Patterns and Mechanisms of Ancestral Histone Protein Inheritance in Budding Yeast
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-a...
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| Published in | PLoS biology Vol. 9; no. 6; p. e1001075 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.06.2011
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1545-7885 1544-9173 1545-7885 |
| DOI | 10.1371/journal.pbio.1001075 |
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| 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. |
|---|---|
| AbstractList | Tracking of ancestral histone proteins over multiple generations of genome replication in yeast reveals that old histones move along genes from 3' toward 5' over time, and that maternal histones move up to around 400 bp during genomic replication. 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. It is widely believed that chromatin, the nucleoprotein packaged state of eukaryotic genomes, can carry epigenetic information and thus transmit gene expression patterns to replicating cells. However, the inheritance of genomic packaging status is subject to mechanistic challenges that do not confront the inheritance of genomic DNA sequence. Most notably, histone proteins must at least transiently dissociate from the maternal genome during replication, and it is unknown whether or not maternal proteins re-associate with daughter genomes near the sequence they originally occupied on the maternal genome. Here, we use a novel method for tracking old proteins to determine where histone proteins accumulate after 1, 3, or 6 generations of growth in yeast. To our surprise, ancestral histones accumulate near the 5' end of long, relatively inactive genes. Using a mathematical model, we show that our results can be explained by the combined effects of histone replacement, histone movement along genes from 3' towards 5' ends, and histone spreading during replication. Our results show that old histones do move but stay relatively close to their original location (within around 400 base-pairs), which places important constraints on how chromatin could potentially carry epigenetic information. Our findings also suggest that accumulation of the ancestral histones that are inherited can influence histone modification patterns. 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. 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.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. Tracking of ancestral histone proteins over multiple generations of genome replication in yeast reveals that old histones move along genes from 3′ toward 5′ over time, and that maternal histones move up to around 400 bp during genomic replication. 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. It is widely believed that chromatin, the nucleoprotein packaged state of eukaryotic genomes, can carry epigenetic information and thus transmit gene expression patterns to replicating cells. However, the inheritance of genomic packaging status is subject to mechanistic challenges that do not confront the inheritance of genomic DNA sequence. Most notably, histone proteins must at least transiently dissociate from the maternal genome during replication, and it is unknown whether or not maternal proteins re-associate with daughter genomes near the sequence they originally occupied on the maternal genome. Here, we use a novel method for tracking old proteins to determine where histone proteins accumulate after 1, 3, or 6 generations of growth in yeast. To our surprise, ancestral histones accumulate near the 5′ end of long, relatively inactive genes. Using a mathematical model, we show that our results can be explained by the combined effects of histone replacement, histone movement along genes from 3′ towards 5′ ends, and histone spreading during replication. Our results show that old histones do move but stay relatively close to their original location (within around 400 base-pairs), which places important constraints on how chromatin could potentially carry epigenetic information. Our findings also suggest that accumulation of the ancestral histones that are inherited can influence histone modification patterns. 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. |
| Audience | Academic |
| Author | Weiner, Assaf van Welsem, Tibor Rando, Oliver J. Friedman, Nir Verzijlbergen, Kitty F. van Leeuwen, Fred Radman-Livaja, Marta |
| AuthorAffiliation | 3 School of Computer Science and Engineering, The Hebrew University, Jerusalem, Israel 1 Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, Massachusetts, United States of America 2 Division of Gene Regulation, Netherlands Cancer Institute, and Netherlands Proteomics Center, Amsterdam, The Netherlands Adolf Butenandt Institute, Germany 4 Alexander Silberman Institute of Life Sciences, The Hebrew University, Jerusalem, Israel |
