The Research Progress of the Endoplasmic Reticulum（ER）Stress Response in Plant

doi:10.13560/j.cnki.biotech.bull.1985.2017-0996

Abstract

Abstract: Endoplasmic reticulum（ER）is a crucial site for the synthesis of membrane proteins and secretory proteins,as well as the preliminary modification of new peptides. Only the peptides that finished their preliminary modification like disulfide bonds formation,hydroxylation and glycosylation,they can enter the Golgi apparatus for further modification and eventually reach their correct protein conformation. However,the folding and modification process is complex and error-prone. If the cells face some endogenous or exogenous stresses,the probability of errors is greatly increased. The misfolded proteins were recognized and retained in ER by ER quality control system. The over-accumulated of the misfolded proteins in ER caused a series of response,which called ER stress response. They are mainly formed by UPR,ERAD,ERQC autophagy and cell death. These processes have been systematically studied in the field of yeasts and animals. This review mainly summarized the conserved mechanism in higher organism and the advances in the plant research. We hope to provide a reference for researchers who are concerned with the process of plant growth,development and plant stress response.

Key words: ER stress, UPR, ERAD, plant, stress

CHEN Qian, XIE Qi. The Research Progress of the Endoplasmic Reticulum（ER）Stress Response in Plant[J]. Biotechnology Bulletin, 2018, 34(1): 15-25.

