Spatial mechanisms of gene regulation in metazoan embryos

Davidson, Eric H.

doi:10.1242/dev.113.1.1

Cited by 233Developmental Biology and Gene RegulationGenomics and Chromatin DynamicsMarine Invertebrate Physiology and Ecology

Spatial mechanisms of gene regulation in metazoan embryos

Davidson, Eric H.·1991·Development

DOI 10.1242/dev.113.1.1

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Abstract

The basic characteristics of embryonic process throughout Metazoa are considered with focus on those aspects that provide insight into how cell specification occurs in the initial stages of development. There appear to be three major types of embryogenesis: Type 1, a general form characteristic of most invertebrate taxa of today, in which lineage plays an important role in the spatial organization of the early embryo, and cell specification occurs in situ, by both autonomous and conditional mechanisms; Type 2, the vertebrate form of embryogenesis, which proceeds by mechanisms that are essentially independent of cell lineage, in which diffusible morphogens and extensive early cell migration are particularly important; Type 3, the form exemplified by long germ band insects in which several different regulatory mechanisms are used to generate precise patterns of nuclear gene expression prior to cellularization. Evolutionary implications of the phylogenetic distribution of these types of embryogenesis are considered. Regionally expressed homeodomain regulators are utilized in all three types of embryo, in similar ways in later and postembryonic development, but in different ways in early embryonic development. A specific downstream molecular function for this class of regulator is proposed, based on evidence obtained in vertebrate systems. This provides a route by which to approach the comparative regulatory strategies underlying the three major types of embryogenesis.

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Both dipleurula and trochophore larvae use Type 1 embryogenesis, which divides the cleavage-stage embryo into polyclonal territories.
“Both utilize Type 1 embryogenesis (see Davidson, 1991;Davidson et al., 1995; and the data discussed above), which divides the cleavage-stage embryo into a set of polyclonal territories.”
From Bilaterian Origins: Significance of New Experimental Observations (2000) · cites this paper as Davidson, 1991

