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Chloroplast nucleoid is organized by membrane association of transcribed genes [SOLINA]

ABSTRACT: Chloroplasts are organelles responsible for photosynthesis. They originated form a procaryotic ancestor in the process of endosymbiosis and contain their own genomes. The chloroplast genome is packaged into a chromatin-like structure known as the nucleoid. The internal arrangement of the nucleoid, molecular mechanisms of DNA packaging and connection of the nucleoid structure to gene expression remain poorly understood. We show that Arabidopsis thaliana chloroplast nucleoids have a unique organization driven by DNA binding to the thylakoid membranes. Membrane association of specific DNA regions is correlated with high levels of transcription, high protein occupancy and reduced DNA accessibility. Genes with low levels of transcription are further away from the membranes, have lower protein occupancy and higher DNA accessibility. Gene-specific disruption of transcription in sigma factor mutants causes a corresponding reduction in membrane association, indicating that RNA polymerase activity causes DNA tethering to the membranes. We propose that transcription organizes the chloroplast nucleoid into a transcriptionally active membrane-associated core and a less active Periphery.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE228229 | GEO | 2023/05/10

REPOSITORIES: GEO

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Project description:Plastids contain multiple copies of the plastid chromosome, folded together with proteins and RNA into nucleoids. The degree to which components of the plastid gene expression and protein biogenesis machineries are nucleoid associated, and the factors involved in plastid DNA organization, repair, and replication, are poorly understood. To provide a conceptual framework for nucleoid function, we characterized the proteomes of highly enriched nucleoid fractions of proplastids and mature chloroplasts isolated from the maize (Zea mays) leaf base and tip, respectively, using mass spectrometry. Quantitative comparisons with proteomes of unfractionated proplastids and chloroplasts facilitated the determination of nucleoid-enriched proteins. This nucleoid-enriched proteome included proteins involved in DNA replication, organization, and repair as well as transcription, mRNA processing, splicing, and editing. Many proteins of unknown function, including pentatricopeptide repeat (PPR), tetratricopeptide repeat (TPR), DnaJ, and mitochondrial transcription factor (mTERF) domain proteins, were identified. Strikingly, 70S ribosome and ribosome assembly factors were strongly overrepresented in nucleoid fractions, but protein chaperones were not. Our analysis strongly suggests that mRNA processing, splicing, and editing, as well as ribosome assembly, take place in association with the nucleoid, suggesting that these processes occur cotranscriptionally. The plastid developmental state did not dramatically change the nucleoid-enriched proteome but did quantitatively shift the predominating function from RNA metabolism in undeveloped plastids to translation and homeostasis in chloroplasts. This study extends the known maize plastid proteome by hundreds of proteins, including more than 40 PPR and mTERF domain proteins, and provides a resource for targeted studies on plastid gene expression. Details of protein identification and annotation are provided in the Plant Proteome Database.

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Chloroplast nucleoid is organized by membrane association of transcribed genes [SOLINA]

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