The developmental transcriptome for Lytechinus variegatus exhibits temporally punctuated gene expression changes

Abstract

Embryonic development is arguably the most complex process an organism undergoes during its lifetime, and understanding this complexity is best approached with a systems-level perspective. The sea urchin has become a highly valuable model organism for understanding developmental specification, morphogenesis, and evolution. As a non-chordate deuterostome, the sea urchin occupies an important evolutionary niche between protostomes and vertebrates. Lytechinus variegatus (Lv) is an Atlantic species that has been well studied, and which has provided important insights into signal transduction, patterning, and morphogenetic changes during embryonic and larval development. The Pacific species, Strongylocentrotus purpuratus (Sp), is another well-studied sea urchin, particularly for gene regulatory networks (GRNs) and cis-regulatory analyses. A well-annotated genome and transcriptome for Sp are available, but similar resources have not been developed for Lv. Here, we provide an analysis of the Lv transcriptome at 11 timepoints during embryonic and larval development. The data indicate that the gene regulatory networks that underlie specification are well-conserved among sea urchin species. We show that the major transitions in variation of embryonic transcription divide the developmental time series into four distinct, temporally sequential phases. Our work shows that sea urchin development occurs via sequential intervals of relatively stable gene expression states that are punctuated by abrupt transitions.

Derivedness Index for Estimating Degree of Phenotypic Evolution of Embryos: A Study of Comparative Transcriptomic Analyses of Chordates and Echinoderms

“…To tackle these problems, we propose a transcriptomic "derivedness index" to address the degree of phenotypic changes observed in embryos, inherited from a common ancestor. Specifically, we compared the gene expression profiles of echinoderms (Tu et al, 2012;Li et al, 2018Li et al, , 2020Hogan et al, 2020) and chordates (Wang et al, 2013;Hu et al, 2017) to test whether echinoderms are more highly derived than chordates.…”

V-type H+ ATPase Activity is Required for Embryonic Dorsal-Ventral Symmetry Breaking

“…VHA is a housekeeping gene that is generally ubiquitously expressed (Sun-Wada and Wada, 2015). Each of the VHA subunits was identified in the Lytechinus variegatus (Lv) transcriptome (Hogan et al, 2020) and found to be expressed at all timepoints with variable expression levels (Fig. S1B; Table S1).…”

“…Each data point represents a minimum of two biologically independent replicates (each in triplicate, for a minimum of 6 measurements). ∆CT values were normalized to LvSetmar expression (Hogan et al, 2020); ∆∆CT values were determined by comparison to controls. Primer sequences used were previously reported (Gildor and Ben-Tabou de-Leon, 2015;Schatzberg et al, 2015), except those for LvAtp6v0a1 (forward: 5'-GCTCCTGCTCCTAGGGAGAT-3' and reverse: 5'-TCTCCATCGTCCATCTCATC-3').…”

“…Sea urchins are basal deuterostomes, and as such, they occupy a key evolutionary position that provides insights into the evolution of chordates and vertebrates and their divergence from radiata and protostomes. As a premier model organism for gene regulatory network analysis that has been studied extensively for over 100 years, sea urchin embryos offer both a breadth of historical investigation and a depth of systemslevel and network analyses (Driesch, 1892;Horstadius, 1935;Davidson et al, 2002;Sodergren et al, 2006;Tu et al, 2014;Foster et al, 2020;Hogan et al, 2020;Li et al, 2020;Massri et al, 2021). In sea urchin embryos, DV specification is mediated by zygotic expression of the TGF-β ligand Nodal on one side of the embryo, which defines that side as ventral and leads to BMP gradient formation (Duboc et al, 2004;Bradham and McClay, 2007;Bradham et al, 2009;Lapraz et al, 2009;Su et al, 2009;Saudemont et al, 2010).…”

Are control of extracellular acid-base balance and regulation of skeleton genes linked to resistance to ocean acidification in adult sea urchins?

“…Therefore, the present study investigated the long-term acid-base physiology of individuals of both species living in or out the plume of a cold volcanic CO2 seep (Levante Bay, Vulcano Island, Sicily), together with the impact on the mechanical properties of their skeleton and the expression of biomineralization-related genes. Based on a number of Omic and functional genomic studies performed on several sea urchin species (Consortium, 2006;Hogan et al, 2019;Livingston et al, 2006;Oliveri et al, 2008), four target genes (p19, msp130 sm50, and can) with known roles in the biomineralization process of both embryos and adults, and a housekeeping gene (z12), were selected for investigate the expression profiles in the samples above described. Orthologous genes of P. lividus and A. lixula, known or, here, preliminary identified and validated, provided the molecular tools of both species for setting-up species-specific Real-Time qPCR assays performing the analyses of gene expression here reported (for sequences identification and experimental setting see S01).…”