Ancestral state reconstruction by comparative analysis of a GRN kernel operating in echinoderms

Erkenbrack, Eric M.; Ako-Asare, Kayla; Miller, Emily; Tekelenburg, Saira; Thompson, Jeffrey R.; Romanò, Laura

doi:10.1007/s00427-015-0527-y

Cited by 18 publications

(18 citation statements)

References 22 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…the transcription factor Not (27,47,71). In Et, qPCR data did not indicate consistent differences in mRNA abundance for NSM regulatory genes (Fig.…”

Section: Nodal Signaling Is a Highly Conserved Mechanism Patterning Ementioning

confidence: 83%

“…the broad differences observed in Et in relation to SM specification, as well as that revealed here in NSM segregation and regulatory states. By comparing these observations with those in other echinoderms, we can begin to appreciate the degree to which embryonic developmental GRNs are constrained or altered over vast evolutionary distances, and can reconstruct the ancestral regulatory states that must have existed in the embryos of echinoderm ancestors (47).…”

Section: Discussion Extensive Divergence Of Ectodermal and Mesodermalmentioning

confidence: 99%

“…Interestingly, in cidaroids, the micromere embryonic address is the location at which numerous euechinoid SM genes are first activated (17,47). These observations suggest that in the ancestral echinoid lineage, the adult skeletogenesis program was co-opted to run in the micromeres.…”

Section: Evolution Of Global Embryonic Domains In Early Development Ofmentioning

confidence: 99%

“…Previous analyses of embryonic regulatory states in Et surveyed SM regulatory factors (17,47) and anterior neural ectoderm specification (75). In addition, two previous studies investigated SM and early endomesodermal micromere regulatory factors in the Pacific-dwelling cidaroid Prionocidaris baculosa (16,99).…”

Section: Evolution Of Global Embryonic Domains In Early Development Ofmentioning

confidence: 99%

“…Although there is evidence of minor alterations to these GRNs, such as a heterochronic shift in snail expression in Lv and Sp (22), numerous studies have made clear the striking conservation of GRN linkages in these lineages. Recent studies of early development of the distantly related, indirect-developing cidaroid sea urchin Eucidaris tribuloides (Et) have revealed that skeletogenic mesoderm specification in this clade is markedly different from that observed in euechinoids (17,18,47). The foregoing observations suggest that comparative analyses of GRN circuitry in early Significance Sea urchins (echinoids) consist of two subclasses, cidaroids and euechinoids.…”

mentioning

confidence: 99%

See 4 more Smart Citations

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

Erkenbrack

2016

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

Self Cite

View full text Add to dashboard Cite

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

show abstract

“…the transcription factor Not (27,47,71). In Et, qPCR data did not indicate consistent differences in mRNA abundance for NSM regulatory genes (Fig.…”

Section: Nodal Signaling Is a Highly Conserved Mechanism Patterning Ementioning

confidence: 83%

Section: Discussion Extensive Divergence Of Ectodermal and Mesodermalmentioning

confidence: 99%

Section: Evolution Of Global Embryonic Domains In Early Development Ofmentioning

confidence: 99%

Section: Evolution Of Global Embryonic Domains In Early Development Ofmentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

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

Erkenbrack

2016

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

Self Cite

View full text Add to dashboard Cite

show abstract

From genome to anatomy: The architecture and evolution of the skeletogenic gene regulatory network of sea urchins and other echinoderms

Shashikant

Khor

Ettensohn

2018

Genesis

View full text Add to dashboard Cite

The skeletogenic gene regulatory network (GRN) of sea urchins and other echinoderms is one of the most intensively studied transcriptional networks in any developing organism. As such, it serves as a pre-eminent model of GRN architecture and evolution. This review summarizes our current understanding of this developmental network. We describe in detail the most comprehensive model of the skeletogenic GRN, one developed for the euechinoid sea urchin Strongylocentrotus purpuratus, including its initial deployment by maternal inputs, its elaboration and stabilization through regulatory gene interactions, and its control of downstream effector genes that directly drive skeletal morphogenesis. We highlight recent comparative studies that have leveraged the euechinoid GRN model to examine the evolution of skeletogenic programs in diverse echinoderms, studies that have revealed both conserved and divergent features of skeletogenesis within the phylum. Lastly, we summarize the major insights that have emerged from analysis of the structure and evolution of the echinoderm skeletogenic GRN and identify key, unresolved questions as a guide for future work.

show abstract

A Conserved Role for VEGF Signaling in Specification of Homologous Mesenchymal Cell Types Positioned at Spatially Distinct Developmental Addresses in Early Development of Sea Urchins

Erkenbrack

Petsios

2017

J Exp Zool Pt B

Self Cite

View full text Add to dashboard Cite

Comparative studies of early development in echinoderms are revealing the tempo and mode of alterations to developmental gene regulatory networks and to the cell types they specify. In euechinoid sea urchins, skeletogenic mesenchyme (SM) ingresses prior to gastrulation at the vegetal pole and aligns into a ring-like array with two bilateral pockets of cells, the sites where spiculogenesis will later occur. In cidaroid sea urchins, the anciently diverged sister clade to euechinoid sea urchins, a homologous SM cell type ingresses later in development, after gastrulation has commenced, and consequently at a distinct developmental address. Thus, a heterochronic shift of ingression of the SM cell type occurred in one of the echinoid lineages. In euechinoids, specification and migration of SM are facilitated by vascular endothelial growth factor (VEGF) signaling. We describe spatiotemporal expression of vegf and vegfr and experimental manipulations targeting VEGF signaling in the cidaroid Eucidaris tribuloides. Spatially, vegf and vegfr mRNA localizes similarly as in euechinoids, suggesting conserved deployment in echinoids despite their spatially distinct development addresses of ingression. Inhibition of VEGF signaling in E. tribuloides suggests its role in SM specification is conserved in echinoids. Temporal discrepancies between the onset of vegf expression and SM ingression likely result in previous observations of SM "random wandering" behavior. Our results indicate that, although the SM cell type in echinoids ingresses into distinct developmental landscapes, it retains a signaling mechanism that restricts their spatial localization to a conserved developmental address where spiculogenesis later occurs.

show abstract

Ancestral state reconstruction by comparative analysis of a GRN kernel operating in echinoderms

Cited by 18 publications

References 22 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

From genome to anatomy: The architecture and evolution of the skeletogenic gene regulatory network of sea urchins and other echinoderms

A Conserved Role for VEGF Signaling in Specification of Homologous Mesenchymal Cell Types Positioned at Spatially Distinct Developmental Addresses in Early Development of Sea Urchins

Contact Info

Product

Resources

About