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Chromatin Mediation of a Transcriptional Memory Effect in Yeast

Previous studies have described a transcriptional “memory effect,” whereby transcript levels of many Abf1-regulated genes in the budding yeast Saccharomyces cerevisiae are undiminished even after Abf1 has dissociated from its regulatory sites. Here we provide additional support for this effect and i...

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Autores principales: Paul, Emily, Tirosh, Itay, Lai, William, Buck, Michael J., Palumbo, Michael J., Morse, Randall H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Genetics Society of America 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4426369/
https://www.ncbi.nlm.nih.gov/pubmed/25748434
http://dx.doi.org/10.1534/g3.115.017418
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author Paul, Emily
Tirosh, Itay
Lai, William
Buck, Michael J.
Palumbo, Michael J.
Morse, Randall H.
author_facet Paul, Emily
Tirosh, Itay
Lai, William
Buck, Michael J.
Palumbo, Michael J.
Morse, Randall H.
author_sort Paul, Emily
collection PubMed
description Previous studies have described a transcriptional “memory effect,” whereby transcript levels of many Abf1-regulated genes in the budding yeast Saccharomyces cerevisiae are undiminished even after Abf1 has dissociated from its regulatory sites. Here we provide additional support for this effect and investigate its molecular basis. We show that the effect is observed in a distinct abf1 ts mutant from that used in earlier studies, demonstrating that it is robust, and use chromatin immunoprecipitation to show that Abf1 association is decreased similarly from memory effect and transcriptionally responsive genes at the restrictive temperature. We also demonstrate that the association of TATA-binding protein and Pol II decreases after the loss of Abf1 binding for transcriptionally responsive genes but not for memory effect genes. Examination of genome-wide nucleosome occupancy data reveals that although transcriptionally responsive genes exhibit increased nucleosome occupancy in abf1 ts yeast, the promoter regions of memory effect targets show no change in abf1 ts mutants, maintaining an open chromatin conformation even after Abf1 eviction. This contrasting behavior reflects different inherent propensity for nucleosome formation between the two classes, driven by the presence of A/T-rich sequences upstream of the Abf1 site in memory effect gene promoters. These sequence-based differences show conservation in closely related fungi and also correlate with different gene expression noise, suggesting a physiological basis for greater access to “memory effect” promoter regions. Thus, our results establish a conserved mechanism underlying a transcriptional memory effect whereby sequences surrounding Abf1 binding sequences affect local nucleosome occupancy following loss of Abf1 binding. Furthermore, these findings demonstrate that sequence-based differences in the propensity for nucleosome occupancy can influence the transcriptional response of genes to an altered regulatory signal.
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spelling pubmed-44263692015-05-13 Chromatin Mediation of a Transcriptional Memory Effect in Yeast Paul, Emily Tirosh, Itay Lai, William Buck, Michael J. Palumbo, Michael J. Morse, Randall H. G3 (Bethesda) Investigations Previous studies have described a transcriptional “memory effect,” whereby transcript levels of many Abf1-regulated genes in the budding yeast Saccharomyces cerevisiae are undiminished even after Abf1 has dissociated from its regulatory sites. Here we provide additional support for this effect and investigate its molecular basis. We show that the effect is observed in a distinct abf1 ts mutant from that used in earlier studies, demonstrating that it is robust, and use chromatin immunoprecipitation to show that Abf1 association is decreased similarly from memory effect and transcriptionally responsive genes at the restrictive temperature. We also demonstrate that the association of TATA-binding protein and Pol II decreases after the loss of Abf1 binding for transcriptionally responsive genes but not for memory effect genes. Examination of genome-wide nucleosome occupancy data reveals that although transcriptionally responsive genes exhibit increased nucleosome occupancy in abf1 ts yeast, the promoter regions of memory effect targets show no change in abf1 ts mutants, maintaining an open chromatin conformation even after Abf1 eviction. This contrasting behavior reflects different inherent propensity for nucleosome formation between the two classes, driven by the presence of A/T-rich sequences upstream of the Abf1 site in memory effect gene promoters. These sequence-based differences show conservation in closely related fungi and also correlate with different gene expression noise, suggesting a physiological basis for greater access to “memory effect” promoter regions. Thus, our results establish a conserved mechanism underlying a transcriptional memory effect whereby sequences surrounding Abf1 binding sequences affect local nucleosome occupancy following loss of Abf1 binding. Furthermore, these findings demonstrate that sequence-based differences in the propensity for nucleosome occupancy can influence the transcriptional response of genes to an altered regulatory signal. Genetics Society of America 2015-03-05 /pmc/articles/PMC4426369/ /pubmed/25748434 http://dx.doi.org/10.1534/g3.115.017418 Text en Copyright © 2015 Paul et al. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution Unported License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Investigations
Paul, Emily
Tirosh, Itay
Lai, William
Buck, Michael J.
Palumbo, Michael J.
Morse, Randall H.
Chromatin Mediation of a Transcriptional Memory Effect in Yeast
title Chromatin Mediation of a Transcriptional Memory Effect in Yeast
title_full Chromatin Mediation of a Transcriptional Memory Effect in Yeast
title_fullStr Chromatin Mediation of a Transcriptional Memory Effect in Yeast
title_full_unstemmed Chromatin Mediation of a Transcriptional Memory Effect in Yeast
title_short Chromatin Mediation of a Transcriptional Memory Effect in Yeast
title_sort chromatin mediation of a transcriptional memory effect in yeast
topic Investigations
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4426369/
https://www.ncbi.nlm.nih.gov/pubmed/25748434
http://dx.doi.org/10.1534/g3.115.017418
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