field of plant cell biology.

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References

  1. Alder NN, Shen Y, Brodsky J, Hendershot LM, Johnson AE (2005) The molecular mechanisms underlying BiP-mediated gating of the Sec61 translocon of the endoplasmic reticulum. J Cell Biol 168:389–399

    Article  PubMed  CAS  Google Scholar 

  2. Altpeter F, Popelka JC, Wieser H (2004) Stable expression of 1Dx5 and 1Dy10 high-molecular-weight glutenin subunit genes in transgenic rye drastically increases the polymeric glutelin fraction in rye flour. Plant Mol Biol 54:783–792

    Article  PubMed  CAS  Google Scholar 

  3. Alvim FC, Carolino SM, Cascardo JC, Nunes CC, Martinez CA, Otoni WC, Fontes EP (2001) Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiol 126:1042–1054

    Article  PubMed  CAS  Google Scholar 

  4. Anderson JV, Li QB, Haskell DW, Guy CL (1994) Structural organization of the spinach endoplasmic reticulum-luminal 70-kilodalton heat-shock cognate gene and expression of 70-kilodalton heat-shock genes during cold acclimation. Plant Physiol 104:1359–1370

    Article  PubMed  CAS  Google Scholar 

  5. Argon Y, Simen BB (1999) GRP94, an ER chaperone with protein and peptide binding properties. Semin Cell Dev Biol 10:495–505

    Article  PubMed  CAS  Google Scholar 

  6. Ben-Zvi A, De Los Rios P, Dietler G, Goloubinoff P (2004) Active solubilization and refolding of stable protein aggregates by cooperative unfolding action of individual hsp70 chaperones. J Biol Chem 279:37298–37303

    Article  PubMed  CAS  Google Scholar 

  7. Blond-Elguindi S, Fourie AM, Sambrook JF, Gething MJ (1993a) Peptide-dependent stimulation of the ATPase activity of the molecular chaperone BiP is the result of conversion of oligomers to active monomers. J Biol Chem 268:12730–12735

    PubMed  CAS  Google Scholar 

  8. Blond-Elguindi S, Cwirla SE, Dower WJ, Lipshutz RJ, Sprang SR, Sambrook JF, Gething MJ (1993b) Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75:717–728

    Article  PubMed  CAS  Google Scholar 

  9. Boisson M, Gomord V, Audran C, Berger N, Dubreucq B, Granier F, Lerouge P, Faye L, Caboch M, Lepiniec L (2001) Arabidopsis glucosidase I mutants reveal a critical role of N-glycan trimming in seed development. EMBO J 20:1010–1019

    Article  PubMed  CAS  Google Scholar 

  10. Bollini R, Ceriotti A, Daminati MG, Vitale A (1985) Glycosylation is not needed for the intracellular transport of phytohemagglutinin in developing Phaseolus vulgaris cotyledons and for the maintenance of its biological activities. Physiol Plant 65:15–22

    Article  CAS  Google Scholar 

  11. Brandizzi F, Hanton S, DaSilva LL, Boevink P, Evans D, Oparka K, Denecke J, Hawes C (2003) ER quality control can lead to retrograde transport from the ER lumen to the cytosol and the nucleoplasm in plants. Plant J 34:269–281

    Article  PubMed  CAS  Google Scholar 

  12. Brodsky JL, Schekman R (1993) A Sec63p-BiP complex from yeast is required for protein translocation in a reconstituted proteoliposome. J Cell Biol 123:1355–1363

    Article  PubMed  CAS  Google Scholar 

  13. Brodsky JL, Hamamoto S, Feldheim D, Schekman R (1993) Reconstitution of protein translocation from solubilized yeast membranes reveals topologically distinct roles for BiP and cytosolic Hsc70. J Cell Biol 120:95–102

    Article  PubMed  CAS  Google Scholar 

  14. Brunati AM, Contri A, Muenchbach M, James P, Marin O, Pinna LA (2000) GRP94 (endoplasmin) co-purifies with and is phosphorylated by Golgi apparatus casein kinase. FEBS Lett 471:151–155

