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.
Highlights
Brachiopods undergo radial cleavage, which is distinct from the stereotyped development of closely related spiralian taxa
Phylogenetic analysis and orthology assignment Full-length or partial complementary DNA (cDNA) sequences were isolated from T. transversa for putative homologs of the transcription factor genes Forkhead C (FoxC), Forkhead D (FoxD), Forkhead F (FoxF), GATA4/5/6, MEF2, Mox, mesoPrx, MyoD, NK1, paraxis, Pax1/9, Six1/2, and twist, the nuclear protein genes dachshund, eyes absent, and Limpet, and the BMP inhibitor gene noggin
Whole-mount in situ expression patterns Mesodermal expression was observed for all 17 genes listed above, and representative photomicrographs of the radial gastrula, asymmetric gastrula, early larval, and late larval stages are presented (Figures 2, 3, 4, 5, 6, 7, 8, and 9)
Summary
Brachiopods undergo radial cleavage, which is distinct from the stereotyped development of closely related spiralian taxa. Mesoderm formation has been studied in detail in these and other model systems, comparatively little is known about mesoderm specification and differentiation in members of the large protostome clade Spiralia [17,18] This clade is defined as including all descendents from the last common ancestor of animals with quartet spiral cleavage (that is, mollusks, annelids, nemerteans, and platyhelminths) and is likely more inclusive than, or a senior synonym of, the clade termed Lophotrochozoa [19,20]. Almost all taxa that display spiral cleavage form visceral mesoderm from a homologous blastomere in the early cleavage stages termed micromere 4d or the mesentoblast [23] In addition to this mesendodermal component of the mesoderm, many spiral cleaving embryos develop mesoderm from ectodermal sources [24,25]
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