In land plants, one of the processes vital to cope with environmental changes is the accumulation of photoprotective flavonoids such as flavonols and anthocyanins. The inactivation of SUCROSE NON-FERMENTING1 RELATED PROTEIN KINASE1 (SnRK1), which acts in a chloroplast-derived sugar signalling pathway, permits the activation of flavonoid biosynthesis in high-light. The present study provides genetic evidence that SnRK1 acts upstream of PRODUCTION OF ANTHOCYANIN PIGMENT1 (PAP1), encoding a crucial transcription factor that activates the anthocyanin branch of flavonoid biosynthesis during high-light acclimation. A time-resolved expression analysis indicates a two-phasic suppression of MYB-LIKE2 (MYBL2), a repressor of anthocyanin production, involving SnRK1 inactivation for anthocyanin accumulation during prolonged high-light exposure. Furthermore, overexpression of PAP1 resulted in the marked suppression of MYB11, MYB12 and MYB111 and FLAVONOL SYNTHASE1, initiating the flavonol branch of the pathway. Analysis of a flavonoid-deficient chalcone synthase mutant overexpressing PAP1 suggests that regulation of flavonoid biosynthesis is PAP1-dependent but independent of flavonoid intermediates and end products. It is proposed that PAP1 suppresses the flavonol branch by an unknown mechanism, thereby promoting the consumption of carbon building blocks for anthocyanin production to permit the fine-tuning of the pathway.