Transcriptomic and metabolomic analyses reveal phenolic metabolism regulated by melatonin in pear peel

Abstract Background Melatonin is a crucial regulator of fruit growth and development. However, the mechanisms by which pre-harvest application of melatonin regulates the metabolism of phenolic compounds in pear pericarp remain poorly understood. Methods In this study, the effect of pre-harvest spraying of melatonin on the synthesis of phenolics in pear peel and the regulatory mechanism were investigated using a multi-disciplinary approach, integrating physiological and biochemical, transcriptomic, and metabolic analyses, and the “Yuluxiang” pear as the test material. Results The pre-harvest spraying of 100 μM melatonin notably increased the single fruit weight, total soluble solids (TSS) and total soluble solids/titratable acid (TSS/TA) ratio. In addition, the spraying regimen elevated the concentrations of phenolic substances, including anthocyanosides, chlorogenic acid, and lignin, in the fruit peel. Three comparison groups (T0 vs. CK0, T1 vs. CK1, and T2 vs. CK2) showed 354, 1385, and 816 differentially expressed genes (DEGs) and 240, 411, and 210 differentially expressed metabolites (DEMs), respectively. Transcriptome results from melatonin treatment significantly affected the key metabolic pathways, including signal transduction, hormone regulation, glucose metabolism, secondary metabolites biosynthesis, phenylpropanoid biosynthesis, and flavonoid biosynthesis. Melatonin treatment also influenced the expression of key genes in phenylpropanoid biosynthesis and flavonoid biosynthesis pathways, such as PAL, C4H, 4CL, CAD, CHS, UFGT, POD, and others. Metabolomic data suggested the melatonin treatment notably stimulated the biosynthesis of l-phenylalanine, cinnamic acid, caffeic acid, ferulic acid, leucocyanidin and uridine 5ʹ-diphospho-d-glucose than control. By examining the expression patterns of transcription factors, we identified 12 transcription factors (TFs), including PbrMYB4, PbrMYB36-like, PbrMYB14, PbrREF4 and PbrNAC6-like, as potential key TFs involved in melatonin-regulated polyphenol biosynthesis. Conclusions The pre-harvest application of 100 μM melatonin can help improve the visual and flavor quality of pear fruits. It can influence the key enzyme genes’ expression of phenolic metabolism while stimulating the production of l-phenylalanine, cinnamic acid, caffeic acid, ferulic acid, leucocyanidin and uridine 5ʹ-diphospho-d-glucose, which promote the biosynthesis of anthocyanidins, phenolic acids, and lignins. These findings provide comprehensive insights into the metabolic mechanisms of melatonin-regulated phenolic compounds in pear peels. Graphical Abstract