Multi-omics profiling of Camellia sinensis reveals mechanisms of bitter metabolism and temperature adaptation during spring warming

Temperature is a key environmental factor regulating secondary metabolism and flavor quality in Camellia sinensis . This study integrated metabolomic and transcriptomic to compare the responses of the evergreen tea cultivar ‘Longjing 43’ (LJ), the light-temperature dual-sensitive albino tea cultivar ‘Zhonghuang 2’ (ZH), and the temperature-sensitive albino tea cultivar ‘Baiye 1’ (BY) under 20°C and 30°C conditions. At 30°C, LJ significantly upregulated F3'5'H , resulting in the accumulation of quercetin glycosides and thereby enhancing the bitterness of the tea leaves. At 20°C, BY may have alleviated the catechin-induced bitterness by accumulating kaempferol glycosides, while ZH exhibited a “transcription–metabolite decoupling” pattern, reflecting the complex flavonoid response resulting from its light–temperature dual regulation of leaf coloration. WGCNA identified two key modules, the green module, which promotes flavonoid biosynthesis, and the Magenta module, which is linked to the suppression of flavonoid biosynthesis. Among the differentially regulated transcription factors, MYB1 regulates flavonoid synthesis, bHLH13 modulates carbon allocation and suppresses phenylpropanoid metabolism in response to light signals, ERF2 activates flavonoid biosynthesis genes via specific binding to the GCC box, and MYC2 coordinates jasmonic acid signaling. Antisense oligonucleotide (AsODN) experiments confirmed that transient silencing of CsMYB1 and CsERF2 led to a significant reduction in catechin content, demonstrating the critical regulatory roles of these two transcription factors in the flavonoid biosynthesis pathway. This study reveals the metabolic regulatory network underlying temperature adaptation in tea plants and provides a theoretical foundation for breeding stress-resilient, high-quality tea cultivars. • ‘Longjing 43’ enhances bitterness under heat via F3'5'H -driven quercetin glycoside accumulation. • ‘Baiye 1’ accumulates kaempferol glycosides under low temperature, potentially reducing bitterness and astringency. • ‘Zhonghuang 2’ shows transcription–metabolite decoupling, reflecting complex light–temperature metabolic interplay.