The Protein Quality Control of Plant Receptor-Like Kinases in the Endoplasmic Reticulum

  • Zhi Hong
  • Jianming LiEmail author
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 13)


Plant receptor-like kinases (RLKs) play important roles in regulating plant growth and development and plant–microbe interactions. Like other eukaryotic membrane and secretory proteins, RLKs are cotranslationally inserted into the endoplasmic reticulum (ER) for chaperone-assisted folding to attain their native structures before reaching the plasma membrane to perceive developmental or environmental signals. The ER also houses complex quality control (ERQC) systems that retain incompletely folded proteins for additional folding attempts but eliminate terminally misfolded proteins by ER-associated degradation (ERAD). However, little is known about how the protein folding and ERQC/ERAD events are executed in the plant ER. Recent genetic and biochemical approaches designed to identify regulators of RLK signaling fortuitously discovered various components of the plant ERQC/ERAD systems. These studies have not only dramatically enhanced our understanding of the plant ERQC/ERAD mechanisms that regulate the cell surface expression of RLKs, but have also provided outstanding tools that could identify additional ERQC/ERAD components and uncover novel RLKs involved in plant environment communications.


Endoplasmic Reticulum Unfold Protein Response Endoplasmic Reticulum Membrane Endoplasmic Reticulum Lumen Dwarf Phenotype 
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.



Works in the authors' laboratories were supported in part by a grant from National Natural Science Foundation of China (31070246) to ZH and a grant from National Institutes of Health (GM060519) to JL.


  1. Aebi M, Gassenhuber J, Domdey H, te Heesen S (1996) Cloning and characterization of the ALG3 gene of Saccharomyces cerevisiae. Glycobiology 6:439–444PubMedCrossRefGoogle Scholar
  2. Anelli T, Sitia R (2008) Protein quality control in the early secretory pathway. EMBO J 27:315–327PubMedCrossRefGoogle Scholar
  3. Anelli T, Alessio M, Bachi A, Bergamelli L, Bertoli G, Camerini S, Mezghrani A, Ruffato E, Simmen T, Sitia R (2003) Thiol-mediated protein retention in the endoplasmic reticulum: the role of ERp44. EMBO J 22:5015–5022PubMedCrossRefGoogle Scholar
  4. Anelli T, Ceppi S, Bergamelli L, Cortini M, Masciarelli S, Valetti C, Sitia R (2007) Sequential steps and checkpoints in the early exocytic compartment during secretory IgM biogenesis. EMBO J 26:4177–4188PubMedCrossRefGoogle Scholar
  5. Appenzeller C, Andersson H, Kappeler F, Hauri HP (1999) The lectin ERGIC-53 is a cargo transport receptor for glycoproteins. Nat Cell Biol 1:330–334PubMedCrossRefGoogle Scholar
  6. Arnold SM, Fessler LI, Fessler JH, Kaufman RJ (2000) Two homologues encoding human UDP-glucose:glycoprotein glucosyltransferase differ in mRNA expression and enzymatic activity. Biochemistry 39:2149–2163PubMedCrossRefGoogle Scholar
  7. Bagola K, Mehnert M, Jarosch E, Sommer T (2010) Protein dislocation from the ER. Biochim Biophys Acta 1808:925–936PubMedGoogle Scholar
  8. Banerjee S, Vishwanath P, Cui J, Kelleher DJ, Gilmore R, Robbins PW, Samuelson J (2007) The evolution of N-glycan-dependent endoplasmic reticulum quality control factors for glycoprotein folding and degradation. Proc Natl Acad Sci USA 104:11676–11681PubMedCrossRefGoogle Scholar
  9. Belkhadir Y, Durbak A, Wierzba M, Schmitz RJ, Aguirre A, Michel R, Rowe S, Fujioka S, Tax FE (2010) Intragenic suppression of a trafficking-defective brassinosteroid receptor mutant in Arabidopsis. Genetics 185:1283–1296PubMedCrossRefGoogle Scholar
  10. Biederer T, Volkwein C, Sommer T (1997) Role of Cue1p in ubiquitination and degradation at the ER surface. Science 278:1806–1809PubMedCrossRefGoogle Scholar
  11. Blond-Elguindi S, Cwirla SE, Dower WJ, Lipshutz RJ, Sprang SR, Sambrook JF, Gething MJ (1993) Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75:717–728PubMedCrossRefGoogle Scholar
  12. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406PubMedCrossRefGoogle Scholar
  13. Boyce JM, Coates D, Fricker MD, Evans DE (1994) Genomic sequence of a calnexin homolog from Arabidopsis thaliana. Plant Physiol 106:1691PubMedCrossRefGoogle Scholar
  14. Braakman I, Bulleid NJ (2011) Protein folding and modification in the mammalian endoplasmic reticulum. Annu Rev Biochem 80:71–99Google Scholar
  15. 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 34:269–281PubMedCrossRefGoogle Scholar
  16. Burda P, Aebi M (1999) The dolichol pathway of N-linked glycosylation. Biochim Biophys Acta 1426:239–257PubMedCrossRefGoogle Scholar
