Integrated transcriptomic and metabolomic analysis reveals regulatory mechanisms underlying coloration differences in the pericarps of two Litchi cultivars

The color of the litchi pericarp, a crucial external quality attribute, is primarily influenced by the accumulation of anthocyanins and the degradation of chlorophyll. Despite this understanding, the metabolic regulatory networks and key molecular nodes responsible for cultivar-specific color variations remain inadequately characterized, thereby hindering efforts to improve quality. This study utilized the red-pericarp cultivar 'Ziniangxi' (ZNX) and the green-pericarp cultivar 'Guanyinlv' (GYL) to conduct integrated metabolomic and transcriptomic analyses. The findings revealed that ZNX pericarps exhibited significantly elevated levels of key anthocyanins, including cyanidin-3-<i>O</i>-galactoside, cyanidin-3-<i>O</i>-glucoside, and cyanidin-3-<i>O</i>-rutinoside. In contrast, GYL pericarps contained only trace amounts of cyanidin-3-<i>O</i>-rutinoside but were rich in flavonoids such as pelargonidin-3-<i>O</i>-galactoside, lonicerin, and rutin. Transcriptome analysis demonstrated that the expression levels of structural genes involved in the anthocyanin biosynthesis pathway were significantly upregulated during the ripening of ZNX fruit. In contrast, in the pericarps of GYL, the expression of <i>CHS</i>, <i>F3H</i>, and <i>ANS</i> genes was downregulated throughout the ripening process, whereas the expression levels of <i>F3'H</i>, <i>UFGT</i>, and <i>GST</i> genes remained consistently low. The study utilized Weighted Gene Co-expression Network Analysis (WGCNA) to identify <i>MYB</i>, <i>ERF</i>, and <i>WRKY</i> TFs, along with salicylic acid signaling genes (<i>NPR1</i>, <i>TGA</i>, <i>PR1</i>) and a cytokinin signaling gene (<i>AHP</i>), which potentially constitute a synergistic regulatory network influencing variations in anthocyanin accumulation. This research elucidates the metabolic and regulatory mechanisms underlying the differentiation of litchi pericarp coloration, thereby advancing the theoretical framework of plant anthocyanin biosynthesis. Furthermore, it offers valuable genetic resources and theoretical insights for the enhancement of litchi's external quality and the development of new cultivars.