Protein Quality Control in the Endoplasmic Reticulum of Plants

Annual Review of Plant Biology

Volumn 69, Issue , 2018, Pages 147-172

  Strasser, Richard ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

Endoplasmic reticulum associated degradation; ERAD; ERQC; Glycoprotein; Glycosylation; Protein folding

Indexed keywords

PLANT PROTEIN; POLYSACCHARIDE;

ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; METABOLISM; PLANT; PROTEIN FOLDING;

ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; PLANT PROTEINS; PLANTS; POLYSACCHARIDES; PROTEIN FOLDING;

EID: 85046727833     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-042817-040331     Document Type: Review

References (157)

1. Aebi M. 2013. N-linked protein glycosylation in the ER. Biochim. Biophys. Acta 1833:2430-37
2. Andème Ondzighi C, Christopher D, Cho E, Chang S, Staehelin L. 2008. Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds. Plant Cell 20:2205-20
3. Apweiler R, Hermjakob H, SharonN. 1999. On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473:4-8
4. Avezov E, Frenkel Z, Ehrlich M, Herscovics A, Lederkremer G. 2008. Endoplasmic reticulum (ER) mannosidase I is compartmentalized and required for N-glycan trimming to Man5-6GlcNAc2 in glycoprotein ER-associated degradation. Mol. Biol. Cell 19:216-25
5. Baer J, Taylor I, Walker JC. 2016. Disrupting ER-associated protein degradation suppresses the abscission defect of a weak hae hsl2 mutant in Arabidopsis. J. Exp. Bot. 67:5473-84
6. Balchin D, Hayer-HartlM, Hartl FU. 2016. In vivo aspects of protein folding and quality control. Science 353:aac4354
7. Baldridge RD, Rapoport TA. 2016. Autoubiquitination of the Hrd1 ligase triggers protein retrotranslocation in ERAD. Cell 166:394-407
8. Benyair R, Ogen-Shtern N, Mazkereth N, Shai B, Ehrlich M, Lederkremer GZ. 2015. Mammalian ER mannosidase I resides in quality control vesicles, where it encounters its glycoprotein substrates. Mol. Biol. Cell 26:172-84
9. Bies C, Blum R, Dudek J, Nastainczyk W, Oberhauser S, et al. 2004. Characterization of pancreatic ERj3p, a homolog of yeast DnaJ-like protein Scj1p. Biol. Chem. 385:389-95
10. Blanco-Herrera F, Moreno AA, Tapia R, Reyes F, Araya M, et al. 2015. The UDP-glucose: Glycoprotein glucosyltransferase (UGGT), a key enzyme in ER quality control, plays a significant role in plant growth as well as biotic and abiotic stress in Arabidopsis thaliana. BMC Plant Biol. 15:127
11. BoissonM, Gomord V, Audran C, Berger N, Dubreucq B, et al. 2001. Arabidopsis glucosidase I mutants reveal a critical role of N-glycan trimming in seed development. EMBO J. 20:1010-19
12. Brandizzi F, Hanton S, DaSilva L, Boevink P, Evans D, et al. 2003. ER quality control can lead to retrograde transport from the ER lumen to the cytosol and the nucleoplasm in plants. Plant J. 34:269-81
13. Bukau B, Weissman J, Horwich A. 2006. Molecular chaperones and protein quality control. Cell 125:443-51
14. Caramelo J, Parodi A. 2008. Getting in and out from calnexin/calreticulin cycles. J. Biol. Chem. 283:10221-25
15. Chaiwanon J, Garcia VJ, Cartwright H, Sun Y, Wang ZY. 2016. Immunophilin-like FKBP42/ TWISTED DWARF1 interacts with the receptor kinase BRI1 to regulate brassinosteroid signaling in Arabidopsis. Mol. Plant 9:593-600
16. Chen Q, Liu R, Wang Q, Xie Q. 2017. ERAD tuning of the HRD1 complex component AtOS9 is modulated by an ER-bound E2, UBC32. Mol. Plant 10:891-94
17. Chen Q, Zhong Y, Wu Y, Liu L, Wang P, et al. 2016. HRD1-mediated ERAD tuning of ERbound E2 is conserved between plants and mammals. Nat. Plants 2:16094