    Article  PubMed  CAS  Google Scholar 

  15. Burn JE, Hurley UA, Birch RJ, Arioli T, Cork A, Williamson RE (2002) The cellulose-deficient Arabidopsis mutant rsw3 is defective in a gene encoding a putative glucosidase II, an enzyme processing N-glycans during ER quality control. Plant J 32:949–960

    Article  PubMed  CAS  Google Scholar 

  16. Bustos MM, Kalkan FA, VandenBosch KA, Hall TC (1991) Differential accumulation of four phaseolin glycoforms in transgenic tobacco. Plant Mol Biol 16:381–395

    Article  PubMed  CAS  Google Scholar 

  17. Cascardo JC, Almeida RS, Buzeli RA, Carolino SM, Otoni WC, Fontes EP (2000) The phosphorylation state and expression of soybean BiP isoforms are differentially regulated following abiotic stresses. J Biol Chem 275:14494–14500

    Article  PubMed  CAS  Google Scholar 

  18. Ceriotti A, Roberts LM (2006) Endoplasmic Reticulum – Associated Protein Degradation in Plant Cells (in this volume). Springer, Berlin Heidelberg New York

    Google Scholar 

  19. Crofts AJ, Leborgne-Castel N, Pesca M, Vitale A, Denecke J (1998) BiP and calreticulin form an abundant complex that is independent of endoplasmic reticulum stress. Plant Cell 10:813–824

    PubMed  CAS  Google Scholar 

  20. Crofts AJ, Leborgne-Castel N, Hillmer S, Robinson DG, Phillipson B, Carlsson LE, Ashford DA, Denecke J (1999) Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. Plant Cell 11:2233–2247

    PubMed  CAS  Google Scholar 

  21. Crosti P, Malerba M, Bianchetti R (2001) Tunicamycin and brefeldin A induce in plant cells a programmed cell death showing apoptotic features. Protoplasma 216:31–38

    Article  PubMed  CAS  Google Scholar 

  22. Cyr DM, Langer T, Douglas MG (1994) DnaJ-like proteins: molecular chaperones and specific regulators of hsp70. Trends Biochem Sci 19:176–181

    Article  PubMed  CAS  Google Scholar 

  23. D'Amico L, Valsasina B, Daminati MG, Fabbrini MS, Nitti G, Bollini R, Ceriotti A, Vitale A (1992) Bean homologs of the mammalian glucose-regulated proteins: induction by tunicamycin and interaction with newly synthesized seed storage proteins in the endoplasmic reticulum. Plant J 2:443–455

    PubMed  Google Scholar 

  24. Denecke J, Goldman MH, Demolder J, Seurinck J, Botterman J (1991) The tobacco luminal binding protein is encoded by a multigene family. Plant Cell 3:1025–1035

    PubMed  CAS  Google Scholar 

  25. Denecke J, Carlsson LE, Vidal S, Hoglund AS, Ek B, van Zeijl MJ, Sinjorgo KM, Palva ET (1995) The tobacco homolog of mammalian calreticulin is present in protein complexes in vivo. Plant Cell 7:391–406

    PubMed  CAS  Google Scholar 

  26. Di Cola A, Frigerio L, Lord JM, Ceriotti A, Roberts LM (2001) Ricin A chain without its partner B chain is degraded after retrotranslocation from the endoplasmic reticulum to the cytosol in plant cells. Proc Natl Acad Sci USA 98:14726–14731

    Article  PubMed  Google Scholar 

  27. Di Cola A, Frigerio L, Lord JM, Roberts LM, Ceriotti A (2005) Endoplasmic reticulum-associated degradation of ricin A chain has unique and plant-specific features. Plant Physiol 137:287–296

    Article  PubMed  CAS  Google Scholar 

  28. Dixon DP, Van Lith M, Edwards R, Benham A (2003) Cloning and initial characterization of the Arabidopsis thaliana endoplasmic reticulum oxidoreductins. Antioxid Redox Signal 5:389–396

