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WIREs Dev Biol
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Establishment of spatial pattern

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Abstract An overview and perspective are presented of mechanisms for the development of spatial pattern in animal embryos. It is intended both for new entrants to developmental biology and for specialists in other fields, with only a basic knowledge of animal life cycles being required. The first event of pattern formation is normally the localization of a cytoplasmic determinant in the egg, either during oogenesis or post‐fertilization. Following cleavage to a multicellular stage, some cells contain the determinant and others do not. The determinant confers a specific developmental pathway on the cells that contain it, often making them the source of the first extracellular signal, or inducing factor. Inducing factors often form concentration gradients to which cells respond by up or downregulating genes at various concentration thresholds. This enables an initial situation consisting of two cell states (with or without the determinant) to generate a multistate pattern. Multiple rounds of gradient signaling, interspersed with phases of morphogenetic movements, can generate a complex pattern using a small number of signals and responding genes. Development proceeds in a hierarchical manner, with broad body subdivisions being specified initially, and becoming successively subdivided to give individual organs and tissues composed of multiple cell types in a characteristic arrangement. Double gradient models can account for embryonic regulation, whereby a similarly proportioned body pattern is formed following removal of material. Processes that are involved at the later stages include the formation of repeating structures by the combination of an oscillator with a gradient, and the formation of tissues with one cell type scattered in a background of another through a process called lateral inhibition. This set of processes make up a ‘developmental toolkit’ which can be deployed in various sequences and combinations to generate a very wide variety of structures and cell types. WIREs Dev Biol 2014, 3:379–388. doi: 10.1002/wdev.144 This article is categorized under: Establishment of Spatial and Temporal Patterns > Cytoplasmic Localization Establishment of Spatial and Temporal Patterns > Gradients Establishment of Spatial and Temporal Patterns > Repeating Patterns and Lateral Inhibition
Generation of complexity from a simple beginning. This embryo has a cytoplasmic determinant at the vegetal end which causes the cells containing it to become the source of a morphogen. Genes controlling the formation of two territories, B and C, are upregulated at appropriate threshold concentrations. Territory A is the default that arises in the absence of any inducing factor. (Reprinted with permission from Ref . Copyright 2013 Wiley‐Blackwell)
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Lateral inhibition. Cell type A produce both the activator and the inhibitor. Where the activator prevails cell type A is stabilized, where the inhibitor prevails cell type A is suppressed. (Reprinted with permission from Ref . Copyright 2013 Wiley‐Blackwell)
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Operation of the somite oscillator over one cycle of somite formation in the chick. The diagrams show the expression pattern of the Hes gene at four times in the cycle, and the graphs show how the level of transcript varies at the points a, b, and c as one somite becomes specified. (Reprinted with permission from Ref . Copyright 2013 Wiley‐Blackwell)
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The developmental hierarchy. This shows the normally accepted mode of formation of pancreatic β cells, involving six developmental steps, each controlled by one or more inducing factors. The inducing factors (NODAL, WNT, FGF, BMP, Notch ligands) are shown in different colors. The final step distinguishes the insulin‐producing β‐cells from other types of endocrine cell also present in pancreatic islets (α, δ, ε, PP), and its mechanism is still under investigation. (Reprinted with permission from Ref . Copyright 2008 American Association for the Advancement of Science)
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Operation of a bistable switch. The figure depicts a temporal sequence of events: in step 2 the gene is upregulated by a regulator, which might be controlled by a morphogen gradient; in step 3 it is also upregulated by its product; in step 4 it remains active because of the product even though the regulator is now gone. (Reprinted with permission from Ref . Copyright 2013 Wiley‐Blackwell)
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Properties of simple morphogen gradients. (a) Normal development of an animal with head and three segments. The thresholds indicate the upregulation of genes whose combinations of activity: 000, 001, 011, 111, represent codes for different body levels. (b) Graft of a second source to the low end causes formation of a U‐shaped gradient and produces a mirror‐symmetrical animal. In this case it is double‐posterior. (c) Cutting the embryo in half results in the formation of less than half of the pattern.
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Generation of bilateral symmetry with two determinants. Two gradients partition the embryo into territories along two axes. The resulting embryo has territories arranged symmetrically around a median plane. (Reprinted with permission from Ref . Copyright 2013 Wiley‐Blackwell)
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Localization of a determinant by a symmetry‐breaking process. (Reprinted with permission from Ref . Copyright 2013 Wiley‐Blackwell)
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Establishment of Spatial and Temporal Patterns > Cytoplasmic Localization
Establishment of Spatial and Temporal Patterns > Gradients
Establishment of Spatial and Temporal Patterns > Repeating Patterns and Lateral Inhibition