18. Chong LP, Wang Y, Gad N, Anderson N, Shah B, Zhao R. 2015. A highly charged region in the middle domain of plant endoplasmic reticulum (ER)-localized heat-shock protein 90 is required for resistance to tunicamycin or high calcium-induced ER stresses. J. Exp. Bot. 66:113-24
19. Christensen A, Svensson K, Thelin L, ZhangW, Tintor N, et al. 2010. Higher plant calreticulins have acquired specialized functions in Arabidopsis. PLOS ONE 5:e11342
20. Clerc S, Hirsch C, Oggier D, Deprez P, Jakob C, et al. 2009. Htm1 protein generates the Nglycan signal for glycoprotein degradation in the endoplasmic reticulum. J. Cell Biol. 184:159-72
21. Crofts AJ, Leborgne-CastelN, Pesca M, Vitale A, Denecke J. 1998. BiP and calreticulin form an abundant complex that is independent of endoplasmic reticulum stress. Plant Cell 10:813-24
22. Cui F, Liu L, Zhao Q, Zhang Z, Li Q, et al. 2012. Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance. Plant Cell 24:233-44
23. D'Alessio C, Dahms NM. 2015. Glucosidase II and MRH-domain containing proteins in the secretory pathway. Curr. Protein Pept. Sci. 16:31-48
24. de Oliveira MVV, Xu G, Li B, de Souza Vespoli L, Meng X, et al. 2016. Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation. Nat. Plants 2:15218
25. Dejgaard K, Theberge JF, Heath-Engel H, Chevet E, Tremblay ML, Thomas DY. 2010. Organization of the Sec61 translocon, studied by high resolution native electrophoresis. J. Proteome Res. 9:1763-71
26. Denecke J, Goldman M, Demolder J, Seurinck J, Botterman J. 1991. The tobacco luminal binding protein is encoded by a multigene family. Plant Cell 3:1025-35
27. Denic V, Quan EM, Weissman JS. 2006. A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation. Cell 126:349-59
28. Deprez P, Gautschi M, Helenius A. 2005. More than one glycan is needed for ER glucosidase II to allow entry of glycoproteins into the calnexin/calreticulin cycle. Mol. Cell 19:183-95
29. Di Cola A, Frigerio L, Lord J, Ceriotti A, Roberts L. 2001. Ricin A chain without its partner B chain is degraded after retrotranslocation from the endoplasmic reticulum to the cytosol in plant cells. PNAS 98:14726-31
30. Doblas VG, Amorim-Silva V, Posé D, Rosado A, Esteban A, et al. 2013. The SUD1 gene encodes a putative E3 ubiquitin ligase and is a positive regulator of 3-hydroxy-3-methylglutaryl coenzyme A reductase activity in Arabidopsis. Plant Cell 25:728-43
31. Dunkley T, Hester S, Shadforth I, Runions J, Weimar T, et al. 2006. Mapping the Arabidopsis organelle proteome. PNAS 103:6518-23
32. Farid A, Malinovsky FG, Veit C, Schoberer J, Zipfel C, Strasser R. 2013. Specialized roles of the conserved subunit OST3/6 of the oligosaccharyltransferase complex in innate immunity and tolerance to abiotic stresses. Plant Physiol. 162:24-38
33. Farid A, Pabst M, Schoberer J, Altmann F, Glössl J, Strasser R. 2011. Arabidopsis thaliana α1, 2-glucosyltransferase (ALG10) is required for efficient N-glycosylation and leaf growth. Plant J. 68:314-25
34. Ferris SP, JaberNS, MolinariM, Arvan P, Kaufman RJ. 2013. UDP-glucose:glycoprotein glucosyltransferase (UGGT1) promotes substrate solubility in the endoplasmic reticulum. Mol. Biol. Cell 24:2597-608
35. ForestiO, FrigerioL, 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 15:2464-75
36. Frenkel Z, Gregory W, Kornfeld S, Lederkremer G. 2003. Endoplasmic reticulum-associated degradation of mammalian glycoproteins involves sugar chain trimming to Man6-5GlcNAc2. J. Biol. Chem. 278:34119-24
