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PMID: 21666805 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Patterns and mechanisms of ancestral histone protein inheritance in budding yeast.

PLoS biology ·Vol. 9 ·No. 6 ·2011-06-00 ·Pages e1001075

Radman-Livaja M, Verzijlbergen KF, Weiner A, van Welsem T, Friedman N, Rando OJ, van Leeuwen F

Abstract

Replicating chromatin involves disruption of histone-DNA contacts and subsequent reassembly of maternal histones on the new daughter genomes. In bulk, maternal histones are randomly segregated to the two daughters, but little is known about the fine details of this process: do maternal histones re-assemble at preferred locations or close to their original loci? Here, we use a recently developed method for swapping epitope tags to measure the disposition of ancestral histone H3 across the yeast genome over six generations. We find that ancestral H3 is preferentially retained at the 5' ends of most genes, with strongest retention at long, poorly transcribed genes. We recapitulate these observations with a quantitative model in which the majority of maternal histones are reincorporated within 400 bp of their pre-replication locus during replication, with replication-independent replacement and transcription-related retrograde nucleosome movement shaping the resulting distributions of ancestral histones. We find a key role for Topoisomerase I in retrograde histone movement during transcription, and we find that loss of Chromatin Assembly Factor-1 affects replication-independent turnover. Together, these results show that specific loci are enriched for histone proteins first synthesized several generations beforehand, and that maternal histones re-associate close to their original locations on daughter genomes after replication. Our findings further suggest that accumulation of ancestral histones could play a role in shaping histone modification patterns.

MeSH Terms
DNA Replication Timing DNA Topoisomerases, Type I/metabolism Genes, Fungal/genetics Histones/chemistry,genetics,metabolism Inheritance Patterns/genetics Kinetics Models, Biological Mutation/genetics Nucleosomes/metabolism Protein Processing, Post-Translational Saccharomyces cerevisiae Proteins/genetics Saccharomycetales/genetics Transcription, Genetic
Chemicals
Histones Nucleosomes Saccharomyces cerevisiae Proteins DNA Topoisomerases, Type I
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Radman-Livaja Marta
Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, Massachusetts, United States of America.
Verzijlbergen Kitty F
Weiner Assaf
van Welsem Tibor
Friedman Nir
Rando Oliver J
van Leeuwen Fred
Conflict of Interest

The authors have declared that no competing interests exist.

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Article Info
Journal
PLoS biology
Abbr.
PLoS Biol
ISSN
1545-7885
DOI
10.1371/journal.pbio.1001075
Published
2011-06-00
Epub
2011-00-07
Pages
e1001075
Language
English
Region
United States
NLM ID
101183755
PMCID
PMC3110181
Subset
IM
Grants
NIGMS NIH HHS · R01 GM079205 · United States
NIGMS NIH HHS · GM079205 · United States
Corrections
CommentIn
PMID: 21666804
External Links
PubMed source DOI: 10.1371/journal.pbio.1001075 PMC Full Text View journal details
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