title: Glutamate receptor-like channel3.3 is involved in mediating glutathione-triggered cytosolic calcium transients, transcriptional changes, and innate immunity responses in Arabidopsis.
abstract: The tripeptide reduced glutathione (GSH; γ-glutamate [Glu]-cysteine [Cys]-glycine) is a major endogenous antioxidant in both animal and plant cells. It also functions as a neurotransmitter mediating communication among neurons in the central nervous system of animals through modulating specific ionotropic Glu receptors (GLRs) in the membrane. Little is known about such signaling roles in plant cells. Here, we report that transient rises in cytosolic calcium triggered by exogenous GSH in Arabidopsis (Arabidopsis thaliana) leaves were sensitive to GLR antagonists and abolished in loss-of-function atglr3.3 mutants. Like the GSH biosynthesis-defective mutant PHYTOALEXIN DEFICIENT2, atglr3.3 showed enhanced susceptibility to the bacterial pathogen Pseudomonas syringae pv tomato DC3000. Pathogen-induced defense marker gene expression was also decreased in atglr3.3 mutants. Twenty-seven percent of genes that were rapidly responsive to GSH treatment of seedlings were defense genes, most of which were dependent on functional AtGLR3.3, while GSH suppressed pathogen propagation through the AtGLR3.3-dependent pathway. Eight previously identified putative AtGLR3.3 ligands, GSH, oxidized glutathione, alanine, asparagine, Cys, Glu, glycine, and serine, all elicited the AtGLR3.3-dependent cytosolic calcium transients, but only GSH and Cys induced the defense response, with the Glu-induced AtGLR3.3-dependent transcription response being much less apparent than that triggered by GSH. Together, these observations suggest that AtGLR3.3 is required for several signaling effects mediated by extracellular GSH, even though these effects may not be causally related.
authors: College of Life Sciences, Inner Mongolia University, Hohhot 010021, China.
authors: Feng
authors: F
authors: Li
authors: Jing
authors: J
authors: Wang
authors: Chunli
authors: C
authors: Ma
authors: Yongxiu
authors: Y
authors: Zhao
authors: Yingchun
authors: Y
authors: Wang
authors: Agula
authors: A
authors: Hasi
authors: Zhi
authors: Z
authors: Qi
mesh_terms: D017360:Arabidopsis / Q000187:drug effects / Q000276:immunology* / Q000378:metabolism / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000276:immunology / Q000378:metabolism*; D002118:Calcium / Q000378:metabolism*; D003600:Cytosol / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D005978:Glutathione / Q000378:metabolism* / Q000494:pharmacology; D007113:Immunity, Innate / Q000187:drug effects; D008024:Ligands; D009154:Mutation; D018515:Plant Leaves / Q000187:drug effects / Q000235:genetics / Q000276:immunology; D030821:Plants, Genetically Modified; D044224:Pseudomonas syringae / Q000472:pathogenicity; D017470:Receptors, Glutamate / Q000235:genetics / Q000276:immunology / Q000378:metabolism*; D036226:Seedlings / Q000235:genetics / Q000276:immunology / Q000382:microbiology
chemical_list: D029681:Arabidopsis Proteins; C516468:GLR3.3 protein, Arabidopsis; D008024:Ligands; D017470:Receptors, Glutamate; D005978:Glutathione; D002118:Calcium
references: Plant Physiol. 2007 Feb;143(2):784-800
references: 17142483
references: Arabidopsis Book. 2011;9:e0154
references: 22303278
references: Plant Physiol. 2000 Aug;123(4):1289-300
references: 10938348
references: Antioxid Redox Signal. 2013 Jun 1;18(16):2106-21
references: 23148658
references: Nature. 1991 Aug 8;352(6335):524-6
