Pigment-Related Mutations Greatly Affect Berry Metabolome in San Marzano Tomatoes

The study describes the alterations in metabolomic profiles of four tomato fruit mutations introgressed into Solanum lycopersicum cv. San Marzano, a well-known Italian traditional variety. Three lines carrying variants affecting the content of all pigments, high pigment-1 (hp-1), hp-2, pigment diluter (pd), and a combination of Anthocyanin fruit and atroviolaceum (Aft_atv), were selected, and characterized. Biochemical analysis of 44 non-polar, 133 polar, and 65 volatile metabolites in ripe fruits revealed a wide range of differences between the variant lines and the recurrent parent San Marzano. Among non-polar compounds, many carotenoids, plastoquinones, and tocopherols increased in the fruit of high pigment lines, as well as in Aft_atv, whose β-carotene levels increased too. Interestingly, pd displayed enriched levels of xanthophylls (all-trans-neoxanthin and luteoxanthin) but, simultaneously, decreased levels of α-and β-/γ-tocopherols. Looking at the metabolites in the polar fraction, a significant decrease in sugar profile was observed in hp-1, pd, and Aft_atv. Conversely, many vitamins and organic acids increased in the hp-2 and Aft_atv lines, respectively. Overall, phenylpropanoids was the metabolic group with the highest extent of polar changes, with considerable increases of many compounds mainly in the case of Aft_atv, followed by the pd and hp-2 lines. Finally, several flavor-related compounds were found to be modified in all mutants, mostly due to increased levels in many benzenoid, lipid, and phenylalanine derivative volatiles, which are associated with sweeter taste and better aroma. Construction of metabolic maps, interaction networks, and correlation matrices gave an integrated representation of the large effect of single variants on the tomato fruit metabolome. In conclusion, the identified differences in the mutated lines might contribute to generating novel phenotypes in the traditional San Marzano type, with increased desirable nutraceutical and organoleptic properties.