How the environment affects early embryonic development

Abstract

In the field of animal reproduction, the environment associated with gametes and embryos refers to the parents’ condition as well as conditions surrounding gametes and embryos in vivo or in vitro. This environment is now known to influence not only the functionality of the early embryo but potentially the future phenotype of the offspring. Using transcriptomic and epigenetic molecular analysis, and the bovine model, recent research has shown that both the female and the male metabolic status, for example age, can affect gene expression and gene programming in the embryo. Evidence demonstrates that milking cows, which are losing weight at the time of conception, generates compromised embryos and offspring with a unique metabolic signature. A similar phenomenon has been associated with different culture conditions and the IVF procedure. The general common consequence of these situations is an embryo behaving on ‘economy’ mode where translation, cell division and ATP production is reduced, potentially to adapt to the perceived future environment. Few epidemiological studies have been done in bovines to assess if these changes result in a different phenotype and more studies are required to associate specific molecular changes in embryos with visible consequences later in life.

Sperm DNA methylation patterns at discrete CpGs and genes involved in embryonic development are related to bull fertility

“…A mutual feature of all these genes is that their role is most likely during early embryonic development. Although the paternal methylome is substantially reprogrammed after fertilisation, specific CpGs preserve their methylation pattern from sperm to the blastocyst [ 101 , 102 ]. Hence, it is reasonable to hypothesise that the altered methylation we observed in sperm of subfertile bulls leads to differences in the expression of these genes, with potential impacts on early development.…”

Cold exposure impacts DNA methylation patterns in cattle sperm

“…The epigenetic changes induced by direct exposure to environmental factors in germ cells of F1 generation induced epigenetic alteration during the germ cell development of embryos, inducing transgenerational effects ( Beck et al, 2017 ). Besides the ICRs of imprinted genes, a large number of specific regions in sperm maintain their methylation patterns during the post-fertilization genome-wide epigenetic reprogramming and transfer germ cell-specific epimutation to offspring ( Keyhan et al, 2021 ; Sirard, 2022 ). In rodents, paternal physiological and metabolic adaptation to environmental factors are linked to the metabolic disorders in offspring ( Rosenwald et al, 2013 ; Ng et al, 2014 ).…”

The interaction between the environment and embryo development in assisted reproduction

“…However, combining all these achievements and findings appears to be very complex, extremely costly and hitherto impossible and confirms the uniqueness of the Fallopian tube in early embryo development ( Leese et al, 2001 ). Reproductive techniques, especially the in vitro production of bovine embryos, are still far from optimal at this sensitive stage of development ( Sirard, 2017 , 2021 ) and should be further refined to be more efficient and sustainable for use in animal breeding ( Ealy et al, 2019 ). In the following, some in vivo approaches are presented in order to meet demands that directly show the influence of environmental changes on the embryonic stages that are used in assisted reproductive technology ( González-Brusi et al, 2020 ).…”

“…In addition to the different expression signatures in response to environmental effects, these changes in embryos can also be identified using DNA methylation patterns [see Sirard (2021) ]. In order to also show epigenetic effects on in vitro/in vivo culture, the DNA methylation pattern of bovine embryos obtained ex vivo was determined in an experimental design before, during and after major embryonic genome activation (EGA).…”