    Article  PubMed  CAS  Google Scholar 

  29. Doerner P (2000) Plant stem cells: the only constant thing is change. Curr Biol 10:R826–R829

    Article  PubMed  CAS  Google Scholar 

  30. Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4:181–191

    Article  PubMed  CAS  Google Scholar 

  31. Ellgaard L, Molinari M, Helenius A (1999) Setting the standards: quality control in the secretory pathway. Science 286:1882–1888

    Article  PubMed  CAS  Google Scholar 

  32. Fontes EB, Shank BB, Wrobel RL, Moose SP, Obrian GR, Wurtzel ET, Boston RS (1991) Characterization of an immunoglobulin binding protein homolog in the maize floury-2 endosperm mutant. Plant Cell 3:483–496

    PubMed  CAS  Google Scholar 

  33. Foresti O, Frigerio L, Holkeri H, de Virgilio M, Vavassori S, Vitale A (2003) A phaseolin domain involved directly in trimer assembly is a determinant for binding by the chaperone BiP. Plant Cell 15:2464–2475

    Article  PubMed  CAS  Google Scholar 

  34. Frand AR, Kaiser CA (2000) Two pairs of conserved cysteines are required for the oxidative activity of Ero1p in protein disulfide bond formation in the endoplasmic reticulum. Mol Biol Cell 11:2833–2843

    PubMed  CAS  Google Scholar 

  35. Gething MJ (1999) Role and regulation of the ER chaperone BiP. Semin Cell Dev Biol 10:465–472

    Article  PubMed  CAS  Google Scholar 

  36. Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45

    Article  PubMed  CAS  Google Scholar 

  37. Gething MJ, McCammon K, Sambrook J (1986) Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell 46:939–950

    Article  PubMed  CAS  Google Scholar 

  38. Gillikin JW, Zhang F, Coleman CE, Bass HW, Larkins BA, Boston RS (1997) A defective signal peptide tethers the floury-2 zein to the endoplasmic reticulum membrane. Plant Physiol 114:345–352

    Article  PubMed  CAS  Google Scholar 

  39. Gillmor CS, Poindexter P, Lorieau J, Palcic MM, Somerville C (2002) Alpha-glucosidase I is required for cellulose biosynthesis and morphogenesis in Arabidopsis. J Cell Biol 156:1003–1013

    Article  PubMed  CAS  Google Scholar 

  40. Goldberger RF, Epstein CJ, Anfinsen CB (1963) Acceleration of reactivation of reduced bovine pancreatic ribonuclease by a microsomal system from rat liver. J Biol Chem 238:628–635

    PubMed  CAS  Google Scholar 

  41. Haas IG, Wabl M (1983) Immunoglobulin heavy chain binding protein. Nature 306:387–389

    Article  PubMed  CAS  Google Scholar 

  42. Hadlington JL, Denecke J (2000) Sorting of soluble proteins in the secretory pathway of plants. Curr Opin Plant Biol 3:461–468

    Article  PubMed  CAS  Google Scholar 

  43. Hamman BD, Hendershot LM, Johnson AE (1998) BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell 92:747–758

    Article  PubMed  CAS  Google Scholar 

  44. Helenius A, Aebi M (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73:1019–1049

    Article  PubMed  CAS  Google Scholar 

  45. Hellman R, Vanhove M, Lejeune A, Stevens FJ, Hendershot LM (1999) The in vivo association of BiP with newly synthesized proteins is dependent on the rate and stability of folding and not simply on the presence of sequences that can bind to BiP. J Cell Biol 144:21–30

    Article  PubMed  CAS  Google Scholar 

  46. Hendershot L, Wei J, Gaut J, Melnick J, Aviel S, Argon Y (1996). Inhibition of immunoglobulin folding and secretion by dominant negative BiP ATPase mutants. Proc Natl Acad Sci USA 93:5269–5274

    CAS  Google Scholar 

  47. Hong E, Davidson A, Kaiser CA (1996) A pathway for targeting soluble misfolded proteins to the yeast vacuole. J Cell Biol 135:623–633

