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

John D Hogan,Jessica L Keenan,Lingqi Luo,Jonas Ibn-Salem,Arjun Lamba,Daphne Schatzberg,Michael L Piacentino,Daniel T Zuch,Amanda B Core,Carolyn Blumberg,Bernd Timmermann,José Horacio Grau,Emily Speranza,Miguel A Andrade-Navarro,Naoki Irie,Albert J Poustka,Cynthia A Bradham

doi:10.1016/j.ydbio.2019.12.002

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. Temporal analysis suggests 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.

Highlights

This study presents the developmental transcriptome for the sea urchin L. variegatus at 11 timepoints during embryonic and larval development, and provides an online database of the sequences along with annotation, Gene Ontology (GO), Pfam, and BLAST information, which we anticipate will be an important resource for the sea urchin community and a foundation for subsequent systems-level efforts, such as tissue-specific sequencing and proteomics
Vegetal/posterior cells become elongated at thickened vegetal plate stage (TVP), prior to the ingression of the skeletogenic primary mesenchyme cells (PMCs, Fig. 1A red) at mesenchyme blastula (MB) stage (Miller and McClay, 1997; Wu et al, 2007)
The PMCs secrete skeletal triradiates that are visible at late gastrula (LG) (Fig. 1A, yellow), and undergo substantial growth between LG and early pluteus (EP) stages (Wolpert and Gustafson, 1961)

Summary

Introduction

Only about half of the gene complement of sea urchins is expressed by the developing embryo, approximately 90% of the signaling ligands, kinases, small GTPases, and transcription factors are expressed during development (Beane et al, 2006b; Bradham et al, 2006; Croce et al, 2006b; Howard-Ashby et al, 2006a; Howard-Ashby et al, 2006b; Lapraz et al, 2006; Materna et al, 2006; Samanta et al, 2006; Sodergren et al, 2006; Walton et al, 2006). Work in more recent decades has uncovered many of the important signals and transcription factors that drive specification and development in these embryos (Logan et al, 1999; Sherwood and McClay, 1999; Angerer et al, 2000; Angerer et al, 2001; Sweet et al, 2002; Oliveri et al, 2003; Bradham et al, 2004; Duboc et al, 2004; Rottinger et al, 2004; Wikramanayake et al, 2004; Duboc et al, 2005; Bradham and McClay, 2006; Oliveri et al, 2006; Duloquin et al, 2007; Duboc et al, 2008; Rottinger et al, 2008; Yaguchi et al, 2008; Bradham et al, 2009; Lapraz et al, 2009; Sethi et al, 2009; Walton et al, 2009; Wei et al, 2009; Yaguchi et al, 2010; Luo and Su, 2012; Sethi et al, 2012; Materna et al, 2013b; McIntyre et al, 2013; Range et al, 2013; Krupke and Burke, 2014; Khadka et al, 2018). The availability of GRN models and global sequence resources has enabled evolutionary, comparative, and population studies at the molecular and network level (Hinman et al, 2003; Gao and Davidson, 2008; Garfield et al, 2013; Wygoda et al, 2014; Erkenbrack et al, 2018)

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