The plastid-encoded RNA polymerase structures a logistic chain for light-induced photosynthesis

The chloroplast is the semi-autonomous organelle of eukaryotes that performs photosynthesis. In higher plants, chloroplast biogenesis depends on a tight transcriptional coordination of both nuclear- and-plastid photosynthesis-associated genes. The plastid-encoded RNA-polymerase (PEP) is composed of a plastid-encoded catalytic core, similar to multi-subunit RNA polymerases, bound to fifteen nuclear-encoded PEP-associated proteins (PAPs). The binding of all the PAPs to the catalytic core is essential for plastid transcription of photosynthesis-associated genes. Our cryo-electron microscopy structure of the native 21-subunit PEP from Sinapis alba reveals the distinctive patterning of PAP interactions, which evolved upon the ancestral cyanobacterial catalytic core acting as a scaffold. Using PAP8 in planta as bait for affinity purification and proximity labeling, we provide the protein landscapes surrounding the PEP and other PAP8-interacting complexes at the transition from skotomorphogenesis to photomorphogenesis. The data highlight multiple functional couplings in which plastid transcription is at the beginning of a spatial logistic chain, extending from transcription to the assembly of the photosynthetic apparatus into the thylakoids. In addition, dark-specific interactions between photoreceptors and PAP8 establish a physical link between an integrated light signaling and plastid functions.