  17. Burda P, te Heesen S, Brachat A, Wach A, Dusterhoft A, Aebi M (1996) Stepwise assembly of the lipid-linked oligosaccharide in the endoplasmic reticulum of Saccharomyces cerevisiae: identification of the ALG9 gene encoding a putative mannosyl transferase. Proc Natl Acad Sci USA 93:7160–7165PubMedCrossRefGoogle Scholar
  18. Burda P, Jakob CA, Beinhauer J, Hegemann JH, Aebi M (1999) Ordered assembly of the asymmetrically branched lipid-linked oligosaccharide in the endoplasmic reticulum is ensured by the substrate specificity of the individual glycosyltransferases. Glycobiology 9:617–625PubMedCrossRefGoogle Scholar
  19. 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 32:949–960PubMedCrossRefGoogle Scholar
  20. Cabral CM, Liu Y, Sifers RN (2001) Dissecting glycoprotein quality control in the secretory pathway. Trends Biochem Sci 26:619–624PubMedCrossRefGoogle Scholar
  21. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92–96PubMedCrossRefGoogle Scholar
  22. Cano-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–5351PubMedCrossRefGoogle Scholar
  23. Caplan JL, Zhu X, Mamillapalli P, Marathe R, Anandalakshmi R, Dinesh-Kumar SP (2009) Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants. Cell Host Microbe 6:457–469PubMedCrossRefGoogle Scholar
  24. Caramelo JJ, Parodi AJ (2007) How sugars convey information on protein conformation in the endoplasmic reticulum. Semin Cell Dev Biol 18:732–742PubMedCrossRefGoogle Scholar
  25. Caramelo JJ, Parodi AJ (2008) Getting in and out from calnexin/calreticulin cycles. J Biol Chem 283:10221–10225PubMedCrossRefGoogle Scholar
  26. Caramelo JJ, Castro OA, de Prat-Gay G, Parodi AJ (2004) The endoplasmic reticulum glucosyltransferase recognizes nearly native glycoprotein folding intermediates. J Biol Chem 279:46280–46285PubMedCrossRefGoogle Scholar
  27. Carla Fama M, Raden D, Zacchi N, Lemos DR, Robinson AS, Silberstein S (2007) The Saccharomyces cerevisiae YFR041C/ERJ5 gene encoding a type I membrane protein with a J domain is required to preserve the folding capacity of the endoplasmic reticulum. Biochim Biophys Acta 1773:232–242PubMedCrossRefGoogle Scholar
  28. Carvalho P, Goder V, Rapoport TA (2006) Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126:361–373PubMedCrossRefGoogle Scholar
  29. Carvalho P, Stanley AM, Rapoport TA (2010) Retrotranslocation of a misfolded luminal ER protein by the ubiquitin-ligase Hrd1p. Cell 143:579–591PubMedCrossRefGoogle Scholar
  30. Ceriotti A (2011) Waste disposal in the endoplasmic reticulum, ROS production and plant salt stress response. Cell Res 21:555–557PubMedCrossRefGoogle Scholar
  31. Ceriotti A, Roberts LM (2006) Endoplasmic reticulum-associated protein degradation in plant cells. In: Robinson DG (ed) The plant endoplasmic reticulum. Springer, Berlin, pp 75–98CrossRefGoogle Scholar
  32. Che P, Bussell JD, Zhou W, Estavillo GM, Pogson BJ, Smith SM (2010) Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis. Sci Signal 3:ra69PubMedCrossRefGoogle Scholar
  33. Chen L, Hamada S, Fujiwara M, Zhu T, Thao NP, Wong HL, Krishna P, Ueda T, Kaku H, Shibuya N, Kawasaki T, Shimamoto K (2010) The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell Host Microbe 7:185–196PubMedCrossRefGoogle Scholar
  34. Choe J, Kelker MS, Wilson IA (2005) Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 309:581–585PubMedCrossRefGoogle Scholar
  35. Christensen A, Svensson K, Persson S, Jung J, Michalak M, Widell S, Sommarin M (2008) Functional characterization of Arabidopsis calreticulin1a: a key alleviator of endoplasmic reticulum stress. Plant Cell Physiol 49:912–924PubMedCrossRefGoogle Scholar
  36. Cipollo JF, Trimble RB (2000) The accumulation of Man(6)GlcNAc(2)-PP-dolichol in the Saccharomyces cerevisiae Δalg9 mutant reveals a regulatory role for the Alg3p α1,3-Man middle-arm addition in downstream oligosaccharide-lipid and glycoprotein glycan processing. J Biol Chem 275:4267–4277PubMedCrossRefGoogle Scholar
  37. Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418PubMedGoogle Scholar
  38. Clark SE, Running MP, Meyerowitz EM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057–2067Google Scholar
  39. Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585PubMedCrossRefGoogle Scholar
  40. Clerc S, Hirsch C, Oggier DM, Deprez P, Jakob C, Sommer T, Aebi M (2009) Htm1 protein generates the N-glycan signal for glycoprotein degradation in the endoplasmic reticulum. J Cell Biol 184:159–172PubMedCrossRefGoogle Scholar
  41. Clouse SD, Sasse JM (1998) BRASSINOSTEROIDS: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451PubMedCrossRefGoogle Scholar
