Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>

ABSTRACT 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 core...

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Autores principales:	Reem S. Eldabagh, Nelson G. Mejia, Rachel L. Barrett, Christopher R. Monzo, Matthew K. So, Jonathan J. Foley, James T. Arnone
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	adjacent-gene coregulation gene expression Saccharomyces cerevisiae spatial positioning Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8b96433179d74dabb430f35bcefc54f2
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spelling	oai:doaj.org-article:8b96433179d74dabb430f35bcefc54f22021-11-15T15:24:23ZSystematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>10.1128/mSphere.00220-182379-5042https://doaj.org/article/8b96433179d74dabb430f35bcefc54f22018-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00220-18https://doaj.org/toc/2379-5042ABSTRACT 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.Reem S. EldabaghNelson G. MejiaRachel L. BarrettChristopher R. MonzoMatthew K. SoJonathan J. FoleyJames T. ArnoneAmerican Society for Microbiologyarticleadjacent-gene coregulationgene expressionSaccharomyces cerevisiaespatial positioningMicrobiologyQR1-502ENmSphere, Vol 3, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	adjacent-gene coregulation gene expression Saccharomyces cerevisiae spatial positioning Microbiology QR1-502
spellingShingle	adjacent-gene coregulation gene expression Saccharomyces cerevisiae spatial positioning Microbiology QR1-502 Reem S. Eldabagh Nelson G. Mejia Rachel L. Barrett Christopher R. Monzo Matthew K. So Jonathan J. Foley James T. Arnone Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
description	ABSTRACT 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.
format	article
author	Reem S. Eldabagh Nelson G. Mejia Rachel L. Barrett Christopher R. Monzo Matthew K. So Jonathan J. Foley James T. Arnone
author_facet	Reem S. Eldabagh Nelson G. Mejia Rachel L. Barrett Christopher R. Monzo Matthew K. So Jonathan J. Foley James T. Arnone
author_sort	Reem S. Eldabagh
title	Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
title_short	Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
title_full	Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
title_fullStr	Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
title_full_unstemmed	Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>
title_sort	systematic identification, characterization, and conservation of adjacent-gene coregulation in the budding yeast <named-content content-type="genus-species">saccharomyces cerevisiae</named-content>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/8b96433179d74dabb430f35bcefc54f2
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Systematic Identification, Characterization, and Conservation of Adjacent-Gene Coregulation in the Budding Yeast <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content>

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