Control of strawberry ripening through melatonin-auxin association

Melatonin has emerged as a hormone-like compound and multiple effects have been reported in fruits. To understand melatonin potential to control temporal ripening of aggregated non-climacteric fruits like strawberries, a preharvest in planta analysis was performed, including endogenous tissue localization of melatonin, its precursors and hydroxylated product (2-hydroxymelatonin) in achenes and receptacles over development. The signaling-ripening properties of melatonin were elucidated by co-accumulation with phytohormones and differential gene expression after application at distinct developmental stages, including fruit set, degreening and initial red. Our key findings illustrate a detailed specific spatiotemporal accumulation of melatonin and 2-hydroxymelatonin in strawberry fruits, with higher contents in achenes at fruit set, while receptacles peaked in ripe fruits. Exogenous melatonin (10^-4 M) had contrasting ripening effects based on application timing. Namely, melatonin accelerated colour development when applied at fruit set, but delayed colour change when applied at degreening and initial red. Gene expression analysis showed that exogenous melatonin induced transcriptional reprogramming, particularly in achenes with a higher number of differentially expressed genes. Moreover, melatonin applications at fruit degreening downregulated Gretchen Hagen 3 (FaGH3.9) 24 h post-application, linked here to reduced conjugated indole-3-acetic acid. Our findings indicate that melatonin delays strawberry ripening and suggest this occurs partly through positive auxin crosstalk, thereby contributing to better understanding the role of melatonin in non-climacteric fruits, and positioning this molecule as a promising target to modulate ripening in breeding programmes or sustainable fruit production systems.