BBX16 mediates the repression of seedling photomorphogenesis downstream of the GUN1-GLK1 module during retrograde signaling

Summary Plastid-to-nucleus retrograde signals (RS) initiated by dysfunctional chloroplasts impact photomorphogenic development. We previously showed that the transcription factor GLK1 acts downstream of the RS-regulator GUN1 in photodamaging conditions to regulate not only the well-established expression of photosynthesis-associated nuclear genes ( PhANGs ) but also to regulate seedling morphogenesis. Specifically, the GUN1/GLK1 module inhibits the light-induced PIF-repressed transcriptional network to suppress cotyledon development when chloroplast integrity is compromised, modulating the area exposed to potentially damaging high light. However, how the GUN1/GLK1 module inhibits photomorphogenesis upon chloroplast damage remained undefined. Here, we report the identification of BBX16 as a novel direct target of GLK1. BBX16 is induced and promotes photomorphogenesis in moderate light and it is repressed via GUN1/GLK1 after chloroplast damage. Additionally, we show that BBX16 represents a regulatory branching point downstream of GUN1/GLK1 in the regulation of PhANG expression and seedling development upon RS activation. The gun1 phenotype in lincomycin and the gun1-like phenotype of GLK1OX are markedly suppressed in gun1bbx16 and GLK1OXbbx16 . This study identifies BBX16 as the first member of the BBX family involved in RS, and defines a molecular bifurcation mechanism operated by GLK1/BBX16 to optimize seedling deetiolation, and to ensure photoprotection in unfavorable light conditions.