Streamlined regulation of chloroplast development in the liverwortMarchantia polymorpha

Abstract

SummaryPhotosynthesis in eukaryotic cells takes place in chloroplasts that develop from undifferentiated plastids in response to light. Two families of transcription factors known as Golden2-like (GLK) and GATA regulate plant chloroplast development, and the MIR171-targeted SCARECROW-LIKE (SCL) GRAS transcription factors regulate chlorophyll biosynthesis. Additionally, the Elongated Hypocotyl 5 (HY5) transcription factor plays a critical role in photomorphogenesis. The extent to which these proteins carry out conserved roles in non-seed plants such as the liverworts is not known. Here we determine the degree of functional conservation of the GLK, GATA, SCL and HY5 proteins in controlling chloroplast development in the model liverwortMarchantia polymorpha. Our results indicate that GATA, SCL and HY5 have a minimal or undetectable role in chloroplast biogenesis but loss of GLK function leads to reduced chloroplast size, underdeveloped thylakoid membranes and lower chlorophyll accumulation. ChIP-seq and RNA-seq analyses revealed that GLK can directly regulate many photosynthetic and chloroplast development-related genes. But there is extensive divergence between its function inM. polymorphaand flowering plants. Collectively our findings suggest that the function of GATA as well as SCL in chloroplast development and the more specialised role of HY5 in photomorphogenesis, either evolved after the divergence of vascular plants from bryophytes, that were lost inM. polymorpha, or that functional redundancy is masking their roles. In contrast, and consistent with its presence in algae, GLK plays a conserved role in chloroplast biogenesis of liverworts and vascular plants.