Transcriptomic and Translatomic Analyses Reveal Insights into the Developmental Regulation of Secondary Metabolism in the Young Shoots of Tea Plants (<i>Camellia sinensis</i> L.)

Accumulation of secondary metabolites in the young shoots of tea plants is developmentally modulated, especially flavonoids. Here, we investigate the developmental regulation mechanism of secondary metabolism in the developing leaves of tea plants using an integrated multiomic approach. For the pair of Leaf2/Bud, the correlation coefficient of the fold change of mRNA and RPFs abundances involved in flavonoid biosynthesis was 0.9359, being higher than that of RPFs and protein (R2 = 0.6941). These correlations were higher than the corresponding correlation coefficients for secondary metabolisms and genome-wide scale. Metabolomic analysis demonstrates that the developmental modulations of the structural genes for flavonoid biosynthesis-related pathways align with the concentration changes of catechin and flavonol glycoside groups. Relatively high translational efficiency (TE > 2) was observed in the four flavonoid structural genes (chalcone isomerase, dihydroflavonol 4-reductase, anthocyanidin synthase, and flavonol synthase). In addition, we originally provided the information on identified small open reading frames (small ORFs) and main ORFs in tea leaves and elaborated that the presence of upstream ORFs may have a repressive effect on the translation of downstream ORFs. Our data suggest that transcriptional regulation coordinates with translational regulation and may contribute to the elevation of translational efficiencies for the structural genes involved in the flavonoid biosynthesis pathways during tea leaf development.茶树幼梢次生代谢产物的积累受发育进程调控，其中黄酮类物质尤为显著。本研究采用整合多组学方法，探究茶树发育叶片中次生代谢的发育调控机制。针对Leaf2/芽（Bud）这一组样本，参与黄酮类生物合成的mRNA与核糖体保护片段（Ribosome-protected fragments, RPFs）丰度的折叠变化相关系数达0.9359，高于RPFs与蛋白质的相关系数（决定系数R²=0.6941）。上述相关系数均高于次生代谢及全基因组范围的对应相关系数。代谢组学分析显示，黄酮类生物合成相关通路的结构基因的发育调控模式与儿茶素及黄酮醇糖苷类物质的浓度变化相一致。在4个黄酮类结构基因（查尔酮异构酶（chalcone isomerase）、二氢黄酮醇4-还原酶（dihydroflavonol 4-reductase）、花青素合酶（anthocyanidin synthase）及黄酮合酶（flavonol synthase））中观察到较高的翻译效率（Translational Efficiency, TE > 2）。此外，本研究首次提供了茶树叶片中已鉴定的小开放阅读框（small open reading frames, small ORFs）及主开放阅读框（main ORFs）的相关信息，并阐明上游开放阅读框（upstream ORFs）的存在可能对下游开放阅读框（downstream ORFs）的翻译产生抑制作用。本研究数据表明，转录调控与翻译调控相互协调，或有助于提升茶树叶片发育过程中黄酮类生物合成通路相关结构基因的翻译效率。