references: 1865907
references: Plant Mol Biol. 2012 Jun;79(3):217-27
references: 22481162
references: Wiley Interdiscip Rev Membr Transp Signal. 2012 Mar;1(2):136-150
references: 22662309
references: Mol Pharmacol. 1992 Feb;41(2):308-14
references: 1347146
references: Arabidopsis Book. 2010;8:e0129
references: 22303255
references: Proc Natl Acad Sci U S A. 2010 Oct 19;107(42):18220-5
references: 20921422
references: Arabidopsis Book. 2011;9:e0142
references: 22303267
references: Oncogene. 2003 Dec 18;22(58):9275-81
references: 14681686
references: Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8955-9
references: 8090752
references: Neuroscience. 2000;95(2):617-24
references: 10658641
references: Proc Natl Acad Sci U S A. 2009 Dec 8;106(49):20995-1000
references: 19933332
references: Proc Natl Acad Sci U S A. 2010 May 18;107(20):9452-7
references: 20439716
references: Mol Biol Evol. 2001 Jul;18(7):1417-20
references: 11420380
references: Acta Pharmacol Sin. 2006 Jul;27(7):853-60
references: 16787569
references: J Pharmacol Sci. 2008 Nov;108(3):227-38
references: 19008644
references: Arabidopsis Book. 2002;1:e0039
references: 22303207
references: J Exp Bot. 2012 Sep;63(14):4995-5001
references: 22516796
references: Prog Neurobiol. 2000 Dec;62(6):649-71
references: 10880854
references: Plant Physiol. 2002 Jan;128(1):21-9
references: 11788749
references: Plant Cell. 1996 Feb;8(2):241-9
references: 8742710
references: Plant J. 2007 Jan;49(1):159-72
references: 17144898
references: J Biol Chem. 1997 Mar 14;272(11):7069-77
references: 9054399
references: Science. 2007 Mar 9;315(5817):1423-6
references: 17347443
references: J Biol Chem. 2009 Apr 10;284(15):9742-54
references: 19189963
references: Mol Plant Microbe Interact. 2012 May;25(5):684-96
references: 22295908
references: Plant Physiol. 2003 Jun;132(2):606-17
references: 12805591
references: Plant Cell Environ. 2013 Jun;36(6):1135-46
references: 23210597
references: FEBS Lett. 2011 Jun 6;585(11):1521-8
references: 21536040
references: Neuroreport. 1991 Jun;2(6):345-7
references: 1832987
references: Plant Cell Environ. 2012 Aug;35(8):1483-99
references: 22394204
references: Plant Signal Behav. 2012 Feb;7(2):210-2
references: 22353869
references: Plant Cell. 2004 Sep;16(9):2448-62
references: 15308753
references: J Plant Physiol. 2008 Sep 8;165(13):1390-403
references: 18171593
references: Plant J. 2008 Sep;55(5):774-86
references: 18466300
references: Plant J. 2012 Mar;69(6):1006-17
references: 22066515
references: Plant J. 2004 Jan;37(1):9-20
references: 14675428
references: Nature. 1998 Nov 12;396(6707):125-6
references: 9823891
references: Plant Signal Behav. 2012 Nov;7(11):1373-7
references: 22918498
references: Plant Physiol. 2008 Feb;146(2):529-38
references: 18162597
references: Science. 2001 May 25;292(5521):1486-7
references: 11379626
references: Proc Natl Acad Sci U S A. 2003 May 27;100(11):6872-7
references: 12738881
references: Plant Physiol. 2011 Jan;155(1):2-18
references: 21205630
references: Science. 2003 Aug 1;301(5633):653-7
references: 12893945
references: J Neurochem. 1995 Mar;64(3):1088-96
references: 7861138
references: Plant Physiol. 2012 May;159(1):266-85
references: 22392279
references: Plant Physiol. 2005 Oct;139(2):949-59
references: 16183832
references: Brain Res. 1993 Apr 9;608(1):33-7
references: 8495346
references: Plant Physiol. 2004 Jul;135(3):1471-9
references: 15247375
references: Mol Cells. 2006 Jun 30;21(3):418-27
references: 16819306