37. Fujimori T, Suno R, Iemura SI, Natsume T, WadaI, Hosokawa N. 2017. Endoplasmic reticulum proteins SDF2 and SDF2L1 act as components of the BiP chaperone cycle to prevent protein aggregation. Genes Cells 22:684-98
38. Gao M, Wang X, Wang D, Xu F, Ding X, et al. 2009. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6:34-44
39. Gauss R, Kanehara K, Carvalho P, Ng DT, Aebi M. 2011. A complex of Pdi1p and the mannosidase Htm1p initiates clearance of unfolded glycoproteins from the endoplasmic reticulum. Mol. Cell 42:782-93
40. Gillmor C, Poindexter P, Lorieau J, Palcic M, Somerville C. 2002. α-glucosidase I is required for cellulose biosynthesis and morphogenesis in Arabidopsis. J. Cell Biol. 156:1003-13
41. Hagiwara M, Ling J, Koenig PA, Ploegh HL. 2016. Posttranscriptional regulation of glycoprotein quality control in the endoplasmic reticulum is controlled by the E2 Ub-conjugating enzyme UBC6e. Mol. Cell 63:753-67
42. Hanson SR, Culyba EK, Hsu TL, Wong CH, Kelly JW, Powers ET. 2009. The core trisaccharide of an N-linked glycoprotein intrinsically accelerates folding and enhances stability. PNAS 106:3131-36
43. Häweker H, Rips S, Koiwa H, Salomon S, Saijo Y, et al. 2010. Pattern recognition receptors require N-glycosylation to mediate plant immunity. J. Biol. Chem. 285:4629-36
44. Helenius A. 1994. How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticulum. Mol. Biol. Cell 5:253-65
45. Helenius A, Aebi M. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73:1019-49
46. Hirsch C, Gauss R, Horn SC, Neuber O, Sommer T. 2009. The ubiquitylation machinery of the endoplasmic reticulum. Nature 458:453-60
47. Hong Z, JinH, Fitchette A, Xia Y, Monk A, et al. 2009. Mutations of anα1, 6mannosyltransferase inhibit endoplasmic reticulum-associated degradation of defective brassinosteroid receptors in Arabidopsis. Plant Cell 21:3792-802
48. Hong Z, Jin H, Tzfira T, Li J. 2008. Multiple mechanism-mediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell 20:3418-29
49. Hong Z, Kajiura H, Su W, Jin H, Kimura A, et al. 2012. Evolutionarily conserved glycan signal to degrade aberrant brassinosteroid receptors in Arabidopsis. PNAS 109:11437-42
50. Horn SC, Hanna J, Hirsch C, Volkwein C, Schütz A, et al. 2009. Usa1 functions as a scaffold of the HRD-ubiquitin ligase. Mol. Cell 36:782-93
51. Hosokawa N, Tremblay LO, Sleno B, Kamiya Y, Wada I, et al. 2010. EDEM1 accelerates the trimming of α1, 2-linked mannose on the C branch of N-glycans. Glycobiology 20:567-75
52. Houck SA, RenHY, MaddenVJ, Bonner JN, Conlin MP, et al. 2014. Quality control autophagy degrades soluble ERAD-resistant conformers of the misfolded membrane protein GnRHR. Mol. Cell 54:166-79
53. Howell SH. 2013. Endoplasmic reticulum stress responses in plants. Annu. Rev. Plant Biol. 64:477-99
54. Hüttner S, Veit C, Schoberer J, Grass J, Strasser R. 2012. Unraveling the function of Arabidopsis thaliana OS9 in the endoplasmic reticulum-associated degradation of glycoproteins. Plant Mol. Biol. 79:21-33
55. Hüttner S, Veit C, Vavra U, Schoberer J, Dicker M, et al. 2014. A context-independent N-glycan signal targets the misfolded extracellular domain of Arabidopsis STRUBBELIG to endoplasmic-reticulumassociated degradation. Biochem. J. 464:401-11
56. Hüttner S, Veit C, Vavra U, Schoberer J, Liebminger E, et al. 2014. Arabidopsis class I α-mannosidases MNS4 and MNS5 are involved in endoplasmic reticulum-associated degradation of misfolded glycoproteins. Plant Cell 26:1712-28
57. Hwang J, Walczak CP, Shaler TA, Olzmann JA, Zhang L, et al. 2017. Characterization of protein complexes of the endoplasmic reticulum-associated degradation E3 ubiquitin ligase Hrd1. J. Biol. Chem. 292:9104-16
