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Genomic Control Process Copyright © 2015 Eric H Chapter 3 Genomic Strategies for Embryonic Development 1. Common Principles of Embryonic Development 80 1.1 Specification in embryogenesis 80 1.2 Properties of the egg 80 1.3 Regulatory anisotropy in eggs/very early cleavage embryos and the initiation of spatial specification 83 1.4 Signaling, and its causal developmental consequences 87 1.5 Differentiation 90 1.6 Morphogenetic functions 91 2. Phylogenetic Framework 93 2.1 Bilaterian phylogeny 93 2.2 Three modes of pregastrular regulatory development 96 2.3 Phylogenetic distribution of modes of embryonic specification 97 3. Genomic Strategies of Control in Mode 1 Embryonic Processes 98 3.1 Mode 1 strategies in the sea urchin embryo GRNs 98 3.2 The sea urchin embryo GRNs and the code for territorial embryonic fate 102 3.3 Endomesoderm specification in the C. elegans embryo 110 4. Genomic Strategies of Control in Mode 2 Embryonic Processes 115 4.1 Global temporal control of transcription in Xenopus and zebrafish embryos 115 4.2 Cis-regulatory signal integration at a key control gene of the Spemann organizer 117 4.3 A brief note on early mammalian embryogenesis 119 5. Global Aspects of A/P Spatial Regulatory Patterning in the Syncytial Drosophila Blastoderm 120 The embryos of Bilateria display astoundingly diverse morphologies. They differ not only in appearance but in apparent developmental strategies, so different that for a century, and even in recent texts, it con- ventionally went without saying that the developmental process had to be presented separately for each species considered. Yet, since it is clear that the Bilateria descend from a common ancestor, we know intuitively that there has to be something fundamentally wrong with this picture. Should we not just focus on the basic developmental mechanisms that all bilaterian embryos utilize? But, on the other hand, it is inescapable that some real and significant differences exist among modes of embryogenesis: to take an extreme case, it is by now (at last) generally realized that the particular mechanisms of spatial specification Genomic Control Process Copyright © 2015 Eric H. Davidson and Isabelle S. Peter. http://dx.doi.org/10.1016/B978-0-12-404729-7.00003-4 Published by Elsevier Inc. All rights reserved. 80 Genomic Control Process in the syncytial Drosophila embryo cannot be taken as a model for how spatially defined gene expression is determined in sea urchin or mouse or frog embryos. To achieve a global view of the control systems for bilaterian embryogenesis we must begin by recognizing what are the fundamental, universally shared ele- ments of mechanism for development that were inherited from the common bilaterian ancestor, and that can be observed in all branches of its modern descendants. But we also need to understand those differ- ences in control mechanism among embryonic processes that are real and profound, rather than superficial and illusory. Thus we may enjoy a rich comparison of the genomic regulatory programs that account for the special features of the various ways in which animals develop, and that show us what is essential and general, while also illuminating mechanisms underlying the endless variety of bilaterian life. 1. Common Principles of Embryonic Development Early in the embryonic development of all bilaterians, specific regulatory states, sets of expressed tran- scription factors, are installed in the appropriate spatial domains of the multicellular embryo. Generally, this is the period in which zygotic gene expression is initiated in response to maternal inputs, and where spatial domains of regulatory gene expression are first formed all over the embryo with respect to the axial coordinates of the future body plan. 1.1 Specification in embryogenesis The informational requirement is the same in all bilaterian embryos: what are the mechanisms which ini- tially specify the diverse territories of the embryo, arranged according to bilateral axes of symmetry? Here “territory” means (with rare exceptions of secondary simplification) a multicellular domain, the cells of which all express a given regulatory state, and this regulatory state mediates their descendants’ fate. From such specified territories given parts of the embryo will uniquely arise. “Specification” is a typically fuzzy term from the older days of embryology, but for us it has a sharp and mechanistic definition. The initiation of specification means neither more nor less than the initial acquisition of a particular transcriptionally controlled regulatory state, i.e., execution of a unique program of regulatory gene expression. Thus the fundamental project of starting an embryo off is installing the correct territorial specifications. Or more precisely, it is the project of activating defined