  42. Cock JM, Vanoosthuyse V, Gaude T (2002) Receptor kinase signalling in plants and animals: distinct molecular systems with mechanistic similarities. Curr Opin Cell Biol 14:230–236PubMedCrossRefGoogle Scholar
  43. Coe H, Michalak M (2010) ERp57, a multifunctional endoplasmic reticulum resident oxidoreductase. Int J Biochem Cell Biol 42:796–799PubMedCrossRefGoogle Scholar
  44. Cormier JH, Tamura T, Sunryd JC, Hebert DN (2009) EDEM1 recognition and delivery of misfolded proteins to the SEL1L-containing ERAD complex. Mol Cell 34:627–633PubMedCrossRefGoogle Scholar
  45. Cox JS, Walter P (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87:391–404PubMedCrossRefGoogle Scholar
  46. Cox JS, Shamu CE, Walter P (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73:1197–1206PubMedCrossRefGoogle Scholar
  47. Deng Y, Humbert S, Liu JX, Srivastava R, Rothstein SJ, Howell SH (2011) Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc Natl Acad Sci USA 108:7247–7252PubMedCrossRefGoogle Scholar
  48. Denic V, Quan EM, Weissman JS (2006) A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation. Cell 126:349–359PubMedCrossRefGoogle Scholar
  49. DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7:1243–1249PubMedCrossRefGoogle Scholar
  50. 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 137:287–296PubMedCrossRefGoogle Scholar
  51. Di Matteo A, Federici L, Mattei B, Salvi G, Johnson KA, Savino C, De Lorenzo G, Tsernoglou D, Cervone F (2003) The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. Proc Natl Acad Sci USA 100:10124–10128PubMedCrossRefGoogle Scholar
  52. Elbein AD, Tropea JE, Mitchell M, Kaushal GP (1990) Kifunensine, a potent inhibitor of the glycoprotein processing mannosidase I. J Biol Chem 265:15599–15605PubMedGoogle Scholar
  53. Eletto D, Dersh D, Argon Y (2010) GRP94 in ER quality control and stress responses. Semin Cell Dev Biol 21:479–485PubMedCrossRefGoogle Scholar
  54. Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4:181–191PubMedCrossRefGoogle Scholar
  55. Feiler HS, Desprez T, Santoni V, Kronenberger J, Caboche M, Traas J (1995) The higher plant Arabidopsis thaliana encodes a functional CDC48 homologue which is highly expressed in dividing and expanding cells. EMBO J 14:5626–5637PubMedGoogle Scholar
  56. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914PubMedCrossRefGoogle Scholar
  57. Flynn GC, Pohl J, Flocco MT, Rothman JE (1991) Peptide-binding specificity of the molecular chaperone BiP. Nature 353:726–730PubMedCrossRefGoogle Scholar
  58. Frank CG, Aebi M (2005) ALG9 mannosyltransferase is involved in two different steps of lipid-linked oligosaccharide biosynthesis. Glycobiology 15:1156–1163PubMedCrossRefGoogle Scholar
  59. Friedrichsen DM, Joazeiro CA, Li J, Hunter T, Chory J (2000) Brassinosteroid-insensitive1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiol 123:1247–1256PubMedCrossRefGoogle Scholar
  60. Frydman J, Hohfeld J (1997) Chaperones get in touch: the Hip-Hop connection. Trends Biochem Sci 22:87–92PubMedCrossRefGoogle Scholar
  61. Fukuda S, Sumii M, Masuda Y, Takahashi M, Koike N, Teishima J, Yasumoto H, Itamoto T, Asahara T, Dohi K, Kamiya K (2001) Murine and human SDF2L1 is an endoplasmic reticulum stress-inducible gene and encodes a new member of the Pmt/rt protein family. Biochem Biophys Res Commun 280:407–414PubMedCrossRefGoogle Scholar
  62. Garza RM, Sato BK, Hampton RY (2009) In vitro analysis of Hrd1p-mediated retrotranslocation of its multispanning membrane substrate 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase. J Biol Chem 284:14710–14722PubMedCrossRefGoogle Scholar
  63. Gauss R, Jarosch E, Sommer T, Hirsch C (2006a) A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery. Nat Cell Biol 8:849–854PubMedCrossRefGoogle Scholar
  64. Gauss R, Sommer T, Jarosch E (2006b) The Hrd1p ligase complex forms a linchpin between ER-lumenal substrate selection and Cdc48p recruitment. EMBO J 25:1827–1835PubMedCrossRefGoogle Scholar
  65. Gish LA, Clark SE (2011) The RLK/Pelle family of kinases. Plant J 66:117–127PubMedCrossRefGoogle Scholar
  66. Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011PubMedCrossRefGoogle Scholar
  67. Hammond C, Helenius A (1994) Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J Cell Biol 126:41–52PubMedCrossRefGoogle Scholar
  68. Hampton RY, Gardner RG, Rine J (1996) Role of 26S proteasome and HRD genes in the degradation of 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein. Mol Biol Cell 7:2029–2044PubMedGoogle Scholar
  69. Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271–274PubMedCrossRefGoogle Scholar
