Regulation Mechanism of JA Signaling on the Expansin Gene SlEXPA8 Affecting Sugar Metabolism in Tomato

Carbohydrates are crucial for plant growth and serve as fundamental energy sources, regulated by multiple factors. In tomato, development is closely linked to hormone-mediated sugar metabolism. Although jasmonic acid (JA) is known to function in signaling and growth regulation, its specific role in sugar metabolism remains unclear. This study demonstrated that JA signaling negatively regulates tomato seedling growth. Exogenous application of the JA activator MeJA suppressed growth, whereas the JA inhibitor DIECA and the JA synthesis mutant spr2 promoted it. Further analysis revealed that JA impaired growth by inhibiting photosynthesis-reducing photosynthetic pigment content and efficiency. MeJA treatment increased fructose and glucose levels but decreased sucrose and starch. These changes resulted from downregulated sucrose synthase (SlSS, SlSPS) activity and expression, alongside upregulated acid invertase (SlAI, SlNI) activity and SlTIV1 expression. Thus, JA restricted tomato seedling growth by suppressing photosynthesis and promoting soluble sugar accumulation. Transcriptome analysis identified SlEXPA8, a JA-responsive expansin gene. JA signaling downregulated SlEXPA8 expression; silencing SlEXPA8 impaired photosynthesis, reduced activities of sucrose-metabolizing enzymes, and lowered sucrose and starch levels, inhibiting seedling growth. Overexpression of SlEXPA8, however, enhanced growth. EMSA, ChIP, GUS, and LUC assays confirmed that SlMYC2 directly bound the SlEXPA8 promoter and regulated its transcription. These findings uncovered a mechanism by which JA signaling modulated sugar metabolism via expansin proteins, offering insights for targeted genetic improvement of tomato seedling vigor.