References

[1] Castellani F, van Rossum B, Diehl A, et al. Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy[J]. Nature, 2002, 420（6911）：98-102.
[2] Schroder M, Kaufman RJ. ER stress and the unfolded protein response[J]. Mutat Res, 2005, 569（1-2）：29-63.
[3] Ellgaard L, Helenius A. Quality control in the endoplasmic reticulum[J]. Nat Rev Mol Cell Biol, 2003, 4（3）：181-191.
[4] Hurtley SM, Helenius A. Protein oligomerization in the endoplasmic reticulum[J]. Annu Rev Cell Biol, 1989, 5：277-307.
[5] Liu JX, Srivastava R, Che P, et al. Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling[J]. Plant J, 2007, 51（5）：897-909.
[6] Thomashow MF. PLANT COLD ACCLIMATION：freezing tolerance genes and regulatory mechanisms[J]. Annu Rev Plant Physiol Plant Mol Biol, 1999, 50：571-599.
[7] Deng Y, Humbert S, Liu JX, et al. Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis[J]. Proc Natl Acad Sci USA, 2011, 108（17）：7247-7252.
[8] Doblas VG, Amorim-Silva V, Pose D, et al. 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[J]. Plant Cell, 2013, 25（2）：728-743.
[9] 杨正婷, 刘建祥. 植物内质网胁迫应答研究进展[J]. 生物技术通报, 2016, 32（10）：84-96.
[10] Kanehara KS, Kawaguchi and Ng DT. The EDEM and Yos9p families of lectin-like ERAD factors[J]. Semin Cell Dev Biol, 2007, 18（6）：743-750.
[11] Clerc S, Hirsch C, Oggier DM, et al. Htm1 protein generates the N-glycan signal for glycoprotein degradation in the endoplasmic reticulum[J]. J Cell Biol, 2009, 184（1）：159-172.
[12] Hammond C, Braakman I, Helenius A. Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control[J]. Proc Natl Acad Sci USA, 1994, 91（3）：913-917.
[13] Parodi AJ. Protein glucosylation and its role in protein folding[J]. Annu Rev Biochem, 2000, 69：69-93.
[14] Jakob CA, Burda P, Roth J, et al. Degradation of misfolded endoplasmic reticulum glycoproteins in Saccharomyces cerevisiae is determined by a specific oligosaccharide structure[J]. J Cell Biol, 1998, 142（5）：1223-1233.
[15] Oda Y, Hosokawa N, Wada I, et al. EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin[J]. Science, 2003, 299（5611）：1394-1397.
[16] Vu KV, Nguyen NT, Jeong CY, et al. Systematic deletion of the ER lectin chaperone genes reveals their roles in vegetative growth and male gametophyte development in Arabidopsis[J]. Plant J, 2017, 89（5）：972-983.
[17] Noguchi T, Fujioka S, Choe S, et al. Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids[J]. Plant Physiol, 1999, 121（3）：743-752.
[18] Jin H, Hong Z, Su W, et al. A plant-specific calreticulin is a key retention factor for a defective brassinosteroid receptor in the endoplasmic reticulum[J]. Proc Natl Acad Sci USA, 2009, 106（32）：13612-13617.
[19] Blanco-Herrera F, Moreno AA, Tapia R, et al. 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[J]. BMC Plant Biol, 2015, 15：127.
[20] Liebminger E, Huttner S, Vavra U, et al. Class I alpha-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana[J]. Plant Cell, 2009, 21（12）：3850-3867.
[21] Huttner S, Veit C, Vavra U, et al. Arabidopsis class I alpha-manno-sidases MNS4 and MNS5 are involved in endoplasmic reticulum-associated degradation of misfolded glycoproteins[J]. Plant Cell, 2014, 26（4）：1712-1728.
[22] Gething MJ. Role and regulation of the ER chaperone BiP[J]. Semin Cell Dev Biol, 1999, 10（5）：465-472.
[23] Howell SH. Endoplasmic reticulum stress responses in plants[J]. Annu Rev Plant Biol, 2013, 64：477-499.
[24] Chakrabarti A, Chen AW, Varner JD. A review of the mammalian unfolded protein response[J]. Biotechnol Bioeng, 2011, 108（12）：2777-2793.
[25] Sun SY, Shi GJ, Sha HB, et al. IRE1 alpha is an endogenous substrate of endoplasmic-reticulum-associated degradation[J]. Nature Cell Biology, 2015, 17（12）：1546-1555.
[26] Chen X, Shen J, Prywes R. The luminal domain of ATF6 senses endoplasmic reticulum（ER）stress and causes translocation of ATF6 from the ER to the Golgi[J]. J Biol Chem, 2002, 277（15）：13045-13052.
[27] Kebache S, Cardin E, Nguyen DT, et al. Nck-1 antagonizes the endoplasmic reticulum stress-induced inhibition of translation[J]. J Biol Chem, 2004, 279（10）：9662-9671.
[28] Nagashima Y, Mishiba K, Suzuki E, et al. Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor[J]. Sci Rep, 2011, 1：29.