  70. Hartmann-Petersen R, Gordon C (2004) Protein degradation: recognition of ubiquitinylated substrates. Curr Biol 14:R754–R756PubMedCrossRefGoogle Scholar
  71. Hassink G, Kikkert M, van Voorden S, Lee SJ, Spaapen R, van Laar T, Coleman CS, Bartee E, Fruh K, Chau V, Wiertz E (2005) TEB4 is a C4HC3 RING finger-containing ubiquitin ligase of the endoplasmic reticulum. Biochem J 388:647–655PubMedCrossRefGoogle Scholar
  72. Hauri HP, Nufer O, Breuza L, Tekaya HB, Liang L (2002) Lectins and protein traffic early in the secretory pathway. Biochem Soc Symp 73–82Google Scholar
  73. Haweker H, Rips S, Koiwa H, Salomon S, Saijo Y, Chinchilla D, Robatzek S, von Schaewen A (2010) Pattern recognition receptors require N-glycosylation to mediate plant immunity. J Biol Chem 285:4629–4636PubMedCrossRefGoogle Scholar
  74. Haze K, Yoshida H, Yanagi H, Yura T, Mori K (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10:3787–3799PubMedGoogle Scholar
  75. Helenius A (1994) How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticulum. Mol Biol Cell 5:253–265PubMedGoogle Scholar
  76. Helenius A, Aebi M (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73:1019–1049PubMedCrossRefGoogle Scholar
  77. Henquet M, Lehle L, Schreuder M, Rouwendal G, Molthoff J, Helsper J, van der Krol S, Bosch D (2008) Identification of the gene encoding the α1,3-mannosyltransferase (ALG3) in Arabidopsis and characterization of downstream N-glycan processing. Plant Cell 20:1652–1664PubMedCrossRefGoogle Scholar
  78. Hirsch C, Gauss R, Horn SC, Neuber O, Sommer T (2009) The ubiquitylation machinery of the endoplasmic reticulum. Nature 458:453–460PubMedCrossRefGoogle Scholar
  79. Hitt R, Wolf DH (2004) Der1p, a protein required for degradation of malfolded soluble proteins of the endoplasmic reticulum: topology and Der1-like proteins. FEMS Yeast Res 4:721–729PubMedCrossRefGoogle Scholar
  80. 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 20:3418–3429PubMedCrossRefGoogle Scholar
  81. Hong Z, Jin H, Fitchette AC, Xia Y, Monk AM, Faye L, Li J (2009) Mutations of an α1,6 mannosyltransferase inhibit endoplasmic reticulum-associated degradation of defective brassinosteroid receptors in Arabidopsis. Plant Cell 21:3792–3802PubMedCrossRefGoogle Scholar
  82. Hosokawa N, Kamiya Y, Kamiya D, Kato K, Nagata K (2009) Human OS-9, a lectin required for glycoprotein endoplasmic reticulum-associated degradation, recognizes mannose-trimmed N-glycans. J Biol Chem 284:17061–17068PubMedCrossRefGoogle Scholar
  83. Hosokawa N, Kamiya Y, Kato K (2010) The role of MRH domain-containing lectins in ERAD. Glycobiology 20:651–660PubMedCrossRefGoogle Scholar
  84. Houston NL, Fan C, Xiang JQ, Schulze JM, Jung R, Boston RS (2005) Phylogenetic analyses identify 10 classes of the protein disulfide isomerase family in plants, including single-domain protein disulfide isomerase-related proteins. Plant Physiol 137:762–778PubMedCrossRefGoogle Scholar
  85. Huang L, Franklin AE, Hoffman NE (1993) Primary structure and characterization of an Arabidopsis thaliana calnexin-like protein. J Biol Chem 268:6560–6566PubMedGoogle Scholar
  86. 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 21:898–908PubMedCrossRefGoogle Scholar
  87. Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102:5280–5285PubMedCrossRefGoogle Scholar
  88. Iwata Y, Sakiyama M, Lee M-H, Koizumi N (2010) Transcriptomic response of Arabidopsis thaliana to tunicamycin-induced endoplasmic reticulum stress. Plant Biotechnol 27:161–171CrossRefGoogle Scholar
  89. Jakob CA, Burda P, Roth J, Aebi M (1998) Degradation of misfolded endoplasmic reticulum glycoproteins in Saccharomyces cerevisiae is determined by a specific oligosaccharide structure. J Cell Biol 142:1223–1233PubMedCrossRefGoogle Scholar
  90. Jakob CA, Bodmer D, Spirig U, Battig P, Marcil A, Dignard D, Bergeron JJ, Thomas DY, Aebi M (2001) Htm1p, a mannosidase-like protein, is involved in glycoprotein degradation in yeast. EMBO Rep 2:423–430PubMedGoogle Scholar
  91. Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925–1934PubMedCrossRefGoogle Scholar
  92. Jin H, Yan Z, Nam KH, Li J (2007) Allele-specific suppression of a defective brassinosteroid receptor reveals a physiological role of UGGT in ER quality control. Mol Cell 26:821–830PubMedCrossRefGoogle Scholar
  93. 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. Proc Natl Acad Sci USA 106:13612–13617PubMedCrossRefGoogle Scholar
  94. Kajiura H, Seki T, Fujiyama K (2010) Arabidopsis thaliana ALG3 mutant synthesizes immature oligosaccharides in the ER and accumulates unique N-glycans. Glycobiology 20:736–751PubMedCrossRefGoogle Scholar
