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WIREs Dev Biol

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The evolution of amniote gastrulation: the blastopore‐primitive streak transition

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Matthew J. Stower, Federica Bertocchini

Published Online: Feb 08 2017

DOI: 10.1002/wdev.262

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In the animal kingdom, gastrulation, the process by which the primary germ layers are formed involves a dramatic transformation in the topology of the cells that give rise to all of the tissues of the adult. Initially formed as a mono‐layer, this tissue, the epiblast, becomes subdivided through the internalization of cells, thereby forming a two (bi‐laminar) or three (tri‐laminar) layered embryo. This morphogenetic process coordinates the development of the fundamental body plan and the three‐body axes (antero‐posterior, dorso‐ventral, and left‐right) and begins a fundamental segregation of cells toward divergent developmental fates. In humans and other mammals, as well as in avians, gastrulating cells internalize along a structure, called the primitive streak, which builds from the periphery toward the center of the embryo. How these morphogenetic movements are orchestrated and evolved has been a question for developmental biologists for many years. Is the primitive streak a feature shared by the whole amniote clade? Insights from reptiles suggest that the primitive streak arose independently in mammals and avians, while the reptilian internalization site is a structure half‐way between an amphibian blastopore and a primitive streak. The molecular machinery driving primitive streak formation has been partially dissected using mainly the avian embryo, revealing a paramount role of the planar cell polarity (PCP) pathway in streak formation. How did the employment of this machinery evolve? The reptilian branch of the amniote clade might provide us with useful tools to investigate the evolution of the amniote internalization site up to the formation of the primitive streak. WIREs Dev Biol 2017, 6:e262. doi: 10.1002/wdev.262 This article is categorized under: Early Embryonic Development > Fertilization to Gastrulation Early Embryonic Development > Gastrulation and Neurulation Comparative Development and Evolution > Body Plan Evolution

Summary of the internalization site of amphibian (a), reptiles (b), avians (c, d), and nonrodent mammals (e, f). (a) Gastrulating amphibian embryo, where involution beginning at the dorsal lip of the blastopore (blue crescent, green arrows) proceeds to occur around the entire circumference of the embryo (gray arrows). (b) Reptile gastrulation, with involution anteriorly (arrows) and the blastoporal plate, the site of ingression, in blue. (c, d) Scheme of a gastrulating chick embryo with the primitive streak (c), and (d) the result of PCP pathway inhibition. (e, f) Scheme of a gastrulating rabbit embryo with the primitive streak (e), and (f) after ROCK treatment, a Rho Kinase inhibitor, a downstream effector of the PCP pathway.

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Gastrulation in the chameleon embryo. (a, b, e–g) Confocal images of a d28 gastrulating chameleon embryo (Chameleon calyptratus). Dorsal view (a) of a phalloidin‐stained embryo, with the blastopore and blastoporal plate indicated in the inset and magnified in panel (b). A sagittal section (e) shows involution in the anterior blastopore (white arrow) and ingression in the posterior part (red arrow). Transversal sections at the level of the blastoporal plate (f, g) show breaking of the BM, as revealed by laminin disruption (yellow arrowheads in (f)). Ingression at the level of the midline (arrow in (g)) and ingressing cells (red arrows in (f)) are indicated. (c, d) In situ hybridization of d12 (c) and d39 (d) chameleon embryos, with Fgf8 and Brachyury, respectively. (h) Scheme of a gastrulating chameleon embryo. Scale bar: 200 m

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Schemes of the mechanism for early streak formation in avians (a, d, g), rabbit (b, e, h), and mouse (c, f, i). (a, d, g) Polonaise movements drive cells toward the posterior midline (a), where PCP‐dependent medio‐lateral intercalation determines the formation of the elongated primitive streak (d, g). (b, e, h) U‐Shape and L‐shape movements drive cells toward the posterior midline region (PGE) in the rabbit (b); PCP‐dependent processional movements drive intercalation of cells in the forming streak (e, h). Red, tip of the streak; orange, middle and posterior streak; yellow, this region indicates the site of Brachyury expression before the streak forms. (c, f, i) In the mouse, while it is still not known what determines the site of primitive streak initiation (c), EMT occurs in the proximal epiblast of the future posterior region, determining the formation of an elongated primitive streak (g, i). Red, orange, and yellow indicate anterior, middle, and posterior parts of the forming streak, respectively.

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Chick embryos at different embryonic stages; prestreak (a, c), early (b, d), mid‐ (e), and late (f) primitive streak. (a, b) Scheme of prestreak and early streak stage chick embryo, respectively. HYP, hypoblast; AP, area pellucida; MZ, marginal zone; AO, area opaca; KC, Koller's sickle. (c) In situ hybridization with the transcription factor Hex, showing the growing hypoblast, reaching half of the width of the AP. (d) In situ with Wnt8c, indicating an early triangular streak (stage 2 HH). (e, f) In situ with Brachyury, indicating a mid‐ (stage 3/3⁺ HH) and late (stage 4 HH) primitive streak. The extent of the AP is indicated by the black‐dotted circle. Anterior to the top, posterior to the bottom. Scale bar: 1 mm.

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Phylogenetic tree of the amniote clade. Simplified phylogenetic tree showing the presence of a primitive streak or a blastopore slit in each group (left part of the drawing). Only mammals and birds evolved a primitive steak.

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