Multi-omics reveals the genetic regulation and functions of long non-coding RNAs in tomato

Long non-coding RNAs (lncRNAs) play vital roles in signal transduction and plant development. However, how lncRNA expression might have been globally altered during Solanum lycopersicum (tomato) breeding and what potential roles they play in regulating metabolite accumulation in fruit remain unclear. Here, we identified 15,548 lncRNAs using RNA-sequencing data from 404 tomato accessions. Among these lncRNAs, 2,115 were identified as high-confidence panel-expressed lncRNAs, which were expressed in more than 100 accessions with high confidence, as validated by strand-specific RNA-seq data. By exploring the variation of expression level and nucleotide diversity of lncRNAs during tomato domestication and improvement, we identified 776 differentially expressed lncRNAs during selective breeding. Furthermore, we determined that 695 lncRNAs were regulated by 1,383 lncRNA expression quantitative trait loci (eQTLs). Among these lncRNAs, 450 were associated with metabolite contents in tomato fruits. Transgenic experiments confirmed that the lncRNA MSTRG.24434.1 co-mapped with 2-phenylethanol at chromosome 8 (lncRNA-PEL8) positively regulates the content of the tomato fruit flavor volatile 2-phenylethanol. The expression levels of all panel-expressed lncRNAs could be used to predict metabolite contents with high accuracy, suggesting that lncRNAs play key roles in global metabolite processes. This study thus presents a multi-omics view of the breeding history of lncRNAs and provides valuable insights into their possible roles in regulating tomato flavor, highlighting their potential application in tomato breeding.