references: Plant Cell Physiol. 2001 Jan;42(1):74-84
references: 11158446
references: Plant J. 2009 May;58(3):437-49
references: 19143998
references: Plant Sci. 2012 Apr;185-186:288-97
references: 22325892
references: Plant Physiol. 2006 Jun;141(2):446-55
references: 16531482
references: Proc Natl Acad Sci U S A. 2012 Oct 2;109(40):16360-5
references: 22988090
references: Plant Physiol. 2010 Jul;153(3):1144-60
references: 20488891
references: Cell Death Differ. 2009 Oct;16(10):1303-14
references: 19662025
references: Int J Mol Sci. 2012;13(3):3145-3175
references: 22489146
references: J Exp Bot. 2004 Aug;55(404):1851-9
references: 15286141
references: Plant Physiol. 2006 Nov;142(3):963-71
references: 17012403
references: Plant Physiol. 2006 Aug;141(4):1666-75
references: 16778014
references: J Biol Chem. 2006 Mar 31;281(13):8864-70
references: 16455645
references: Neurotox Res. 1999 Dec;1(2):119-40
references: 12835108
references: Neurologia. 2012 Jun;27(5):301-10
references: 22217527
references: Mol Plant Microbe Interact. 2007 Aug;20(8):900-11
references: 17722694
references: Plant J. 2003 Jul;35(2):193-205
references: 12848825
references: Annu Rev Plant Biol. 2010;61:593-620
references: 20192754
references: Plant Physiol. 1995 Aug;108(4):1673-1678
references: 12228572
references: Plant J. 1998 Oct;16(1):73-8
references: 9807829
references: Plant Cell Physiol. 2004 Oct;45(10):1380-9
references: 15564521
references: Genetics. 2010 Oct;186(2):585-93
references: 20647506
references: Neurochem Res. 2007 Aug;32(8):1357-64
references: 17401648
references: PLoS Pathog. 2009 Feb;5(2):e1000301
references: 19214217
references: Neurochem Res. 1997 Sep;22(9):1165-71
references: 9251108
references: Nature. 2001 Nov 29;414(6863):562-5
references: 11734859
references: Amino Acids. 2008 Jan;34(1):75-80
references: 17701096
references: Plant Cell Environ. 2012 Feb;35(2):454-84
references: 21777251
references: Plant Mol Biol. 1999 Apr;39(6):1189-96
references: 10380805
references: Cell. 2012 May 25;149(5):1112-24
references: 22632974
references: Annu Rev Physiol. 2012;74:225-43
references: 22054239
references: Plant Cell. 2006 Feb;18(2):340-9
references: 16377757
references: Mol Biol Evol. 1999 Jun;16(6):826-38
references: 10368960
references: Toxicol Appl Pharmacol. 2004 Feb 15;195(1):12-22
references: 14962501
references: Mol Plant Pathol. 2013 Jan;14(1):58-70
references: 22947164
references: Mol Plant Microbe Interact. 2002 Jun;15(6):608-16
references: 12059109
references: Neurosci Lett. 1993 Jun 25;156(1-2):153-7
references: 8414178
references: Plant Physiol. 2012 May;159(1):40-6
references: 22447719
references: J Physiol. 2012 Jan 1;590(1):73-91
references: 22106181
references: Plant J. 2001 Nov;28(3):293-305
references: 11722772
references: Physiol Plant. 2009 Jul;136(3):284-98
references: 19453511
references: Science. 2011 Apr 22;332(6028):434-7
references: 21415319
references: Plant J. 2003 Sep;35(6):800-10
references: 12969432
references: Biochem J. 2011 Dec 15;440(3):355-65
references: 21848515
references: Plant Cell. 2010 Mar;22(3):541-63
references: 20354197
references: Plant J. 2008 Mar;53(6):999-1012
references: 18088327
references: Plant Physiol. 2004 Jun;135(2):1113-28
references: 15181213
references: J Neurochem. 1999 Sep;73(3):889-902
references: 10461878
references: Plant Cell. 2007 Mar;19(3):1081-95
references: 17384171
references: Mol Plant Microbe Interact. 2012 Mar;25(3):421-30
references: 22316300
references: Neurochem Int. 2000 Aug-Sep;37(2-3):299-306
references: 10812215