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PMID: 26556351 Published · epublish English Journal Article Research Support, Non-U.S. Gov't Review

Endoplasmic Reticulum Stress Signaling in Plant Immunity--At the Crossroad of Life and Death.

International journal of molecular sciences ·Vol. 16 ·No. 11 ·2015-11-05 ·Pages 26582-98

Kørner CJ, Du X, Vollmer ME, Pajerowska-Mukhtar KM

Abstract

Rapid and complex immune responses are induced in plants upon pathogen recognition. One form of plant defense response is a programmed burst in transcription and translation of pathogenesis-related proteins, of which many rely on ER processing. Interestingly, several ER stress marker genes are up-regulated during early stages of immune responses, suggesting that enhanced ER capacity is needed for immunity. Eukaryotic cells respond to ER stress through conserved signaling networks initiated by specific ER stress sensors tethered to the ER membrane. Depending on the nature of ER stress the cell prioritizes either survival or initiates programmed cell death (PCD). At present two plant ER stress sensors, bZIP28 and IRE1, have been described. Both sensor proteins are involved in ER stress-induced signaling, but only IRE1 has been additionally linked to immunity. A second branch of immune responses relies on PCD. In mammals, ER stress sensors are involved in activation of PCD, but it is unclear if plant ER stress sensors play a role in PCD. Nevertheless, some ER resident proteins have been linked to pathogen-induced cell death in plants. In this review, we will discuss the current understanding of plant ER stress signaling and its cross-talk with immune signaling.

Keywords
Arabidopsis ER stress signaling IRE1 plant immune responses programmed cell death
MeSH Terms
Animals Apoptosis Endoplasmic Reticulum Stress Host-Pathogen Interactions Plant Immunity Plant Physiological Phenomena Signal Transduction
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kørner Camilla J
Department of Biology, University of Alabama at Birmingham, 1300 University Blvd., Birmingham, AL 35294, USA. ckoerner@uab.edu.
Du Xinran
Department of Biology, University of Alabama at Birmingham, 1300 University Blvd., Birmingham, AL 35294, USA. xinrandu@uab.edu.
Vollmer Marie E
Department of Biology, University of Alabama at Birmingham, 1300 University Blvd., Birmingham, AL 35294, USA. mvollmer@uab.edu.
Pajerowska-Mukhtar Karolina M
Department of Biology, University of Alabama at Birmingham, 1300 University Blvd., Birmingham, AL 35294, USA. kmukhtar@uab.edu.
References (122)
122 references, click to expand
  1. ER stress, autophagy, and RNA viruses.
    Front Microbiol. 2014 Aug 05;5:388 PMID: 25140166
  2. Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling.
    Plant J. 2007 Sep;51(5):897-909 PMID: 17662035
  3. Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele.
    Proc Natl Acad Sci U S A. 2009 Dec 29;106(52):22522-7 PMID: 20007779
  4. BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1alpha.
    Mol Cell. 2009 Mar 27;33(6):679-91 PMID: 19328063
  5. Independently evolved virulence effectors converge onto hubs in a plant immune system network.
    Science. 2011 Jul 29;333(6042):596-601 PMID: 21798943
  6. Stress management at the ER: regulators of ER stress-induced apoptosis.
    Pharmacol Ther. 2012 Jun;134(3):306-16 PMID: 22387231
  7. Conserved and plant-unique strategies for overcoming endoplasmic reticulum stress.
    Front Plant Sci. 2014 Feb 26;5:69 PMID: 24616733
  8. Membrane aberrancy and unfolded proteins activate the endoplasmic reticulum stress sensor Ire1 in different ways.
    Mol Biol Cell. 2011 Sep;22(18):3520-32 PMID: 21775630
  9. Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis.
    Plant J. 2010 Feb;61(4):661-71 PMID: 19947982
  10. TGBp3 triggers the unfolded protein response and SKP1-dependent programmed cell death.
    Mol Plant Pathol. 2013 Apr;14(3):241-55 PMID: 23458484
  11. BAX inhibitor-1 regulates autophagy by controlling the IRE1α branch of the unfolded protein response.
    EMBO J. 2011 Nov 2;30(21):4465-78 PMID: 21926971
  12. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase.
    Cell. 1993 Jun 18;73(6):1197-206 PMID: 8513503
  13. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis.
