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

Juanjuan Yu; Juan M Gonzalez; Zhiping Dong; Qianru Shan; Bowen Tan; Jin Koh; Tong Zhang; Ning Zhu; Craig Dufresne; Gregory B Martin; Sixue Chen

doi:10.3389/fpls.2021.768693

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

Front Plant Sci. 2021 Dec 3:12:768693. doi: 10.3389/fpls.2021.768693. eCollection 2021.

Authors

Juanjuan Yu¹, Juan M Gonzalez^{2

3}, Zhiping Dong¹, Qianru Shan¹, Bowen Tan², Jin Koh², Tong Zhang², Ning Zhu², Craig Dufresne⁴, Gregory B Martin^{3

5}, Sixue Chen²

Affiliations

¹ Henan International Joint Laboratory of Agricultural Microbial Ecology and Technology, College of Life Sciences, Henan Normal University, Xinxiang, China.
² Department of Biology, Genetics Institute, Plant Molecular and Cellular Biology Program, University of Florida, Gainesville, FL, United States.
³ Boyce Thompson Institute for Plant Research, Ithaca, NY, United States.
⁴ Thermo Fisher Scientific Inc., West Palm Beach, FL, United States.
⁵ Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, United States.

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.

Keywords: Pseudomonas syringae; effector-triggered immunity; pattern-triggered immunity; phosphoproteomics; proteomics; tomato.