Dark-inducible BGH2 suppresses GLK transcription factors and maintains plastid homeostasis to promote light adaptation

Abstract Light is an essential energy source for plants, but it can cause harmful photooxidative damage that induces cell death. When dark-germinated plants are exposed to the light, etioplasts differentiate into chloroplasts, converting protochlorophyllide (Pchlide) into chlorophyll, while excessive free Pchlide accumulation in etioplasts causes reactive oxygen species (ROS) generation and cell death under light conditions. Despite this knowledge, the molecular mechanisms by which dark-germinated plants adapt to the light environment via transcriptional regulation of chlorophyll biosynthesis remain unclear. We previously identified BRZ-INSENSITIVE-PALE GREEN 4 (BPG4) as a light-inducible chloroplast homeostasis factor. Here, we identified the BPG4 paralog BPG4 HOMOLOGOUS GENE 2 (BGH2) as a nucleus-localized plastid regulator required for light adaptation in Arabidopsis thaliana. Dark-inducible BGH2 interacts with GOLDEN2-LIKE 1 (GLK1) and GLK2, master transcription factors regulating chlorophyll biosynthesis. This interaction suppresses excessive photosynthesis-associated nuclear gene (PhANG) expression, avoids Pchlide overaccumulation in the dark, prevents ROS generation, and promotes healthy cotyledon greening during de-etiolation. BPG4 and BGH2 expression is regulated by GLK and PHYTOCHROME-INTERACTING FACTOR transcription factors under light and dark conditions. Overall, our findings suggest that BGH2 plays an essential role in fine-tuning chlorophyll biosynthesis and etioplast homeostasis by inhibiting GLK transcriptional activity and excessive PhANG expression in the dark.