Nodal/activin signaling establishes oral–aboral polarity in the early sea urchin embryo

Flowers, Vera Lynn; Courteau, Girard R.; Poustka, Albert J.; Weng, Wei; Venuti, Judith M.

doi:10.1002/dvdy.20194

Cited by 70 publications

(105 citation statements)

References 66 publications

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“…In euechinoids, the ectoderm is segregated into a diverse set of regulatory states defined by the future location of the stomodaeum (46,54,55). A critical factor in establishing O-A (47) polarity in sea urchins is Nodal (35,38). Nodal ligand, via activation by SMAD signaling, is directly upstream of nodal, not, lefty, and chordin in oral ectoderm (OE) (40,56).…”

Section: Resultsmentioning

confidence: 99%

“…Abundant comparative evidence exists for other euechinoid taxa as well, including Lytechinus variegatus (Lv) (31)(32)(33)(34)(35)(36)(37) and Paracentrotus lividus (Pl) (38)(39)(40)(41)(42). Data from these indirectdeveloping euechinoids indicate that although these taxa diverged from one another ∼90 mya (9, 43), very little appreciable change to their developmental GRNs has accrued (44)(45)(46).…”

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confidence: 99%

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Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Erkenbrack

2016

Proc. Natl. Acad. Sci. U.S.A.

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Developmental gene regulatory networks (GRNs) are assemblages of gene regulatory interactions that direct ontogeny of animal body plans. Studies of GRNs operating in the early development of euechinoid sea urchins have revealed that little appreciable change has occurred since their divergence ∼90 million years ago (mya). These observations suggest that strong conservation of GRN architecture was maintained in early development of the sea urchin lineage. Testing whether this holds for all sea urchins necessitates comparative analyses of echinoid taxa that diverged deeper in geological time. Recent studies highlighted extensive divergence of skeletogenic mesoderm specification in the sister clade of euechinoids, the cidaroids, suggesting that comparative analyses of cidaroid GRN architecture may confer a greater understanding of the evolutionary dynamics of developmental GRNs. Here I report spatiotemporal patterning of 55 regulatory genes and perturbation analyses of key regulatory genes involved in euechinoid oral-aboral patterning of nonskeletogenic mesodermal and ectodermal domains in early development of the cidaroid Eucidaris tribuloides. These results indicate that developmental GRNs directing mesodermal and ectodermal specification have undergone marked alterations since the divergence of cidaroids and euechinoids. Notably, statistical and clustering analyses of echinoid temporal gene expression datasets indicate that regulation of mesodermal genes has diverged more markedly than regulation of ectodermal genes. Although research on indirectdeveloping euechinoid sea urchins suggests strong conservation of GRN circuitry during early embryogenesis, this study indicates that since the divergence of cidaroids and euechinoids, developmental GRNs have undergone significant, cell typebiased alterations.gene regulatory network | echinoderms | sea urchin embryogenesis | embryonic axis specification | echinoids

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Erkenbrack

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…3K; Duboc et al, 2004). During this time, nodal expression appears in about a third of the embryo, with transcripts localized in the presumptive ectoderm (Duboc et al, 2004;Flowers et al, 2004). At the prism and pluteus stages of gastrulation, nodal expression increases, although levels remain lower than those seen throughout the blastula stages.…”

Section: Nodal Signaling In Invertebrate Deuterostomesmentioning

confidence: 98%

“…Nodal expression is restricted to the presumptive oral ectoderm, which marks the future oral side of the larva ( Fig. 3L; Duboc et al, 2004;Flowers et al, 2004). The archenteron, which is guided by mesenchyme cells, then bends towards the prospective oral region in response to the signals (Wray, 1997).…”

Section: Nodal Signaling In Invertebrate Deuterostomesmentioning

confidence: 99%

Nodal signaling and the evolution of deuterostome gastrulation

Chea

Wright

Swalla

2005

Developmental Dynamics

101

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Chordates, including vertebrates, evolved within a group of animals called the deuterostomes. All holoblastic deuterostomes gastrulate at the vegetal pole and the blastopore becomes the anus, while a mouth is formed at the anterior or to the oral side. Nodal is a member of the TGF-␤ superfamily of signaling molecules that are important in signaling between cells during many embryonic processes in vertebrate embryos. Nodal has also been found in other invertebrate deuterostomes, such as ascidians and sea urchins, but, so far, is missing in protostomes. Nodal has been shown to be particularly important in determining left-right asymmetries in vertebrate embryos, but less information is available for its developmental role in the invertebrate deuterostomes. We review gastrulation in the deuterostomes, then examine nodal expression early during mesoderm formation and later during the establishment of asymmetries in both vertebrates and invertebrates. Nodal is expressed asymmetrically on the left side in chordates and on the presumptive oral side of the embryo in echinoid echinoderms. The expression of nodal is in different germ layers in embryos of different phyla. Expression is in the ectoderm in most of the invertebrate deuterostomes, and in the mesoderm in vertebrates. We summarize the work that has been published to date, especially nodal expression in the invertebrate deuterostomes, and suggest future experiments to better understand the evolution of nodal signaling and deuterostome gastrulation. Developmental Dynamics 234:269 -278, 2005.

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“…The primary axis defining the plane of bilateral symmetry is historical information that is preformed in the structurally polarized cytoplasm of the egg, whereas the secondary axis emerges epigenetically via the activities of two genes: nodal and lefty [9][10][11][12]. Both nodal and lefty encode diffusible extracellular proteins that are produced beginning at about the 60-120 cell morula stage.…”

Section: A Developmental Paradigm: Sea Urchin Embryogenesismentioning

confidence: 99%

Information as a Manifestation of Development

Coffman

2011

Information

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Information manifests a reduction in uncertainty or indeterminacy. As such it can emerge in two ways: by measurement, which involves the intentional choices of an observer; or more generally, by development, which involves systemically mutual ('self-organizing') processes that break symmetry. The developmental emergence of information is most obvious in ontogeny, but pertains as well to the evolution of ecosystems and abiotic dissipative structures. In this review, a seminal, well-characterized ontogenetic paradigm-the sea urchin embryo-is used to show how cybernetic causality engenders the developmental emergence of biological information at multiple hierarchical levels of organization. The relevance of information theory to developmental genomics is also discussed.

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Nodal/activin signaling establishes oral–aboral polarity in the early sea urchin embryo

Cited by 70 publications

References 66 publications

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Nodal signaling and the evolution of deuterostome gastrulation

Information as a Manifestation of Development

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