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Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia

BACKGROUND: The symbiotic relationship between cnidarians and dinoflagellates is one of the most widespread endosymbiosis in our oceans and provides the ecological basis of coral reef ecosystems. Although many studies have been undertaken to unravel the molecular mechanisms underlying these symbiose...

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Autores principales: Nawaz, Kashif, Cziesielski, Maha J., Mariappan, Kiruthiga G., Cui, Guoxin, Aranda, Manuel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9717517/
https://www.ncbi.nlm.nih.gov/pubmed/36456984
http://dx.doi.org/10.1186/s12915-022-01469-y
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author Nawaz, Kashif
Cziesielski, Maha J.
Mariappan, Kiruthiga G.
Cui, Guoxin
Aranda, Manuel
author_facet Nawaz, Kashif
Cziesielski, Maha J.
Mariappan, Kiruthiga G.
Cui, Guoxin
Aranda, Manuel
author_sort Nawaz, Kashif
collection PubMed
description BACKGROUND: The symbiotic relationship between cnidarians and dinoflagellates is one of the most widespread endosymbiosis in our oceans and provides the ecological basis of coral reef ecosystems. Although many studies have been undertaken to unravel the molecular mechanisms underlying these symbioses, we still know little about the epigenetic mechanisms that control the transcriptional responses to symbiosis. RESULTS: Here, we used the model organism Exaiptasia diaphana to study the genome-wide patterns and putative functions of the histone modifications H3K27ac, H3K4me3, H3K9ac, H3K36me3, and H3K27me3 in symbiosis. While we find that their functions are generally conserved, we observed that colocalization of more than one modification and or DNA methylation correlated with significantly higher gene expression, suggesting a cooperative action of histone modifications and DNA methylation in promoting gene expression. Analysis of symbiosis genes revealed that activating histone modifications predominantly associated with symbiosis-induced genes involved in glucose metabolism, nitrogen transport, amino acid biosynthesis, and organism growth while symbiosis-suppressed genes were involved in catabolic processes. CONCLUSIONS: Our results provide new insights into the mechanisms of prominent histone modifications and their interaction with DNA methylation in regulating symbiosis in cnidarians. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01469-y.
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spelling pubmed-97175172022-12-03 Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia Nawaz, Kashif Cziesielski, Maha J. Mariappan, Kiruthiga G. Cui, Guoxin Aranda, Manuel BMC Biol Research Article BACKGROUND: The symbiotic relationship between cnidarians and dinoflagellates is one of the most widespread endosymbiosis in our oceans and provides the ecological basis of coral reef ecosystems. Although many studies have been undertaken to unravel the molecular mechanisms underlying these symbioses, we still know little about the epigenetic mechanisms that control the transcriptional responses to symbiosis. RESULTS: Here, we used the model organism Exaiptasia diaphana to study the genome-wide patterns and putative functions of the histone modifications H3K27ac, H3K4me3, H3K9ac, H3K36me3, and H3K27me3 in symbiosis. While we find that their functions are generally conserved, we observed that colocalization of more than one modification and or DNA methylation correlated with significantly higher gene expression, suggesting a cooperative action of histone modifications and DNA methylation in promoting gene expression. Analysis of symbiosis genes revealed that activating histone modifications predominantly associated with symbiosis-induced genes involved in glucose metabolism, nitrogen transport, amino acid biosynthesis, and organism growth while symbiosis-suppressed genes were involved in catabolic processes. CONCLUSIONS: Our results provide new insights into the mechanisms of prominent histone modifications and their interaction with DNA methylation in regulating symbiosis in cnidarians. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01469-y. BioMed Central 2022-12-02 /pmc/articles/PMC9717517/ /pubmed/36456984 http://dx.doi.org/10.1186/s12915-022-01469-y Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Nawaz, Kashif
Cziesielski, Maha J.
Mariappan, Kiruthiga G.
Cui, Guoxin
Aranda, Manuel
Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title_full Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title_fullStr Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title_full_unstemmed Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title_short Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title_sort histone modifications and dna methylation act cooperatively in regulating symbiosis genes in the sea anemone aiptasia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9717517/
https://www.ncbi.nlm.nih.gov/pubmed/36456984
http://dx.doi.org/10.1186/s12915-022-01469-y
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