Integrative Proteomic and Phosphoproteomic Analyses of Pattern- and Effector-Triggered Immunity in Tomato

Plants have evolved a two-layered immune system consisting of pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). PTI and ETI are functionally linked, but also have distinct characteristics. Unraveling how these immune systems coordinate plant responses against pathogens is cruci...

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Autores principales: Juanjuan Yu, Juan M. Gonzalez, Zhiping Dong, Qianru Shan, Bowen Tan, Jin Koh, Tong Zhang, Ning Zhu, Craig Dufresne, Gregory B. Martin, Sixue Chen
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Publicado: Frontiers Media S.A. 2021
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Acceso en línea:https://doaj.org/article/9369beebb6e94ab08171db64754633b3
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spelling oai:doaj.org-article:9369beebb6e94ab08171db64754633b32021-12-03T05:10:05ZIntegrative Proteomic and Phosphoproteomic Analyses of Pattern- and Effector-Triggered Immunity in Tomato1664-462X10.3389/fpls.2021.768693https://doaj.org/article/9369beebb6e94ab08171db64754633b32021-12-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fpls.2021.768693/fullhttps://doaj.org/toc/1664-462XPlants have evolved a two-layered immune system consisting of pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). PTI and ETI are functionally linked, but also have distinct characteristics. Unraveling how these immune systems coordinate plant responses against pathogens is crucial for understanding the regulatory mechanisms underlying plant defense. Here we report integrative proteomic and phosphoproteomic analyses of the tomato-Pseudomonas syringae (Pst) pathosystem with different Pst mutants that allow the dissection of PTI and ETI. A total of 225 proteins and 79 phosphopeptides differentially accumulated in tomato leaves during Pst infection. The abundances of many proteins and phosphoproteins changed during PTI or ETI, and some responses were triggered by both PTI and ETI. For most proteins, the ETI response was more robust than the PTI response. The patterns of protein abundance and phosphorylation changes revealed key regulators involved in Ca2+ signaling, mitogen-activated protein kinase cascades, reversible protein phosphorylation, reactive oxygen species (ROS) and redox homeostasis, transcription and protein turnover, transport and trafficking, cell wall remodeling, hormone biosynthesis and signaling, suggesting their common or specific roles in PTI and/or ETI. A NAC (NAM, ATAF, and CUC family) domain protein and lipid particle serine esterase, two PTI-specific genes identified from previous transcriptomic work, were not detected as differentially regulated at the protein level and were not induced by PTI. Based on integrative transcriptomics and proteomics data, as well as qRT-PCR analysis, several potential PTI and ETI-specific markers are proposed. These results provide insights into the regulatory mechanisms underlying PTI and ETI in the tomato-Pst pathosystem, and will promote future validation and application of the disease biomarkers in plant defense.Juanjuan YuJuan M. GonzalezJuan M. GonzalezZhiping DongQianru ShanBowen TanJin KohTong ZhangNing ZhuCraig DufresneGregory B. MartinGregory B. MartinSixue ChenFrontiers Media S.A.articletomatopattern-triggered immunityeffector-triggered immunityproteomicsphosphoproteomicsPseudomonas syringaePlant cultureSB1-1110ENFrontiers in Plant Science, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic tomato
pattern-triggered immunity
effector-triggered immunity
proteomics
phosphoproteomics
Pseudomonas syringae
Plant culture
SB1-1110
spellingShingle tomato
pattern-triggered immunity
effector-triggered immunity
proteomics
phosphoproteomics
Pseudomonas syringae
Plant culture
SB1-1110
Juanjuan Yu
Juan M. Gonzalez
Juan M. Gonzalez
Zhiping Dong
Qianru Shan
Bowen Tan
Jin Koh
Tong Zhang
Ning Zhu
Craig Dufresne
Gregory B. Martin
Gregory B. Martin
Sixue Chen
Integrative Proteomic and Phosphoproteomic Analyses of Pattern- and Effector-Triggered Immunity in Tomato
description Plants have evolved a two-layered immune system consisting of pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). PTI and ETI are functionally linked, but also have distinct characteristics. Unraveling how these immune systems coordinate plant responses against pathogens is crucial for understanding the regulatory mechanisms underlying plant defense. Here we report integrative proteomic and phosphoproteomic analyses of the tomato-Pseudomonas syringae (Pst) pathosystem with different Pst mutants that allow the dissection of PTI and ETI. A total of 225 proteins and 79 phosphopeptides differentially accumulated in tomato leaves during Pst infection. The abundances of many proteins and phosphoproteins changed during PTI or ETI, and some responses were triggered by both PTI and ETI. For most proteins, the ETI response was more robust than the PTI response. The patterns of protein abundance and phosphorylation changes revealed key regulators involved in Ca2+ signaling, mitogen-activated protein kinase cascades, reversible protein phosphorylation, reactive oxygen species (ROS) and redox homeostasis, transcription and protein turnover, transport and trafficking, cell wall remodeling, hormone biosynthesis and signaling, suggesting their common or specific roles in PTI and/or ETI. A NAC (NAM, ATAF, and CUC family) domain protein and lipid particle serine esterase, two PTI-specific genes identified from previous transcriptomic work, were not detected as differentially regulated at the protein level and were not induced by PTI. Based on integrative transcriptomics and proteomics data, as well as qRT-PCR analysis, several potential PTI and ETI-specific markers are proposed. These results provide insights into the regulatory mechanisms underlying PTI and ETI in the tomato-Pst pathosystem, and will promote future validation and application of the disease biomarkers in plant defense.
format article
author Juanjuan Yu
Juan M. Gonzalez
Juan M. Gonzalez
Zhiping Dong
Qianru Shan
Bowen Tan
Jin Koh
Tong Zhang
Ning Zhu
Craig Dufresne
Gregory B. Martin
Gregory B. Martin
Sixue Chen
author_facet Juanjuan Yu
Juan M. Gonzalez
Juan M. Gonzalez
Zhiping Dong
Qianru Shan
Bowen Tan
Jin Koh
Tong Zhang
Ning Zhu
Craig Dufresne
Gregory B. Martin
Gregory B. Martin
Sixue Chen
author_sort Juanjuan Yu
title Integrative Proteomic and Phosphoproteomic Analyses of Pattern- and Effector-Triggered Immunity in Tomato
title_short Integrative Proteomic and Phosphoproteomic Analyses of Pattern- and Effector-Triggered Immunity in Tomato
title_full Integrative Proteomic and Phosphoproteomic Analyses of Pattern- and Effector-Triggered Immunity in Tomato
title_fullStr Integrative Proteomic and Phosphoproteomic Analyses of Pattern- and Effector-Triggered Immunity in Tomato
title_full_unstemmed Integrative Proteomic and Phosphoproteomic Analyses of Pattern- and Effector-Triggered Immunity in Tomato
title_sort integrative proteomic and phosphoproteomic analyses of pattern- and effector-triggered immunity in tomato
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/9369beebb6e94ab08171db64754633b3
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