    Science. 2003 Apr 4;300(5616):135-9 PMID: 12624178
  14. AtBAG7, an Arabidopsis Bcl-2-associated athanogene, resides in the endoplasmic reticulum and is involved in the unfolded protein response.
    Proc Natl Acad Sci U S A. 2010 Mar 30;107(13):6088-93 PMID: 20231441
  15. Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR.
    Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15973-8 PMID: 19717464
  16. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response.
    Science. 2006 Jul 7;313(5783):104-7 PMID: 16825573
  17. Classes of programmed cell death in plants, compared to those in animals.
    J Exp Bot. 2011 Oct;62(14):4749-61 PMID: 21778180
  18. Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response.
    Science. 2011 Sep 30;333(6051):1891-4 PMID: 21852455
  19. Induction of protein secretory pathway is required for systemic acquired resistance.
    Science. 2005 May 13;308(5724):1036-40 PMID: 15890886
  20. The dynamic of the splicing of bZIP60 and the proteins encoded by the spliced and unspliced mRNAs reveals some unique features during the activation of UPR in Arabidopsis thaliana.
    PLoS One. 2015;10(4):e0122936 PMID: 25860807
  21. MicroRNA-30c-2* limits expression of proadaptive factor XBP1 in the unfolded protein response.
    J Cell Biol. 2012 Mar 19;196(6):689-98 PMID: 22431749
  22. BINDING PROTEIN is a master regulator of the endoplasmic reticulum stress sensor/transducer bZIP28 in Arabidopsis.
    Plant Cell. 2013 Apr;25(4):1416-29 PMID: 23624714
  23. Spatial analysis of arabidopsis thaliana gene expression in response to Turnip mosaic virus infection.
    Mol Plant Microbe Interact. 2007 Apr;20(4):358-70 PMID: 17427806
  24. Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana.
    J Biol Chem. 2005 Sep 23;280(38):32914-20 PMID: 16043487
  25. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum.
    Genes Dev. 2004 Dec 15;18(24):3066-77 PMID: 15601821
  26. Functional integration between defence and IRE1-mediated ER stress response in rice.
    Sci Rep. 2012;2:670 PMID: 22993695
  27. Loss of calmodulin binding to Bax inhibitor-1 affects Pseudomonas-mediated hypersensitive response-associated cell death in Arabidopsis thaliana.
    J Biol Chem. 2009 Oct 9;284(41):27998-8003 PMID: 19674971
  28. The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants.
    PLoS Genet. 2014 Mar;10(3):e1004243 PMID: 24675811
  29. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase.
    Nature. 1999 Jan 21;397(6716):271-4 PMID: 9930704
  30. Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase.
    Nat Chem Biol. 2014 Jun;10(6):450-6 PMID: 24776930
  31. Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme.
    J Biol Chem. 1991 Aug 5;266(22):14486-90 PMID: 1860857
  32. Significance of inducible defense-related proteins in infected plants.
    Annu Rev Phytopathol. 2006;44:135-62 PMID: 16602946
  33. The Pseudomonas syringae type III effector HopD1 suppresses effector-triggered immunity, localizes to the endoplasmic reticulum, and targets the Arabidopsis transcription factor NTL9.
    New Phytol. 2014 Mar;201(4):1358-70 PMID: 24329768
  34. The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death.
    Plant Cell. 2012 Feb;24(2):794-809 PMID: 22337916
  35. AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis.
    Plant J. 2012 Jan;69(2):266-77 PMID: 21914012
  36. Activating transcription factor-6 (ATF6) mediates apoptosis with reduction of myeloid cell leukemia sequence 1 (Mcl-1) protein via induction of WW domain binding protein 1.
    J Biol Chem. 2011 Oct 7;286(40):35227-35 PMID: 21841196
  37. Arabidopsis heterotrimeric G-proteins play a critical role in host and nonhost resistance against Pseudomonas syringae pathogens.
    PLoS One. 2013;8(12):e82445 PMID: 24349286
  38. Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid.
    Proc Natl Acad Sci U S A. 2015 Jul 28;112(30):9166-73 PMID: 26139525
  39. Metacaspase-8 modulates programmed cell death induced by ultraviolet light and H2O2 in Arabidopsis.
    J Biol Chem. 2008 Jan 11;283(2):774-83 PMID: 17998208
  40. Regulated translation initiation controls stress-induced gene expression in mammalian cells.
    Mol Cell. 2000 Nov;6(5):1099-108 PMID: 11106749
  41. Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains.
