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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...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8584673/ https://www.ncbi.nlm.nih.gov/pubmed/34724007 http://dx.doi.org/10.1371/journal.ppat.1010017 |
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author | Jeleńska, Joanna Lee, Jiyoung Manning, Andrew J. Wolfgeher, Donald J. Ahn, Youngjoo Walters-Marrah, George Lopez, Ivan E. Garcia, Lissette McClerklin, Sheri A. Michelmore, Richard W. Kron, Stephen J. Greenberg, Jean T. |
author_facet | Jeleńska, Joanna Lee, Jiyoung Manning, Andrew J. Wolfgeher, Donald J. Ahn, Youngjoo Walters-Marrah, George Lopez, Ivan E. Garcia, Lissette McClerklin, Sheri A. Michelmore, Richard W. Kron, Stephen J. Greenberg, Jean T. |
author_sort | Jeleńska, Joanna |
collection | PubMed |
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 AvrPto1(Psy)-triggered immunity. HopZ3 acetylates AvrPto1(Psy) 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 AvrPto1(Psy)-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 AvrPto1(Psy) 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 AvrPto1(Psy) 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 | Online Article Text |
id | pubmed-8584673 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-85846732021-11-12 Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1–tomato PTO immune complex via acetylation Jeleńska, Joanna Lee, Jiyoung Manning, Andrew J. Wolfgeher, Donald J. Ahn, Youngjoo Walters-Marrah, George Lopez, Ivan E. Garcia, Lissette McClerklin, Sheri A. Michelmore, Richard W. Kron, Stephen J. Greenberg, Jean T. PLoS Pathog Research Article 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 AvrPto1(Psy)-triggered immunity. HopZ3 acetylates AvrPto1(Psy) 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 AvrPto1(Psy)-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 AvrPto1(Psy) 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 AvrPto1(Psy) 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. Public Library of Science 2021-11-01 /pmc/articles/PMC8584673/ /pubmed/34724007 http://dx.doi.org/10.1371/journal.ppat.1010017 Text en © 2021 Jeleńska et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Jeleńska, Joanna Lee, Jiyoung Manning, Andrew J. Wolfgeher, Donald J. Ahn, Youngjoo Walters-Marrah, George Lopez, Ivan E. Garcia, Lissette McClerklin, Sheri A. Michelmore, Richard W. Kron, Stephen J. Greenberg, Jean T. Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1–tomato PTO immune complex via acetylation |
title | 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_short | 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 |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8584673/ https://www.ncbi.nlm.nih.gov/pubmed/34724007 http://dx.doi.org/10.1371/journal.ppat.1010017 |
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