Although remarkable progress has been made toward understanding carotenoid biosynthesis, the mechanisms that regulate the transcription of carotenogenic genes remain poorly understood. Lycopene β-cyclases (LCYb) are critical enzymes located at the branch point of the carotenoid biosynthetic pathway. Here, we used the promoter sequence of LCYb1 as bait in a yeast one-hybrid screen for promoter-binding proteins from sweet orange (Citrus sinensis). This screen identified a MADS transcription factor, CsMADS6, that was coordinately expressed with fruit development and coloration. Acting as a nucleus-localized transcriptional activator, CsMADS6 directly bound the promoter of LCYb1 and activated its expression. Overexpression of CsMADS6 in citrus calli increased carotenoid contents and induced the expression of LCYb1 and other carotenogenic genes, including phytoene synthase (PSY), phytoene desaturase (PDS), and carotenoid cleavage dioxygenase1 (CCD1). CsMADS6 up-regulated the expression of PSY, PDS, and CCD1 by directly binding to their promoters, which suggested the multitargeted regulation of carotenoid metabolism by CsMADS6. In addition, the ectopic expression of CsMADS6 in tomato (Solanum lycopersicum) affected carotenoid contents and the expression of carotenogenic genes. The sepals of CsMADS6-overexpressing tomato lines exhibited dramatic changes in carotenoid profiles, accompanied by changes in plastid ultrastructure. Global transcriptome analysis of transgenic sepals revealed that CsMADS6 regulates a series of pathways that promote increases in flux through the carotenoid pathway. Overall, these findings establish that CsMADS6 directly regulates LCYb1 and other carotenogenic genes to coordinately and positively modulate carotenoid metabolism in plants, which may provide strategies to improve the nutritional quality of crops.
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