Physiological and Molecular Approaches Revealing Mechanisms of Fruit Abscission and Pre-Harvest Drop Management in Apple (Malus × domestica Borkh.)

Abstract

Pre-harvest fruit drop (PFD) is a major constraint on yield and profitability in commercial apple (Malus × domestica Borkh.) production, with susceptible cultivars like 'Honeycrisp' often experiencing significant losses. While current management using ethylene inhibitors such as aminoethoxyvinylglycine (AVG) effectively reduces PFD, it often delays ripening, suppresses anthocyanin biosynthesis, and degrades overall market quality. In this study, the efficacy of various plant growth regulators (PGRs), including ACC (1-aminocyclopropane-1-carboxylic acid), ethephon, and AVG, was first evaluated over two consecutive years (2023–2024). The integrated application of ACC+AVG was found to be the most effective strategy, reducing PFD by 27.05–46.30% while simultaneously intensifying red coloration by upregulating anthocyanin biosynthetic genes such as MdCHS, MdCHI, and MdDFR. Because this treatment showed no significant shift in internal ethylene concentration (IEC) compared to the untreated control, further investigation was conducted to determine whether fruit abscission and ripening are biologically coupled or regulated independently. Subsequently, IEC and key maturity indices—including firmness, soluble solids content (Brix), and starch index—were compared between dropped and retained fruits after gentle agitation at the same phenological stage. These indices were found to be statistically indistinguishable, indicating that fruit abscission can occur independently of ripening progression. This confirmed the functional decoupling between the two processes and prompted an investigation into the specific tissue-level site where this regulation occurs. Transcriptomic profiling of the pedicel abscission zone (AZ) and the fruit cortex was then performed across two critical phenological windows: one week before anticipated commercial harvest and one-week post-harvest. A profound tissue-specific divergence was identified, with 848 differentially expressed genes (DEGs) in the pedicel compared to only 21 in the cortex, establishing the pedicel as the primary site of abscission regulation. To narrow the focus further, pedicel-specific gene modules were characterized and identified as responsible for coordinated shifts in auxin signaling and oxidative stress during abscission. Based on these molecular findings, a translational field study was conducted to test if targeting these specific pathways could control PFD without affecting ethylene dynamics. Field applications of synthetic auxin (NAA) and the antioxidant melatonin were found to significantly reduce PFD (23.30% and 26.08%, respectively) relative to the control. Notably, melatonin induced expression of the peroxisomal protease MdLON2 in the pedicel, suggesting that oxidative homeostasis is a critical regulator of the abscission process. Together, these results establish a tissue-specific framework for fruit abscission that is functionally independent of ripening. By demonstrating that the pedicel acts as the primary "control center" for dropping, this work provides a translational basis for targeted interventions that extend the harvest window while maintaining the quality of 'Honeycrisp' apples.