Mesodermal gene expression during the embryonic and larval development of the articulate brachiopod Terebratalia transversa

Abstract

BackgroundBrachiopods undergo radial cleavage, which is distinct from the stereotyped development of closely related spiralian taxa. The mesoderm has been inferred to derive from the archenteron walls following gastrulation, and the primary mesoderm derivative in the larva is a complex musculature. To investigate the specification and differentiation of the mesoderm in the articulate brachiopod Terebratalia transversa, we have identified orthologs of genes involved in mesoderm development in other taxa and investigated their spatial and temporal expression during the embryonic and larval development of T. transversa.ResultsOrthologs of 17 developmental regulatory genes with roles in the development of the mesoderm in other bilaterian animals were found to be expressed in the developing mesoderm of T. transversa. Five genes, Tt.twist, Tt.GATA456, Tt.dachshund, Tt.mPrx, and Tt.NK1, were found to have expression throughout the archenteron wall at the radial gastrula stage, shortly after the initiation of gastrulation. Three additional genes, Tt.Pax1/9, Tt.MyoD, and Tt.Six1/2, showed expression at this stage in only a portion of the archenteron wall. Tt.eya, Tt.FoxC, Tt.FoxF, Tt.Mox, Tt.paraxis, Tt.Limpet, and Tt.Mef2 all showed initial mesodermal expression during later gastrula or early larval stages. At the late larval stage, Tt.dachshund, Tt.Limpet, and Tt.Mef2 showed expression in nearly all mesoderm cells, while all other genes were localized to specific regions of the mesoderm. Tt.FoxD and Tt.noggin both showed expression in the ventral mesoderm at the larval stages, with gastrula expression patterns in the archenteron roof and blastopore lip, respectively.ConclusionsExpression analyses support conserved roles for developmental regulators in the specification and differentiation of the mesoderm during the development of T. transversa. Expression of multiple mesodermal factors in the archenteron wall during gastrulation supports previous morphological observations that this region gives rise to larval mesoderm. Localized expression domains during gastrulation and larval development evidence early regionalization of the mesoderm and provide a basis for hypotheses regarding the molecular regulation underlying the complex system of musculature observed in the larva.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0004-8) contains supplementary material, which is available to authorized users.

Cleavage modification did not alter blastomere fates during bryozoan evolution

“…This molecular map is similar not only to the typical spiral-cleaving embryos, but also to brachiopod embryos [87, 129], whose embryos have a much greater number of cells and no stereotypic cleavage pattern [164]. Thus, a single cell in the bryozoan embryo expressing gata456 might be homologous to a whole region of gata456 expression in the brachiopod embryo [87], as suggested by Hejnol [5].…”

Cell Proliferation Pattern and Twist Expression in an Aplacophoran Mollusk Argue Against Segmented Ancestry of Mollusca

“…Our results thus support the notion that the mollusks split off from a common ancestral annelid-mollusk lineage before segmentation was established. This reasoning is in line with data on twist expression in gastropods (Nederbragt et al, 2002;Perry et al, 2015) and other nonsegmented animals such as nemertines, brachiopods, and priapulids Passamaneck et al, 2015), as well as with data on the myo-and neurogenesis in polyplacophorans and solenogasters (Friedrich et al, 2002;Voronezhskaya et al, 2002;Wanninger and Haszprunar, 2002;Scherholz et al, 2013;Redl et al, 2014), which likewise do not show any sign of rudimentary segmentation during ontogeny.…”

Deployment of regulatory genes during gastrulation and germ layer specification in a model spiralian mollusc Crepidula

“…For example Notch/ Hes signaling is known to be involved in contact mediated cell specification in other systems (Drosophila, Greenwald, 1998;mammals, Kageyama and Ohtsuka, 1999). Likewise, twist expression has been noted later during the specification of anterior mesoderm in brachiopods (Passamaneck et al, 2015). Given the fact that little is known about the morphogenetic behavior of either source of mesoderm in spiralians, it will be very interesting to correlate gene expression and cell behavior in these animals as more detailed descriptions of their development become available.…”

“…Much effort has centered on deciphering the molecular basis for specifying distinct ectodermal, endodermal, and mesodermal germ layers during development and great progress has been made to understand germ layer specification in deuterostomes (e.g., echinoderms, chordates), ecdysozoans (e.g., fly, nematode), and cnidarians (Byrum and Martindale, 2004;Martindale et al, 2004;Magie et al, 2007;Sawyer et al, 2010;Gorfinkiel et al, 2011;Peter and Davidson, 2011;R€ ottinger et al, 2012;Solnica-Krezel and Sepich, 2012). In contrast, germ layer specification is not well understood in the Spiralia, a major branch of bilaterians (Boyle et al, 2014;Passamaneck et al, 2015). The Spiralia contains animals such as annelids, molluscs, brachiopods, phoronids, rotifers, among others, with diverse larval and adult body plans (Hejnol, 2010;Henry, 2014).…”