Comparative RNA-seq analysis of tomato (Solanum lycopersicum L.) provides insights into natural and postharvest ripening

Tomato is a popular fruit known for their delicious flavor and nutritional value. However, there are significant differences in taste, nutritional content, and storage properties between tomato that natural ripening and postharvest ripening. In this study, we employed RNA-seq to identify 31,905 transcripts in tomato fruit at mature green stage (MG) and red stage ripened naturally on the vine (NR) or during postharvest storage (PR). Our study included a comprehensive comparative analysis of transcriptome between natural and postharvest ripening tomato, involving analyses such as differential expression of genes, alternative splicing (AS), long noncoding RNAs (lncRNAs), transcription factors (TFs), and microRNAs (miRNAs). We discovered 5684 mRNAs, 492 lncRNAs, and 12 miRNAs associated with natural ripening, and 6662 mRNAs, 529 lncRNAs, and 12 miRNAs linked to postharvest ripening. Seven pathways were enriched across two comparisons, with 81.1 % (NR vs.MG) and 84.1 % (PR vs. MG) of differentially expressed mRNAs (DEms) enriched in carbon metabolism and amino acids biosynthesis. Glycolysis/gluconeogenesis, citrate cycle (TCA cycle), valine, leucine and isoleucine degradation, and proteasome were specifically enriched in NR vs. MG. Cysteine and methionine metabolism, as well as phenylalanine, tyrosine and tryptophan biosynthesis were uniquely enriched in PR vs. MG. Additionally, ten pathways were enriched in PR vs. NR, with 78.0 % of DEms enriched in carbon metabolism, amino acids biosynthesis and ribosome. Furthermore, target analysis of lncRNAs and TFs highlighted their influence on various metabolic pathways through cis-/trans- regulatory or transcriptional regulation. Subsequently, we developed lncRNA-TF-mRNA/TF-lncRNA-mRNA networks that exhibited distinct characteristics in both natural and postharvest ripening. The ceRNA network analysis showed 5 ceRNA networks comprising 10 lncRNAs, 4 miRNAs, and 75 mRNAs that differed between natural and postharvest ripening. Overall, our study provides a comprehensive comparative analysis of natural and postharvest ripening fruit, offering valuable insights for future study on the regulatory mechanisms of fruit ripening.