58. Ihara Y, Cohen-Doyle MF, Saito Y, Williams DB. 1999. Calnexin discriminates between protein conformational states and functions as a molecular chaperone in vitro. Mol. Cell 4:331-41
59. Ishiguro S, Watanabe Y, Ito N, Nonaka H, Takeda N, et al. 2002. SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins. EMBO J. 21:898-908
60. Jakob C, Burda P, Roth J, Aebi M. 1998. Degradation ofmisfolded endoplasmic reticulum glycoproteins in Saccharomyces cerevisiae is determined by a specific oligosaccharide structure. J. Cell Biol. 142:1223-33
61. Jeong IS, Lee S, Bonkhofer F, Tolley J, Fukudome A, et al. 2018. Purification and characterization of Arabidopsis thaliana oligosaccharyltransferase complexes from the native host: a protein super-expression system for structural studies. Plant J. 94:131-45
62. Jin H, Hong Z, Su W, Li J. 2009. A plant-specific calreticulin is a key retention factor for a defective brassinosteroid receptor in the endoplasmic reticulum. PNAS 106:13612-17
63. Jin H, Yan Z, Nam K, Li J. 2007. Allele-specific suppression of a defective brassinosteroid receptor reveals a physiological role of UGGT in ER quality control. Mol. Cell 26:821-30
64. Jin Y, Zhuang M, Hendershot LM. 2009. ERdj3, a luminal ER DnaJ homologue, binds directly to unfolded proteins in the mammalian ER: identification of critical residues. Biochemistry 48:41-49
65. Kamauchi S, Nakatani H, Nakano C, Urade R. 2005. Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J. 272:3461-76
66. Kelleher D, Gilmore R. 2006. An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16:47R-62R
67. Kim JH, Nguyen NH, Nguyen NT, Hong SW, Lee H. 2013. Loss of all three calreticulins, CRT1, CRT2 and CRT3, causes enhanced sensitivity to water stress in Arabidopsis. Plant Cell Rep. 32:1843-53
68. Kirst ME, Meyer DJ, Gibbon BC, Jung R, Boston RS. 2005. Identification and characterization of endoplasmic reticulum-associated degradation proteins differentially affected by endoplasmic reticulum stress. Plant Physiol. 138:218-31
69. Klein EM, Mascheroni L, Pompa A, Ragni L, Weimar T, et al. 2006. Plant endoplasmin supports the protein secretory pathway and has a role in proliferating tissues. Plant J. 48:657-73
70. Koiwa H, Li F, McCully M, Mendoza I, Koizumi N, et al. 2003. The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell 15:2273-84
71. Kozlov G, Mu ñoz-Escobar J, Castro K, Gehring K. 2017. Mapping the ER interactome: the P domains of calnexin and calreticulin as plurivalent adapters for foldases and chaperones. Structure 25:1415-22
72. Kozlov G, Pocanschi CL, Rosenauer A, Bastos-Aristizabal S, Gorelik A, et al. 2010. Structural basis of carbohydrate recognition by calreticulin. J. Biol. Chem. 285:38612-20
73. Kreibich G, Ulrich BL, SabatiniDD. 1978. Proteins of roughmicrosomal membranes related to ribosome binding. I. Identification of ribophorins I and II, membrane proteins characteristics of roughmicrosomes. J. Cell Biol. 77:464-87
74. Kumari S, Roy S, Singh P, Singla-Pareek SL, Pareek A. 2013. Cyclophilins: proteins in search of function. Plant Signal. Behav. 8:e22734
75. Lamriben L, Graham JB, Adams BM, Hebert DN. 2016. N-glycan-based ER molecular chaperone and protein quality control system: the calnexin binding cycle. Traffic 17:308-26
76. Lerouxel O, Mouille G, Andème-Onzighi C, BruyantM, SévenoM, et al. 2005. Mutants inDEFECTIVE GLYCOSYLATION, an Arabidopsis homolog of an oligosaccharyltransferase complex subunit, show protein underglycosylation and defects in cell differentiation and growth. Plant J. 42:455-68
