Perturbations of the ZED1 pseudokinase activate plant immunity.
Acetylation
Arabidopsis
/ genetics
Arabidopsis Proteins
/ chemistry
Bacterial Proteins
/ chemistry
Carrier Proteins
/ chemistry
Host Microbial Interactions
/ genetics
Models, Immunological
Mutation
Phosphotransferases
/ genetics
Plant Immunity
Protein Interaction Domains and Motifs
Protein Kinases
/ chemistry
Pseudomonas syringae
/ immunology
Journal
PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921
Informations de publication
Date de publication:
07 2019
07 2019
Historique:
received:
22
03
2019
accepted:
08
06
2019
revised:
16
07
2019
pubmed:
4
7
2019
medline:
3
1
2020
entrez:
4
7
2019
Statut:
epublish
Résumé
The Pseudomonas syringae acetyltransferase HopZ1a is delivered into host cells by the type III secretion system to promote bacterial growth. However, in the model plant host Arabidopsis thaliana, HopZ1a activity results in an effector-triggered immune response (ETI) that limits bacterial proliferation. HopZ1a-triggered immunity requires the nucleotide-binding, leucine-rich repeat domain (NLR) protein, ZAR1, and the pseudokinase, ZED1. Here we demonstrate that HopZ1a can acetylate members of a family of 'receptor-like cytoplasmic kinases' (RLCK family VII; also known as PBS1-like kinases, or PBLs) and promote their interaction with ZED1 and ZAR1 to form a ZAR1-ZED1-PBL ternary complex. Interactions between ZED1 and PBL kinases are determined by the pseudokinase features of ZED1, and mutants designed to restore ZED1 kinase motifs can (1) bind to PBLs, (2) recruit ZAR1, and (3) trigger ZAR1-dependent immunity in planta, all independently of HopZ1a. A ZED1 mutant that mimics acetylation by HopZ1a also triggers immunity in planta, providing evidence that effector-induced perturbations of ZED1 also activate ZAR1. Overall, our results suggest that interactions between these two RLCK families are promoted by perturbations of structural features that distinguish active from inactive kinase domain conformations. We propose that effector-induced interactions between ZED1/ZRK pseudokinases (RLCK family XII) and PBL kinases (RLCK family VII) provide a sensitive mechanism for detecting perturbations of either kinase family to activate ZAR1-mediated ETI.
Identifiants
pubmed: 31269090
doi: 10.1371/journal.ppat.1007900
pii: PPATHOGENS-D-19-00547
pmc: PMC6634424
doi:
Substances chimiques
Arabidopsis Proteins
0
Bacterial Proteins
0
Carrier Proteins
0
ZAR1 protein, Arabidopsis
0
ZED1 protein, Arabidopsis
0
Phosphotransferases
EC 2.7.-
Protein Kinases
EC 2.7.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1007900Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):496-501
pubmed: 20018686
New Phytol. 2014 Aug;203(3):713-6
pubmed: 24841753
Curr Opin Microbiol. 2016 Feb;29:49-55
pubmed: 26599514
Mol Cell. 2004 Sep 10;15(5):661-75
pubmed: 15350212
Trends Immunol. 2017 Oct;38(10):744-757
pubmed: 28579324
FASEB J. 1995 May;9(8):576-96
pubmed: 7768349
Plant Cell. 2008 Apr;20(4):934-46
pubmed: 18381924
Science. 2006 May 26;312(5777):1211-4
pubmed: 16728640
Nat Struct Mol Biol. 2016 Sep;23(9):847-52
pubmed: 27525589
J Vis Exp. 2009 Jun 10;(28):
pubmed: 19516240
Nucleic Acids Res. 2016 Jul 8;44(W1):W242-5
pubmed: 27095192
PLoS Genet. 2010 Apr 01;6(4):e1000894
pubmed: 20368970
Trends Biochem Sci. 2014 Oct;39(10):475-86
pubmed: 25220378
Nat Protoc. 2007;2(1):35-7
pubmed: 17401335
Plant J. 1998 Dec;16(6):735-43
pubmed: 10069079
Annu Rev Biochem. 2012;81:587-613
pubmed: 22482904
Plant Methods. 2017 Jul 21;13:59
pubmed: 28736574
Science. 1988 Jul 1;241(4861):42-52
pubmed: 3291115
Science. 2019 Apr 5;364(6435):
pubmed: 30948527
Cell Host Microbe. 2010 Apr 22;7(4):290-301
pubmed: 20413097
J Mol Biol. 1993 Dec 5;234(3):779-815
pubmed: 8254673
New Phytol. 2019 Jan;221(2):1001-1009
pubmed: 30156705
Proc Natl Acad Sci U S A. 2008 Sep 23;105(38):14377-82
