Integrated transcriptome and metabolome reveal that SlSYTA modulates ROS responses driving resistance defense in Solanum lycopersicum

Abstract

Abstract Synaptotagmin A (SYTA), renowned for its indispensable role in mammalian vesicle trafficking, has recently captured attention in plant biology owing to its potential regulatory functions. This study meticulously delves into the involvement of Solanum lycopersicum SlSYTA in plant immunity, focusing on its response to an array of pathogens affecting tomatoes. Our comprehensive inquiry uncovers that SlSYTA overexpression heightens susceptibility to tobacco mosaic virus (TMV), Phytophthora capsici, Botrytis cinerea, and Pseudomonas syringae pv. tomato DC3000, whereas RNA interference (RNAi) plants show a robust and encompassing resistance to these pathogens. Remarkably, our findings shed light on SlSYTA's negative regulation of pivotal aspects of pattern-triggered immunity (PTI) defense, notably hindering the reactive oxygen species (ROS) burst, impeding stomatal closure, and curtailing callose deposition. Through meticulous scrutiny via transcriptome and metabolome analyses, our studies reveal SlSYTA's profound impact on diverse plant defense pathways, specifically influencing phenylpropanoid metabolism, hormone signaling, and oxidative phosphorylation, primarily via NADPH synthesis modulation in the pentose phosphate pathway, and ultimately interplay within ROS signaling. Collectively, our research presents groundbreaking insights into the intricate molecular mechanisms governing plant immunity, emphasizing the significant role of SlSYTA in orchestrating plant responses to biotic stress.