Deployment of a retinal determination gene network drives directed cell migration in the sea urchin embryo

Abstract

Gene regulatory networks (GRNs) provide a systems-level orchestration of an organism's genome encoded anatomy. As biological networks are revealed, they continue to answer many questions including knowledge of how GRNs control morphogenetic movements and how GRNs evolve. The migration of the small micromeres to the coelomic pouches in the sea urchin embryo provides an exceptional model for understanding the genomic regulatory control of morphogenesis. An assay using the robust homing potential of these cells reveals a ‘coherent feed-forward’ transcriptional subcircuit composed of Pax6, Six3, Six1/2, Eya, and Dach1 that is responsible for the directed homing mechanism of these multipotent progenitors. The linkages of that circuit are strikingly similar to a circuit involved in retinal specification in Drosophila suggesting that systems-level tasks can be highly conserved even though the tasks drive unrelated processes in different animals.DOI: http://dx.doi.org/10.7554/eLife.08827.001

Expression of genes and proteins of the pax‐six‐eya‐dach network in the metamorphic sea urchin: Insights into development of the enigmatic echinoderm body plan and sensory structures

“…The functional studies that show perturbing the PSEDN in early embryos inhibits coelomic pouch development (Martik and McClay, ) and reduces expression of all of these genes in the left coelom (Luo and Su, ) further support a role for the PSEDN in pentamery. Further gene function analyses are required to determine outcomes for hydrocoele formation.…”

“…There is increasing appreciation that GRNs, highly conserved across the Metazoa, can provide a framework to investigate evolution of development in their context‐specific interactions (Davidson and Erwin, ; Arnone et al, , ; Israel et al, ). For the sea urchin, the PSEDN has been shown to be involved in small micromere cell migration (Martik and McClay, ), and its constituent genes are expressed in the left coelomic pouch (Luo and Su, ), the structure that gives rise to the five hydrocoele lobes that form the pentameral echinoderm body plan (Morris et al, ; Morris, ; Smith et al, ). Here we show that in the metamorphic sea urchin PSEDN genes are expressed in early (40 hr) ( Dach , Eya , Six1/2 ) and/or in late (96 hr) ( Pax6 , Six3/6 ) larvae, notably in the five hydrocoele lobes, supporting a role for this GRN in the development of pentamery.…”

“…The presence of some of these genes in sensory cells in sponges suggests that the Pax‐Six‐Eya part of this network is ancient (Fortunato et al, ). The PSEDN is a highly conserved gene unit that has been redeployed over evolutionary time for several roles including embryonic cell migration in sea urchins and placode and muscle development in vertebrates (Heanue et al, ; Relaix and Buckingham, ; Donner and Maas, ; Silver and Rebay, : Kozmik et al, ; Martik and McClay, ). It is suggested to function as a sub‐circuit within larger GRNs (Treisman, ; Bebenek et al, ; Colosimo et al, ; Kozmik, ; Mazet et al, ).…”

Methods to label, isolate, and image sea urchin small micromeres, the primordial germ cells (PGCs)

“…After gastrulation the small micromeres migrate into the coelomic pouches (Campanale et al, 2014) in a characteristic 5 left-3 right pattern that seems to be controlled by a gene regulatory network that produces these asymmetrical distributions (Luo & Su, 2012; Martik & McClay, 2015). …”

The Developmental Transcriptome forLytechinus variegatusExhibits Temporally Punctuated Gene Expression Changes

“…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). This work has culminated in gene regulatory network (GRN) models that describe the specification of the endomesoderm and the ectoderm Su et al, 2009;Saudemont et al, 2010;Peter and Davidson, 2011;Rafiq et al, 2012;Materna et al, 2013a;Li et al, 2014), and more recently, efforts have been made to connect the specification networks to morphogenesis (Annunziata and Arnone, 2014; Saunders and McClay, 2014;Martik and McClay, 2015). Sea urchins are nonchordate deuterostomes, and as such, they occu...…”