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Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology

Prokaryotes utilize polycistronic messages (operons) to co-translate proteins involved in the same biological processes. Whether eukaryotes achieve similar regulation by selectively assembling and translating monocistronic messages derived from different chromosomes is unknown. We employed transcrip...

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Autores principales: Nair, Rohini R, Zabezhinsky, Dmitry, Gelin-Licht, Rita, Haas, Brian J, Dyhr, Michael CA, Sperber, Hannah S, Nusbaum, Chad, Gerst, Jeffrey E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8137142/
https://www.ncbi.nlm.nih.gov/pubmed/33942720
http://dx.doi.org/10.7554/eLife.66050
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author Nair, Rohini R
Zabezhinsky, Dmitry
Gelin-Licht, Rita
Haas, Brian J
Dyhr, Michael CA
Sperber, Hannah S
Nusbaum, Chad
Gerst, Jeffrey E
author_facet Nair, Rohini R
Zabezhinsky, Dmitry
Gelin-Licht, Rita
Haas, Brian J
Dyhr, Michael CA
Sperber, Hannah S
Nusbaum, Chad
Gerst, Jeffrey E
author_sort Nair, Rohini R
collection PubMed
description Prokaryotes utilize polycistronic messages (operons) to co-translate proteins involved in the same biological processes. Whether eukaryotes achieve similar regulation by selectively assembling and translating monocistronic messages derived from different chromosomes is unknown. We employed transcript-specific RNA pulldowns and RNA-seq/RT-PCR to identify yeast mRNAs that co-precipitate as ribonucleoprotein (RNP) complexes. Consistent with the hypothesis of eukaryotic RNA operons, mRNAs encoding components of the mating pathway, heat shock proteins, and mitochondrial outer membrane proteins multiplex in trans, forming discrete messenger ribonucleoprotein (mRNP) complexes (called transperons). Chromatin capture and allele tagging experiments reveal that genes encoding multiplexed mRNAs physically interact; thus, RNA assembly may result from co-regulated gene expression. Transperon assembly and function depends upon histone H4, and its depletion leads to defects in RNA multiplexing, decreased pheromone responsiveness and mating, and increased heat shock sensitivity. We propose that intergenic associations and non-canonical histone H4 functions contribute to transperon formation in eukaryotic cells and regulate cell physiology.
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spelling pubmed-81371422021-05-21 Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology Nair, Rohini R Zabezhinsky, Dmitry Gelin-Licht, Rita Haas, Brian J Dyhr, Michael CA Sperber, Hannah S Nusbaum, Chad Gerst, Jeffrey E eLife Cell Biology Prokaryotes utilize polycistronic messages (operons) to co-translate proteins involved in the same biological processes. Whether eukaryotes achieve similar regulation by selectively assembling and translating monocistronic messages derived from different chromosomes is unknown. We employed transcript-specific RNA pulldowns and RNA-seq/RT-PCR to identify yeast mRNAs that co-precipitate as ribonucleoprotein (RNP) complexes. Consistent with the hypothesis of eukaryotic RNA operons, mRNAs encoding components of the mating pathway, heat shock proteins, and mitochondrial outer membrane proteins multiplex in trans, forming discrete messenger ribonucleoprotein (mRNP) complexes (called transperons). Chromatin capture and allele tagging experiments reveal that genes encoding multiplexed mRNAs physically interact; thus, RNA assembly may result from co-regulated gene expression. Transperon assembly and function depends upon histone H4, and its depletion leads to defects in RNA multiplexing, decreased pheromone responsiveness and mating, and increased heat shock sensitivity. We propose that intergenic associations and non-canonical histone H4 functions contribute to transperon formation in eukaryotic cells and regulate cell physiology. eLife Sciences Publications, Ltd 2021-05-04 /pmc/articles/PMC8137142/ /pubmed/33942720 http://dx.doi.org/10.7554/eLife.66050 Text en © 2021, Nair et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Nair, Rohini R
Zabezhinsky, Dmitry
Gelin-Licht, Rita
Haas, Brian J
Dyhr, Michael CA
Sperber, Hannah S
Nusbaum, Chad
Gerst, Jeffrey E
Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
title Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
title_full Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
title_fullStr Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
title_full_unstemmed Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
title_short Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
title_sort multiplexed mrna assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8137142/
https://www.ncbi.nlm.nih.gov/pubmed/33942720
http://dx.doi.org/10.7554/eLife.66050
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