77. Li J, Zhao-Hui C, Batoux M, Nekrasov V, Roux M, et al. 2009. Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. PNAS 106:15973-78
78. Li LM, Lü SY, Li RJ. 2017. The Arabidopsis endoplasmic reticulum associated degradation pathways are involved in the regulation of heat stress response. Biochem. Biophys. Res. Commun. 487:362-67
79. Li Q, Wei H, Liu L, Yang X, Zhang X, Xie Q. 2017. Unfolded protein response activation compensates endoplasmic reticulum-associated degradation deficiency in Arabidopsis. J. Integr. Plant Biol. 59:506-21
80. Liebminger E, Hüttner S, Vavra U, Fischl R, Schoberer J, et al. 2009. Class I α-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana. Plant Cell 21:3850-67
81. Liu L, Cui F, Li Q, Yin B, Zhang H, et al. 2011. The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance. Cell Res. 21:957-69
82. Liu Y, Burgos JS, Deng Y, Srivastava R, Howell SH, Bassham DC. 2012. Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis. Plant Cell 24:4635-51
83. Liu Y, Li J. 2013. A conserved basic residue cluster is essential for the protein quality control function of the Arabidopsis calreticulin 3. Plant Signal. Behav. 8:e23864
84. Liu Y, Zhang C, Wang D, Su W, Liu L, et al. 2015. EBS7 is a plant-specific component of a highly conserved endoplasmic reticulum-associated degradation system in Arabidopsis. PNAS 112:12205-10
85. Liu YC, Fujimori DG, Weissman JS. 2016. Htm1p-Pdi1p is a folding-sensitive mannosidase that marks N-glycoproteins for ER-associated protein degradation. PNAS 113:E4015-24
86. Loibl M, Wunderle L, Hutzler J, Schulz BL, Aebi M, Strahl S. 2014. Protein O-mannosyltransferases associate with the translocon to modify translocating polypeptide chains. J. Biol. Chem. 289:8599-611
87. Lü S, ZhaoH, Des Marais DL, ParsonsEP, WenX, et al. 2012. ArabidopsisECERIFERUM9involvement in cuticle formation and maintenance of plant water status. Plant Physiol. 159:930-44
88. Luan S, Kudla J, Gruissem W, Schreiber SL. 1996. Molecular characterization of a FKBP-type immunophilin from higher plants. PNAS 93:6964-69
89. Ma ZX, Leng YJ, Chen GX, Zhou PM, Ye D, Chen LQ. 2015. The THERMOSENSITIVE MALE STERILE 1 interacts with the BiPs via DnaJ domain and stimulates their ATPase enzyme activities in Arabidopsis. PLOS ONE 10:e0132500
90. Marshall RS, Jolliffe NA, Ceriotti A, Snowden CJ, Lord JM, et al. 2008. The role of CDC48 in the retro-translocation of non-ubiquitinated toxin substrates in plant cells. J. Biol. Chem. 283:15869-77
91. Martínez I, ChrispeelsM. 2003. Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 15:561-76
92. Maruyama D, Endo T, Nishikawa S. 2010. BiP-mediated polar nuclei fusion is essential for the regulation of endosperm nuclei proliferation in Arabidopsis thaliana. PNAS 107:1684-89
93. Maruyama D, Sugiyama T, Endo T, Nishikawa S. 2014. Multiple BiP genes of Arabidopsis thaliana are required for male gametogenesis and pollen competitiveness. Plant Cell Physiol. 55:801-10
94. Mehnert M, Sommer T, Jarosch E. 2014. Der1 promotes movement of misfolded proteins through the endoplasmic reticulum membrane. Nat. Cell Biol. 16:77-86
95. Meunier L, Usherwood YK, Chung KT, Hendershot LM. 2002. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell 13:4456-69
96. Mohorko E, Glockshuber R, Aebi M. 2011. Oligosaccharyltransferase: the central enzyme of N-linked protein glycosylation. J. Inherit. Metab. Dis. 34:869-78
97. MolinariM, Calanca V, Galli C, Lucca P, Paganetti P. 2003. Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299:1397-400
