The SWI2/SNF2 Chromatin-Remodeling ATPase BRAHMA Regulates Chlorophyll Biosynthesis in Arabidopsis

Abstract

Chlorophyll biosynthesis is critical for chloroplast development and photosynthesis in plants. Although reactions in the chlorophyll biosynthetic pathway have been largely known, little is known about the regulatory mechanisms of this pathway. In this study, we found that the dark-grown knockout and knockdown mutants as well as RNA-interference transgenic seedlings of BRAHMA (BRM), which encodes an SWI2/SNF2 chromatin-remodeling ATPase, had higher greening rates, accumulated less protochlorophyllide, and produced less reactive oxygen species than Arabidopsis wild-type plants did upon light exposure. The expression of NADPH:protochlorophyllide oxidoreductase A (PORA), PORB, and PORC, which catalyze a key step in chlorophyll biosynthesis, was increased in the brm mutants. We found that BRM physically interacted with the bHLH transcription factor PHYTOCHROME-INTERACTING FACTOR 1 (PIF1) through its N-terminal domains. Furthermore, we demonstrated that BRM was directly recruited to the cis-regulatory regions of PORC, but not of PORA and PORB, at least partially in a PIF1-dependent manner and the level of histone H3 lysine 4 tri-methylation (H3K4me3) at PORC loci was increased in the brm mutant. Taken together, our data indicate that the chromatin-remodeling enzyme BRM modulates PORC expression through interacting with PIF1, providing a novel regulatory mechanism by which plants fine-tune chlorophyll biosynthesis during the transition from heterotrophic to autotrophic growth.