FAR1-RELATED SEQUENCE 5 prevents photobleaching under short days by balancing chlorophyll biosynthetic gene expression

Plants must precisely regulate the expression of chlorophyll biosynthetic genes to prevent overaccumulation of photosensitive intermediates that cause photobleaching. GOLDEN 2-LIKEs activate the expression of certain chlorophyll biosynthetic genes, including HEMA1, but not others, such as HEMC, suggesting the involvement of additional regulatory factors to balance the expression of chlorophyll biosynthetic genes. We report that the Arabidopsis (Arabidopsis thaliana) far1-related sequence 5 (frs5) mutant undergoes photobleaching under short-day (SD) but not long-day (LD) conditions. Under SD, the frs5 mutant accumulates high protochlorophyllide (PChlide) levels at dawn, leading to reactive oxygen species production and photobleaching upon light exposure. FRS5 directly binds to the HEMC promoter to activate its expression. Accordingly, HEMC expression remains low in the frs5 mutant regardless of the time of day. Paradoxically, the overaccumulation of PChlide at dawn in the frs5 mutant results from low HEMC expression, as the phenotype can be rescued by either FRS5 or additional copies of HEMC. A weak hemC allele mutant also accumulates PChlide at dawn and undergoes photobleaching under SD but not LD. We demonstrate that reduced HEMC expression leads to the accumulation of porphobilinogen and prolongs PChlide synthesis into the night, causing PChlide accumulation at dawn and subsequent photobleaching upon light exposure. Our results support that FRS5 prevents photobleaching by maintaining balanced expression of chlorophyll biosynthetic genes.