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Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast Saccharomyces cerevisiae

It is essential that cells orchestrate gene expression for the specific niche that they occupy, and this often requires coordination of the expression of large sets of genes. There are multiple regulatory systems that exist for modulation of gene expression, including the adjacent-gene coregulation...

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Autores principales: Eldabagh, Reem S., Mejia, Nelson G., Barrett, Rachel L., Monzo, Christopher R., So, Matthew K., Foley, Jonathan J., Arnone, James T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6001612/
https://www.ncbi.nlm.nih.gov/pubmed/29898982
http://dx.doi.org/10.1128/mSphere.00220-18
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author Eldabagh, Reem S.
Mejia, Nelson G.
Barrett, Rachel L.
Monzo, Christopher R.
So, Matthew K.
Foley, Jonathan J.
Arnone, James T.
author_facet Eldabagh, Reem S.
Mejia, Nelson G.
Barrett, Rachel L.
Monzo, Christopher R.
So, Matthew K.
Foley, Jonathan J.
Arnone, James T.
author_sort Eldabagh, Reem S.
collection PubMed
description It is essential that cells orchestrate gene expression for the specific niche that they occupy, and this often requires coordination of the expression of large sets of genes. There are multiple regulatory systems that exist for modulation of gene expression, including the adjacent-gene coregulation of the rRNA and ribosome biogenesis and ribosomal protein families. Both gene families exhibit a nonrandom genomic distribution, often clustered directly adjacent to another member of the same family, which results in a tighter transcriptional coordination among adjacent paired genes than that of the unpaired genes within each regulon and can result in a shared promoter that coordinates expression of the pairs. This nonrandom genomic distribution has been seen in a few functionally related gene families, and many of these functional pairings are conserved across divergent fungal lineages. To date, the significance of these observations has not been extended in a systematic way to characterize how prevalent the role of adjacent-gene coregulation is in transcriptional regulation. In the present study, we systematically analyzed the transcriptional coherence of the functional pairs compared to the singletons within all gene families defined by the Gene Ontology Slim designation, using Saccharomyces cerevisiae as a model system, finding that clusters exhibit a tighter transcriptional correlation under specific contexts. We found that the longer a functional pairing is conserved the tighter its response to broad stress and nutritional responses, that roughly 25% of gene families exhibit a nonrandom genomic distribution, and that many of these clusters are conserved. This suggests that adjacent-gene coregulation is a widespread, yet underappreciated, transcriptional mechanism. IMPORTANCE The spatial positioning of genes throughout the genome arrangement can alter their expression in many eukaryotic organisms. Often this results in a genomic context-specific effect on transcription. One example of this is through the clustering of functionally related genes, which results in adjacent-gene coregulation in the budding yeast Saccharomyces cerevisiae. In the present study, we set out to systematically characterize the prevalence of this phenomenon, finding the genomic organization of functionally related genes into clusters is a characteristic of myriad gene families. These arrangements are found in many evolutionarily divergent fungi and thus represent a widespread, yet underappreciated, layer of transcriptional regulation.
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spelling pubmed-60016122018-06-15 Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast Saccharomyces cerevisiae Eldabagh, Reem S. Mejia, Nelson G. Barrett, Rachel L. Monzo, Christopher R. So, Matthew K. Foley, Jonathan J. Arnone, James T. mSphere Research Article It is essential that cells orchestrate gene expression for the specific niche that they occupy, and this often requires coordination of the expression of large sets of genes. There are multiple regulatory systems that exist for modulation of gene expression, including the adjacent-gene coregulation of the rRNA and ribosome biogenesis and ribosomal protein families. Both gene families exhibit a nonrandom genomic distribution, often clustered directly adjacent to another member of the same family, which results in a tighter transcriptional coordination among adjacent paired genes than that of the unpaired genes within each regulon and can result in a shared promoter that coordinates expression of the pairs. This nonrandom genomic distribution has been seen in a few functionally related gene families, and many of these functional pairings are conserved across divergent fungal lineages. To date, the significance of these observations has not been extended in a systematic way to characterize how prevalent the role of adjacent-gene coregulation is in transcriptional regulation. In the present study, we systematically analyzed the transcriptional coherence of the functional pairs compared to the singletons within all gene families defined by the Gene Ontology Slim designation, using Saccharomyces cerevisiae as a model system, finding that clusters exhibit a tighter transcriptional correlation under specific contexts. We found that the longer a functional pairing is conserved the tighter its response to broad stress and nutritional responses, that roughly 25% of gene families exhibit a nonrandom genomic distribution, and that many of these clusters are conserved. This suggests that adjacent-gene coregulation is a widespread, yet underappreciated, transcriptional mechanism. IMPORTANCE The spatial positioning of genes throughout the genome arrangement can alter their expression in many eukaryotic organisms. Often this results in a genomic context-specific effect on transcription. One example of this is through the clustering of functionally related genes, which results in adjacent-gene coregulation in the budding yeast Saccharomyces cerevisiae. In the present study, we set out to systematically characterize the prevalence of this phenomenon, finding the genomic organization of functionally related genes into clusters is a characteristic of myriad gene families. These arrangements are found in many evolutionarily divergent fungi and thus represent a widespread, yet underappreciated, layer of transcriptional regulation. American Society for Microbiology 2018-06-13 /pmc/articles/PMC6001612/ /pubmed/29898982 http://dx.doi.org/10.1128/mSphere.00220-18 Text en Copyright © 2018 Eldabagh et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Eldabagh, Reem S.
Mejia, Nelson G.
Barrett, Rachel L.
Monzo, Christopher R.
So, Matthew K.
Foley, Jonathan J.
Arnone, James T.
Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast Saccharomyces cerevisiae
title Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast Saccharomyces cerevisiae
title_full Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast Saccharomyces cerevisiae
title_fullStr Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast Saccharomyces cerevisiae
title_full_unstemmed Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast Saccharomyces cerevisiae
title_short Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast Saccharomyces cerevisiae
title_sort systematic identification, characterization, and conservation of adjacent-gene coregulation in the budding yeast saccharomyces cerevisiae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6001612/
https://www.ncbi.nlm.nih.gov/pubmed/29898982
http://dx.doi.org/10.1128/mSphere.00220-18
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