Co-option of an oral-aboral patterning mechanism to control left-right differentiation: the direct-developing sea urchin Heliocidaris erythrogramma is sinistralized, not ventralized, by NiCl2.
Larval dorsoventral (DV) and left-right (LR) axial patterning unfold progressively in sea urchin development, leading to commitment of the major embryonic regions by the gastrula stage. The direct-developing sea urchin Heliocidaris erythrogramma has lost oral-aboral differentiation along the DV axis but has accelerated vestibular ectoderm development on the left side. NiCl(2) radializes indirect-developing sea urchins by shifting cells toward a ventral fate (oral ectoderm). We treated embryos of H. erythrogramma and the indirect-developing H. tuberculata with NiCl(2). H. tuberculata was ventralized exactly like other indirect developers, establishing that basic patterning mechanisms are conserved in this genus. H. erythrogramma was also radialized; timing, dosage response, and some morphological features were similar to those in other sea urchins. Ectodermal explant and recombination experiments demonstrate that the effect of nickel is autonomous to the ectoderm, another feature in common with indirect developers. However, H. erythrogramma is distinctly sinistralized rather than ventralized, its cells shifting toward a left-side fate (vestibular ectoderm). This geometric contrast in the midst of pervasive functional similarity suggests that nickel-sensitive processes in H. erythrogramma axial patterning, homologous to those in indirect developers, have been redeployed, and hence co-opted, from their ancestral role in DV axis determination to a new role in LR axis determination. We discuss DV and LR axial patterning and their evolutionary transformation.
Minsuk
Sharon B
SB
Department of Biology, Indiana Molecular Biology Institute, Indiana University, Bloomington, IN 47405, USA. sharon.minsuk@kli.ac.at
Raff
Rudolf A
RA
D000818:Animals; D019521:Body Patterning / Q000502:physiology*; D002454:Cell Differentiation; D002455:Cell Division; D002478:Cells, Cultured; D004625:Embryo, Nonmammalian / Q000187:drug effects / Q000196:embryology* / Q000378:metabolism; D005775:Gastrula / Q000166:cytology / Q000187:drug effects; D007814:Larva / Q000187:drug effects / Q000254:growth & development; D009532:Nickel / Q000633:toxicity*; D012617:Sea Urchins / Q000196:embryology*
C022838:nickel chloride; D009532:Nickel