    Proc Natl Acad Sci U S A. 2013 Mar 19;110(12):4628-33 PMID: 23487760
  42. Arabidopsis eIF2alpha kinase GCN2 is essential for growth in stress conditions and is activated by wounding.
    BMC Plant Biol. 2008;8:134 PMID: 19108716
  43. Control of Tobacco mosaic virus movement protein fate by CELL-DIVISION-CYCLE protein48.
    Plant Physiol. 2012 Dec;160(4):2093-108 PMID: 23027663
  44. Elevated ATF4 expression, in the absence of other signals, is sufficient for transcriptional induction via CCAAT enhancer-binding protein-activating transcription factor response elements.
    J Biol Chem. 2009 Aug 7;284(32):21241-8 PMID: 19509279
  45. Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions.
    Plant Physiol. 2005 Mar;137(3):1147-59 PMID: 15728340
  46. A NAC transcription factor and SNI1 cooperatively suppress basal pathogen resistance in Arabidopsis thaliana.
    Nucleic Acids Res. 2012 Oct;40(18):9182-92 PMID: 22826500
  47. Extra-Large G Proteins Expand the Repertoire of Subunits in Arabidopsis Heterotrimeric G Protein Signaling.
    Plant Physiol. 2015 Sep;169(1):512-29 PMID: 26157115
  48. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor.
    Cell. 2001 Dec 28;107(7):881-91 PMID: 11779464
  49. A meta-analysis reveals the commonalities and differences in Arabidopsis thaliana response to different viral pathogens.
    PLoS One. 2012;7(7):e40526 PMID: 22808182
  50. Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response.
    Plant Cell. 2008 Nov;20(11):3107-21 PMID: 19017746
  51. Endoplasmic reticulum-quality control chaperones facilitate the biogenesis of Cf receptor-like proteins involved in pathogen resistance of tomato.
    Plant Physiol. 2012 Aug;159(4):1819-33 PMID: 22649272
  52. 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 U S A. 2011 Apr 26;108(17):7247-52 PMID: 21482766
  53. Bcl-2 family on guard at the ER.
    Am J Physiol Cell Physiol. 2009 May;296(5):C941-53 PMID: 19279228
  54. Plant ERD2-like proteins function as endoplasmic reticulum luminal protein receptors and participate in programmed cell death during innate immunity.
    Plant J. 2012 Oct;72(1):57-69 PMID: 22595145
  55. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  56. The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum.
    Plant Cell. 2014 Jan;26(1):497-515 PMID: 24488961
  57. BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis.
    J Biol Chem. 2008 Feb 8;283(6):3200-10 PMID: 18039663
  58. Rice black-streaked dwarf virus P10 induces membranous structures at the ER and elicits the unfolded protein response in Nicotiana benthamiana.
    Virology. 2013 Dec;447(1-2):131-9 PMID: 24210107
  59. The plant-specific transcription factor gene NAC103 is induced by bZIP60 through a new cis-regulatory element to modulate the unfolded protein response in Arabidopsis.
    Plant J. 2013 Oct;76(2):274-86 PMID: 23869562
  60. Vacuolar processing enzyme: an executor of plant cell death.
    Curr Opin Plant Biol. 2005 Aug;8(4):404-8 PMID: 15939660
  61. GCN2-dependent phosphorylation of eukaryotic translation initiation factor-2alpha in Arabidopsis.
    J Exp Bot. 2008;59(11):3131-41 PMID: 18603615
  62. IRE1: ER stress sensor and cell fate executor.
    Trends Cell Biol. 2013 Nov;23(11):547-55 PMID: 23880584
  63. Cloning of mammalian Ire1 reveals diversity in the ER stress responses.
    EMBO J. 1998 Oct 1;17(19):5708-17 PMID: 9755171
  64. The unfolded protein response is triggered by a plant viral movement protein.
    Plant Physiol. 2011 Jun;156(2):741-55 PMID: 21474436
  65. Molecular characterization of two Arabidopsis Ire1 homologs, endoplasmic reticulum-located transmembrane protein kinases.
    Plant Physiol. 2001 Nov;127(3):949-62 PMID: 11706177
  66. Stress sensing in plants by an ER stress sensor/transducer, bZIP28.
    Front Plant Sci. 2014 Feb 26;5:59 PMID: 24616727
  67. Unfolded protein response in plants: one master, many questions.
    Curr Opin Plant Biol. 2015 Oct;27:59-66 PMID: 26149756
  68. The UPR branch IRE1-bZIP60 in plants plays an essential role in viral infection and is complementary to the only UPR pathway in yeast.
