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Rtt109 promotes nucleosome replacement ahead of the replication fork

DNA replication perturbs chromatin by triggering the eviction, replacement, and incorporation of nucleosomes. How this dynamic is orchestrated in time and space is poorly understood. Here, we apply a genetically encoded sensor for histone exchange to follow the time-resolved histone H3 exchange prof...

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Detalles Bibliográficos
Autores principales: Jonas, Felix, Yaakov, Gilad, Barkai, Naama
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9248883/
https://www.ncbi.nlm.nih.gov/pubmed/35609993
http://dx.doi.org/10.1101/gr.276674.122
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author Jonas, Felix
Yaakov, Gilad
Barkai, Naama
author_facet Jonas, Felix
Yaakov, Gilad
Barkai, Naama
author_sort Jonas, Felix
collection PubMed
description DNA replication perturbs chromatin by triggering the eviction, replacement, and incorporation of nucleosomes. How this dynamic is orchestrated in time and space is poorly understood. Here, we apply a genetically encoded sensor for histone exchange to follow the time-resolved histone H3 exchange profile in budding yeast cells undergoing slow synchronous replication in nucleotide-limiting conditions. We find that new histones are incorporated not only behind, but also ahead of the replication fork. We provide evidence that Rtt109, the S-phase-induced acetyltransferase, stabilizes nucleosomes behind the fork but promotes H3 replacement ahead of the fork. Increased replacement ahead of the fork is independent of the primary Rtt109 acetylation target H3K56 and rather results from Vps75-dependent Rtt109 activity toward the H3 N terminus. Our results suggest that, at least under nucleotide-limiting conditions, selective incorporation of differentially modified H3s behind and ahead of the replication fork results in opposing effects on histone exchange, likely reflecting the distinct challenges for genome stability at these different regions.
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spelling pubmed-92488832022-12-01 Rtt109 promotes nucleosome replacement ahead of the replication fork Jonas, Felix Yaakov, Gilad Barkai, Naama Genome Res Research DNA replication perturbs chromatin by triggering the eviction, replacement, and incorporation of nucleosomes. How this dynamic is orchestrated in time and space is poorly understood. Here, we apply a genetically encoded sensor for histone exchange to follow the time-resolved histone H3 exchange profile in budding yeast cells undergoing slow synchronous replication in nucleotide-limiting conditions. We find that new histones are incorporated not only behind, but also ahead of the replication fork. We provide evidence that Rtt109, the S-phase-induced acetyltransferase, stabilizes nucleosomes behind the fork but promotes H3 replacement ahead of the fork. Increased replacement ahead of the fork is independent of the primary Rtt109 acetylation target H3K56 and rather results from Vps75-dependent Rtt109 activity toward the H3 N terminus. Our results suggest that, at least under nucleotide-limiting conditions, selective incorporation of differentially modified H3s behind and ahead of the replication fork results in opposing effects on histone exchange, likely reflecting the distinct challenges for genome stability at these different regions. Cold Spring Harbor Laboratory Press 2022-06 /pmc/articles/PMC9248883/ /pubmed/35609993 http://dx.doi.org/10.1101/gr.276674.122 Text en © 2022 Jonas et al.; Published by Cold Spring Harbor Laboratory Press https://creativecommons.org/licenses/by-nc/4.0/This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see https://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) .
spellingShingle Research
Jonas, Felix
Yaakov, Gilad
Barkai, Naama
Rtt109 promotes nucleosome replacement ahead of the replication fork
title Rtt109 promotes nucleosome replacement ahead of the replication fork
title_full Rtt109 promotes nucleosome replacement ahead of the replication fork
title_fullStr Rtt109 promotes nucleosome replacement ahead of the replication fork
title_full_unstemmed Rtt109 promotes nucleosome replacement ahead of the replication fork
title_short Rtt109 promotes nucleosome replacement ahead of the replication fork
title_sort rtt109 promotes nucleosome replacement ahead of the replication fork
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9248883/
https://www.ncbi.nlm.nih.gov/pubmed/35609993
http://dx.doi.org/10.1101/gr.276674.122
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