    Article  PubMed  CAS  Google Scholar 

  48. Hunter BG, Beatty MK, Singletary GW, Hamaker BR, Dilkes BP, Larkins BA, Jung R (2002) Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell 14:2591–2612

    Article  PubMed  CAS  Google Scholar 

  49. Hurtley SM, Helenius A (1989) Protein oligomerization in the endoplasmic reticulum. Annu Rev Cell Biol 5:277–307

    Article  PubMed  CAS  Google Scholar 

  50. Hurtley SM, Bole DG, Hoover-Litty H, Helenius A, Copeland CS (1989) Interactions of misfolded influenza virus hemagglutinin with binding protein (BiP). J Cell Biol 108:2117–2126

    Article  PubMed  CAS  Google Scholar 

  51. Immormino RM, Dollins DE, Shaffer PL, Soldano KL, Walker MA, Gewirth DT (2004) Ligand-induced conformational shift in the N-terminal domain of GRP94, an Hsp90 chaperone. J Biol Chem 279:46162–46171

    Article  PubMed  CAS  Google Scholar 

  52. Ishiguro S, Watanabe Y, Ito N, Nonaka H, Takeda N, Sakai T, Kanaya H, Okada K (2002) SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins. EMBO J 21:898–908

    Article  PubMed  CAS  Google Scholar 

  53. Jelitto-Van Dooren EP, Vidal S, Denecke J (1999) Anticipating endoplasmic reticulum stress. A novel early response before pathogenesis-related gene induction. Plant Cell 11:1935–1944

    PubMed  CAS  Google Scholar 

  54. Jorgensen MU, Emr SD, Winther JR (1999) Ligand recognition and domain structure of Vps10p, a vacuolar protein sorting receptor in Saccharomyces cerevisiae. Eur J Biochem 260:461–469

    Article  PubMed  CAS  Google Scholar 

  55. Kalinski A, Rowley DL, Loer DS, Foley C, Buta G, Herman EM (1995) Binding-protein expression is subject to temporal, developmental and stress-induced regulation in terminally differentiated soybean organs. Planta 195:611–621

    Article  PubMed  CAS  Google Scholar 

  56. Kawagoe Y, Suzuki K, Tasaki M, Yasuda H, Akagi K, Katoh E, Nishizawa NK, Ogawa M, Takaiwa F (2005) The critical role of disulfide bond formation in protein sorting in the endosperm of rice. Plant Cell 17:1141–1153

    Article  PubMed  CAS  Google Scholar 

  57. Kelleher DJ, Karaoglu D, Mandon EC, Gilmore R (2003) Oligosaccharyltransferase isoforms that contain different catalytic STT3 subunits have distinct enzymatic properties. Mol Cell 12:101–111

    Article  PubMed  CAS  Google Scholar 

  58. Kikuchi S et al. (2003) Collection, mapping, and annotation of over 28 000 cDNA clones from japonica rice: the rice full-length cDNA consortium. Science 301:376–379

    Article  PubMed  Google Scholar 

  59. Kim CS, Hunter BG, Kraft J, Boston RS, Yans S, Jung R, Larkins BA (2004) A defective signal peptide in a 19-kd α-zein protein causes the unfolded protein response and an opaque endosperm phenotype in the maize De∗-B30 mutant. Plant Physiol 134:380–387

    Article  PubMed  CAS  Google Scholar 

  60. Kleizen B, Braakman I (2004) Protein folding and quality control in the endoplasmic reticulum. Curr Opin Cell Biol 16:343–349

    Article  PubMed  CAS  Google Scholar 

  61. Koiwa H, Li F, McCully MG, Mendoza I, Koizumi N, Manabe Y, Nakagawa Y, Zhu J, Rus A, Pardo JM, Bressan RA, Hasegawa PM (2003) The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell 15:2273–2284

