Tomato (Solanum lycopersicum) is an extensively cultivated vegetable, and its growth and fruit quality can be significantly impaired by low temperatures. The widespread presence of N6-methyladenosine (m6A) modification on RNA is involved in a diverse range of stress response processes. There is a significant knowledge gap regarding the precise roles of m6A modification in tomato, particularly for cold stress response. Here, we assessed the m6A modification landscape of S. lycopersicum ‘Micro-Tom’ leaves in response to low-temperature stress. Furthermore, we investigated the potential relationship among m6A modification, transcriptional regulation, alternative polyadenylation events, and protein translation via MeRIP-seq, RNA-seq, and protein mass spectrometry. After omic date analysis, 11 378 and 10 735 significant m6A peak associated genes were identified in the control and cold treatment tomato leaves, respectively. Additionally, we observed a UGUACAK (K = G/U) motif under both conditions. Differential m6A site associated genes most likely play roles in protein translation regulatory pathway. Besides directly altering gene expression levels, m6A also leads to differential poly(A) site usage under low-temperature. Finally, 24 important candidate genes associated with cold stress were identified by system-level multi-omic analysis. Among them, m6A modification levels were increased in SBPase (Sedoheptulose-1,7-bisphosphatase, Solyc05g052600.4) mRNA, causing distal poly(A) site usage, downregulation of mRNA expression level, and increased protein abundance. Through these, tomato leaves try to maintain normal photosynthetic carbon assimilation and nitrogen metabolism under low-temperature condition. The comprehensive investigation of the m6A modification landscape and multi-omics analysis provide valuable insights into the epigenetic regulatory mechanisms in tomato cold stress response.

中文翻译：

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多组学分析揭示了低温胁迫响应中番茄的表观转录组学和蛋白质组学调控网络


番茄 （Solanum lycopersicum） 是一种广泛种植的蔬菜，低温会严重损害其生长和果实品质。RNA 上广泛存在的 N6-甲基腺苷 （m6A） 修饰与多种应激反应过程有关。关于 m6A 修饰在番茄中的确切作用存在很大的知识差距，特别是对于寒冷胁迫反应。在这里，我们评估了石松 'Micro-Tom' 叶对低温胁迫的 m6A 修饰景观。此外，我们通过 MeRIP-seq、RNA-seq 和蛋白质质谱研究了 m6A 修饰、转录调控、替代多聚腺苷酸化事件和蛋白质翻译之间的潜在关系。经过组学数据分析，在对照和冷处理番茄叶片中分别鉴定出 11 378 和 10 735 个重要的 m6A 峰值相关基因。此外，我们在两种条件下都观察到了 UGUACAK （K = G/U） 基序。差异 m6A 位点相关基因最有可能在蛋白质翻译调节途径中发挥作用。除了直接改变基因表达水平外，m6A 还会导致低温下 poly（A） 位点的差异使用。最后，通过系统级多组学分析鉴定出 24 个与冷胁迫相关的重要候选基因。其中，SBPase （景庚酮糖-1,7-二磷酸酶，Solyc05g052600.4） mRNA 中的 m6A 修饰水平升高，导致远端 poly（A） 位点的使用，mRNA 表达水平下调，蛋白质丰度增加。通过这些，番茄叶片在低温条件下试图维持正常的光合碳同化和氮代谢。 对 m6A 修饰景观和多组学分析的全面研究为番茄寒冷应激反应中的表观遗传调控机制提供了有价值的见解。