98. MolinariM, Galli C, Vanoni O, Arnold SM, Kaufman RJ. 2005. Persistent glycoprotein misfolding activates the glucosidase II/UGT1-driven calnexin cycle to delay aggregation and loss of folding competence. Mol. Cell 20:503-12
99. Müller J, Piffanelli P, Devoto A, Miklis M, Elliott C, et al. 2005. Conserved ERAD-like quality control of a plant polytopic membrane protein. Plant Cell 17:149-63
100. Müller LM, LindnerH, Pires ND, Gagliardini V, GrossniklausU. 2016. A subunit of the oligosaccharyltransferase complex is required for interspecific gametophyte recognition in Arabidopsis. Nat. Commun. 7:10826
101. Neal S, Jaeger PA, Duttke SH, Benner CK, Glass C, et al. 2018. TheDfm1Derlin is required for ERAD retrotranslocation of integral membrane proteins. Mol. Cell 69:306-20. e4
102. Nekrasov V, Li J, Batoux M, Roux M, Chu Z, et al. 2009. Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J. 28:3428-38
103. Neubert P, Strahl S. 2016. Protein O-mannosylation in the early secretory pathway. Curr. Opin. Cell Biol. 41:100-8
104. Niemann MC, Bartrina I, Ashikov A, Weber H, Novák O, et al. 2015. Arabidopsis ROCK1 transports UDP-GlcNAc/UDP-GalNAc and regulates ER protein quality control and cytokinin activity. PNAS 112:291-96
105. Ninagawa S, Okada T, Sumitomo Y, Kamiya Y, Kato K, et al. 2014. EDEM2 initiates mammalian glycoprotein ERAD by catalyzing the first mannose trimming step. J. Cell Biol. 206:347-56
106. Noh S, Kwon C, Oh D, Moon J, Chung W. 2003. Expression of an evolutionarily distinct novel BiP gene during the unfolded protein response in Arabidopsis thaliana. Gene 311:81-91
107. Ohta M, Takaiwa F. 2014. Emerging features of ER resident J-proteins in plants. Plant Signal. Behav. 9:e28194
108. Olson LJ, Orsi R, Alculumbre SG, Peterson FC, Stigliano ID, et al. 2013. Structure of the lectin mannose 6-phosphate receptor homology (MRH) domain of glucosidase II, an enzyme that regulates glycoprotein folding quality control in the endoplasmic reticulum. J. Biol. Chem. 288:16460-75
109. Park CJ, Bart R, Chern M, Canlas PE, Bai W, Ronald PC. 2010. Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLOS ONE 5:e9262
110. Park CJ, SharmaR, LefebvreB, Canlas PE, Ronald PC. 2013. The endoplasmic reticulum-quality control component SDF2 is essential for XA21-mediated immunity in rice. Plant Sci. 210:53-60
111. Pearse BR, Gabriel L, Wang N, Hebert DN. 2008. A cell-based reglucosylation assay demonstrates the role of GT1 in the quality control of a maturing glycoprotein. J. Cell Biol. 181:309-20
112. Persson S, Rosenquist M, Svensson K, Galvão R, Boss WF, Sommarin M. 2003. Phylogenetic analyses and expression studies reveal two distinct groups of calreticulin isoforms in higher plants. Plant Physiol. 133:1385-96
113. Pfeffer S, Dudek J, Gogala M, Schorr S, Linxweiler J, et al. 2014. Structure of the mammalian oligosaccharyl-transferase complex in the native ER protein translocon. Nat. Commun. 5:3072
114. Pfeiffer A, Stephanowitz H, Krause E, Volkwein C, Hirsch C, et al. 2016. A complex of Htm1 and the oxidoreductase Pdi1 accelerates degradation of misfolded glycoproteins. J. Biol. Chem. 291:12195-207
115. Pimpl P, Taylor J, Snowden C, Hillmer S, Robinson D, Denecke J. 2006. Golgi-mediated vacuolar sorting of the endoplasmic reticulum chaperone BiP may play an active role in quality control within the secretory pathway. Plant Cell 18:198-211
116. Pisoni GB, MolinariM. 2016. Five questions (with their answers) on ER-associated degradation. Traffic 17:341-50
