Preimplantation embryo gene expression: 56 years of discovery, and counting

The biology of preimplantation embryo gene expression began 56 years ago with studies of the effects of protein synthesis inhibition and discovery of changes in embryo metabolism and related enzyme activities. The field accelerated rapidly with the emergence of embryo culture systems and progressively evolving methodologies that have allowed early questions to be re-addressed in new ways and in greater detail, leading to deeper understanding and progressively more targeted studies to discover ever more fine details. The advent of technologies for assisted reproduction, preimplantation genetic testing, stem cell manipulations, artificial gametes, and genetic manipulation, particularly in experimental animal models and livestock species, has further elevated the desire to understand preimplantation development in greater detail. The questions that drove enquiry from the earliest years of the field remain drivers of enquiry today. Our understanding of the crucial roles of oocyte-expressed RNA and proteins in early embryos, temporal patterns of embryonic gene expression, and mechanisms controlling embryonic gene expression has increased exponentially over the past five and a half decades as new analytical methods emerged. This review combines early and recent discoveries on gene regulation and expression in mature oocytes and preimplantation stage embryos to provide a comprehensive understanding of preimplantation embryo biology and to anticipate exciting future advances that will build upon and extend what has been discovered so far.