Flavonols are important plant photoprotectants to defence UV-B irradiation, however, the underlying transcriptional regulatory mechanism of rapid flavonol accumulation in response to UV-B remains unknown. In this study, content of flavonols was significantly induced from 0.11 to 3.80 mg/g fresh weight by UV-B irradiation in leaves of Morella rubra seedlings. MrERF34 was identified as an activator that can regulate the expression of MrFLS2, and promoted flavonol biosynthesis with activator MrMYB12 under UV-B treatment. Transient overexpression of MrERF34 resulted in higher flavonol accumulation, while virus-induced gene silencing of MrERF34 reduced the content of flavonols in bayberry leaves. We further demonstrated that a repressor MrERF4 inhibited the expression of MrERF34 and MrMYB12 as well as MrFLS2 via ERF-associated-amphiphilic repression motif. Exposure to UV-B reduced the promoter activity and transcription of MrERF4, which weakened the inhibitory effect of MrERF4 on MrERF34, MrMYB12, and MrFLS2, leading to a tremendous accumulation of flavonols. Such inhibitory roles of MrERF4 in regulation of flavonol biosynthesis were further validated by transient overexpression in leaves of Nicotiana benthamiana and M. rubra. These findings enrich the synergistical regulatory mechanisms between repressor and activators in flavonol biosynthesis, and provide new insights into photoprotectants biosynthesis to mitigate UV-B stress in plants.
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