    PLoS Genet. 2015 Apr;11(4):e1005164 PMID: 25875739
  69. Caspases and programmed cell death in the hypersensitive response of plants to pathogens.
    Curr Biol. 1998 Oct 8;8(20):1129-32 PMID: 9778530
  70. Bax Inhibitor-1, a conserved cell death suppressor, is a key molecular switch downstream from a variety of biotic and abiotic stress signals in plants.
    Int J Mol Sci. 2009 Jun;10(7):3149-67 PMID: 19742129
  71. An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus.
    PLoS Pathog. 2013;9(10):e1003670 PMID: 24130484
  72. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus.
    EMBO J. 1996 Jun 17;15(12):3028-39 PMID: 8670804
  73. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma.
    Mol Cell. 2000 Oct;6(4):961-7 PMID: 11090634
  74. A kiss of death--proteasome-mediated membrane fusion and programmed cell death in plant defense against bacterial infection.
    Genes Dev. 2009 Nov 1;23(21):2449-54 PMID: 19884251
  75. The HSF-like transcription factor TBF1 is a major molecular switch for plant growth-to-defense transition.
    Curr Biol. 2012 Jan 24;22(2):103-12 PMID: 22244999
  76. Characterization of Arabidopsis thaliana GCN2 kinase roles in seed germination and plant development.
    Plant Signal Behav. 2015;10(4):e992264 PMID: 25912940
  77. Functional interplay between Arabidopsis NADPH oxidases and heterotrimeric G protein.
    Mol Plant Microbe Interact. 2013 Jun;26(6):686-94 PMID: 23441575
  78. Dissecting Arabidopsis Gβ signal transduction on the protein surface.
    Plant Physiol. 2012 Jul;159(3):975-83 PMID: 22570469
  79. The endoplasmic reticulum binding protein BiP displays dual function in modulating cell death events.
    Plant Physiol. 2014 Feb;164(2):654-70 PMID: 24319082
  80. Heterotrimeric G proteins serve as a converging point in plant defense signaling activated by multiple receptor-like kinases.
    Plant Physiol. 2013 Apr;161(4):2146-58 PMID: 23424249
  81. Signal transduction by IRE1-mediated splicing of bZIP50 and other stress sensors in the endoplasmic reticulum stress response of rice.
    Plant J. 2012 Mar;69(6):946-56 PMID: 22050533
  82. The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation.
    Plant J. 2008 Dec;56(6):984-96 PMID: 18702674
  83. Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis.
    Sci Signal. 2010;3(141):ra69 PMID: 20876872
  84. An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28.
    Plant Cell. 2007 Dec;19(12):4111-9 PMID: 18156219
  85. Defects in IRE1 enhance cell death and fail to degrade mRNAs encoding secretory pathway proteins in the Arabidopsis unfolded protein response.
    Proc Natl Acad Sci U S A. 2013 Apr 2;110(14):5713-8 PMID: 23509268
  86. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1.
    Science. 2000 Jan 28;287(5453):664-6 PMID: 10650002
  87. Enhanced calreticulin expression promotes calcium-dependent apoptosis in postnatal cardiomyocytes.
    Mol Cells. 2008 May 31;25(3):390-6 PMID: 18443415
  88. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death.
    Science. 2004 Aug 6;305(5685):855-8 PMID: 15297671
  89. A plasma membrane-tethered transcription factor, NAC062/ANAC062/NTL6, mediates the unfolded protein response in Arabidopsis.
    Plant J. 2014 Sep;79(6):1033-43 PMID: 24961665
  90. Proglobulin processing enzyme in vacuoles isolated from developing pumpkin cotyledons.
    Plant Physiol. 1987 Oct;85(2):440-5 PMID: 16665717
  91. Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants.
    Cell Host Microbe. 2009 Nov 19;6(5):457-69 PMID: 19917500
  92. The heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice.
    Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):13307-12 PMID: 12237405
  93. Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation.
    Autophagy. 2008 Oct;4(7):949-51 PMID: 18769111
  94. ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response.
    Mol Cell Biol. 2000 Sep;20(18):6755-67 PMID: 10958673
  95. Overexpression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance to Blumeria graminis.
    Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5555-60 PMID: 12704231
  96. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses.
