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

Abstract

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

Conserved regulatory state expression controlled by divergent developmental gene regulatory networks in echinoids

“…In E. tribuloides, only one NSM domain forms before gastrulation, and this co-expresses Et-myc, Et-gcm, Et-gatae and Et-ets1/2. The subdivision of NSM cell fates was shown to occur shortly after the onset of gastrulation (Erkenbrack, 2016). In the endoderm, both species express gatae, myc, blimp1 and foxa in AE, and bra, hox11/ 13b, eve and wnt8 in PE (Peter and Davidson, 2011b).…”

Paleogenomics of echinoids reveals an ancient origin for the double-negative specification of micromeres in sea urchins

“…In contrast, cidaroids have shown remarkable morphological conservation, and the earliest fossil cidaroids are almost morphologically identical to cidaroids living in the oceans today (20,21). Comparative studies of GRN architecture between cidaroids and euechinoids have revealed extensive differences in the wiring of their early developmental GRNs (8,22,23), and have served to inform our understanding of the genomic underpinning of the myriad morphological differences in their embryonic and larval development (24,25).…”

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

“…The variance in our data for VEGF transcripts around the onset of transcription likely reflects both the low abundance of this transcript and the sensitivity of our qPCR assay. This temporal sequence in E. tribuloides is similar to other NODAL‐responsive regulatory genes and is 3–4 hr removed from the onset of nodal —similar to chordin (Erkenbrack, ). Shortly after gastrulation commenced at 24 hpf, vegf signaling was not detected by WMISH, which is likely due to low levels of mRNA product (Fig.…”

“…Embryos were cultured in controlled conditions at 22°C. Probe preparation, embryo fixation, whole‐mount in situ hybridization (WMISH) and quantification of RNA transcript abundance by quantitative PCR (qPCR) were all conducted as previously described (Erkenbrack and Davidson, ; Erkenbrack, ; Erkenbrack et al., ). In S. purpuratus , there are three annotated VEGF ligands (VEGF, VEGF2, and VEGF3) and two annotated VEGF receptors (VEGFR‐7‐IG and VEGFR‐10‐IG) (Duloquin et al., ).…”