Cargando…

Recruitment of histone modifications to assist mRNA dosage maintenance after degeneration of cytosine DNA methylation during animal evolution

Following gene duplication, mRNA expression of the duplicated gene is reduced to maintain mRNA dosage. In mammals, this process is achieved with increased cytosine DNA methylation of the promoters of duplicated genes to suppress transcriptional initiation. However, not all animal species possess a f...

Descripción completa

Detalles Bibliográficos
Autores principales: Chang, Andrew Ying-Fei, Liao, Ben-Yang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5580711/
https://www.ncbi.nlm.nih.gov/pubmed/28720579
http://dx.doi.org/10.1101/gr.221739.117
_version_ 1783260947979173888
author Chang, Andrew Ying-Fei
Liao, Ben-Yang
author_facet Chang, Andrew Ying-Fei
Liao, Ben-Yang
author_sort Chang, Andrew Ying-Fei
collection PubMed
description Following gene duplication, mRNA expression of the duplicated gene is reduced to maintain mRNA dosage. In mammals, this process is achieved with increased cytosine DNA methylation of the promoters of duplicated genes to suppress transcriptional initiation. However, not all animal species possess a full apparatus for cytosine DNA methylation. For such species, such as the roundworm (Caenorhabditis elegans, “worm” hereafter) or fruit fly (Drosophila melanogaster, “fly” hereafter), it is unclear how reduced expression of duplicated genes has been achieved evolutionarily. Here, we hypothesize that in the absence of a classical cytosine DNA methylation pathway, histone modifications play an increasing role in maintaining mRNA dosage following gene duplication. We initially verified that reduced gene expression of duplicated genes had occurred in the worm, fly, and mouse (Mus musculus). Next, several histone marks, with the capacity to control mRNA abundance in the models studied, were examined. In the worm and fly, but not in the mouse, multiple histone modifications were found to assist mRNA dosage maintenance following gene duplication events and the possible involvement of adenine DNA methylation in this process was excluded. Furthermore, the histone marks and acting regions that mediated the reduction in duplicated gene expression were found to be largely organism specific. Thus, it appears that many of the histone marks that maintain mRNA dosage were independently recruited during the evolution of worms and flies to compensate for the loss of cytosine DNA methylation machinery from their genomes.
format Online
Article
Text
id pubmed-5580711
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Cold Spring Harbor Laboratory Press
record_format MEDLINE/PubMed
spelling pubmed-55807112018-03-01 Recruitment of histone modifications to assist mRNA dosage maintenance after degeneration of cytosine DNA methylation during animal evolution Chang, Andrew Ying-Fei Liao, Ben-Yang Genome Res Research Following gene duplication, mRNA expression of the duplicated gene is reduced to maintain mRNA dosage. In mammals, this process is achieved with increased cytosine DNA methylation of the promoters of duplicated genes to suppress transcriptional initiation. However, not all animal species possess a full apparatus for cytosine DNA methylation. For such species, such as the roundworm (Caenorhabditis elegans, “worm” hereafter) or fruit fly (Drosophila melanogaster, “fly” hereafter), it is unclear how reduced expression of duplicated genes has been achieved evolutionarily. Here, we hypothesize that in the absence of a classical cytosine DNA methylation pathway, histone modifications play an increasing role in maintaining mRNA dosage following gene duplication. We initially verified that reduced gene expression of duplicated genes had occurred in the worm, fly, and mouse (Mus musculus). Next, several histone marks, with the capacity to control mRNA abundance in the models studied, were examined. In the worm and fly, but not in the mouse, multiple histone modifications were found to assist mRNA dosage maintenance following gene duplication events and the possible involvement of adenine DNA methylation in this process was excluded. Furthermore, the histone marks and acting regions that mediated the reduction in duplicated gene expression were found to be largely organism specific. Thus, it appears that many of the histone marks that maintain mRNA dosage were independently recruited during the evolution of worms and flies to compensate for the loss of cytosine DNA methylation machinery from their genomes. Cold Spring Harbor Laboratory Press 2017-09 /pmc/articles/PMC5580711/ /pubmed/28720579 http://dx.doi.org/10.1101/gr.221739.117 Text en © 2017 Chang and Liao; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research
Chang, Andrew Ying-Fei
Liao, Ben-Yang
Recruitment of histone modifications to assist mRNA dosage maintenance after degeneration of cytosine DNA methylation during animal evolution
title Recruitment of histone modifications to assist mRNA dosage maintenance after degeneration of cytosine DNA methylation during animal evolution
title_full Recruitment of histone modifications to assist mRNA dosage maintenance after degeneration of cytosine DNA methylation during animal evolution
title_fullStr Recruitment of histone modifications to assist mRNA dosage maintenance after degeneration of cytosine DNA methylation during animal evolution
title_full_unstemmed Recruitment of histone modifications to assist mRNA dosage maintenance after degeneration of cytosine DNA methylation during animal evolution
title_short Recruitment of histone modifications to assist mRNA dosage maintenance after degeneration of cytosine DNA methylation during animal evolution
title_sort recruitment of histone modifications to assist mrna dosage maintenance after degeneration of cytosine dna methylation during animal evolution
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5580711/
https://www.ncbi.nlm.nih.gov/pubmed/28720579
http://dx.doi.org/10.1101/gr.221739.117
work_keys_str_mv AT changandrewyingfei recruitmentofhistonemodificationstoassistmrnadosagemaintenanceafterdegenerationofcytosinednamethylationduringanimalevolution
AT liaobenyang recruitmentofhistonemodificationstoassistmrnadosagemaintenanceafterdegenerationofcytosinednamethylationduringanimalevolution