Growing an Embryo from a Single Cell: A Hurdle in Animal Life

Abstract

A requirement that an animal be able to feed to grow constrains how a cell can grow into an animal, and it forces an alternation between growth (increase in mass) and proliferation (increase in cell number). A growth-only phase that transforms a stem cell of ordinary proportions into a huge cell, the oocyte, requires dramatic adaptations to help a nucleus direct a 10(5)-fold expansion of cytoplasmic volume. Proliferation without growth transforms the huge egg into an embryo while still accommodating an impotent nucleus overwhelmed by the voluminous cytoplasm. This growth program characterizes animals that deposit their eggs externally, but it is changed in mammals and in endoparasites. In these organisms, development in a nutritive environment releases the growth constraint, but growth of cells before gastrulation requires a new program to sustain pluripotency during this growth.

Figure 1.

Insertion of a new module of development distinguishes early mammalian embryogenesis from that of its predecessors. Most animals deposit very large eggs in the external environment where they develop into a feeding organism without nutrition or growth. Cleavage cell cycles divide the egg into blastomeres that immediately initiate pattern formation and differentiation to produce an embryo, called phylotypic, because all of the species of a phylum look similar at this stage. Even the embryos of other phyla are similar in shape and size at this stage. Mammalian embryogenesis, as exemplified by the mouse, begins with a much smaller egg (magnified somewhat here) and a distinctly different early program of development. The cells resulting from the initial divisions do not gastrulate. First, extra embryonic tissues are produced as the embryo grows enormously and rapidly. Only then does it gastrulate and establish strong parallels to the ancestral program of embryogenesis. The mammalian module of development (boxed) is inserted early during development (*) so that the earliest divisions are dramatically changed and many of the attributes of the early events of the ancestral program are deferred along with gastrulation.