skip to main content


Title: Genomic insights of body plan transitions from bilateral to pentameral symmetry in Echinoderms
Echinoderms are an exceptional group of bilaterians that develop pentameral adult symmetry from a bilaterally symmetric larva. However, the genetic basis in evolution and development of this unique transformation remains to be clarified. Here we report newly sequenced genomes, developmental transcriptomes, and proteomes of diverse echinoderms including the green sea urchin (L. variegatus), a sea cucumber (A. japonicus), and with particular emphasis on a sister group of the earliest-diverged echinoderms, the feather star (A. japonica). We learned that the last common ancestor of echinoderms retained a well-organized Hox cluster reminiscent of the hemichordate, and had gene sets involved in endoskeleton development. Further, unlike in other animal groups, the most conserved developmental stages were not at the body plan establishing phase, and genes normally involved in bilaterality appear to function in pentameric axis development. These results enhance our understanding of the divergence of protostomes and deuterostomes almost 500 Mya.  more » « less
Award ID(s):
1656752
NSF-PAR ID:
10216625
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more » ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; « less
Date Published:
Journal Name:
Communications biology
Volume:
3
Issue:
371
ISSN:
2399-3642
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract The Echinodermata is characterized by a secondarily evolved pentameral body plan. While the evolutionary origin of this body plan has been the subject of debate, the molecular mechanisms underlying its development are poorly understood. We assembled a de novo developmental transcriptome from the embryo through metamorphosis in the sea star Parvulastra exigua. We use the asteroid model as it represents the basal-type echinoderm body architecture. Global variation in gene expression distinguished the gastrula profile and showed that metamorphic and juvenile stages were more similar to each other than to the pre-metamorphic stages, pointing to the marked changes that occur during metamorphosis. Differential expression and gene ontology (GO) analyses revealed dynamic changes in gene expression throughout development and the transition to pentamery. Many GO terms enriched during late metamorphosis were related to neurogenesis and signalling. Neural transcription factor genes exhibited clusters with distinct expression patterns. A suite of these genes was up-regulated during metamorphosis (e.g. Pax6, Eya, Hey, NeuroD, FoxD, Mbx, and Otp). In situ hybridization showed expression of neural genes in the CNS and sensory structures. Our results provide a foundation to understand the metamorphic transition in echinoderms and the genes involved in development and evolution of pentamery. 
    more » « less
  2. ABSTRACT Sea urchins and other echinoderms are important experimental models for studying developmental processes. The lack of approaches for conditional gene perturbation, however, has made it challenging to investigate the late developmental functions of genes that have essential roles during early embryogenesis and genes that have diverse functions in multiple tissues. The doxycycline-controlled Tet-On system is a widely used molecular tool for temporally and spatially regulated transgene expression. Here, we optimized the Tet-On system to conditionally induce gene expression in sea urchin embryos. Using this approach, we explored the roles the MAPK signaling plays in skeletogenesis by expressing genes that perturb the pathway specifically in primary mesenchyme cells during later stages of development. We demonstrated the wide utility of the Tet-On system by applying it to a second sea urchin species and in cell types other than the primary mesenchyme cells. Our work provides a robust and flexible platform for the spatiotemporal regulation of gene expression in sea urchins, which will considerably enhance the utility of this prominent model system. 
    more » « less
  3. SUMMARY  
    more » « less
  4. Abstract

    Evolution is proposed to result, in part, from acquisition of new developmental programs. One such example is the appearance of the micromeres in a sea urchin that form by an asymmetric cell division at the 4thembryonic cleavage and function as a major signaling center in the embryo. Micromeres are not present in other echinoderms and thus are  considered as a derived feature, yet its acquisition mechanism is unknown. Here, we report that the polarity factor AGS and its associated proteins are responsible for micromere formation. Evolutionary modifications of AGS protein seem to have provided the cortical recruitment and binding of AGS to the vegetal cortex, contributing to formation of micromeres in the sea urchins. Indeed, introduction of sea urchin AGS into the sea star embryo induces asymmetric cell divisions, suggesting that the molecular evolution of AGS protein is key in the transition of echinoderms to micromere formation and the current developmental style of sea urchins not seen in other echinoderms.

     
    more » « less
  5. As analyses of developmental mechanisms extend to ever more species, it becomes important to understand not just what is conserved or altered during evolution, but why. Closely related species that exhibit extreme phenotypic divergence can be uniquely informative in this regard. A case in point is the sea urchin genus Heliocidaris, which contains species that recently evolved a life history involving nonfeeding larvae following nearly half a billion years of prior evolution with feeding larvae. The resulting shift in selective regimes produced rapid and surprisingly extensive changes in developmental mechanisms that are otherwise highly conserved among echinoderm species. The magnitude and extent of these changes challenges the notion that conservation of early development in echinoderms is largely due to internal constraints that prohibit modification and instead suggests that natural selection actively maintains stability of inherently malleable trait developmental mechanisms over immense time periods. Knowing how and why natural selection changed during the evolution of nonfeeding larvae can also reveal why developmental mechanisms do and do not change in particular ways. 
    more » « less