  95. Kamauchi S, Nakatani H, Nakano C, Urade R (2005) Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J 272:3461–3476PubMedCrossRefGoogle Scholar
  96. Kanehara K, Xie W, Ng DT (2010) Modularity of the Hrd1 ERAD complex underlies its diverse client range. J Cell Biol 188:707–716PubMedCrossRefGoogle Scholar
  97. Kang JS, Frank J, Kang CH, Kajiura H, Vikram M, Ueda A, Kim S, Bahk JD, Triplett B, Fujiyama K, Lee SY, von Schaewen A, Koiwa H (2008) Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus. Proc Natl Acad Sci USA 105:5933–5938PubMedCrossRefGoogle Scholar
  98. Kato K, Kamiya Y (2007) Structural views of glycoprotein-fate determination in cells. Glycobiology 17:1031–1044PubMedCrossRefGoogle Scholar
  99. Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–3851PubMedGoogle Scholar
  100. Kelleher DJ, Gilmore R (2006) An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16:47R–62RPubMedCrossRefGoogle Scholar
  101. Kikkert M, Doolman R, Dai M, Avner R, Hassink G, van Voorden S, Thanedar S, Roitelman J, Chau V, Wiertz E (2004) Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum. J Biol Chem 279:3525–3534PubMedCrossRefGoogle Scholar
  102. Kinoshita T, Cano-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433:167–171PubMedCrossRefGoogle Scholar
  103. Knop M, Finger A, Braun T, Hellmuth K, Wolf DH (1996) Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast. EMBO J 15:753–763PubMedGoogle Scholar
  104. 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 15:2273–2284PubMedCrossRefGoogle Scholar
  105. Koizumi N, Martinez IM, Kimata Y, Kohno K, Sano H, Chrispeels MJ (2001) Molecular characterization of two Arabidopsis Ire1 homologs, endoplasmic reticulum-located transmembrane protein kinases. Plant Physiol 127:949–962PubMedCrossRefGoogle Scholar
  106. Kolade OO, Bamford VA, Ancillo Anton G, Jones JD, Vera P, Hemmings AM (2006) In vitro characterization of the cysteine-rich capping domains in a plant leucine rich repeat protein. Biochim Biophys Acta 1764:1043–1053PubMedGoogle Scholar
  107. Kostova Z, Tsai YC, Weissman AM (2007) Ubiquitin ligases, critical mediators of endoplasmic reticulum-associated degradation. Semin Cell Dev Biol 18:770–779PubMedCrossRefGoogle Scholar
  108. Lee SW, Han SW, Bartley LE, Ronald PC (2006) From the Academy: Colloquium review. Unique characteristics of Xanthomonas oryzae pv. oryzae AvrXa21 and implications for plant innate immunity. Proc Natl Acad Sci USA 103:18395–18400PubMedCrossRefGoogle Scholar
  109. Lee SW, Han SW, Sririyanum M, Park CJ, Seo YS, Ronald PC (2009) A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 326:850–853PubMedCrossRefGoogle Scholar
  110. Lehti-Shiu MD, Zou C, Hanada K, Shiu SH (2009) Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150:12–26PubMedCrossRefGoogle Scholar
  111. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938PubMedCrossRefGoogle Scholar
  112. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222PubMedCrossRefGoogle Scholar
  113. Li J, Zhao-Hui C, Batoux M, Nekrasov V, Roux M, Chinchilla D, Zipfel C, Jones JD (2009) Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. Proc Natl Acad Sci USA 106:15973–15978PubMedCrossRefGoogle Scholar
  114. Liang J, Yin C, Doong H, Fang S, Peterhoff C, Nixon RA, Monteiro MJ (2006) Characterization of erasin (UBXD2): a new ER protein that promotes ER-associated protein degradation. J Cell Sci 119:4011–4024PubMedCrossRefGoogle Scholar
  115. Lilley BN, Ploegh HL (2004) A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429:834–840PubMedCrossRefGoogle Scholar
  116. Liu L, Cui F, Li Q, Yin B, Zhang H, Lin B, Wu Y, Xia R, Tang S, Xie Q (2011) The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance. Cell Res. doi:10.1038/cr.2010.181Google Scholar
  117. Liu JX, Howell SH (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22:2930–2942PubMedCrossRefGoogle Scholar
  118. Liu JX, Srivastava R, Che P, Howell SH (2007a) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19:4111–4119PubMedCrossRefGoogle Scholar
  119. Liu JX, Srivastava R, Che P, Howell SH (2007b) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909PubMedCrossRefGoogle Scholar
  120. Lord JM, Ceriotti A, Roberts LM (2002) ER dislocation: Cdc48p/p97 gets into the AAAct. Curr Biol 12:R182–R184PubMedCrossRefGoogle Scholar
  121. Lu X, Tintor N, Mentzel T, Kombrink E, Boller T, Robatzek S, Schulze-Lefert P, Saijo Y (2009) Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc Natl Acad Sci USA 106:22522–22527PubMedCrossRefGoogle Scholar