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The organic matrix of the skeletal spicule of sea urchin embryos.
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The marginal zone and its contribution to the hypoblast and primitive streak of the chick embryo
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Posterior pattern formation in C. elegans involves position-specific expression of a gene containing a homeobox
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Differential antero‐posterior expression of two proteins encoded by a homeobox gene in Xenopus and mouse embryos.
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A homeo domain protein reveals the metameric nature of the developing chick hindbrain.Preprint
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Embryonic expression of a gut-specific esterase in Caenorhabditis elegans
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Lithium evokes expression of vegetal-specific molecules in the animal blastomeres of sea urchin embryos.
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A genomic regulatory network for development
Davidson, E. H., Rast, J. P., Oliveri, P., Ransick, A., Calestani, C., Yuh, C.-H., Minokawa, T., Amore, G., Hinman, V., Arenas-Mena, C., et al. (2002) · Science · doi:10.1126/science.1069883 · Cited by 1,567 · see citing works
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Anther Development: Basic Principles and Practical Applications
Goldberg, R. B., Beals, T. P., & Sanders, P. M. (1993) · The Plant Cell · doi:10.1105/tpc.5.10.1217 · Cited by 835 · see citing works
The hardwiring of development: organization and function of genomic regulatory systems
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Direct regulation of decapentaplegic by Ultrabithorax and its role in Drosophila midgut morphogenesis
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A critical reappraisal of the fossil record of the bilaterian phyla
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An early marker of axial pattern in the chick embryo and its respecification by retinoic acid
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Expression of the Hox gene complex in the indirect development of a sea urchin
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A comparative molecular approach to mesodermal patterning in basal deuterostomes: the expression pattern of Brachyury in the enteropneust hemichordate Ptychodera flava
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Bilaterian Origins: Significance of New Experimental Observations
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Mammalian Inscuteable Regulates Spindle Orientation and Cell Fate in the Developing Retina
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Whole mount in situ hybridization shows Endo 16 to be a marker for the vegetal plate territory in sea urchin embryos
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Polarity of the mouse embryo is anticipated before implantation
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Conserved Anterior Boundaries of Hox Gene Expression in the Central Nervous System of the LeechHelobdella
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Late Precambrian bilaterians: grades and clades.
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Homeobox genes and pattern formation in the vertebrate limb
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Theetsmultigene family is conserved throughout the Metazoa
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Mesoderm-inducing factors and the control of gastrulation
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Who came first--larvae or adults? origins of bilaterian metazoan larvae
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Modular cis-regulatory organization of developmentally expressed genes: two genes transcribed territorially in the sea urchin embryo, and additional examples.
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Cleavage patterns and the topology of the metazoan tree of life
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Gene expression profiles in young adult Ciona intestinalis
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A homology domain shared between Drosophila optomotor-blind and mouse Brachyury is involved in DNA binding
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The echinoid immune system and the phylogenetic occurrence of immune mechanisms in deuterostomes
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Later embryogenesis: regulatory circuitry in morphogenetic fields
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Towards a phylogeny of the Metazoa: evaluating alternative phylogenetic positions of Platyhelminthes, Nemertea, and Gnathostomulida, with a critical reappraisal of cladistic characters
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Timing of initiation of muscle‐specific gene expression in the ascidian embryo precedes that of developmental fate restriction in lineage cells
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Ancient mechanisms of visual sense organ development based on comparison of the gene networks controlling larval eye, ocellus, and compound eye specification in Drosophila
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On nitric oxide signaling, metamorphosis, and the evolution of biphasic life cycles
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Evolution of animal body plans: the role of metazoan phylogeny at the interface between pattern and process
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Spatial and temporal information processing in the sea urchin embryo: modular and intramodular organization of the CyIIIa gene cis-regulatory system
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Expression Pattern of Brachyury and Not in the Sea Urchin: Comparative Implications for the Origins of Mesoderm in the Basal Deuterostomes
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Boolean logic and character state identity: pitfalls of character coding in metazoan cladistics
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The retinoic acid machinery in invertebrates: Ancestral elements and vertebrate innovations
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Spatial Control of the Gap Gene knirps in the Drosophila Embryo by Posterior Morphogen System
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Cell Fate Maps in theIlyanassa obsoletaEmbryo beyond the Third Division
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The Echinoderm Immune System
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Cellularization in locust embryos occurs before blastoderm formation
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Complexity and organization of DNA-protein interactions in the 5′-regulatory region of an endoderm-specific marker gene in the sea urchin embryo
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The Development and Evolution of Polyembryonic Insects
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Spatial integration among cells forming the cranial peripheral nervous system
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Roles of Secretion and the Cytoskeleton in Cell Adhesion and Polarity Establishment inPelvetia compressaZygotes
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Larvae in Invertebrate Development and Evolution
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Altering cell fates in sea urchin embryos by overexpressing SpOtx, an orthodenticle-related protein
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The evolution of echinoderm development is driven by several distinct factors
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Placozoa and the evolution of Metazoa and intrasomatic cell differentiation
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Two distinct phenotypes caused by two different missense mutations in the same codon of the VHL gene
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Evolution of segmentation genes in insects
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Cell fate specification in the C. elegans embryo
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Cis-regulatory logic driving glial cells missing: Self-sustaining circuitry in later embryogenesis
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Gene expression during the oocyte‐to‐embryo transition in mammals
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Cell mixing during early epiboly in the zebrafish embryo
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Engrailed Expression during Development of a Lamprey, Lampetra japonica: A Possible Clue to Homologies between Agnathan and Gnathostome Muscles of the Mandibular Arch
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Germ Layers and the Germ-Layer Theory Revisited
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The Development of Radial and Biradial Symmetry: The Evolution of Bilaterality
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Specification of Primary Pigment Cell and Outer Photoreceptor Fates byBarH1Homeobox Gene in the DevelopingDrosophilaEye
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Quantitative assessment of Hox complex expression in the indirect development of the polychaete annelid Chaetopterus sp.
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Molecular biology of embryonic development: how far have we come in the last ten years?
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Cell‐autonomous expression and position‐dependent repression by Li+ of two zygotic genes during sea urchin early development.
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Hindgut specification and cell‐adhesion functions of Sphox11/13b in the endoderm of the sea urchin embryo
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Very early and transient vegetal-plate expression of SpKrox1, a Krüppel/Krox gene from Strongylocentrotus purpuratus
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Morphological evolution and embryonic developmental diversity in metazoa
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Spatial expression of a forkhead homologue in the sea urchin embryo
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Homeobox-containing gene transiently expressed in a spatially restricted pattern in the early sea urchin embryo.
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Hematopoiesis and T‐cell specification as a model developmental system
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ERK1/2 is an ancestral organising signal in spiral cleavage
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How embryos work: a comparative view of diverse modes of cell fate specification
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Genomic Strategies for Embryonic Development
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Understanding Embryonic Development: A Contemporary View
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Lineage-specific gene expression and the regulative capacities of the sea urchin embryo: a proposed mechanism
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Authors: Davidson, E. H.
Affiliations: California Institute of Technology (US)
Corresponding author: Davidson, Eric H.
Venue: Development
Publisher: The Company of Biologists
Published: 1991-09-01
Volume: 113
Issue: 1
Pages: 1-26
ISSN: 0950-1991 (ISSN-L)
1477-9129
DOI: 10.1242/dev.113.1.1
OpenAlex: W2135876222
Cited by: 233
References: 260
Citations by year: 2026: 2 · 2025: 2 · 2024: 2 · 2023: 5 · 2022: 3 · 2021: 1 · 2020: 3 · 2019: 3 · 2018: 1 · 2017: 5 · 2016: 4 · 2015: 1 · 2014: 2 · 2012: 4
FWCI: 7.80
Type: journal article
Language: en
Open access: closed
Licence: www.biologists.com/user-licence-1-1/ (vor)
Locations: Development (publishedVersion)
PubMed (publishedVersion)
CaltechAUTHORS (California Institute of Technology) (submittedVersion)
HighWire Press Open Archive (submittedVersion)
Funders: Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD05753)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Keywords: cell specification, morphogens, cell migration, homeodomain transcription factor, spatial patterning, nuclear gene expression, evolutionary developmental biology, vertebrate embryonic development
MeSH terms: Animals, Cell Differentiation, Embryo, Mammalian, Embryo, Nonmammalian, Biological Evolution, Gene Expression Regulation, Genes, Homeobox, Insecta, Invertebrates, Morphogenesis, Vertebrates

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Spatial mechanisms of gene regulation in metazoan embryos

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