Integrated transcriptomics and metabolomics analysis reveal LcSWEET12 regulating sugar accumulation in litchi (Litchi chinensis Sonn.)

Soluble sugars constitute one of the key quality-determining traits of litchifruit and contribute substantially to flavour formation. 'Heli' (HL) is a traditional litchi cultivar, and its bud mutant 'Dongtianxianli' (DTXL) displays brighter fruit colour, higher soluble-sugar content and lower acidity. To dissect the molecular basis underlying these phenotypic differences, we performed comparative transcriptomic and metabolomic analyses between DTXL and HL. A total of 1 904 differentially accumulated metabolites (DAMs, fold-change ≥ 1.2/≤0.83) and 10 454 differentially expressed genes (DEGs, q-value ≤ 0.5) were identified in the fruit peel. In the pulp, 1 958 DAMs and 10 240 DEGs were detected. Functional enrichment analyses revealed that genes involved in phenylpropanoid and flavonoid biosynthesis were predominantly up-regulated in the peel. By contrast, pathways including the tricarboxylic acid (TCA) cycle, glycolysis, starch-and-sucrose metabolism and plant-hormone signal transduction were enriched in the pulp. Via integrative transcriptome-metabolome analysis, we identified LcSWEET12 as a candidate gene linked to sugar accumulation. In litchi overexpression of LcSWEET12 elevated soluble-sugar levels by 40 % relative to control, while silencing of LcSWEET12 decreased soluble-sugar by 22 %. Further assays demonstrated that sugar, drought, and ABA decrease the LcSWEET12 protein content and its phosphorylation levels. Collectively, this study generates comprehensive metabolomic and transcriptomic datasets for fruit quality in 'Heli' and its bud mutant 'Dongtianxianli', clarifies the functional role of LcSWEET12 in sugar accumulation, and provides novel insights for litchi fruit-quality improvement.