  122. Maattanen P, Gehring K, Bergeron JJ, Thomas DY (2010) Protein quality control in the ER: the recognition of misfolded proteins. Semin Cell Dev Biol 21:500–511PubMedCrossRefGoogle Scholar
  123. Marshall RS, Jolliffe NA, Ceriotti A, Snowden CJ, Lord JM, Frigerio L, Roberts LM (2008) The role of CDC48 in the retro-translocation of non-ubiquitinated toxin substrates in plant cells. J Biol Chem 283:15869–15877PubMedCrossRefGoogle Scholar
  124. Martinez IM, Chrispeels MJ (2003) Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 15:561–576PubMedCrossRefGoogle Scholar
  125. Matlack KE, Misselwitz B, Plath K, Rapoport TA (1999) BiP acts as a molecular ratchet during posttranslational transport of prepro-a factor across the ER membrane. Cell 97:553–564PubMedCrossRefGoogle Scholar
  126. McCracken AA, Brodsky JL (1996) Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin, and ATP. J Cell Biol 132:291–298PubMedCrossRefGoogle Scholar
  127. Medicherla B, Kostova Z, Schaefer A, Wolf DH (2004) A genomic screen identifies Dsk2p and Rad23p as essential components of ER-associated degradation. EMBO Rep 5:692–697PubMedCrossRefGoogle Scholar
  128. 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 13:4456–4469PubMedCrossRefGoogle Scholar
  129. Michalak M, Groenendyk J, Szabo E, Gold LI, Opas M (2009) Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem J 417:651–666PubMedCrossRefGoogle Scholar
  130. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104:19613–19618PubMedCrossRefGoogle Scholar
  131. Molinari M (2007) N-glycan structure dictates extension of protein folding or onset of disposal. Nat Chem Biol 3:313–320PubMedCrossRefGoogle Scholar
  132. Molinari M, 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 20:503–512PubMedCrossRefGoogle Scholar
  133. Mori K, Ma W, Gething MJ, Sambrook J (1993) A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74:743–756PubMedCrossRefGoogle Scholar
  134. 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 17:149–163PubMedCrossRefGoogle Scholar
  135. Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–212PubMedCrossRefGoogle Scholar
  136. Nekrasov V, Li J, Batoux M, Roux M, Chu ZH, Lacombe S, Rougon A, Bittel P, Kiss-Papp M, Chinchilla D, van Esse HP, Jorda L, Schwessinger B, Nicaise V, Thomma BP, Molina A, Jones JD, Zipfel C (2009) Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J 28:3428–3438PubMedCrossRefGoogle Scholar
  137. Nishikawa SI, Fewell SW, Kato Y, Brodsky JL, Endo T (2001) Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation. J Cell Biol 153:1061–1070PubMedCrossRefGoogle Scholar
  138. Noguchi T, Fujioka S, Choe S, Takatsuto S, Yoshida S, Yuan H, Feldmann KA, Tax FE (1999) Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiol 121:743–752PubMedCrossRefGoogle Scholar
  139. 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 311:81–91PubMedCrossRefGoogle Scholar
  140. Oda Y, Hosokawa N, Wada I, Nagata K (2003) EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299:1394–1397PubMedCrossRefGoogle Scholar
  141. Ostrovsky O, Ahmed NT, Argon Y (2009) The chaperone activity of GRP94 toward insulin-like growth factor II is necessary for the stress response to serum deprivation. Mol Biol Cell 20:1855–1864PubMedCrossRefGoogle Scholar
  142. Ostrovsky O, Eletto D, Makarewich C, Barton ER, Argon Y (2010) Glucose regulated protein 94 is required for muscle differentiation through its control of the autocrine production of insulin-like growth factors. Biochim Biophys Acta 1803:333–341PubMedCrossRefGoogle Scholar
  143. Otero JH, Lizak B, Hendershot LM (2010) Life and death of a BiP substrate. Semin Cell Dev Biol 21:472–478PubMedCrossRefGoogle Scholar
  144. 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:e9262PubMedCrossRefGoogle Scholar
  145. Pattison RJ, Amtmann A (2009) N-glycan production in the endoplasmic reticulum of plants. Trends Plant Sci 14:92–99PubMedCrossRefGoogle Scholar
  146. 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 9:1869–1880PubMedCrossRefGoogle Scholar
  147. 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 126:1092–1104PubMedCrossRefGoogle Scholar
  148. Persson S, Rosenquist M, Svensson K, Galvao R, Boss WF, Sommarin M (2003) Phylogenetic analyses and expression studies reveal two distinct groups of calreticulin isoforms in higher plants. Plant Physiol 133:1385–1396PubMedCrossRefGoogle Scholar
  149. Pilon M, Schekman R, Romisch K (1997) Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. EMBO J 16:4540–4548PubMedCrossRefGoogle Scholar
  150. Pimpl P, Taylor JP, Snowden C, Hillmer S, Robinson DG, 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 18:198–211PubMedCrossRefGoogle Scholar
