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Divergence of Ectodermal and Mesodermal Gene Regulatory Network Linkages in Early Development of Sea Urchins

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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 Eric M. Erkenbracka,1,2 aDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125 Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved October 5, 2016 (received for review August 3, 2016) Developmental gene regulatory networks (GRNs) are assemblages of to study in sea urchins, whose lineages have undergone multiple gene regulatory interactions that direct ontogeny of animal body changes in life history strategies (8). Importantly, an excellent fossil plans. Studies of GRNs operating in the early development of record affords dating of evolutionary events (9), which has established euechinoid sea urchins have revealed that little appreciable change has that the sister subclasses of sea urchins—cidaroids and euechinoids— occurred since their divergence ∼90 million years ago (mya). These diverged at least 268 million years ago (mya) (10). Differences in observations suggest that strong conservation of GRN architecture the timing of developmental events in embryogenesis of cida- was maintained in early development of the sea urchin lineage. Test- roids and euechinoids have long been a topic of interest, but ing whether this holds for all sea urchins necessitates comparative have become the subject of molecular research only recently analyses of echinoid taxa that diverged deeper in geological time. (11–18). Recent studies highlighted extensive divergence of skeletogenic me- Research on the early development of the euechinoid purple soderm specification in the sister clade of euechinoids, the cidaroids, sea urchin Strongylocentrotus purpuratus (Sp) has brought into suggesting that comparative analyses of cidaroid GRN architecture high resolution the players and molecular logic directing devel- may confer a greater understanding of the evolutionary dynamics of opmental GRNs that specify Sp’s early embryonic domains developmental GRNs. Here I report spatiotemporal patterning of 55 (19–30). Abundant comparative evidence exists for other eue- regulatory genes and perturbation analyses of key regulatory genes chinoid taxa as well, including Lytechinus variegatus (Lv) (31–37) involved in euechinoid oral–aboral patterning of nonskeletogenic me- and Paracentrotus lividus (Pl)(38–42). Data from these indirect- sodermal and ectodermal domains in early development of the cida- developing euechinoids indicate that although these taxa diverged roid Eucidaris tribuloides. These results indicate that developmental from one another ∼90 mya (9, 43), very little appreciable change GRNs directing mesodermal and ectodermal specification have to their developmental GRNs has accrued (44–46). Although undergone marked alterations since the divergence of cidaroids there is evidence of minor alterations to these GRNs, such as a and euechinoids. Notably, statistical and clustering analyses of heterochronic shift in snail expression in Lv and Sp (22), numerous echinoid temporal gene expression datasets indicate that regu- studies have made clear the striking conservation of GRN linkages lation of mesodermal genes has diverged more markedly than in these lineages. Recent studies of early development of the regulation of ectodermal genes. Although research on indirect- distantly related, indirect-developing cidaroid sea urchin Euci- developing euechinoid sea urchins suggests strong conserva- daris tribuloides (Et) have revealed that skeletogenic mesoderm tion of GRN circuitry during early embryogenesis, this study specification in this clade is markedly different from that ob- indicates that since the divergence of cidaroids and euechinoids, served in euechinoids (17, 18, 47). The foregoing observations developmental GRNs have undergone significant, cell type– suggest that comparative analyses of GRN circuitry in early biased alterations. Significance gene regulatory network | echinoderms | sea urchin embryogenesis | embryonic axis specification | echinoids Sea urchins (echinoids) consist of two subclasses, cidaroids and euechinoids. Research on gene regulatory networks (GRNs) in the ntegral to early development of a bilaterian is the development early development of three euechinoids indicates that little ap- Iof the three embryonic tissue-layer domains: endoderm, ecto- preciable change has occurred to their linkages since they di- derm, and mesoderm. Asymmetrically distributed RNA and verged ∼90 million years ago (mya). I asked whether this proteins in the egg provide the initial inputs into this process and conservation extends to all echinoids. I systematically analyzed thereby determine the spatial coordinates of domain