117. Pollier J, Moses T, González-Guzmán M, De Geyter N, Lippens S, et al. 2013. The protein quality control system manages plant defence compound synthesis. Nature 504:148-52
118. Ritter C, Quirin K, Kowarik M, Helenius A. 2005. Minor folding defects trigger local modification of glycoproteins by the ER folding sensor GT. EMBO J. 24:1730-38
119. Römisch K. 2017. A case for Sec61 channel involvement in ERAD. Trends Biochem. Sci. 42:171-79
120. RuggianoA, Foresti O, CarvalhoP. 2014. ER-associated degradation: protein quality control and beyond. J. Cell Biol. 204:869-79
121. Saijo Y, Tintor N, Lu X, Rauf P, Pajerowska-Mukhtar K, et al. 2009. Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J. 28:3439-49
122. Schmitz A, Herzog V. 2004. Endoplasmic reticulum-associated degradation: exceptions to the rule. Eur. J. Cell Biol. 83:501-9
123. Schoberer J, Botchway SW. 2014. Investigating protein-protein interactions in the plant endomembrane system using multiphoton-induced FRET-FLIM. Methods Mol. Biol. 1209:81-95
124. Schoebel S, Mi W, Stein A, Ovchinnikov S, Pavlovicz R, et al. 2017. Cryo-EM structure of the proteinconducting ERAD channel Hrd1 in complex with Hrd3. Nature 548:352-55
125. Schott A, Ravaud S, Keller S, Radzimanowski J, Viotti C, et al. 2010. Arabidopsis stromal-derived factor2 (SDF2) is a crucial target of the unfolded protein response in the endoplasmic reticulum. J. Biol. Chem. 285:18113-21
126. Schulz BL, Stirnimann CU, Grimshaw JP, Brozzo MS, Fritsch F, et al. 2009. Oxidoreductase activity of oligosaccharyltransferase subunits Ost3p and Ost6p defines site-specific glycosylation efficiency. PNAS 106:11061-66
127. Shental-Bechor D, Levy Y. 2008. Effect of glycosylation on protein folding: a close look at thermodynamic stabilization. PNAS 105:8256-61
128. Shin YJ, Vavra U, Veit C, Strasser R. 2018. The glycan-dependent ERAD machinery degrades topologically diverse misfolded proteins. Plant J. In press. doi: 10. 1111/tpj. 13851
129. Soussilane P, Soussillane P, D'Alessio C, Paccalet T, Fitchette A, et al. 2009. N-glycan trimming by glucosidase II is essential for Arabidopsis development. Glycoconj. J. 26:597-607
130. Srivastava R, Deng Y, Shah S, Rao AG, Howell SH. 2013. BINDING PROTEIN is a master regulator of the endoplasmic reticulum stress sensor/transducer bZIP28 in Arabidopsis. Plant Cell 25:1416-29
131. Stigliano ID, Alculumbre SG, Labriola CA, Parodi AJ, D'Alessio C. 2011. Glucosidase II and N-glycan mannose content regulate the half-lives of monoglucosylated species in vivo. Mol. Biol. Cell 22:1810-23
132. Strasser R. 2016. Plant protein glycosylation. Glycobiology 26:926-39
133. Su W, Liu Y, Xia Y, Hong Z, Li J. 2011. Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis. PNAS 108:870-75
134. Su W, Liu Y, Xia Y, Hong Z, Li J. 2012. The Arabidopsis homolog of the mammalian OS-9 protein plays a key role in the endoplasmic reticulum-associated degradation of misfolded receptor-like kinases. Mol. Plant 5:929-40
135. Sun T, Zhang Q, GaoM, Zhang Y. 2014. Regulation of SOBIR1 accumulation and activation of defense responses in bir1-1 by specific components of ER quality control. Plant J. 77:748-56
136. Szathmary R, Bielmann R, Nita-Lazar M, Burda P, Jakob CA. 2005. Yos9 protein is essential for degradation of misfolded glycoproteins and may function as lectin in ERAD. Mol. Cell 19:765-75
137. 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
138. Tannous A, Patel N, Tamura T, Hebert DN. 2015. Reglucosylation by UDP-glucose:glycoprotein glucosyltransferase 1 delays glycoprotein secretion but not degradation. Mol. Biol. Cell 26:390-405