[29] Harding HP, Calfon M, Urano F, et al. Transcriptional and translational control in the Mammalian unfolded protein response[J]. Annu Rev Cell Dev Biol, 2002, 18：575-599.
[30] Kaufman RJ, Scheuner D, Schroder M, et al. The unfolded protein response in nutrient sensing and differentiation[J]. Nat Rev Mol Cell Biol, 2002, 3（6）：411-421.
[31] Kimata Y, Kimata YI, Shimizu Y, et al. Genetic evidence for a role of BiP/Kar2 that regulates Ire1 in response to accumulation of unfolded proteins[J]. Mol Biol Cell, 2003, 14（6）：2559-2569.
[32] Srivastava R, Chen YN, Deng Y, et al. Elements proximal to and within the transmembrane domain mediate the organelle-to-organelle movement of bZIP28 under ER stress conditions[J]. Plant Journal, 2012, 70（6）：1033-1042.
[33] Sun L, Lu SJ, Zhang SS, et al. The Lumen-facing domain is important for the biological function and organelle-to-organelle movement of bZIP28 during ER stress in Arabidopsis[J]. Mol Plant, 2013, 6（5）：1605-1615.
[34] Liu JX, Srivastava R. Che P, et al. An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28[J]. Plant Cell, 2007, 19（12）：4111-4119.
[35] Che P, Bussell JD, Zhou W, et al. Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis[J]. Sci Signal, 2010, 3（141）：ra69.
[36] Liu JX, Howell SH. Managing the protein folding demands in the endoplasmic reticulum of plants[J]. New Phytol, 2016, 211（2）：418-428.
[37] Gao H, Brandizzi F, Benning C, et al. A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana[J]. Proc Natl Acad Sci USA, 2008, 105（42）：16398-16403.
[38] Liu JX, Howell SH. Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants[J]. Plant Cell, 2010, 22（9）：2930-2942.
[39] Zhang SS, Yang H, Ding L, et al. Tissue-specific transcriptomics reveals an important role of the unfolded protein response in maintaining fertility upon heat stress in Arabidopsis[J]. Plant Cell, 2017, 29：1007-1023.
[40] Yang ZT, Wang MJ, Sun L, et al. The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants[J]. PLoS Genet, 2014, 10（3）：e1004243.
[41] Yang ZT, Lu SJ, Wang MJ, et al. A plasma membrane-tethered transcription factor, NAC062/ANAC062/NTL6, mediates the unfolded protein response in Arabidopsis[J]. Plant J, 2014, 79（6）：1033-1043.
[42] Seo PJ, Kim MJ, Park JY, et al. Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis[J]. Plant J, 2010, 61（4）：661-671.
[43] McCracken AA, Brodsky JL. Assembly of ER-associated protein degradation in vitro：dependence on cytosol, calnexin, and ATP[J]. J Cell Biol, 1996, 132（3）：291-298.
[44] Buchberger A. ERQC Autophagy：yet another way to die[J]. Mol Cell, 2014, 54（1）：3-4.
[45] Houck SA, Ren HY, Madden VJ, et al. Quality control autophagy degrades soluble erad-resistant conformers of the misfolded membrane protein GnRHR[J]. Mol Cell, 2014, 54（1）：166-179.
[46] Vembar SS, Brodsky JL. One step at a time：endoplasmic reticulum-associated degradation[J]. Nat Rev Mol Cell Biol, 2008, 9（12）：944-957.
[47] Imai Y. Parkin suppresses unfolded protein stress-induced cell death through Its E3 Ubiquitin-protein ligase activity[J]. Journal of Biological Chemistry, 2000, 275（46）：35661-35664.
[48] Liu LJ, Cui F, Li QL, et al. The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance[J]. Cell Res, 2011, 21（6）：957-969.
[49] Koenig PA, Nicholls PK, Schmidt FI, et al. The E2 ubiquitin-conjugating enzyme UBE2J1 is required for spermiogenesis in mice[J]. Journal of Biological Chemistry, 2014, 289（50）：34490-34502.
[50] Sun S, Shi G, Han X, et al. Sel1L is indispensable for mammalian endoplasmic reticulum-associated degradation, endoplasmic reticulum homeostasis, and survival[J]. Proc Natl Acad Sci USA, 2014, 111（5）：E582-591.
[51] Wang YY, Wang WH, Cai JH, et al. Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening[J]. Genome Biology, 2014, 15（12）.
[52] Ushioda R, Hoseki J, Nagata K. Glycosylation-independent ERAD pathway serves as a backup system under ER stress[J]. Mol Biol Cell, 2013, 24（20）：3155-3163.
[53] Fu XL, Gao DS. Endoplasmic reticulum proteins quality control and the unfolded protein response：the regulative mechanism of organisms against stress injuries[J]. Biofactors, 2014, 40（6）：569-585.