| AuthorAffiliation_xml | – name: 4 Alexander Silberman Institute of Life Sciences, The Hebrew University, Jerusalem, Israel – name: 1 Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, Massachusetts, United States of America – name: Adolf Butenandt Institute, Germany – name: 3 School of Computer Science and Engineering, The Hebrew University, Jerusalem, Israel – name: 2 Division of Gene Regulation, Netherlands Cancer Institute, and Netherlands Proteomics Center, Amsterdam, The Netherlands |
| Author_xml | – sequence: 1 givenname: Marta surname: Radman-Livaja fullname: Radman-Livaja, Marta – sequence: 2 givenname: Kitty F. surname: Verzijlbergen fullname: Verzijlbergen, Kitty F. – sequence: 3 givenname: Assaf surname: Weiner fullname: Weiner, Assaf – sequence: 4 givenname: Tibor surname: van Welsem fullname: van Welsem, Tibor – sequence: 5 givenname: Nir surname: Friedman fullname: Friedman, Nir – sequence: 6 givenname: Oliver J. surname: Rando fullname: Rando, Oliver J. – sequence: 7 givenname: Fred surname: van Leeuwen fullname: van Leeuwen, Fred |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21666805$$D View this record in MEDLINE/PubMed https://hal.science/hal-02193327$$DView record in HAL |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2011 Public Library of Science 2011 Radman-Livaja et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Radman-Livaja M, Verzijlbergen KF, Weiner A, van Welsem T, Friedman N, et al. (2011) Patterns and Mechanisms of Ancestral Histone Protein Inheritance in Budding Yeast. PLoS Biol 9(6): e1001075. doi:10.1371/journal.pbio.1001075 Attribution Radman-Livaja et al. 2011 |
| Copyright_xml | – notice: COPYRIGHT 2011 Public Library of Science – notice: 2011 Radman-Livaja et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Radman-Livaja M, Verzijlbergen KF, Weiner A, van Welsem T, Friedman N, et al. (2011) Patterns and Mechanisms of Ancestral Histone Protein Inheritance in Budding Yeast. PLoS Biol 9(6): e1001075. doi:10.1371/journal.pbio.1001075 – notice: Attribution – notice: Radman-Livaja et al. 2011 |
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| DOI | 10.1371/journal.pbio.1001075 |
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| DocumentTitleAlternate | Transgenerational Histone Retention in Yeast |
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| Keywords | DNA Topoisomerases, Type I Saccharomycetales Inheritance Patterns Models, Biological Saccharomyces cerevisiae Proteins Histones DNA Replication Timing Genes, Fungal Nucleosomes Transcription, Genetic Protein Processing, Post-Translational Kinetics Mutation |
| Language | English |
| License | Attribution: http://creativecommons.org/licenses/by This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. Creative Commons Attribution License |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 ObjectType-Article-2 ObjectType-Feature-1 The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: FvL OJR KFV MRL. Performed the experiments: KFV MRL. Analyzed the data: MRL AW NF OJR. Contributed reagents/materials/analysis tools: TvW. Wrote the paper: MRL KFV AW NF OJR FvL. |
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| Snippet | Replicating chromatin involves disruption of histone-DNA contacts and subsequent reassembly of maternal histones on the new daughter genomes. In bulk, maternal... Tracking of ancestral histone proteins over multiple generations of genome replication in yeast reveals that old histones move along genes from 3' toward 5'... Tracking of ancestral histone proteins over multiple generations of genome replication in yeast reveals that old histones move along genes from 3′ toward 5′... Replicating chromatin involves disruption of histone-DNA contacts and subsequent reassembly of maternal histones on the new daughter genomes. In bulk,... |
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| SubjectTerms | Analysis Biochemistry, Molecular Biology Biology Chromatin Deoxyribonucleic acid DNA DNA Replication Timing DNA Topoisomerases, Type I - metabolism Epigenetics Genes, Fungal - genetics Genetic aspects Genetics Genomics Histones Histones - chemistry Histones - genetics Histones - metabolism Inheritance Patterns - genetics Kinetics Life Sciences Models, Biological Mutation - genetics Nucleosomes - metabolism Physiological aspects Protein Processing, Post-Translational Proteins Saccharomyces cerevisiae Saccharomyces cerevisiae Proteins - genetics Saccharomycetales - genetics Transcription, Genetic Yeast Yeast fungi Yeasts |
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| Title | Patterns and Mechanisms of Ancestral Histone Protein Inheritance in Budding Yeast |
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