Transcriptomic landscapes of tissue-specific color transition in eggplant reveal regulatory roles of lncRNAs and alternative splicing in anthocyanin biosynthesis

Color transitions from green to purple in eggplant (Solanum melongena L.) flowers and berries result from biosynthesis and accumulation of chlorophyll and anthocyanins, compounds with antioxidant activity. While structural genes (CHS, CHI, F3’H, DFR, ANS, UGT) and regulatory transcription factors (MYB, bHLH, WD40) in the anthocyanin pathway are well characterized, fine-scale transcriptional regulation is less understood. Long non-coding RNAs (lncRNAs) contribute to pre- and post-transcriptional regulation, whereas alternative splicing (AS) events could control exclusively post-transcriptional modifications. Thus, here we performed an integrated transcriptomic analysis of mRNAs, lncRNAs and AS events to investigate fine regulation of anthocyanin biosynthesis.A PacBio assembly of the eggplant cultivar “Black Beauty” genome was generated, allowing the computational prediction and expression analysis of all transcripts, including lncRNAs and AS events, from green and purple stages of fruit peel and flower corolla. We identified 4,126 lncRNAs and 34,745 novel transcript isoforms and tissue-specific regulatory networks, built with Spearman correlation coefficient, revealed multiple lncRNAs and AS events associated with anthocyanin biosynthesis and regulatory genes. Total quantification of anthocyanins in both fruit peel and flower corolla enabled the construction of putative tissue-specific models of anthocyanin transcriptional regulation.This study provides a starting point to improve the knowledge of the fine-tuning anthocyanin regulation at the transcription level, highlighting tissue-specific lncRNAs and AS events linked to regulatory genes, and offering, to our knowledge, the first evidence of lncRNA involvement in anthocyanin biosynthesis in eggplant.