Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1-tomato PTO immune complex via acetylation.

The plant pathogen Pseudomonas syringae secretes multiple effectors that modulate plant defenses. Some effectors trigger defenses due to specific recognition by plant immune complexes, whereas others can suppress the resulting immune responses. The HopZ3 effector of P. syringae pv. syringae B728a (P...

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Autores principales: Joanna Jeleńska, Jiyoung Lee, Andrew J Manning, Donald J Wolfgeher, Youngjoo Ahn, George Walters-Marrah, Ivan E Lopez, Lissette Garcia, Sheri A McClerklin, Richard W Michelmore, Stephen J Kron, Jean T Greenberg
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Publicado: Public Library of Science (PLoS) 2021
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Acceso en línea:https://doaj.org/article/3028edd84eb74705ab7886f5ab35cdf3
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spelling oai:doaj.org-article:3028edd84eb74705ab7886f5ab35cdf32021-12-02T19:59:54ZPseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1-tomato PTO immune complex via acetylation.1553-73661553-737410.1371/journal.ppat.1010017https://doaj.org/article/3028edd84eb74705ab7886f5ab35cdf32021-11-01T00:00:00Zhttps://doi.org/10.1371/journal.ppat.1010017https://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374The plant pathogen Pseudomonas syringae secretes multiple effectors that modulate plant defenses. Some effectors trigger defenses due to specific recognition by plant immune complexes, whereas others can suppress the resulting immune responses. The HopZ3 effector of P. syringae pv. syringae B728a (PsyB728a) is an acetyltransferase that modifies not only components of plant immune complexes, but also the Psy effectors that activate these complexes. In Arabidopsis, HopZ3 acetylates the host RPM1 complex and the Psy effectors AvrRpm1 and AvrB3. This study focuses on the role of HopZ3 during tomato infection. In Psy-resistant tomato, the main immune complex includes PRF and PTO, a RIPK-family kinase that recognizes the AvrPto effector. HopZ3 acts as a virulence factor on tomato by suppressing AvrPto1Psy-triggered immunity. HopZ3 acetylates AvrPto1Psy and the host proteins PTO, SlRIPK and SlRIN4s. Biochemical reconstruction and site-directed mutagenesis experiments suggest that acetylation acts in multiple ways to suppress immune signaling in tomato. First, acetylation disrupts the critical AvrPto1Psy-PTO interaction needed to initiate the immune response. Unmodified residues at the binding interface of both proteins and at other residues needed for binding are acetylated. Second, acetylation occurs at residues important for AvrPto1Psy function but not for binding to PTO. Finally, acetylation reduces specific phosphorylations needed for promoting the immune-inducing activity of HopZ3's targets such as AvrPto1Psy and PTO. In some cases, acetylation competes with phosphorylation. HopZ3-mediated acetylation suppresses the kinase activity of SlRIPK and the phosphorylation of its SlRIN4 substrate previously implicated in PTO-signaling. Thus, HopZ3 disrupts the functions of multiple immune components and the effectors that trigger them, leading to increased susceptibility to infection. Finally, mass spectrometry used to map specific acetylated residues confirmed HopZ3's unusual capacity to modify histidine in addition to serine, threonine and lysine residues.Joanna JeleńskaJiyoung LeeAndrew J ManningDonald J WolfgeherYoungjoo AhnGeorge Walters-MarrahIvan E LopezLissette GarciaSheri A McClerklinRichard W MichelmoreStephen J KronJean T GreenbergPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 17, Iss 11, p e1010017 (2021)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
Joanna Jeleńska
Jiyoung Lee
Andrew J Manning
Donald J Wolfgeher
Youngjoo Ahn
George Walters-Marrah
Ivan E Lopez
Lissette Garcia
Sheri A McClerklin
Richard W Michelmore
Stephen J Kron
Jean T Greenberg
Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1-tomato PTO immune complex via acetylation.
description The plant pathogen Pseudomonas syringae secretes multiple effectors that modulate plant defenses. Some effectors trigger defenses due to specific recognition by plant immune complexes, whereas others can suppress the resulting immune responses. The HopZ3 effector of P. syringae pv. syringae B728a (PsyB728a) is an acetyltransferase that modifies not only components of plant immune complexes, but also the Psy effectors that activate these complexes. In Arabidopsis, HopZ3 acetylates the host RPM1 complex and the Psy effectors AvrRpm1 and AvrB3. This study focuses on the role of HopZ3 during tomato infection. In Psy-resistant tomato, the main immune complex includes PRF and PTO, a RIPK-family kinase that recognizes the AvrPto effector. HopZ3 acts as a virulence factor on tomato by suppressing AvrPto1Psy-triggered immunity. HopZ3 acetylates AvrPto1Psy and the host proteins PTO, SlRIPK and SlRIN4s. Biochemical reconstruction and site-directed mutagenesis experiments suggest that acetylation acts in multiple ways to suppress immune signaling in tomato. First, acetylation disrupts the critical AvrPto1Psy-PTO interaction needed to initiate the immune response. Unmodified residues at the binding interface of both proteins and at other residues needed for binding are acetylated. Second, acetylation occurs at residues important for AvrPto1Psy function but not for binding to PTO. Finally, acetylation reduces specific phosphorylations needed for promoting the immune-inducing activity of HopZ3's targets such as AvrPto1Psy and PTO. In some cases, acetylation competes with phosphorylation. HopZ3-mediated acetylation suppresses the kinase activity of SlRIPK and the phosphorylation of its SlRIN4 substrate previously implicated in PTO-signaling. Thus, HopZ3 disrupts the functions of multiple immune components and the effectors that trigger them, leading to increased susceptibility to infection. Finally, mass spectrometry used to map specific acetylated residues confirmed HopZ3's unusual capacity to modify histidine in addition to serine, threonine and lysine residues.
format article
author Joanna Jeleńska
Jiyoung Lee
Andrew J Manning
Donald J Wolfgeher
Youngjoo Ahn
George Walters-Marrah
Ivan E Lopez
Lissette Garcia
Sheri A McClerklin
Richard W Michelmore
Stephen J Kron
Jean T Greenberg
author_facet Joanna Jeleńska
Jiyoung Lee
Andrew J Manning
Donald J Wolfgeher
Youngjoo Ahn
George Walters-Marrah
Ivan E Lopez
Lissette Garcia
Sheri A McClerklin
Richard W Michelmore
Stephen J Kron
Jean T Greenberg
author_sort Joanna Jeleńska
title Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1-tomato PTO immune complex via acetylation.
title_short Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1-tomato PTO immune complex via acetylation.
title_full Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1-tomato PTO immune complex via acetylation.
title_fullStr Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1-tomato PTO immune complex via acetylation.
title_full_unstemmed Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1-tomato PTO immune complex via acetylation.
title_sort pseudomonas syringae effector hopz3 suppresses the bacterial avrpto1-tomato pto immune complex via acetylation.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/3028edd84eb74705ab7886f5ab35cdf3
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