    Science. 1998 Jun 12;280(5370):1763-6 PMID: 9624056
  97. Molecular cloning of an arabidopsis homologue of GCN2, a protein kinase involved in co-ordinated response to amino acid starvation.
    Planta. 2003 Aug;217(4):668-75 PMID: 12905023
  98. Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants.
    Plant J. 2003 Jan;33(2):271-83 PMID: 12535341
  99. Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis.
    Proc Natl Acad Sci U S A. 2013 Nov 26;110(48):19633-8 PMID: 24145452
  100. IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses.
    PLoS One. 2012;7(2):e31944 PMID: 22359644
  101. Heterotrimeric G protein-coupled signaling in plants.
    Annu Rev Plant Biol. 2014;65:365-84 PMID: 24313842
  102. A membrane-bound NAC transcription factor as an integrator of biotic and abiotic stress signals.
    Plant Signal Behav. 2010 May;5(5):481-3 PMID: 20139739
  103. Plant-bacterial pathogen interactions mediated by type III effectors.
    Curr Opin Plant Biol. 2012 Aug;15(4):469-76 PMID: 22465133
  104. Keeping the eIF2 alpha kinase Gcn2 in check.
    Biochim Biophys Acta. 2014 Sep;1843(9):1948-68 PMID: 24732012
  105. The unfolded protein response: from stress pathway to homeostatic regulation.
    Science. 2011 Nov 25;334(6059):1081-6 PMID: 22116877
  106. Receptor quality control in the endoplasmic reticulum for plant innate immunity.
    EMBO J. 2009 Nov 4;28(21):3439-49 PMID: 19763087
  107. Membrane-associated transcription factor peptidase, site-2 protease, antagonizes ABA signaling in Arabidopsis.
    New Phytol. 2015 Oct;208(1):188-97 PMID: 25919792
  108. IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates.
    Cell. 2009 Aug 7;138(3):562-75 PMID: 19665977
  109. Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis.
    J Cell Biol. 2009 Sep 21;186(6):783-92 PMID: 19752026
  110. Arabidopsis extra large G-protein 2 (XLG2) interacts with the Gbeta subunit of heterotrimeric G protein and functions in disease resistance.
    Mol Plant. 2009 May;2(3):513-25 PMID: 19825634
  111. A unique vacuolar processing enzyme responsible for conversion of several proprotein precursors into the mature forms.
    FEBS Lett. 1991 Dec 2;294(1-2):89-93 PMID: 1743299
  112. Live to die another way: modes of programmed cell death and the signals emanating from dying cells.
    Nat Rev Mol Cell Biol. 2015 Jun;16(6):329-44 PMID: 25991373
  113. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells.
    J Biol Chem. 2004 Oct 29;279(44):45495-502 PMID: 15322075
  114. Arabidopsis type I metacaspases control cell death.
    Science. 2010 Dec 3;330(6009):1393-7 PMID: 21097903
  115. Heterotrimeric G protein signaling in the Arabidopsis unfolded protein response.
    Proc Natl Acad Sci U S A. 2007 Mar 6;104(10):3817-22 PMID: 17360436
  116. The role of vacuole in plant cell death.
    Cell Death Differ. 2011 Aug;18(8):1298-304 PMID: 21637288
  117. GmNAC30 and GmNAC81 integrate the endoplasmic reticulum stress- and osmotic stress-induced cell death responses through a vacuolar processing enzyme.
    Proc Natl Acad Sci U S A. 2013 Nov 26;110(48):19627-32 PMID: 24145438
  118. Exogenous salicylic acid activates two signaling arms of the unfolded protein response in Arabidopsis.
    Plant Cell Physiol. 2014 Oct;55(10):1772-8 PMID: 25138441
  119. Multiple roles of the ER stress sensor IRE1 demonstrated by gene targeting in rice.
    Sci Rep. 2012;2:944 PMID: 23230509
  120. Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity.
    EMBO J. 2009 Nov 4;28(21):3428-38 PMID: 19763086
  121. Function of endoplasmic reticulum calcium ATPase in innate immunity-mediated programmed cell death.
    EMBO J. 2010 Mar 3;29(5):1007-18 PMID: 20075858
  122. JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis.
    Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2432-7 PMID: 12591950
Article Info
Journal
International journal of molecular sciences
Abbr.
Int J Mol Sci
ISSN
1422-0067
Published
2015-11-05
Epub
2015-00-05
Pages
26582-98
Language
English
Region
Switzerland
NLM ID
101092791
PMCID
PMC4661823
Subset
IM
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