An Insight into the Hormonal Interplay Regulating Pigment Changes and Colour Development in the Peel of ‘Granny Smith’, ‘OPAL®’ and ‘Royal Gala’ Apples

Abstract

Three apple cultivars with different peel colour and known ripening dynamics were examined throughout development and on-tree ripening to unravel how the hormonal crosstalk may influence colour changes. Our results indicate that the colour of ripe apples in ‘Granny Smith’ and ‘Opal®’ cultivars was primarily influenced by chlorophyll levels masking the contribution of other pigments, whilst the development of red colour in the ‘Royal Gala’ was not only due to an important loss of chlorophyll during ripening but also to anthocyanins accumulation. The interplay amongst indole-3-acetic acid (IAA), ethylene and abscisic acid (ABA) seemed to control pigment content during the later stages of development, indicating that variations in the hormonal profile contribute to colour differences in ripe apples. In ‘Granny Smith’ apples, basal levels of IAA, ethylene and ABA were associated with the inhibition of chlorophyll loss, which was responsible for its green colour, despite the presence of high carotenoid levels. In contrast, the peel of ‘Opal®’ and ‘Royal Gala’ apples underwent a degreening process facilitated by the IAA-mediated activation of ethylene metabolism, in a crosstalk facilitated by MdARF5. The accumulation of anthocyanins in the peel of ‘Royal Gala’ apples seemed to be regulated in an ethylene-dependent manner, with MdMYB1 acting as the mediator between ethylene signalling and the anthocyanins biosynthesis and vacuolar transport pathways. On the other hand, the decline in carotenoid content during fruit development in the three cultivars appeared to be regulated at the catabolic level through ABA and its derivatives and possibly also facilitated by ethylene-mediated mechanisms. Notably, chlorophyll levels, crucial for the observed colour changes, were likely controlled by MdGLK1, a transcription factor involved in chloroplast biogenesis, working in coordination with ethylene-dependent catabolic enzymes. Overall, understanding the cultivar-specific hormonal regulation of apple colour provides valuable insights for developing preharvest and postharvest strategies to ensure an optimal fruit colour aligned with consumer preferences.