Comparative analysis reveals epigenomic evolution related to species traits and genomic imprinting in mammals

DNA methylation is an epigenetic modification that plays a crucial role in various regulatory processes, including gene expression regulation, transposable element repression, and genomic imprinting. However, most studies on DNA methylation have been conducted in humans and other model species, wher...

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Main Authors: Yisi Hu, Shenli Yuan, Xin Du, Jiang Liu, Wenliang Zhou, Fuwen Wei
Format: Article
Language:English
Published: Elsevier 2023-05-01
Series:The Innovation
Online Access:http://www.sciencedirect.com/science/article/pii/S2666675823000620
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author Yisi Hu
Shenli Yuan
Xin Du
Jiang Liu
Wenliang Zhou
Fuwen Wei
author_facet Yisi Hu
Shenli Yuan
Xin Du
Jiang Liu
Wenliang Zhou
Fuwen Wei
author_sort Yisi Hu
collection DOAJ
description DNA methylation is an epigenetic modification that plays a crucial role in various regulatory processes, including gene expression regulation, transposable element repression, and genomic imprinting. However, most studies on DNA methylation have been conducted in humans and other model species, whereas the dynamics of DNA methylation across mammals remain poorly explored, limiting our understanding of epigenomic evolution in mammals and the evolutionary impacts of conserved and lineage-specific DNA methylation. Here, we generated and gathered comparative epigenomic data from 13 mammalian species, including two marsupial species, to demonstrate that DNA methylation plays critical roles in several aspects of gene evolution and species trait evolution. We found that the species-specific DNA methylation of promoters and noncoding elements correlates with species-specific traits such as body patterning, indicating that DNA methylation might help establish or maintain interspecies differences in gene regulation that shape phenotypes. For a broader view, we investigated the evolutionary histories of 88 known imprinting control regions across mammals to identify their evolutionary origins. By analyzing the features of known and newly identified potential imprints in all studied mammals, we found that genomic imprinting may function in embryonic development through the binding of specific transcription factors. Our findings show that DNA methylation and the complex interaction between the genome and epigenome have a significant impact on mammalian evolution, suggesting that evolutionary epigenomics should be incorporated to develop a unified evolutionary theory.
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spelling doaj.art-8ada259988474bc6b4ea2842522a30702023-05-11T04:24:47ZengElsevierThe Innovation2666-67582023-05-0143100434Comparative analysis reveals epigenomic evolution related to species traits and genomic imprinting in mammalsYisi Hu0Shenli Yuan1Xin Du2Jiang Liu3Wenliang Zhou4Fuwen Wei5CAS Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China; Center for Evolution and Conservation Biology, Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, ChinaCAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, ChinaCAS Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaCAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, ChinaCenter for Evolution and Conservation Biology, Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, ChinaCAS Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China; Center for Evolution and Conservation Biology, Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China; Corresponding authorDNA methylation is an epigenetic modification that plays a crucial role in various regulatory processes, including gene expression regulation, transposable element repression, and genomic imprinting. However, most studies on DNA methylation have been conducted in humans and other model species, whereas the dynamics of DNA methylation across mammals remain poorly explored, limiting our understanding of epigenomic evolution in mammals and the evolutionary impacts of conserved and lineage-specific DNA methylation. Here, we generated and gathered comparative epigenomic data from 13 mammalian species, including two marsupial species, to demonstrate that DNA methylation plays critical roles in several aspects of gene evolution and species trait evolution. We found that the species-specific DNA methylation of promoters and noncoding elements correlates with species-specific traits such as body patterning, indicating that DNA methylation might help establish or maintain interspecies differences in gene regulation that shape phenotypes. For a broader view, we investigated the evolutionary histories of 88 known imprinting control regions across mammals to identify their evolutionary origins. By analyzing the features of known and newly identified potential imprints in all studied mammals, we found that genomic imprinting may function in embryonic development through the binding of specific transcription factors. Our findings show that DNA methylation and the complex interaction between the genome and epigenome have a significant impact on mammalian evolution, suggesting that evolutionary epigenomics should be incorporated to develop a unified evolutionary theory.http://www.sciencedirect.com/science/article/pii/S2666675823000620
spellingShingle Yisi Hu
Shenli Yuan
Xin Du
Jiang Liu
Wenliang Zhou
Fuwen Wei
Comparative analysis reveals epigenomic evolution related to species traits and genomic imprinting in mammals
The Innovation
title Comparative analysis reveals epigenomic evolution related to species traits and genomic imprinting in mammals
title_full Comparative analysis reveals epigenomic evolution related to species traits and genomic imprinting in mammals
title_fullStr Comparative analysis reveals epigenomic evolution related to species traits and genomic imprinting in mammals
title_full_unstemmed Comparative analysis reveals epigenomic evolution related to species traits and genomic imprinting in mammals
title_short Comparative analysis reveals epigenomic evolution related to species traits and genomic imprinting in mammals
title_sort comparative analysis reveals epigenomic evolution related to species traits and genomic imprinting in mammals
url http://www.sciencedirect.com/science/article/pii/S2666675823000620
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