The Proteasome Acts as a Hub for Plant Immunity and Is Targeted by Pseudomonas Type III Effectors.
Recent evidence suggests that the ubiquitin-proteasome system is involved in several aspects of plant immunity and that a range of plant pathogens subvert the ubiquitin-proteasome system to enhance their virulence. Here, we show that proteasome activity is strongly induced during basal defense in Arabidopsis (Arabidopsis thaliana). Mutant lines of the proteasome subunits RPT2a and RPN12a support increased bacterial growth of virulent Pseudomonas syringae pv tomato DC3000 (Pst) and Pseudomonas syringae pv maculicola ES4326. Both proteasome subunits are required for pathogen-associated molecular pattern-triggered immunity responses. Analysis of bacterial growth after a secondary infection of systemic leaves revealed that the establishment of systemic acquired resistance (SAR) is impaired in proteasome mutants, suggesting that the proteasome also plays an important role in defense priming and SAR In addition, we show that Pst inhibits proteasome activity in a type III secretion-dependent manner. A screen for type III effector proteins from Pst for their ability to interfere with proteasome activity revealed HopM1, HopAO1, HopA1, and HopG1 as putative proteasome inhibitors. Biochemical characterization of HopM1 by mass spectrometry indicates that HopM1 interacts with several E3 ubiquitin ligases and proteasome subunits. This supports the hypothesis that HopM1 associates with the proteasome, leading to its inhibition. Thus, the proteasome is an essential component of pathogen-associated molecular pattern-triggered immunity and SAR, which is targeted by multiple bacterial effectors.
Plant Metabolism Group, Leibniz Institute of Vegetable and Ornamental Crops, 14979 Großbeeren, Germany (S.Ü., F.B.); suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.|School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (A.S., S.G.-I., A.J., V.N.); suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.|Plant Molecular Genetics Department, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, 28049 Madrid, Spain (S.G.-I.); and suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.|Institut of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (F.B.) suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.
Suayib
0000-0002-8049-296X
S
Üstün
Plant Metabolism Group, Leibniz Institute of Vegetable and Ornamental Crops, 14979 Großbeeren, Germany (S.Ü., F.B.).|School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (A.S., S.G.-I., A.J., V.N.).|Plant Molecular Genetics Department, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, 28049 Madrid, Spain (S.G.-I.); and.|Institut of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (F.B.).
Arsheed
A
Sheikh
Plant Metabolism Group, Leibniz Institute of Vegetable and Ornamental Crops, 14979 Großbeeren, Germany (S.Ü., F.B.).|School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (A.S., S.G.-I., A.J., V.N.).|Plant Molecular Genetics Department, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, 28049 Madrid, Spain (S.G.-I.); and.|Institut of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (F.B.).
Selena
S
Gimenez-Ibanez
Plant Metabolism Group, Leibniz Institute of Vegetable and Ornamental Crops, 14979 Großbeeren, Germany (S.Ü., F.B.).|School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (A.S., S.G.-I., A.J., V.N.).|Plant Molecular Genetics Department, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, 28049 Madrid, Spain (S.G.-I.); and.|Institut of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (F.B.).
Alexandra
0000-0003-2571-8708
A
Jones
Plant Metabolism Group, Leibniz Institute of Vegetable and Ornamental Crops, 14979 Großbeeren, Germany (S.Ü., F.B.); suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.|School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (A.S., S.G.-I., A.J., V.N.); suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.|Plant Molecular Genetics Department, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, 28049 Madrid, Spain (S.G.-I.); and suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.|Institut of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (F.B.) suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.
Vardis
0000-0003-0069-6004
V
Ntoukakis
Plant Metabolism Group, Leibniz Institute of Vegetable and Ornamental Crops, 14979 Großbeeren, Germany (S.Ü., F.B.); suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.|School of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (A.S., S.G.-I., A.J., V.N.); suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.|Plant Molecular Genetics Department, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, 28049 Madrid, Spain (S.G.-I.); and suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.|Institut of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (F.B.) suayib.ustun@slu.se v.ntoukakis@warwick.ac.uk boernke@igzev.de.
Frederik
0000-0003-3558-0482
F
Börnke
D017360:Arabidopsis / Q000201:enzymology* / Q000382:microbiology*; D029681:Arabidopsis Proteins / Q000378:metabolism; D058947:Bacterial Secretion Systems; D004198:Disease Susceptibility; D054884:Host-Pathogen Interactions; D009154:Mutation / Q000235:genetics; D000069452:Pathogen-Associated Molecular Pattern Molecules / Q000378:metabolism; D010935:Plant Diseases / Q000382:microbiology; D057865:Plant Immunity; D046988:Proteasome Endopeptidase Complex / Q000378:metabolism*; D021122:Protein Subunits / Q000378:metabolism; D044224:Pseudomonas syringae / Q000378:metabolism*; D020156:Salicylic Acid / Q000378:metabolism; D015398:Signal Transduction; D014026:Nicotiana / Q000382:microbiology
D029681:Arabidopsis Proteins; D058947:Bacterial Secretion Systems; D000069452:Pathogen-Associated Molecular Pattern Molecules; D021122:Protein Subunits; D046988:Proteasome Endopeptidase Complex; D020156:Salicylic Acid