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

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.

Acknowledgements

We would like to thank Professor Yule Liu (Tsinghua University, Beijing, China) for providing the VIGS vector and TMV-GFP. This study was partly supported by the National Natural Science Foundation of China (31870147), the science and technology projects of Chongqing Company of China Tobacco Corporation (B20221NY1307, B20212-NY2312) and the China Scholarship Council (202306990064).

Author contributions

S.T. performed the experiments and wrote the original draft. C.L. performed the formal analysis. F.L. and X.W. leveraged software to analyze raw data. G.Q. and J.D. verified data validation. Q.W., Y.W. and Q.P. graphed the data. X.M. guided the experiment and provided protocol. X.S. performed writing, review, and editing, supervision, project administration, and funding acquisition. All authors critically revised and approved the final manuscript.

Data availability statement

Sequence reads of transcriptome have been deposited in the NCBI Sequence Read Archive (SRA) under accession number PRJNA1086573. The raw metabolome data has been uploaded to Metabolights (https://www.ebi.ac.uk/metabolights/) and the National Genomics Data Center (https://www.cncb.ac.cn/), and the project IDs are MTBLS9722 (In Curation) and OMIX006287, respectively. Other data generated or analyzed during this study are included in this article.

Conflict of interests

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary information

Supplementary data are available at Horticulture Research online.

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