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

ABSTRACT: 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.

SUBMITTER: Yu J

PROVIDER: S-EPMC8677958 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Plants have evolved a two-layered immune system that mainly includes pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) against pathogen attack. PTI and ETI signaling are functionally linked, but also distinct due to specific perceived ligands and activation modes. Unraveling how PTI and ETI coordinate the immune responses against pathogens is crucial for understanding the regulatory mechanisms in plant immunity. To better understand the protein profiling and phosphorylation events during PTI and ETI, we employed integrated whole proteome and phosphoproteome analyses in the tomato-Pst pathosystem with different Pst DC3000 mutants that allow dissection of different layers of immune responses. A total of 225 proteins and 79 phosphopeptides were differentially regulated in tomato leaves during immune responses. Our proteomics results indicate that some overlapping immune responses are triggered by both PTI and ETI-inducing treatment, and ETI response is more robust than PTI response for most proteins. The change patterns of protein abundance and phosphorylation revealed some key regulators involved in Ca2+ signaling, mitogen-activated protein kinase cascades, and reversible protein phosphorylation, ROS and redox homeostasis, direct defense, transcription machinery and protein turnover, cell wall remodeling, hormone biosynthesis, as well as immune molecule accumulation, are modulated during PTI and/or ETI, suggesting their common or specific roles in plant immune responses. However, NAC domain protein and lipid particle serine esterase, two PTI-specific genes from previous transcriptomic work, have not been detected as differentially regulated in our proteomic analysis, and they were proved to be not PTI-specific inducible and therefore cannot be used as PTI-reporters through “overlapping circle” pattern assay. These results provide insights into the fine-tuned regulatory mechanisms between PTI and ETI in-Pst pathosystem, which will springboard further investigations into the sophisticated mechanisms in plant immunity.

Dataset Information

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

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