  151. Plemper RK, Bohmler S, Bordallo J, Sommer T, Wolf DH (1997) Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature 388:891–895PubMedCrossRefGoogle Scholar
  152. Ponting CP (2000) Novel repeats in ryanodine and IP3 receptors and protein O-mannosyltransferases. Trends Biochem Sci 25:48–50PubMedGoogle Scholar
  153. Qin C, Qian W, Wang W, Wu Y, Yu C, Jiang X, Wang D, Wu P (2008) GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:18308–18313PubMedCrossRefGoogle Scholar
  154. Quan EM, Kamiya Y, Kamiya D, Denic V, Weibezahn J, Kato K, Weissman JS (2008) Defining the glycan destruction signal for endoplasmic reticulum-associated degradation. Mol Cell 32:870–877PubMedCrossRefGoogle Scholar
  155. Raasi S, Wolf DH (2007) Ubiquitin receptors and ERAD: a network of pathways to the proteasome. Semin Cell Dev Biol 18:780–791PubMedCrossRefGoogle Scholar
  156. Ramos RR, Swanson AJ, Bass J (2007) Calreticulin and Hsp90 stabilize the human insulin receptor and promote its mobility in the endoplasmic reticulum. Proc Natl Acad Sci USA 104:10470–10475PubMedCrossRefGoogle Scholar
  157. Rancour DM, Dickey CE, Park S, Bednarek SY (2002) Characterization of AtCDC48. Evidence for multiple membrane fusion mechanisms at the plane of cell division in plants. Plant Physiol 130:1241–1253PubMedCrossRefGoogle Scholar
  158. Rapoport TA (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450:663–669PubMedCrossRefGoogle Scholar
  159. Reddy P, Sparvoli A, Fagioli C, Fassina G, Sitia R (1996) Formation of reversible disulfide bonds with the protein matrix of the endoplasmic reticulum correlates with the retention of unassembled Ig light chains. EMBO J 15:2077–2085PubMedGoogle Scholar
  160. Richly H, Rape M, Braun S, Rumpf S, Hoege C, Jentsch S (2005) A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 120:73–84PubMedCrossRefGoogle Scholar
  161. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519–529PubMedCrossRefGoogle Scholar
  162. Rudiger S, Buchberger A, Bukau B (1997) Interaction of Hsp70 chaperones with substrates. Nat Struct Biol 4:342–349PubMedCrossRefGoogle Scholar
  163. Saijo Y (2010) ER quality control of immune receptors and regulators in plants. Cell Microbiol 12:716–724PubMedCrossRefGoogle Scholar
  164. Saijo Y, Tintor N, Lu X, Rauf P, Pajerowska-Mukhtar K, Haweker H, Dong X, Robatzek S, Schulze-Lefert P (2009) Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J 28:3439–3449PubMedCrossRefGoogle Scholar
  165. Sanders CR, Myers JK (2004) Disease-related misassembly of membrane proteins. Annu Rev Biophys Biomol Struct 33:25–51PubMedCrossRefGoogle Scholar
  166. Satoh T, Chen Y, Hu D, Hanashima S, Yamamoto K, Yamaguchi Y (2010) Structural basis for oligosaccharide recognition of misfolded glycoproteins by OS-9 in ER-associated degradation. Mol Cell 40:905–916PubMedCrossRefGoogle Scholar
  167. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S, Kaufman RJ (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7:1165–1176PubMedCrossRefGoogle Scholar
  168. Schmitz A, Herzog V (2004) Endoplasmic reticulum-associated degradation: exceptions to the rule. Eur J Cell Biol 83:501–509PubMedCrossRefGoogle Scholar
  169. Schott A, Ravaud S, Keller S, Radzimanowski J, Viotti C, Hillmer S, Sinning I, Strahl S (2010) Arabidopsis stromal-derived Factor2 (SDF2) is a crucial target of the unfolded protein response in the endoplasmic reticulum. J Biol Chem 285:18113–18121PubMedCrossRefGoogle Scholar
  170. Schuberth C, Buchberger A (2005) Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-associated protein degradation. Nat Cell Biol 7:999–1006PubMedCrossRefGoogle Scholar
  171. Shen J, Chen X, Hendershot L, Prywes R (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3:99–111PubMedCrossRefGoogle Scholar
  172. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2011) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64:204–214CrossRefGoogle Scholar
  173. Shirasu K (2009) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60:139–164PubMedCrossRefGoogle Scholar
  174. Shiu SH, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768PubMedCrossRefGoogle Scholar
  175. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806PubMedCrossRefGoogle Scholar
  176. 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. Proc Natl Acad Sci USA 108:870–875PubMedCrossRefGoogle Scholar
  177. Suzuki T, Park H, Kwofie MA, Lennarz WJ (2001) Rad23 provides a link between the Png1 deglycosylating enzyme and the 26S proteasome in yeast. J Biol Chem 276:21601–21607PubMedCrossRefGoogle Scholar
  178. Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11:515–528PubMedCrossRefGoogle Scholar