formation the spatiotemporal expression and function of regulatory genes (1, 2). In the context of these maternal factors, zygotic tran- segregating euechinoid ectoderm and mesoderm in a cidaroid. I scription of distinct sets of regulatory genes occurs in specific report marked divergence of GRN architecture in early embryonic regions of the embryo, initiating the genomically encoded regu- specification of the oral–aboral axis in echinoids. Although I found latory program and its output of regulatory genes. In this way, evidence for diverged regulation of both mesodermal and ecto- the embryo becomes populated by distinct sets of transcription dermal genes, comparative analyses indicated that, since factors and cell signaling molecules called regulatory states (3). these two clades diverged 268 mya, mesodermal GRNs have un- Providing each cell with its molecularly distinct and functional dergone significantly more alterations than ectodermal GRNs. identity, regulatory states are the spatial readout of developmental gene regulatory networks (GRNs) (4, 5). Author contributions: E.M.E. designed research, performed research, analyzed data, and Sea urchins (class Echinodea) have long served as model sys- wrote the paper. tems for studying the mechanisms of early development and, The author declares no conflict of interest. more recently, to study fundamental aspects of developmental This article is a PNAS Direct Submission. GRNs. Mechanisms of early development can be readily studied 1Present address: Department of Ecology and Evolutionary Biology, Yale University, New in sea urchins owing to invariant cleavage patterns that give rise Haven, CT 06511. to early specification of blastomeres and cell lineages with rela- 2Email: [email protected]. tively clear boundaries of embryonic domains (6, 7). Evolution This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. and mechanisms of developmental programs also lend themselves 1073/pnas.1612820113/-/DCSupplemental. E7202–E7211 | PNAS | Published online November 3, 2016 www.pnas.org/cgi/doi/10.1073/pnas.1612820113 Downloaded by guest on September 24, 2021 development of cidaroids and euechinoids have the potential Overall, regulatory genes expressed in ectodermal domains ex- PNAS PLUS to illuminate the tempo and mode of evolution of develop- hibited stronger signals of conservation relative to those expressed mental GRNs. in mesodermal domains. These results suggest that embryonic do- In the present work, I coupled comparative spatiotemporal mains and cell types in early development of sea urchins have gene expression analyses with experimental manipulations of evolved at different rates since the divergence of the two echinoid regulatory genes specifying euechinoid nonskeletogenic me- sister subclasses. Alterations to GRN architecture have occurred sodermal (NSM) and ectodermal domains in the cidaroid Et to frequently throughout the network since their divergence. In addi- reveal how these GRNs have changed since the divergence of tion, these results offer an in-principle explanation for the rapid echinoids. This study focused on oral–aboral (O-A; or dorsal- changes in developmental processes during the convergent evolu- ventral) patterning, which has consequences for both the tion of direct-developing, nonfeeding sea urchins (50–53). ectoderm and mesoderm and is highly conserved in deutero- stomes (46, 48, 49). I present evidence that deployment and in- Results teractions of regulatory genes specifying sea urchin ectoderm Conserved Deployment of Euechinoid Ectodermal Regulatory Genes and mesoderm have diverged substantially in indirect-developing in the Cidaroid Et. In euechinoids, the ectoderm is segregated into echinoids. Importantly, comparative data and analyses suggest a diverse set of regulatory states defined by the future location of that regulatory linkages occurring in ectodermal GRNs have the stomodaeum (46, 54, 55). A critical factor in establishing O-A undergone fewer alterations—and thus are less divergent– (47) polarity in sea urchins is Nodal (35, 38). Nodal ligand, via than those occurring among regulatory genes in mesoder- activation by SMAD signaling, is directly upstream of nodal, not, mal domains. The conclusions are supported by comparative lefty, and chordin in oral ectoderm (OE) (40, 56). In Et, zygotic spatiotemporal data, statistical analyses of timecourse gene transcription of nodal, not, and lefty begins by early blastula stage expression data in three taxa of echinoids, and perturbation (Fig. 1 D and J and SI Appendix,Fig.S1D). In contrast to analyses. euechinoids, transcriptional activation of chordin does not occur BIOLOGY DEVELOPMENTAL Fig. 1. Spatiotemporal dynamics of 11 euechinoid ectodermal and mesodermal regulatory genes in the cidaroid
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