The ethylene response factor ERF1A regulates UV-C-induced delayed ripening in peach fruit

Ultraviolet-C (UV-C) irradiation delays fruit ripening, yet the underlying mechanisms remain unclear. We investigated tissue-specific responses of peach fruit (Prunus persica L. Batsch) to UV-C by analyzing the peel and flesh separately. UV-C treatment altered central metabolism, promoted anthocyanin accumulation and coloration, and delayed ripening, as evidenced by reduced fruit softening and water loss. However, UV-C enhanced ethylene production and upregulated ethylene-related genes, indicating a reconfiguration of the ethylene response. Among UV-C-responsive genes, the APETALA2/Ethylene Response Factor (AP2/ERF) transcription factor family was most affected, with Ethylene Response Factor 1A (ERF1A) showing the strongest induction in the treated peel, suggesting its role as a key integrator of the UV-C-induced ripening delay. UV-C increased the levels of DNA 5-methylcytosine and RNA N6-methyladenosine in the peel, without altering cytosine methylation or causing mutations in ERF1A. Silencing ERF1A via RNA interference confirmed that it regulates ethylene production, softening, and ripening-associated metabolites. Immunolocalization revealed changes in the cell wall components of ERF1A-silenced fruit, including arabinogalactan, pectin, and xyloglucan. ERF1A-silenced peels exhibited elevated auxin and salicylic acid levels and reduced abscisic acid content. Additionally, ERF1A suppression altered the biosynthesis of sugars, phenolic compounds, and volatiles. We found extensive proteome reprogramming in ERF1A-silenced peels and identified putative ERF1A target genes that either contain ERF1A-binding sites or are associated with firmness, ethylene signaling, phytohormone metabolism, and color. Notably, Carboxylesterase 11 (PpCXE11), Carboxylesterase 13 (PpCXE13), and Salicylic acid-binding protein 2 (PpSABP2) emerged as potential ERF1A targets. These findings identify ERF1A as a central regulator mediating UV-C-induced ripening delay through modulation of ethylene signaling and downstream ripening pathways.