sets of regulatory genes in particular sets of cells located in particular spatial domains of the embryo. A prerequisite is of course generation of multiple embryonic cells (“blastomeres”) which are formed by division of the pre-formed mass of egg cytoplasm by cell membranes as the nuclei divide (“cleavage”). In all but amniote eggs (which absorb nutrients from their environment) there is no net growth during this period, and the number of ribosomes for example is the same in a postgastrular embryo that consists of hundreds or thousands of cells as in the newly fertilized egg of the same species (Davidson, 1986). Certain mechanisms of embryogenesis are utilized by all Bilateria, and these mechanisms can be regarded as universal principles of early bilaterian development (this is not to say that some such mechanisms are not used outside the Bilateria as well). In the following sections we consider these common Bilaterian regulatory strategies from the standpoint of the underlying genomic control mechanisms, which constitute a legacy from the distant Precambrian ancestor. 1.2 Properties of the egg Animal eggs have four major functional properties necessary for embryonic development. In order of their historical discovery, these are: first, their genetic function, that they convey a pronucleus contain- ing a complete haploid genome to the future zygote (i.e., the egg following fertilization and pronuclear Chapter 3 | Genomic Strategies for Embryonic Development 81 fusion); second, their logistic function, that in addition to the genome they carry an immense store of the molecular requirements for life to be utilized by the embryo; third, their activation function, that they biochemically respond to fertilization or the events immediately preceding fertilization by dramatically revving up protein synthesis and metabolism; and fourth, their spatial regulatory func- tion, that they provide asymmetrically localized regulatory molecules which are directly utilized by the early embryo in its axial specification processes. Their genetic function was discovered in the late 1870s and early 1880s by careful observation of meiosis, fertilization, pronuclear fusion, and mitosis. Their logistic function was suspected from measurements of their huge RNA and protein content in the 1930s, 1940s, and 1950s (Brachet, 1933), and proved by the discovery of maternal mRNA and its utilization for embryonic protein synthesis in the 1960s (Brachet et al., 1963; Monroy and Tyler, 1963; Denny and Tyler, 1964; Gross and Cousineau, 1964). Their activation function was first indi- cated by observations on oxidative metabolism following fertilization in the premolecular biology era, and the biochemical sequence of events leading to activation of protein synthesis was uncovered in the decades after 1970. Their spatial regulatory function, though long suspected (cf. the 1896 quote from E.B. Wilson in Chapter 2), was correctly predicted to indicate cytoplasmic sequestration of specific gene regulatory factors in eggs decades ago Davidson,( 1968; Davidson and Britten, 1971). But only recently, as we discuss in the next section, have abundant examples been authenticated by modern molecular biology. Here we are focused on the unusual features of genomic regulatory control in oogenesis that, after fer- tilization has taken place, enable the egg to execute these three major classes of function besides genetic transmission. During oogenesis the oocyte must accumulate the large and complex storehouse of RNAs and proteins needed for its logistic function, as well as generate the latent cytoskeletal and enzymatic machin- ery needed for its fertilization response function. And somehow it must acquire spatial polarity, and with respect to the future embryonic axes localize cytoplasmic molecules that directly or indirectly will serve to differentially activate genes in those blastomere nuclei inheriting these special cytoplasmic domains. The oocyte genomes are always active in the accumulation of macromolecular maternal products (more of which below), but they never work alone. For example, yolk protein, the major source of amino acids used for protein synthesis during embryogenesis, which is also the main protein constitu- ent of the mature oocyte, is always made by differentiated cells elsewhere and is the consequence of their own transcriptional control programs. Yolk gene expression is usually hormonally responsive. The yolk protein enters the oocyte by endocytic processes. The extreme example of oogenetic reli- ance on non-oocyte genomes is what is termed “meroistic” oogenesis, in which during growth the oocyte is syncytially connected through open canals to multiple “nurse cells” or “trophic cells” which are also of germ line origin (for review see Davidson, 1986). The nuclei
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