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

Hu, Yisi; Yuan, Shenli; Du, Xin; Liu, Jiang; Zhou, Wen‐Liang; Wei, Fuwen

doi:10.1016/j.xinn.2023.100434

Cited by 4 publications

(4 citation statements)

References 93 publications

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“…Moreover, a fine-tuned pattern of imprinting has been shown for paternally-expressed NAP1L5, with an expression distribution in pig tissues differing from those in mice and cattle ( Jiang et al, 2011 ). Genome-wide comparative analyses suggest that changes in methylation are a potentially important source for shaping lineage- and species-specific innovations, as exemplified with imprinting ( Hu et al, 2023 ). Livestock mammals such as cattle and pigs display epigenomic-specific features that make them particularly attractive to investigate the contribution of imprinting and epigenomic evolution to phenotypic variation ( Lu et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Livestock species as emerging models for genomic imprinting

Hubert,

Perret,

Riquet

et al. 2024

Front. Cell Dev. Biol.

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Genomic imprinting is an epigenetically-regulated process of central importance in mammalian development and evolution. It involves multiple levels of regulation, with spatio-temporal heterogeneity, leading to the context-dependent and parent-of-origin specific expression of a small fraction of the genome. Genomic imprinting studies have therefore been essential to increase basic knowledge in functional genomics, evolution biology and developmental biology, as well as with regard to potential clinical and agrigenomic perspectives. Here we offer an overview on the contribution of livestock research, which features attractive resources in several respects, for better understanding genomic imprinting and its functional impacts. Given the related broad implications and complexity, we promote the use of such resources for studying genomic imprinting in a holistic and integrative view. We hope this mini-review will draw attention to the relevance of livestock genomic imprinting studies and stimulate research in this area.

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Section: Discussionmentioning

confidence: 99%

Livestock species as emerging models for genomic imprinting

Hubert,

Perret,

Riquet

et al. 2024

Front. Cell Dev. Biol.

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“…Geyer et al (2016) found that exposure to the demethylating agent 5-aza-C significantly inhibited egg production and embryo development in the planorbid snail, Biomphalaria glabrata [38]. In a study with sexually mature specimens of Cornu aspersum, Drăghici et al (2023) reported significant hypermethylation of the ovotestis compared to the hepatopancreas [79], possibly reflecting the more stringent regulation of genes crucial for reproductive processes in the former organ [83,85]. The foregoing authors also identified significantly elevated transcript levels for several key genes of the DNA methylation machinery in the gonadal structures of B. glabrata compared to somatic tissues, such as the head/foot, central nervous system, buccal mass, salivary glands, hepatopancreas, stomach, heart, kidneys, and mantle edge.…”

Section: Dna Methylation Is An Important Player In Reproduction Growt...mentioning

confidence: 99%

DNA Methylation Machinery in Gastropod Mollusks

Haidar,

Georgescu,

Drăghici

et al. 2024

Life

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The role of DNA methylation in mollusks is just beginning to be understood. This review synthesizes current knowledge on this potent molecular hallmark of epigenetic control in gastropods—the largest class of mollusks and ubiquitous inhabitants of diverse habitats. Their DNA methylation machinery shows a high degree of conservation in CG maintenance methylation mechanisms, driven mainly by DNMT1 homologues, and the presence of MBD2 and MBD2/3 proteins as DNA methylation readers. The mosaic-like DNA methylation landscape occurs mainly in a CG context and is primarily confined to gene bodies and housekeeping genes. DNA methylation emerges as a critical regulator of reproduction, development, and adaptation, with tissue-specific patterns being observed in gonadal structures. Its dynamics also serve as an important regulatory mechanism underlying learning and memory processes. DNA methylation can be affected by various environmental stimuli, including as pathogens and abiotic stresses, potentially impacting phenotypic variation and population diversity. Overall, the features of DNA methylation in gastropods are complex, being an essential part of their epigenome. However, comprehensive studies integrating developmental stages, tissues, and environmental conditions, functional annotation of methylated regions, and integrated genomic-epigenomic analyses are lacking. Addressing these knowledge gaps will advance our understanding of gastropod biology, ecology, and evolution.

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“…DNA methylation is a stable epigenomic mark that plays an important role in gene regulation (e.g. genomic imprinting and silencing), embryonic development, and evolution ( Jones 2012 ; Li et al 2018 ; Lu et al 2021 ; Hu et al 2023 ). Cross-species comparisons of DNA methylome have revealed the evolutionary features of methylation and contributed to the understanding of the genetic basis of complex traits and diseases in humans ( Fukuda et al 2017 ; Blake et al 2020 ).…”

Section: Introductionmentioning

confidence: 99%

“…These DNA HypoMRs are involved in embryonic development and species-specific phenotypes, such as cognitive behavior in humans ( Mendizabal et al 2016 ). Furthermore, a previous study in 13 mammalian species reported that genes with hypomethylated promoters were mainly involved in developmental processes, whereas genes with hypermethylated promoters were predominantly enriched in immune system processes ( Hu et al 2023 ). Although comparative methylome analysis has been widely performed in primates, especially in humans, it has not been extensively studied in ruminant livestock species.…”

Section: Introductionmentioning

confidence: 99%

Cross-Species Comparative DNA Methylation Reveals Novel Insights into Complex Trait Genetics among Cattle, Sheep, and Goats

Chen,

Liu,

Shi

et al. 2024

Molecular Biology and Evolution

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The cross-species characterization of evolutionary changes in the functional genome can facilitate the translation of genetic findings across species and the interpretation of the evolutionary basis underlying complex phenotypes. Yet, this has not been fully explored between cattle, sheep, goats, and other mammals. Here, we systematically characterized the evolutionary dynamics of DNA methylation and gene expression in three somatic tissues (i.e., brain, liver, and skeletal muscle) and sperm across seven mammalian species, including three ruminant livestock species (cattle, sheep, and goats), humans, pigs, mice, and dogs, by generating and integrating 160 DNA methylation and transcriptomic datasets. We demonstrate dynamic changes of DNA hypomethylated regions (HypoMRs) and hypermethylated regions (HyperMRs) in tissue-type manner across cattle, sheep, and goats. Specifically, based on the phylo-epigenetic model of DNA methylome, we identified a total of 25,074 HypoMR extension events specific to cattle, which participated in rewiring tissue-specific regulatory network. Furthermore, by integrating genome-wide association studies (GWAS) of 50 cattle traits, we provided novel insights into the genetic and evolutionary basis of complex phenotypes in cattle. Overall, our study provides a valuable resource for exploring the evolutionary dynamics of the functional genome and highlights the importance of cross-species characterization of multi-omics datasets for the evolutionary interpretation of complex phenotypes in cattle livestock.

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

Cited by 4 publications

References 93 publications

Livestock species as emerging models for genomic imprinting

Livestock species as emerging models for genomic imprinting

DNA Methylation Machinery in Gastropod Mollusks

Cross-Species Comparative DNA Methylation Reveals Novel Insights into Complex Trait Genetics among Cattle, Sheep, and Goats

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