  179. Tamura K, Yamada K, Shimada T, Hara-Nishimura I (2004) Endoplasmic reticulum-resident proteins are constitutively transported to vacuoles for degradation. Plant J 39:393–402PubMedCrossRefGoogle Scholar
  180. Torii KU (2009) Transmembrane receptors in plants: receptor kinases and their ligands. Annu Plant Rev 33:1–29Google Scholar
  181. Trombetta ES (2003) The contribution of N-glycans and their processing in the endoplasmic reticulum to glycoprotein biosynthesis. Glycobiology 13:77R–91RPubMedCrossRefGoogle Scholar
  182. van der Hoorn RA, Wulff BB, Rivas S, Durrant MC, van der Ploeg A, de Wit PJ, Jones JD (2005) Structure-function analysis of cf-9, a receptor-like protein with extracytoplasmic leucine-rich repeats. Plant Cell 17:1000–1015PubMedCrossRefGoogle Scholar
  183. Vembar SS, Brodsky JL (2008) One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 9:944–957PubMedCrossRefGoogle Scholar
  184. Vert G, Nemhauser JL, Geldner N, Hong F, Chory J (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Cell Dev Biol 21:177–201PubMedCrossRefGoogle Scholar
  185. Vitale A, Boston RS (2008) Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic 9:1581–1588PubMedCrossRefGoogle Scholar
  186. von Numers N, Survila M, Aalto M, Batoux M, Heino P, Palva ET, Li J (2010) Requirement of a homolog of glucosidase II b-subunit for EFR-mediated defense signaling in Arabidopsis thaliana. Mol Plant 3:740–750CrossRefGoogle Scholar
  187. Wanderling S, Simen BB, Ostrovsky O, Ahmed NT, Vogen SM, Gidalevitz T, Argon Y (2007) GRP94 is essential for mesoderm induction and muscle development because it regulates insulin-like growth factor secretion. Mol Biol Cell 18:3764–3775PubMedCrossRefGoogle Scholar
  188. Wang D, Weaver ND, Kesarwani M, Dong X (2005a) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040PubMedCrossRefGoogle Scholar
  189. Wang N, Daniels R, Hebert DN (2005b) The cotranslational maturation of the type I membrane glycoprotein tyrosinase: the heat shock protein 70 system hands off to the lectin-based chaperone system. Mol Biol Cell 16:3740–3752PubMedCrossRefGoogle Scholar
  190. Werner ED, Brodsky JL, McCracken AA (1996) Proteasome-dependent endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate. Proc Natl Acad Sci USA 93:13797–13801PubMedCrossRefGoogle Scholar
  191. Williams DB (2006) Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum. J Cell Sci 119:615–623PubMedCrossRefGoogle Scholar
  192. Wilson JD, Liu Y, Bentivoglio CM, Barlowe C (2006) Sel1p/Ubx2p participates in a distinct Cdc48p-dependent endoplasmic reticulum-associated degradation pathway. Traffic 7:1213–1223PubMedCrossRefGoogle Scholar
  193. 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 49:1547–1562PubMedCrossRefGoogle Scholar
  194. 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 393:384–389PubMedCrossRefGoogle Scholar
  195. Yang Y, Li Z (2005) Roles of heat shock protein gp96 in the ER quality control: redundant or unique function? Mol Cells 20:173–182PubMedCrossRefGoogle Scholar
  196. Yang Y, Liu B, Dai J, Srivastava PK, Zammit DJ, Lefrancois L, Li Z (2007) Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26:215–226PubMedCrossRefGoogle Scholar
  197. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, Brown MS, Goldstein JL (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6:1355–1364PubMedCrossRefGoogle Scholar
  198. Ye Y, Shibata Y, Yun C, Ron D, Rapoport TA (2004) A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429:841–847PubMedCrossRefGoogle Scholar
  199. Yoshida Y, Tanaka K (2010) Lectin-like ERAD players in ER and cytosol. Biochim Biophys Acta 1800:172–180PubMedCrossRefGoogle Scholar
  200. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881–891PubMedCrossRefGoogle Scholar
  201. Zhang M, Henquet M, Chen Z, Zhang H, Zhang Y, Ren X, van der Krol S, Gonneau M, Bosch D, Gong Z (2009) LEW3, encoding a putative α1,2-mannosyltransferase (ALG11) in N-linked glycoprotein, plays vital roles in cell-wall biosynthesis and the abiotic stress response in Arabidopsis thaliana. Plant J 60:983–999PubMedCrossRefGoogle Scholar
  202. Zhu X, Zeng Y, Lehrman MA (1992) Evidence that the hamster tunicamycin resistance gene encodes UDP-GlcNAc:dolichol phosphate N-acetylglucosamine-1-phosphate transferase. J Biol Chem 267:8895–8902PubMedGoogle Scholar
  203. Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12:414–420PubMedCrossRefGoogle Scholar
  204. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.School of Life SciencesNanjing UniversityNanjingChina
  2. 2.Department of Molecular, Cellular, and Developmental BiologyUniversity of MichiganAnn ArborUSA

Personalised recommendations