139. Totani K, Ihara Y, Matsuo I, Ito Y. 2006. Substrate specificity analysis of endoplasmic reticulum glucosidase II using synthetic high mannose-type glycans. J. Biol. Chem. 281:31502-8
140. Ushioda R, Hoseki J, Araki K, Jansen G, Thomas DY, Nagata K. 2008. ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER. Science 321:569-72
141. Van Hoewyk D. 2017. Defects in endoplasmic reticulum-associated degradation (ERAD) increase selenate sensitivity in Arabidopsis. Plant Signal. Behav. In press. https://doi. org/10. 1080/ 15592324. 2016. 1171451
142. Vassilakos A, Michalak M, Lehrman MA, Williams DB. 1998. Oligosaccharide binding characteristics of the molecular chaperones calnexin and calreticulin. Biochemistry 37:3480-90
143. Vasudevan D, Haltiwanger RS. 2014. Novel roles for O-linked glycans in protein folding. Glycoconj. J. 31:417-26
144. Vembar S, Brodsky J. 2008. One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 9:944-57
145. Vu KV, Nguyen NT, Jeong CY, Lee YH, Lee H, Hong SW. 2017. Systematic deletion of the ER lectin chaperone genes reveals their roles in vegetative growth and male gametophyte development in Arabidopsis. Plant J. 89:972-83
146. Wang D, Weaver ND, Kesarwani M, Dong X. 2005. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036-40
147. Wild R, Kowal J, Eyring J, Ngwa EM, Aebi M, Locher KP. 2018. Structure of the yeast oligosaccharyltransferase complex gives insight into eukaryotic N-glycosylation. Science 359:545-50
148. Wu G, Otegui MS, Spalding EP. 2010. The ER-localized TWD1 immunophilin is necessary for localization of multidrug resistance-like proteins required for polar auxin transport in Arabidopsis roots. Plant Cell 22:3295-304
149. Xu C, Ng DT. 2015. O-mannosylation: the other glycan player of ER quality control. Semin. Cell Dev. Biol. 41:129-34
150. Xu C, Wang S, Thibault G, Ng DT. 2013. Futile protein folding cycles in the ER are terminated by the unfolded protein O-mannosylation pathway. Science 340:978-81
151. Yamamoto M, Kawanabe M, Hayashi Y, Endo T, Nishikawa S. 2010. A vacuolar carboxypeptidase mutant of Arabidopsis thaliana is degraded by the ERAD pathway independently of its N-glycan. Biochem. Biophys. Res. Commun. 393:384-89
152. Yamamoto M, Maruyama D, Endo T, Nishikawa S. 2008. Arabidopsis thaliana has a set of J proteins in the endoplasmic reticulum that are conserved from yeast to animals and plants. Plant Cell Physiol. 49:1547-62
153. Yang X, Srivastava R, Howell SH, Bassham DC. 2016. Activation of autophagy by unfolded proteins during endoplasmic reticulum stress. Plant J. 85:83-95
154. Yuen CYL, Wang P, Kang BH, Matsumoto K, Christopher DA. 2017. A non-classical member of the protein disulfide isomerase family, PDI7 of Arabidopsis thaliana, localizes to the cis-Golgi and endoplasmic reticulum membranes. Plant Cell Physiol. 58:1103-17
155. Yuen CYL, Wong K, Christopher DA. 2016. Phylogenetic characterization and promoter expression analysis of a novel hybrid protein disulfide isomerase/cargo receptor subfamily unique to plants and chromalveolates. Mol. Genet. Genom. 291:455-69
156. Zhao B, Lv M, Feng Z, Campbell T, Liscum E, Li J. 2016. TWISTED DWARF 1 associates with BRASSINOSTEROID-INSENSITIVE 1 to regulate early events of the brassinosteroid signaling pathway. Mol. Plant 9:582-92
157. Zuber C, Spiro MJ, Guhl B, Spiro RG, Roth J. 2000. Golgi apparatus immunolocalization of endomannosidase suggests post-endoplasmic reticulum glucose trimming: implications for quality control. Mol. Biol. Cell 11:4227-40