    Article  PubMed  CAS  Google Scholar 

  62. Koizumi N, Ujino T, Sano H, Chrispeels MJ (1999) Overexpression of a gene that encodes the first enzyme in the biosynthesis of asparagine-linked glycans makes plants resistant to tunicamycin and obviates the tunicamycin-induced unfolded protein response. Plant Physiol 121:353–361

    Article  PubMed  CAS  Google Scholar 

  63. Kozutsumi Y, Segal M, Normington K, Gething MJ, Sambrook J (1988) The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 332:462–464

    Article  PubMed  CAS  Google Scholar 

  64. Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238–246

    Article  PubMed  CAS  Google Scholar 

  65. Larreta R, Soto M, Alonso C, Requena JM (2000) Leishmania infantum: gene cloning of the GRP94 homologue, its expression as recombinant protein, and analysis of antigenicity. Exp Parasitol 96:108–115

    Article  PubMed  CAS  Google Scholar 

  66. Leborgne-Castel N, Jelitto-Van Dooren EP, Crofts AJ, Denecke J (1999) Overexpression of BiP in tobacco alleviates endoplasmic reticulum stress. Plant Cell 11:459–470

    PubMed  CAS  Google Scholar 

  67. Lee AS (2001) The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci 26:504–510

    Article  PubMed  CAS  Google Scholar 

  68. Lerouge P, Cabanes-Macheteau M, Rayon C, Fischette-Laine AC, Gomord V, Faye L (1998) N-Glycoprotein biosynthesis in plants: recent developments and future trends. Plant Mol Biol 38:31–48

    Article  PubMed  CAS  Google Scholar 

  69. Lerouxel O, Mouille G, Andeme-Onzighi C, Bruyant MP, Seveno M, Loutelier-Bourhis C, Driouich A, Hofte H, Lerouge P (2005) Mutants in DEFECTIVE GLYCOSYLATION, an Arabidopsis homolog of an oligosaccharyltransferase complex subunit, show protein underglycosylation and defects in cell differentiation and growth. Plant J 42:455–468

    Article  PubMed  CAS  Google Scholar 

  70. Levitan A, Trebitsh T, Kiss V, Pereg Y, Dangoor I, Danon A (2005) Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum. Proc Natl Acad Sci USA 102:6225–6230

    Article  PubMed  CAS  Google Scholar 

  71. Li X, Su RT, Hsu HT, Sze H (1998) The molecular chaperone calnexin associates with the vacuolar H+-ATPase from oat seedlings. Plant Cell 10:119–130

    PubMed  CAS  Google Scholar 

  72. Lupattelli F, Pedrazzini E, Bollini R, Vitale A, Ceriotti A (1997) The rate of phaseolin assembly is controlled by the glucosylation state of its N-linked oligosaccharide chains. Plant Cell 9:597–609

    PubMed  CAS  Google Scholar 

  73. Lyman SK, Schekman R (1995) Interaction between BiP and Sec63p is required for the completion of protein translocation into the ER of Saccharomyces cerevisiae. J Cell Biol 131:1163–1171

    Article  PubMed  CAS  Google Scholar 

  74. Lyman SK, Schekman R (1997) Binding of secretory precursor polypeptides to a translocon subcomplex is regulated by BiP. Cell 88:85–96

    Article  PubMed  CAS  Google Scholar 

  75. Mainieri D, Rossi M, Archinti M, Bellucci M, De Marchis F, Vavassori S, Pompa A, Arcioni S, Vitale A (2004) Zeolin. A new recombinant storage protein constructed using maize γ-zein and bean phaseolin. Plant Physiol 136:3447–3456

    Article  PubMed  CAS  Google Scholar 

  76. Mariani P, Navazio L, Zuppini A (2003) Calreticulin and the endoplasmic reticulum in plant biology. In: Eggleton P, Michalak M (eds) Calreticulin, 2nd ed. Eurekah.com and Kluwer/Plenum, New York, pp 94–104

    Chapter  Google Scholar 

  77. Marocco A, Santucci A, Cerioli S, Motto M, Di Fonzo N, Thompson R, Salamini F (1991) Three high-lysine mutations control the level of ATP-binding HSP70-like proteins in maize endosperm. Plant Cell 3:507–515

