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

2024 · doi:10.1101/2024.10.25.620210
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The cryo-EM structure of the 21-subunit PEP reveals how nuclear-encoded PAPs interact with the core polymerase to regulate plastid transcription, linking light signaling to photosynthetic apparatus assembly.

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The paper studied how higher plants coordinate transcription of photosynthesis-associated genes during chloroplast development, focusing on the plastid-encoded RNA polymerase (PEP) and its 15 plastid-associated proteins. Using cryo-electron microscopy of the native 21-subunit PEP from Sinapis alba, plus in planta affinity purification and proximity labeling with PAP8, the authors mapped PAP interaction patterns and protein landscapes across the transition from skotomorphogenesis to photomorphogenesis, highlighting functional couplings that connect plastid transcription to later assembly of the photosynthetic apparatus in thylakoid membranes. A key caveat is that the reported mechanistic insights rely on structural/interaction mapping in this plant system rather than direct functional perturbation across all possible stages. The paper does not explicitly discuss endometriosis or adenomyosis; it was included in the corpus via a keyword match in the upstream search index.

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Abstract

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.
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Abstract 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. Competing Interest Statement The authors have declared no competing interest. Footnotes francois-xavier.gillet{at}univ-lyon1.fr; gregory.effantin{at}ibs.fr; gian-luca.freiherr-von-scholley{at}esrf.fr; sabine.brugiere{at}cea.fr; maud.turquand{at}unine.ch; noor.pasha{at}universite-paris-saclay.fr; daphna.fenel{at}ibs.fr; alicia.vallet{at}ibs.fr; yohann.coute{at}cea.fr; david.cobessi{at}ibs.fr; robert.blanvillain{at}cea.fr

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