Transcriptomics of fruit ripening in a tomato wide cross and genetic analysis of differentially expressed genes among parents and hybrid

•Omic techniques advance breeding, revealing 17.26% genome-wide gene expression in tomatoes.•Data from RNA-Seq unveils 84 significant GOs in tomato ripening, identifying 1364 common genes.•Gene action analysis highlights the dominance of wild genotypes, offering candidate genes for molecular markers development.•Tomatoes with a narrow genetic basis hold potential for targeted breeding improvements.•Novel framework in tomato breeding identifies key genes and wild genotype prepotent influence in ripening. Omic techniques have been used in recent years to support and make robust progress in breeding programs for different species. RNA-Seq is a powerful method for the analysis of transcriptomes to reveal genes with differential expression massively. The cultivated tomato (Solanum lycopersicum) is a crop with a narrow genetic basis in which fruit quality and wild genotypes are usually important targets to improve through breeding programs for obtaining new varieties. A novel framework was carried out using differential expression data (at three tomato fruit ripening stages), automatic Gene Ontology (GO) annotation, and estimating the Gene Action in our genotypes (two parental genotypes: the cultivated cv. Caimanta, the exotic LA0722 of S. pimpinellifolium, and their interspecific F1). The results indicate differential expression in all three genotypes, with an average of 17.26% of genes expressed throughout the genome. Functionality prediction detected 84 significant GO-terms related to the ripening process, by the FGGA method. In addition, we discovered 1,364 common genes among the GO-terms detected previously. Finally, a gene action analysis was carried out and high levels of non-additive effects towards the wild genotype LA0722 (59.90% of the total genes, with 40.10% towards the cultivated genotype) were detected. This finding implies that the hybrid genotype is similar to the exotic parents for traits related to tomato fruit ripening, which could account for prepotent effects. Genomic regions underlying the expression of these transcripts could be target regions to develop molecular markers for assisting breeding programs.