    PubMed  CAS  Google Scholar 

  78. Matlack KE, Misselwitz B, Plath K, Rapoport TA (1999) BiP acts as a molecular ratchet during posttranslational transport of prepro-alpha factor across the ER membrane. Cell 97:553–564

    Article  PubMed  CAS  Google Scholar 

  79. Mayer U, Torres-Ruiz RA, Berleth T, Miséra S, Jürgens G (1991) Mutations affecting body organization in the Arabidopsis embryo. Nature 353:402–407

    Article  Google Scholar 

  80. McCracken AA, Brodsky JL (2003) Evolving questions and paradigm shifts in endoplasmic-reticulum-associated degradation (ERAD). Bioessays 25:868–877

    Article  PubMed  CAS  Google Scholar 

  81. Melnick J, Dul JL, Argon Y (1994) Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 370:373–375

    Article  PubMed  CAS  Google Scholar 

  82. Muench DG, Wu Y, Zhang Y, Li X, Boston RS, Okita TW (1997) Molecular cloning, expression and subcellular localization of a BiP homolog from rice endosperm tissue. Plant Cell Physiol 38:404–412

    Article  PubMed  CAS  Google Scholar 

  83. Muller J, Piffanelli P, Devoto A, Miklis M, Elliott C, Ortmann B, Schulze-Lefert P, Panstruga R (2005) Conserved ERAD-like quality control of a plant polytopic membrane protein. Plant Cell 17:149–163

    Article  PubMed  CAS  Google Scholar 

  84. Munro S, Pelham HR (1986) An hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46:291–300

    Article  PubMed  CAS  Google Scholar 

  85. Nicchitta CV, Blobel G (1993) Lumenal proteins of the mammalian endoplasmic reticulum are required to complete protein translocation. Cell 73:989–998

    Article  PubMed  CAS  Google Scholar 

  86. Nishikawa S, Hirata A, Nakano A (1994) Inhibition of endoplasmic reticulum (ER)-to-Golgi transport induces relocalization of binding protein (BiP) within the ER to form the BiP bodies. Mol Biol Cell 5:1129–1143

    PubMed  CAS  Google Scholar 

  87. Noh SJ, Kwon CS, Oh DH, Moon JS, Chung WI (2003) Expression of an evolutionarily distinct novel BiP gene during the unfolded protein response in Arabidopsis thaliana. Gene 311:81–91

    Article  PubMed  CAS  Google Scholar 

  88. Nuttall J, Vine N, Hadlington JL, Drake P, Frigerio L, Ma JK (2002) ER-resident chaperone interactions with recombinant antibodies in transgenic plants. Eur J Biochem 269:6042–6051

    Article  PubMed  CAS  Google Scholar 

  89. Orsi A, Sparvoli F, Ceriotti A (2001) Role of individual disulfide bonds in the structural maturation of a low molecular weight glutenin subunit. J Biol Chem 276:32322–32329

    Article  PubMed  CAS  Google Scholar 

  90. 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 44:173–182

    Article  PubMed  CAS  Google Scholar 

  91. Parinov S, Sevugan M, Ye D, Yang WC, Kumaran M, Sundaresan V (1999) Analysis of flanking sequences from dissociation insertion lines: a database for reverse genetics in Arabidopsis. Plant Cell 11:2263–2270

    PubMed  CAS  Google Scholar 

  92. Pedrazzini E, Giovinazzo G, Bielli A, de Virgilio M, Frigerio L, Pesca M, Faoro F, Bollini R, Ceriotti A, Vitale A (1997) Protein quality control along the route to the plant vacuole. Plant Cell 9:1869–1880

    PubMed  CAS  Google Scholar 

  93. Persson S, Harper J (2006) The ER and Cell Calcium (in this volume). Springer, Berlin Heidelberg New York

    Google Scholar 

  94. Persson S, Wyatt SE, Love J, Thompson WF, Robertson D, Boss WF (2001) The Ca2+ status of the endoplasmic reticulum is altered by induction of calreticulin expression in transgenic plants. Plant Physiol 126:1092–1104

