Anthocyanins are important pigment of blood orange (Citrus sinensis). While nutrient availability is known to affect fruit pigmentation, the specific role of mineral elements and their underlying mechanisms remain largely unclear. Our filed experiment in two blood orange orchards at the same site but with different fertilizer recipes resulted in distinct variations in anthocyanin content in the fruit peel. This study identified magnesium (Mg) as the primary influencing factor, accounting for up to 25% of the positive variance in peel anthocyanin accumulation. Transcriptomic analysis combined with exogenous Mg treatments revealed significantly differential expression of key structural genes involved in anthocyanin biosynthesis, including CsDFR and CsANS. Furthermore, the expression of the nutrient-responsive transcription factor CsbZIP53 exhibited a dose-dependent response to Mg concentrations. In vivo quantitative analyses of tobacco leaves and blood orange peel demonstrated that Mg promotes the expression of CsbZIP53. Overexpressing CsbZIP53 in citrus leaves upregulated the expression of genes involved in anthocyanin biosynthesis and increased the relative accumulation of anthocyanin aglycones. Dual-luciferase reporter assays and electrophoretic mobility shift assay revealed that CsbZIP53 activates the transcription of CsDFR and CsANS, achieved by specifically recognizing and binding to the G-box motifs within the promoters of these target genes. Taken together, we propose a model whereby Mg upregulated CsbZIP53, which subsequently targets might bind to the G-box regions of target gene promoters to upregulate anthocyanin biosynthetic genes. From the perspective of application and practice, we recommend the supplementing Mg fertilizers from the fruit expansion stage through to maturity, to improve fruit coloration and overall quality of blood orange fruits.
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