A vacuolar invertase gene <i>SlVI</i> modulates sugar metabolism and postharvest fruit quality and stress resistance in tomato

Sugars act as signaling molecules to modulate various growth processes and enhance plant tolerance to various abiotic and biotic stresses. Moreover, sugars contribute to the postharvest flavor in fleshy fruit crops. To date, the regulation of sugar metabolism and its effect in plant growth, fruit ripening, postharvest quality, and stress resistance remains not fully understood. In this study, we investigated the role of tomato gene encoding a vacuolar invertase, hydrolyzing sucrose to glucose and fructose. <i>SlVI</i> is specifically expressed during the tomato fruit ripening process. We found that overexpression of <i>SlVI</i> resulted in increased leaf size and early flowering, while knockout of <i>SlVI</i> led to increased fruit sucrose content, enhanced fruit firmness, and elevated resistance of postharvest fruit to <i>Botrytis cinerea.</i> Moreover, the content of naringenin and total soluble solids was significantly increased in <i>SlVI</i> knockout fruit at postharvest stage. Transcriptome analysis showed a negative feedback regulation triggered by sucrose accumulation in <i>SlVI</i> knockout fruit resulting in a downregulation of <i>BAM3</i> and <i>AMY2,</i> which are critical for starch degradation. Moreover, genes associated with cell wall, cutin, wax, and flavonoid biosynthesis and pathogen resistance were upregulated in <i>SlVI</i> knockout fruit. Conversely, the expression levels of genes involved in cell wall degradation were decreased in knockout fruit. These results are consistent with the enhanced postharvest quality and resistance. Our findings not only provide new insights into the relationship between tomato fruit sucrose content and postharvest fruit quality, but also suggest new strategies to enhance fruit quality and extend postharvest shelf life.