Metabolic remodeling underlying citrus segment drying: Insights from lignin non-accumulating granulation in Harumi tangor vesicles

Segment drying significantly impairs citrus fruit quality during ripening and postharvest storage, notably causing flavor loss and mostly vesicle granulation. The “Disorder of cell wall metabolism” hypothesis has shed light on the relevant mechanism, proposing that activation of the cell wall component synthesis, particularly lignin, plays a crucial role in this disorder. This study investigates whether granulated vesicles lacking lignin accumulation could still be explained by this hypothesis. We employed a comprehensive method to analyze metabolic pathway changes in Harumi tangor granulated vesicles. Physiologically, these granulated vesicles exhibit depletion of sugars and organic acids, coupled with an increase in cell wall components like cellulose and pectin, but not lignin. Our metabolomics analysis identified 627 metabolites with altered levels during granulation, while transcriptomics revealed 2298 genes with differential expression. Significant metabolic remodeling was observed in vesicles during lignin non-accumulating granulation. Despite no lignin accumulation, its synthesis pathway was transcriptionally active. Cellulose accumulation was linked to the activation of its synthesis pathway at the transcriptional level. Similarly, pectin accumulation stemmed from alterations of its metabolism, including the activation of de-methylesterification. A notable decrease in sucrose, hexose, and glucose levels was linked to reduced sucrose synthesis, enhanced sucrose degradation, and moderate increase in hexose degradation. Citrate breakdown in these granulated vesicles was likely driven by the acetyl-CoA synthesis pathway and γ-aminobutyrate shunt, indicated by increased enzyme activities and transcriptional alterations. Notably, the γ-aminobutyrate shunt is not activated in vesicles during lignin-accumulating granulation. These findings endorse the hypothesis that cell wall metabolism disorder leads to nutrient depletion and lignin non-accumulating granulation. Moreover, they imply that non-accumulating lignin may represent an early stage in vesicle granulation, offering critical insights into metabolic pathway changes during citrus granulation. •Granulated vesicles in Harumi tangor accumulate cellulose and pectin, not lignin.•Lignin synthesis pathway was transcriptionally activated in granulated vesicles.•Cellulose synthesis and pectin de-methylesterification may be activated in granulated vesicles.•Acetyl-CoA synthesis and γ-aminobutyrate shunt likel