Multi-omics analysis reveals the epitranscriptomic and proteomic regulation network of tomato in low-temperature stress response

Abstract

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.