    Article  PubMed  CAS  Google Scholar 

  95. Phillipson BA, Pimpl P, daSilva LL, Crofts AJ, Taylor JP, Movafeghi A, Robinson DG, Denecke J (2001) Secretory bulk flow of soluble proteins is COPII dependent. Plant Cell 13:2005–2020

    PubMed  CAS  Google Scholar 

  96. Pimpl P, Movafeghi A, Coughlan S, Denecke J, Hillmer S, Robinson DG (2000) In situ localization and in vitro induction of plant COPI-coated vesicles. Plant Cell 12:2219–2236

    PubMed  CAS  Google Scholar 

  97. Pouyssegur J, Shiu RP, Pastan I (1977) Induction of two transformation-sensitive membrane polypeptides in normal fibroblasts by a block in glycoprotein synthesis or glucose deprivation. Cell 11:941–947

    Article  PubMed  CAS  Google Scholar 

  98. Randall JJ, Sutton DW, Hanson SF, Kemp JD (2005) BiP and zein binding domains within the delta zein protein. Planta 221:656–666

    Article  PubMed  CAS  Google Scholar 

  99. Ray S, Anderson JM, Urmeev FI, Goodwin SB (2003) Rapid induction of a protein disulfide isomerase and defense-related genes in wheat in response to the hemibiotrophic fungal pathogen Mycosphaerella graminicola. Plant Mol Biol 53:701–14

    Article  PubMed  CAS  Google Scholar 

  100. Rosser MF, Trotta BM, Marshall MR, Berwin B, Nicchitta CV (2004) Adenosine nucleotides and the regulation of GRP94–client protein interactions. Biochemistry 43:8835–8845

    Article  PubMed  CAS  Google Scholar 

  101. Rutkowski DT, Kaufman RJ (2004) A trip to the ER: coping with stress. Trends Cell Biol 14:20–28

    Article  PubMed  CAS  Google Scholar 

  102. Shimoni Y, Zhu XZ, Levanony H, Segal G, Galili G (1995) Purification, characterization, and intracellular localization of glycosylated protein disulfide isomerase from wheat grains. Plant Physiol 108:327–335

    Article  PubMed  CAS  Google Scholar 

  103. Schmitz A, Herzog V (2004) Endoplasmic reticulum-associated degradation: exceptions to the rule. Eur J Cell Biol 83:501–509

    Article  PubMed  Google Scholar 

  104. Semenza JC, Hardwick KG, Dean N, Pelham HR (1990) ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61:1349–1357

    Article  PubMed  CAS  Google Scholar 

  105. Shewry PR, Napier JA, Tatham AS (1995) Seed storage proteins: structures and biosynthesis. Plant Cell 7:945–956

    PubMed  CAS  Google Scholar 

  106. Shorrosh BS, Dixon RA (1991) Molecular cloning of a putative plant endomembrane protein resembling vertebrate protein disulfide-isomerase and a phosphatidylinositol-specific phospholipase C. Proc Natl Acad Sci USA 88:10941–10945

    Article  PubMed  CAS  Google Scholar 

  107. Sparvoli F, Faoro F, Daminati MG, Ceriotti A, Bollini R (2000) Misfolding and aggregation of vacuolar glycoproteins in plant cells. Plant J 24:825–836

    Article  PubMed  CAS  Google Scholar 

  108. Takemoto Y, Coughlan SJ, Okita TW, Satoh H, Ogawa M, Kumamaru T (2002) The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiol 128:1212–1222

    Article  PubMed  CAS  Google Scholar 

  109. Tamura K, Yamada K, Shimada T, Hara-Nishimura I (2004) Endoplasmic reticulum-resident proteins are constitutively transported to vacuoles for degradation. Plant J 39:393–402

