Environmentally driven transcriptomic and metabolic changes associated to colour differences in yellow peel apples

Apple is among the most cultivated fruit worldwide and is characterised by its high adaptation to diverse growing environments. This said, little is still known about how different environments can regulate at the metabolic or molecular level specific apple quality traits such as the yellow fruit peel color. In this study, changes in specific pigments (carotenoids and chlorophylls), antioxidants as well as differences in the transcriptome were investigated by comparing the peel of 'Golden Reinders' apples grown at different valley (ca. 200 masl) and mountain orchards (ca. 1000 masl). The mountain environment favoured the development of the optimal yellow colour, which was not caused by an enhanced accumulation of carotenoids but rather by a decrease in the chlorophyll content. Increased content of antioxidants (tocopherols, ascorbate and some phenolic compounds) was also observed in yellow apples. Consistent with these observations, RNA-seq analysis showed that the yellow phenotype was associated to higher expression of genes related to chloroplast functions as well as oxidative stress whereas plastid morphology analysis revealed the presence of membranous structures tentatively derived from thylakoids and likely associated to enhanced ROS levels in the peel of mountain apples. Time-course analysis over the last stages of apple development and ripening (from 60 to 100% of the final fruit size) further revealed that the environment differentially modulated isoprenoids and phenylpropanoids metabolism pointed out a key role for H2O2 in triggering apple peel degreening. Overall, the results presented herein provide new insights on how different environmental conditions regulate pigment and antioxidant metabolism in apple fruit leading to noticeable differences in the apple peel color.