GC-MS/LC-MS and transcriptome analyses revealed the metabolisms of fatty acid and flavonoid in olive fruits (Olea europaea L.)

•‘Arbequina’ and ‘Frantoio selection’ were suitable for oil extraction, and ‘Nikitskii Ⅰ’ could be used both for table olives and olive oil purposes.•‘Arbequina’, ‘Frantoio selection’ and ‘Nikitskii Ⅰ’ displayed the obvious advantages in total flavonoid contents, unsaturated fatty acids/fatty acids and oleic acid/fatty acids, respectively.•44 and 32 differentially expressed genes were detected in olive fruits related to the biosynthesis of fatty acid and flavonoid, respectively. Olive (Olea europaea L.) is an economical fruit tree for the usage of oil extraction and table olives. It is favored by consumers because of abundant unsaturated fatty acids and flavonoids, but little known about the genetic mechanisms. This study identifies the fruit traits of three olive cultivars ‘Arbequina’, ‘Frantoio selection’ and ‘Nikitskii Ⅰ’, first planted in the conditions of acid soil and rainy summer and further elucidates the fatty acid and flavonoid biosynthesis mechanism by multi-omics analysis. ‘Arbequina’ and ‘Frantoio selection’ had medium flesh/pit ratios (3.94, 3.53) and oil contents (15.95%, 12.95%) and were suitable for oil extraction. ‘Nikitskii Ⅰ’ had a big flesh/pit ratio (6.25) and medium oil content (13.13%) and could be used both for table olives and oil purpose. Totally, 37 fatty acid and 35 flavonoid compounds were detected by gas chromatography-mass spectrometry and liquid chromatography-mass spectrometry technologies with the average Pearson correlation indexes of 0.985 and 0.971 among different cultivars, respectively. Transcriptome analysis identified 14,684 differentially expressed genes with 1008 common differential genes. Furthermore, enrichment analysis showed 15 and 8 pathways involved in fatty acid and flavonoid metabolism with 44 and 32 prior transcripts tested, respectively. Overall, among the three cultivars, ‘Frantoio selection’ and ‘Nikitskii Ⅰ’ displayed a larger difference and they showed the high ratios of unsaturated fatty acids/fatty acids and oleic acid/fatty acids, respectively. While ‘Arbequina’ presented a big advantage in flavonoid compounds and expressions of related genes. The study provides the excellent materials and candidate genes for genetically improving of the quality of olive oil.