Reversible Glc-conjugation/hydrolysis modulates the homeostasis of lunularic acid in Marchantia polymorpha growth

The circadian clock efficiently coordinates growth regulators and plant growth in the temporal regulation of physiological processes. The involvement of the growth-regulator-clock in governing the spatio-temporal regulation of plant growth and development remains unexplained in the nonvascular liverworts. In this study, we aimed to assess the relationship between the putative liverwort growth regulator lunularic acid (LA) levels and the growth variation of Marchantia polymorpha according to the circadian clock. LA level exhibited a similar circadian rhythm as gemmalings' accelerated growth during the light phase, and UV-B stress experiments implied that the surge in LA levels at the start of the light phase could serve as a circadian rhythm-based prediction for preempting UV-B injury, with LA serving as a protective shield against UV-B irradiation. Notably, Glc-conjugation/hydrolysis, buffering the anabolism-catabolism of endogenous LA, was rhythmically regulated. Furthermore, the reversible conversion between LA and LA-4'-O-glucoside (mediated by glucosyltransferases MpUGT744A1 and β-glucosidases MpBGLU2/3) was characterized both in vitro and in vivo and evidenced to be relevant to diurnal variation in LA level. Interaction between MpUGT744A1 and MpBGLU2 ensures the efficient metabolic flux between LA and LA-GE. These findings shed light on the regulatory mechanisms that govern LA metabolism and the importance of understanding the temporal aspects of LA for Marchantia's adaptive response to environmental stressors such as UV-B radiation.