Developmental Morphokinetics and the Transcriptomic Profile of Bovine First-Cleaved Embryos: Normal vs. Abnormal Divisions

While early embryonic loss affects the conception rate in lactating cows, the underlying mechanisms remain unknown. Here, we examined whether the developmental morphokinetics and transcriptomic profiles of cleaved embryos are associated with developmental competence. Developing bovine embryos were produced in vitro, and their morphokinetics were monitored through 190 h using a time-lapse system. The proportion of embryos that developed to the blastocyst stage was lower following abnormal cleavage, i.e., reverse, direct, or unequal, relative to normally cleaved embryos (p < 0.05). In a second set of experiments, exploratory RNA-seq analysis was performed on first-cleaved embryos, which were individually collected immediately after the first division; embryos were defined by the time-lapse system as normally, directly, or unequally cleaved (n = 6 per group), or reverse-cleaved (n = 5). Analysis revealed 672 genes that were differentially expressed between normally and abnormally cleaved embryos (adjusted p < 0.05). Abnormally cleaved embryos differed in pathways associated with energy production and metabolism. The most profound difference in gene expression (n = 632) was between unequally and normally cleaved embryos, mainly in genes affiliated with the oxidative phosphorylation pathway. These findings support the concept that the morphokinetic pattern of early embryonic cleavage is associated with developmental competence. We therefore suggest that the observed differential expression profiles in abnormally cleaved embryos might be involved in the mechanism underlying early embryonic loss.