Gene expression patterns in a novel animal appendage: the sea urchin pluteus arm

Abstract

The larval arms of echinoid plutei are used for locomotion and feeding. They are composed of internal calcite skeletal rods covered by an ectoderm layer bearing a ciliary band. Skeletogenesis includes an autonomous molecular differentiation program in primary mesenchyme cells (PMCs), initiated when PMCs leave the vegetal plate for the blastocoel, and a patterning of the differentiated skeletal units that requires molecular cues from the overlaying ectoderm. The arms represent a larval feature that arose in the echinoid lineage during the Paleozoic and offers a subject for the study of gene co-option in the evolution of novel larval features. We isolated new molecular markers in two closely related but differently developing species, Heliocidaris tuberculata and Heliocidaris erythrogramma. We report the expression of a larval arm-associated ectoderm gene tetraspanin, as well as two new PMC markers, advillin and carbonic anhydrase. Tetraspanin localizes to the animal half of blastula stage H. tuberculata and then undergoes a restriction into the putative oral ectoderm and future location of the postoral arms, where it continues to be expressed at the leading edge of both the postoral and anterolateral arms. In H. erythrogramma, its expression initiates in the animal half of blastulae and expands over the entire ectoderm from gastrulation onward. Advillin and carbonic anhydrase are upregulated in the PMCs postgastrulation and localized to the leading edge of the growing larval arms of H. tuberculata but do not exhibit coordinated expression in H. erythrogramma larvae. The tight spatiotemporal regulation of these genes in H. tuberculata along with other ontogenetic and phylogenetic evidence suggest that pluteus arms are novel larval organs, distinguishable from the processes of skeletogenesis per se. The dissociation of expression control in H. erythrogramma suggest that coordinate gene expression in H. tuberculata evolved as part of the evolution of pluteus arms, and is not required for larval or adult development.

Evolution and Function of acis-Regulatory Module for Mesophyll-Specific Gene Expression in the C4 DicotFlaveria trinervia

“…Changes in the expression of a particular gene can result from alterations either in its cis-regulatory sequences or in the deployment and function of the transcription factors that control gene expression, or both (Love et al, 2007). Evolutionary biologists have collected convincing evidence that supports the view that changes in the spatiotemporal expression patterns of genes are a principal mechanism for the evolution of novelty, both in morphological and biochemical traits (Doebley and Lukens, 1998).…”

The conserved genetic background for pluteus arm development in brittle stars and sea urchin

“…Postoral arms are defined as the bilateral subregions within the boundary ectoderm (BE), adjacent to the endoderm, on either side of the larva (McIntyre et al 2013(McIntyre et al , 2014. Expression of vascular endothelial growth factor (vegf), fibroblast growth factor A, (fgfA), wnt5, strim1, and tet also mark the postoral arm domain (Duloquin et al 2007;Love et al 2007;R€ ottinger et al 2008;Cavalieri et al 2011;McIntyre et al 2013). TGF-b signals along the oral-aboral axis refine the postoral arm domain into the bilateral small regions (McIntyre et al 2013(McIntyre et al , 2014.…”

What Genes and Genomes Tell us about Calcium Carbonate Biomineralization

“…Only three of them are found in the PMC EST database and one of them is especially prevalent; it has a consensus signal sequence and a C-terminal glycolipid anchor, suggesting that it is an extracellular enzyme. It is an ortholog to the carbonic anhydrase cDNAs cloned by Love et al [76] in Heliocidaris tuberculata and H. erythrogramma, and it is the same gene that was partially cloned from Strongylocentrotus purpuratus. Livingston et al [32] used in situ hybridization analysis to demonstrate that this carbonic anhydrase gene (SPU_012518) is expressed only in PMCs in S. purpuratus embryos.…”

“…They also showed that this same gene is expressed in adult spines. In addition, Love et al [76] show that this gene is specifically expressed by the PMCs at the leading edge of the lengthening spicule in Heliocidaris species. Given its expression pattern, this carbonic anhydrase gene seems very likely to be playing an important role in sea urchin biomineralization.…”