Seasonal influence on tomato fruit metabolome profile: Implications for ABA signaling in multi-stress resilience

The increasing effects of climate change are leading to an increase in the number and intensity of extreme events, making it essential to study how plants respond to various stresses occurring simultaneously. A crucial regulator of plant responses to abiotic stress is abscisic acid (ABA), as its accumulation in response to stress leads to transcriptomic and metabolomic changes that contribute to plant stress tolerance. In the present study, we investigated how ABA, stress conditions (salinity, water deficit and their combination) and seasons (autumn-winter and spring-summer) regulate tomato fruit yield and metabolism using tomato wild type (WT) and the ABA-deficient flacca mutant ( flc ) under stress conditions in cold and warm seasons. Our results showed that the applied stresses did not have the same effect in the warm season as in the cold season. In WT plants, the levels of other flavonoids, lignans and other polyphenols were higher in summer fruits, whereas the levels of anthocyanins, flavanols, flavonols, phenolic acids and stilbenes were higher in winter fruits. Furthermore, the significant increase in anthocyanins and flavonols was associated with the combination of salinity + water deficit in both seasons. Additionally, under certain conditions, flc mutants showed an enrichment of the superclasses of benzenoids and organosulphur compounds. The synthesis of phenolic compounds in flc fruits was also significantly different compared to WT plants. Thus, the metabolic profile of tomato fruits varies significantly with endogenous ABA levels, season of cultivation and applied stress treatments, highlighting the multifactorial nature of plant responses to combined environmental factors. • Our study found key metabolic markers linked to tomato fruit response to stress, highlighting the role of ABA levels in yield. • The enrichment of metabolic markers linked to ABA deficiency was stronger in summer, suggesting their key role in heat stress response, potentially influenced by light intensity. • Our results highlighted the role of phenylpropanoid metabolism in tomato responses to single and combined stresses, especially in ABA-deficient mutants.