Evolutionary epigenomic analyses in mammalian early embryos reveal species-specific innovations and conserved principles of imprinting

Lu, Xukun; Wang, Lijuan; Wang, Leyun; Wang, Huili; Xu, Qianhua; Xiang, Yunlong; Chen, Chaolei; Kong, Feng; Xia, Weikun; Lin, Zili; Ma, Sinan; Liu, Ling; Wang, Xiangguo; Ni, Hemin; Li, Wei; Guo, Yong; Xie, Wei

doi:10.1126/sciadv.abi6178

Cited by 43 publications

(80 citation statements)

References 83 publications

(201 reference statements)

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“…Conversely, H3K36me3 domains are more widespread in the mouse, likely reflecting a greater prevalence of non-genic transcripts in the mouse (39). Analysis of recently published H3K27me3 CUT&RUN data from rat oocytes (60) reveals a strong correlation with our data (Spearman rank correlation 0.95, Sup. fig.…”

Section: Resultssupporting

confidence: 85%

Conservation and divergence of canonical and non-canonical imprinting in murids

Albert

Kobayashi

Inoue

et al. 2022

Preprint

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BackgroundGenomic imprinting affects gene expression in a parent-of-origin manner and has a profound impact on complex traits including growth and behaviour. While the rat is widely used to model human pathophysiology, few imprinted genes have been identified in this murid. To systematically identify imprinted genes and genomic imprints in the rat, we used low input methods for genome-wide analyses of gene expression and DNA methylation to profile embryonic and extra-embryonic tissues at allele-specific resolution.ResultsWe identify 14 and 26 imprinted genes in these tissues, respectively, with 10 of these genes imprinted in both tissues. Comparative analyses with mouse revealed that orthologous imprinted gene expression and associated canonical DNA methylation imprints are conserved in the embryo proper of the Muridae family. However, only 3 paternally expressed imprinted genes are conserved in the extra-embryonic tissue of murids, all of which are associated with non-canonical H3K27me3 imprints. The discovery of 8 novel non-canonical imprinted genes unique to the rat is consistent with more rapid evolution of extra-embryonic imprinting. Meta-analysis of novel imprinted genes revealed multiple mechanisms by which species-specific imprinted expression may be established, including H3K27me3 deposition in the oocyte, the birth of ZFP57 binding motifs and the insertion of endogenous retroviral promoters.ConclusionsIn summary, we provide a comprehensive list of imprinted loci in the rat, reveal the extent of conservation of imprinted gene expression, and identify potential mechanisms responsible for the evolution of species-specific imprinting.

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Section: Resultssupporting

confidence: 85%

Conservation and divergence of canonical and non-canonical imprinting in murids

Albert

Kobayashi

Inoue

et al. 2022

Preprint

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“…Comprehensive genome scans for imprinted genes in species with little or no previous evidence for GI bring important information, since it promotes the understanding of both GI evolution and related phenomena such as methylation reprogramming and allele-specific expression, which regulate key biological processes in vertebrates ( Frésard et al, 2014 ; Zhuo et al, 2017 ; Skvortsova et al, 2019 ). A recent epigenome comparison across five placental mammals notably showed striking species-specific features, with distinct GI mechanisms between humans, nonrodents and rodents ( Lu et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Genomic Imprinting in the New Omics Era: A Model for Systems-Level Approaches

Hubert

Demars

2022

Front. Genet.

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Genomic imprinting represents a noteworthy inheritance mechanism leading to allele-specific regulations dependent of the parental origin. Imprinted loci are especially involved in essential mammalian functions related to growth, development and behavior. In this mini-review, we first offer a summary of current representations associated with genomic imprinting through key results of the three last decades. We then outline new perspectives allowed by the spread of new omics technologies tackling various interacting levels of imprinting regulations, including genomics, transcriptomics and epigenomics. We finally discuss the expected contribution of new omics data to unresolved big questions in the field.

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“…A characterization of the molecular events accompanying the maturation of the oocyte, fertilization and the early cleavage stages of embryonic development may provide some insight into what can potentially go wrong in those pregnancies that fail in these early stages. Omics technologies have enabled in-depth analysis of molecular mechanisms of bovine preimplantation development including a catalog of the transcripts present (17,18,(38)(39)(40) and the state of the epigenome (DNA methylation status (41,42), chromatin dynamics (43,44), histone modifications (45), and the range of small RNAs (46,47)). However, the mRNA translation landscape and particularly the translational controls operating on specific mRNAs in oocytes and embryos remain largely unstudied.…”

Section: Discussionmentioning

confidence: 99%

High-resolution Ribosome Profiling Reveals Translational Selectivity for Transcripts in Bovine Preimplantation Embryo Development

Jiang¹,

Zhu²,

Tong

et al. 2022

Preprint

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High resolution ribosome fractionation and low-input ribosome profiling of bovine oocytes and preimplantation embryos has enabled us to define the translational landscapes of early embryo development at an unprecedented level. We analyzed the transcriptome, polysome- and non-polysome-bound RNA profiles of bovine oocytes (GV and MII stage) and early embryos at 2-, 8-cell, morula, and blastocyst stage, and revealed four modes of translational selectivity: i. selective translation of non-abundant mRNAs, ii. active, but modest translation of a selection of highly expressed mRNAs, iii. translationally suppressed abundant to moderately abundant mRNAs, and iv. mRNAs associated specifically with monosomes. A strong translational selection of low abundance mRNAs encoding protein components involved in metabolic pathways and lysosome was found throughout bovine oocyte and preimplantation development. In particular, genes encoding components involved in mitochondrial function were prioritized for translation. Notably, transcripts encoding proteins regulating chromatin modifications selectively translated in oocytes. We found that the translational dynamics largely reflects transcriptional profiles in oocytes and 2-cell embryos, but observed marked shift in translational control in 8-cell embryos associated with the main phase of embryonic genome activation. Subsequently, transcription and translation become better synchronized in morulae and blastocysts. Together, these data reveal a unique spatiotemporal translational regulation that accompanies bovine preimplantation development.

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Evolutionary epigenomic analyses in mammalian early embryos reveal species-specific innovations and conserved principles of imprinting

Abstract: Evolutionary analyses reveal conservation and divergence of epigenetic transition during early development across mammals.

Cited by 43 publications

References 83 publications

Conservation and divergence of canonical and non-canonical imprinting in murids

Conservation and divergence of canonical and non-canonical imprinting in murids

Genomic Imprinting in the New Omics Era: A Model for Systems-Level Approaches

High-resolution Ribosome Profiling Reveals Translational Selectivity for Transcripts in Bovine Preimplantation Embryo Development

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