Seasonal differences in softening of early-harvested ‘Royal Gala’ apple fruit are correlated with at-harvest biomarkers indicative of abiotic stress responses

Softening of apple fruit depends on maturity at harvest and a range of orchard and environmental factors. We investigated seasonal effects on ‘Royal Gala’ storage performance independent of maturity and separate from potential orchard effects. In two consecutive seasons, fruit were harvested at four times: very early (H1), early (H2), commercial (H3) and late (H4), and were cold-stored at 0.5 °C for 100 d followed by a shelf-life period. In Year 1, fruit from H1 and H2 softened much less during storage than did fruit from Year 2. Later-harvested fruit (H3 and H4) did not show this seasonal difference and softened similarly in storage. A combined at-harvest transcriptomic and metabolomic study was analysed using mixOmics. Retained firmness in storage was correlated with increased abundance of transcripts indicative of abiotic stress, including those encoding universal stress protein, a drought stress protein, and several heat shock proteins and aquaporins. Greater softening in storage was correlated with higher abundance of fewer and different stress genes, and genes involved in cell wall metabolism. The data suggest that preharvest stresses experienced by the fruit have a profound effect on subsequent softening, at least in early-harvested fruit before ripening-related ethylene becomes the main driver. Ten potential at-harvest biomarkers were identified, including titratable acidity, erythritol and eight transcripts (notably Universal stress protein PHOS32-like and Homeobox leucine zipper protein HAT5-like). These could be useful for predicting the subsequent storage performance of batches of fruit.