pubmed: 18787129
Cell Host Microbe. 2014 Mar 12;15(3):329-38
pubmed: 24629339
J Am Soc Mass Spectrom. 1994 Nov;5(11):976-89
pubmed: 24226387
Trends Biochem Sci. 2015 Nov;40(11):628-647
pubmed: 26481499
Mol Plant Microbe Interact. 2016 Dec;29(12):919-924
pubmed: 27996374
Nat Struct Biol. 2002 Apr;9(4):273-7
pubmed: 11896404
Plant Signal Behav. 2014;9(1):e27563
pubmed: 24398910
Science. 2008 Jul 25;321(5888):557-60
pubmed: 18653891
Plant J. 1997 Mar;11(3):605-12
pubmed: 9107046
Plant Cell. 2009 Jun;21(6):1846-59
pubmed: 19509331
Plant J. 2014 Apr;78(1):31-43
pubmed: 24461462
Science. 2019 Apr 5;364(6435):
pubmed: 30948526
Adv Protein Chem Struct Biol. 2011;82:1-35
pubmed: 21501817
Curr Protoc Bioinformatics. 2014 Dec 12;48:4.11.1-39
pubmed: 25501943
Biochem Soc Trans. 2013 Aug;41(4):969-74
pubmed: 23863165
Cell Host Microbe. 2018 Apr 11;23(4):485-497.e5
pubmed: 29649442
Plant J. 1998 Apr;14(2):247-57
pubmed: 9628020
J Bacteriol. 2008 Apr;190(8):2880-91
pubmed: 18263728
Bioessays. 2016 Aug;38(8):769-81
pubmed: 27339076
Microbiol Mol Biol Rev. 2016 Oct 26;80(4):1011-1027
pubmed: 27784797
Mol Plant Microbe Interact. 2019 May;32(5):550-565
pubmed: 30480480
Nat Plants. 2017 Mar 13;3:17027
pubmed: 28288096
Science. 2016 Dec 2;354(6316):
pubmed: 27934708
J Mol Biol. 2004 Oct 8;343(1):1-28
pubmed: 15381417
Proc Natl Acad Sci U S A. 2014 Mar 4;111(9):3632-7
pubmed: 24532660
Sci Rep. 2017 Jun 15;7(1):3557
pubmed: 28620210
Nat Commun. 2018 Oct 3;9(1):3735
pubmed: 30282993
Trends Cell Biol. 2006 Sep;16(9):443-52
pubmed: 16879967
Cell Host Microbe. 2011 Feb 17;9(2):137-46
pubmed: 21320696
BMC Bioinformatics. 2006 Jul 12;7:339
pubmed: 16836757
Syst Biol. 2003 Oct;52(5):696-704
pubmed: 14530136
New Phytol. 2017 Jul;215(2):711-724
pubmed: 28499073
Structure. 2016 Jan 5;24(1):7-24
pubmed: 26745528
Sci Rep. 2017 Jul 14;7(1):5487
pubmed: 28710392
Plant Physiol. 2017 Aug;174(4):2038-2053
pubmed: 28652264
Science. 2003 Aug 29;301(5637):1230-3
pubmed: 12947197
Mol Plant Microbe Interact. 2017 Jun;30(6):502-512
pubmed: 28353399
Plant J. 2014 Jul;79(1):56-66
pubmed: 24750441
Cell Host Microbe. 2015 Sep 9;18(3):285-95
pubmed: 26355215
Cell Microbiol. 2012 Jul;14(7):1071-84
pubmed: 22372664
Mol Cell. 2014 Sep 18;55(6):891-903
pubmed: 25201411
Semin Cell Dev Biol. 2016 Aug;56:134-149
pubmed: 27208725
Genome Biol. 2009;10(5):107
pubmed: 19519932
Proc Natl Acad Sci U S A. 2006 Dec 5;103(49):18574-9
pubmed: 17116858
New Phytol. 2015 Dec;208(4):1157-68
pubmed: 26103463
J Exp Bot. 2007;58(13):3503-11
pubmed: 17951602
Trends Biochem Sci. 2011 Feb;36(2):65-77
pubmed: 20971646
Nature. 2006 Nov 16;444(7117):323-9
pubmed: 17108957
Proc Natl Acad Sci U S A. 2013 Nov 12;110(46):18722-7
pubmed: 24170858
EMBO J. 2016 Nov 15;35(22):2468-2483
pubmed: 27679653
PLoS Pathog. 2012 Feb;8(2):e1002523
pubmed: 22319451
G3 (Bethesda). 2017 Mar 10;7(3):911-921
pubmed: 28122947
Acta Crystallogr D Biol Crystallogr. 1993 May 1;49(Pt 3):362-5
pubmed: 15299527
Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W557-9
pubmed: 15980534
Cell Rep. 2015 Nov 24;13(8):1670-82
pubmed: 26586425
Cell Res. 2012 Aug;22(8):1304-8
pubmed: 22547027
PLoS Pathog. 2013 Oct;9(10):e1003715
pubmed: 24204266
Syst Biol. 2006 Aug;55(4):539-52
pubmed: 16785212
Front Immunol. 2013 Oct 21;4:348
pubmed: 24155748
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Syst Biol. 2010 May;59(3):307-21
pubmed: 20525638
Plant Physiol. 2015 Dec;169(4):2950-62
pubmed: 26432875
Nat Protoc. 2007;2(1):1-4
pubmed: 17401330
J Mol Biol. 2003 Mar 14;327(1):159-71
pubmed: 12614615
Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2531-6
pubmed: 17277084
Nucleic Acids Res. 1988 Oct 25;16(20):9877
pubmed: 3186459
Biochim Biophys Acta. 2010 Mar;1804(3):440-4
pubmed: 19879387
Nature. 2012 Apr 15;485(7396):114-8
pubmed: 22504181
G3 (Bethesda). 2019 Feb 7;9(2):535-547
pubmed: 30573466