    Article  PubMed  CAS  Google Scholar 

  110. Taylor MA, Ross HA, McRae D, Stewart D, Roberts I, Duncan G, Wright F, Millam S, Davies HV (2000) A potato α-glucosidase gene encodes a glycoprotein-processing α-glucosidase II-like activity: demonstration of enzyme activity and effects of down-regulation in transgenic plants. Plant J 24:305–316

    Article  PubMed  CAS  Google Scholar 

  111. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Google Scholar 

  112. Vitale A (2001) Uncovering secretory secrets: inhibition of endoplasmic reticulum (ER) glucosidases suggests a critical role for ER quality control in plant growth and development. Plant Cell 13:1260–1262

    PubMed  CAS  Google Scholar 

  113. Vitale A, Bielli A, Ceriotti A (1995) The binding protein associates with monomeric phaseolin. Plant Physiol 107:1411–1418

    PubMed  CAS  Google Scholar 

  114. Vitale A, Ceriotti A (2004) Protein quality control mechanisms and protein storage in the endoplasmic reticulum. A conflict of interests? Plant Physiol 136:3420–3426

    Article  PubMed  CAS  Google Scholar 

  115. Vitale A, Denecke J (1999) The endoplasmic reticulum—gateway of the secretory pathway. Plant Cell 11:615–628

    PubMed  CAS  Google Scholar 

  116. Vogel JP, Misra LM, Rose MD (1990) Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast. J Cell Biol 110:1885–1895

    Article  PubMed  CAS  Google Scholar 

  117. von Schaewen A, Sturm A, O'Neill J, Chrispeels MJ (1993) Isolation of a mutant Arabidopsis plant that lacks N-acetyl glucosaminyl transferase I and is unable to synthesize Golgi-modified complex N-linked glycans. Plant Physiol 102:1109–1118

    Article  Google Scholar 

  118. Walther-Larsen H, Brandt J, Collinge DB, Thordal-Christensen H (1993) A pathogen-induced gene of barley encodes an HSP90 homologue showing striking similarity to vertebrate forms resident in the endoplasmic reticulum. Plant Mol Biol 21:1097–1108

    Article  PubMed  CAS  Google Scholar 

  119. Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040

    Article  PubMed  CAS  Google Scholar 

  120. Wick P, Gansel X, Oulevey C, Page V, Studer I, Durst M, Sticher L (2003) The expression of the t-SNARE AtSNAP33 is induced by pathogens and mechanical stimulation. Plant Physiol 132:343–351

    Article  PubMed  CAS  Google Scholar 

  121. Young BP, Craven RA, Reid PJ, Willer M, Stirling CJ (2001) Sec63p and Kar2p are required for the translocation of SRP-dependent precursors into the yeast endoplasmic reticulum in vivo. EMBO J 20:262–271

    Article  PubMed  CAS  Google Scholar 

  122. Zhang F, Boston RS (1992) Increases in binding protein (BiP) accompany changes in protein body morphology in three high-lysine mutants of maize. Protoplasma 171:142–152

    Article  CAS  Google Scholar 

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Acknowledgments

The hard work, critical discussion and dedication of past and present students as well as post-doctoral fellows is gratefully acknowledged. We also wish to thank the many other colleagues with whom we have discussed over recent years the issues covered in this review. This work was supported in part by Research Training Networks contract HPRN-CT-2002-00262 (Biointeractions) of the European Union.

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Authors and Affiliations

  1. Istituto di Biologia e Biotecnologia Agraria, Consiglio Nazionale delle Ricerche, via Bassini 15, 20129, Milano, Italy

    Alessandro Vitale

  2. Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, LS2 9JT, Leeds, UK

    Jürgen Denecke

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  1. Alessandro Vitale
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  2. Jürgen Denecke
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Correspondence to Alessandro Vitale .

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David G. Robinson

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Vitale, A., Denecke, J. (2006). The ER Folding Helpers: A Connection Between Protein Maturation, Stress Responses and Plant Development. In: Robinson, D.G. (eds) The Plant Endoplasmic Reticulum. Plant Cell Monographs, vol 4. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_065

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