Functions of Tomato (Solanum lycopersicum L.) Signal Transducer and Activator of Transcription (STAT) in Seed Germination and Low-Temperature Stress Response

Tomato (<i>Solanum lycopersicum</i> L.) is one of the major vegetable crops worldwide. Research on the Janus kinase-signal transducer and activator of transcription (JAK-STAT) signaling pathway in tomatoes and other plant systems is extremely limited. In this study, the roles of STAT, a crucial element of the JAK-STAT signaling pathway in tomato seed germination and low-temperature stress responses are examined, employing gene family analysis and genetic transformation. The results indicate that the <i>S. lycopersicum</i> genome contains only one member of the STAT gene family, <i>SlSTAT</i>. Subcellular localization experiments reveal that SlSTAT is found in both the cytoplasm and nucleus, suggesting its potential involvement in biological functions within these cellular compartments. Among the 26 different tomato tissue/organs tested, <i>SlSTAT</i> exhibited higher expression levels in hypocotyl (8 days past germination; 8 DPG), and low expression of <i>SlSTAT</i> significantly reduced the germination rate and impacted biomass at 8 DPG. In addition, the <i>SlSTAT</i> gene was significantly downregulated during low-temperature treatment. Compared with the wild-type (WT) tomatoes, the <i>SlSTAT</i>-overexpressing plants showed more resistance to low-temperature conditions, whereas the downexpressing tomatoes exhibited increased sensitivity. The expressions of low-temperature marker genes (<i>SlCBF1</i>-<i>3</i>) and <i>N</i>⁶-methyladenosine (m⁶A)-modification-related genes (m⁶A writer, reader, and eraser genes) were detected to explore possible molecular mechanisms by which <i>SlSTAT</i> causes changes in tomato low-temperature stress resistance. The expression changes of <i>SlCBF1</i>-<i>3</i> in transgenic plants do not merely follow a straightforward linear relationship with the changes in <i>SlSTAT</i> expression, suggesting a more complex molecular mechanism and a non-direct interaction between SlSTAT and the promoters of <i>SlCBFs</i>. On the other hand, <i>SlSTAT</i> also changes the expression levels of RNA m⁶A-modification-related genes, especially <i>SlFIP37</i> (writer gene), <i>SlYTP8/9</i> (reader genes), and <i>SlALKBH8</i> (eraser gene), ultimately leading to changes in the levels of m⁶A modification. These research findings lay the groundwork for exploring functions of JAK-STAT pathway in tomato development and stress responses, expanding the scope of JAK-STAT signaling studies in plant systems.