[54] Su W, Liu Y, Xia Y, et al. The Arabidopsis homolog of the mammalian OS-9 protein plays a key role in the endoplasmic reticulum-associated degradation of misfolded receptor-like kinases[J]. Mol Plant, 2012, 5（4）：929-940.
[55] Huttner S, Veit C, Schoberer J, et al. Unraveling the function of Arabidopsis thaliana OS9 in the endoplasmic reticulum-associated degradation of glycoproteins[J]. Plant Mol Biol, 2012, 79（1-2）：21-33.
[56] Wiertz EJ, Tortorella D, Bogyo M, et al. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction[J]. Nature, 1996, 384（6608）：432-438.
[57] Pilon M, Schekman R, Romisch K. Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation[J]. EMBO J, 1997, 16（15）：4540-4548.
[58] Knop M, Finger A, Braun T, et al. Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast[J]. EMBO J, 1996, 15（4）：753-763.
[59] Carvalho P, Stanley AM, Rapoport TA. Retrotranslocation of a misfolded luminal ER protein by the ubiquitin-ligase Hrd1p[J]. Cell, 2010, 143（4）：579-591.
[60] Schoebel S, Mi W, Stein A, et al. Cryo-EM structure of the protein-conducting ERAD channel Hrd1 in complex with Hrd3[J]. Nature, 2017, 548（7667）：352-355.
[61] Chen Q, Zhong YW, Wu YR, et al. HRD1-mediated ERAD tuning of ER-bound E2 is conserved between plants and mammals[J]. Nat Plants, 2016, 2：16094.
[62] Li QL, Wei H, Liu LJ, et al. Unfolded protein response activation compensates endoplasmic reticulum-associated degradation deficiency in Arabidopsis[J]. J Integr Plant Biol, 2017, 59（7）：506-521.
[63] Zhao H, Zhang H, Cui P, et al. The Putative E3 ubiquitin ligase ECERIFERUM9 regulates abscisic acid biosynthesis and response during seed germination and postgermination growth in Arabidopsis[J]. Plant Physiol, 2014, 165（3）：1255-1268.
[64] Li LM, Lu SY, Li RJ, The Arabidopsis endoplasmic reticulum associated degradation pathways are involved in the regulation of heat stress response[J]. Biochem Biophys Res Commun, 2017, 487（2）：362-367.
[65] Merulla J, Fasana E, Solda T, et al. Specificity and regulation of the endoplasmic reticulum-associated degradation machinery[J]. Traffic, 2013, 14（7）：767-777.
[66] Chen Q, Liu RJ. Wang Q, et al. ERAD Tuning of the HRD1 complex component AtOS9 is modulated by an ER-Bound E2, UBC32[J]. Mol Plant, 2017, 10（6）：891-894.
[67] Perlmutter DH. Alpha-1-antitrypsin deficiency：importance of proteasomal and autophagic degradative pathways in disposal of liver disease-associated protein aggregates[J]. Annu Rev Med, 2011, 62：333-345.
[68] Feng L, et al. Ubiquitin ligase SYVN1/HRD1 facilitates degradation of the SERPINA1 Z variant/alpha-1-antitrypsin Z variant via SQSTM1/p62-dependent selective autophagy[J]. Autophagy, 2017, 13（4）：686-702.
[69] Yang X, Srivastava R, Howell SH, et al. Activation of autophagy by unfolded proteins during endoplasmic reticulum stress[J]. Plant J, 2016, 85（1）：83-95.
[70] Liu Y, Burgos JS, Deng Y, et al. Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis[J]. Plant Cell, 2012, 24（11）：4635-4651.
[71] Gallois P, Makishima T, Hecht V, et al. An Arabidopsis thaliana cDNA complementing a hamster apoptosis suppressor mutant[J]. Plant J, 1997, 11（6）：1325-1331.
[72] Danon A, Rotari VI, Gordon A, et al. Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and defender against apoptotic death[J]. J Biol Chem, 2004, 279（1）：779-787.
[73] Lerouxel O, Mouille G, Andeme-Onzighi C, et al. Mutants in DEFECTIVE GLYCOSYLATION, an Arabidopsis homolog of an oligosaccharyltransferase complex subunit, show protein underglycosylation and defects in cell differentiation and growth[J]. Plant J, 2005, 42（4）：455-468.
[74] Koiwa H, Li F, McCully MG, et al. The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress[J]. Plant Cell, 2003, 15（10）：2273-2284.
[75] Su W, Liu Y, Xia Y, et al. Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis[J]. Proc Natl Acad Sci USA, 2011, 108 （2）：870-875.
[76] Lee HK, Cho SK, Son O, et al. Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic plants[J]. Plant Cell, 2013, 21（2）：622-641.
[77] Cui F, Liu LJ, Zhao QZ, et al. Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance [J]. Plant Cell, 2012, 24（1）：233-244.
[78] van Nocker S, Walker JM, Vierstra RD. The Arabidopsis thaliana UBC7/13/14 genes encode a family of multiubiquitin chain-forming E2 enzymes[J]. J Biol Chem, 1996, 271（21）：12150-12158.