The moss flavone synthase I positively regulates the tolerance of plants to drought stress and UV-B radiation

•Flavones were the most abundant flavonoids in the Antarctic moss Pohlia nutans.•PnFNSI is the first characterized type I flavone synthase from moss species.•PnFNSI is cold-adapted enzymes with an optimal temperature between 15～20 °C.•PnFNSI can catalyze the conversion of naringenin to apigenin.•PnFNSI enhances the plant tolerance to drought stress and UV-B radiation. Flavonoids are extensively distributed secondary metabolites in land plants. They play a critical role in plant evolution from aquatic to terrestrial and plant adaption to ultraviolet radiation. However, the downstream branching pathway of flavonoids and its regulatory mechanism in bryophytes, which are the most ancient of terrestrial plants, remain unclear. Here, a type I flavone synthase (PnFNSI) was characterized from the Antarctic moss Pohlia nutans. PnFNSI was primarily distributed in the cytoplasm, as detected by subcellular localization. PnFNSI could catalyze the conversion of naringenin to apigenin with an optimal temperature between 15 and 20 °C in vitro. Overexpression of PnFNSI in Arabidopsis alleviated the growth restriction caused by naringenin and accumulated apigenin product. PnFNSI-overexpressing plants showed enhanced plant tolerance to drought stress and UV-B radiation. PnFNSI also increased the enzyme activities and gene transcription levels of reactive oxygen species (ROS) scavengers, protecting plants against oxidative stress. Moreover, overexpression of PnFNSI enhanced the flavone biosynthesis pathway in Arabidopsis. Therefore, this moss FNSI-type enzyme participates in flavone metabolism, conferring protection against drought stress and UV-B radiation.