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

Abstract

Background: During gastrulation, endoderm and mesoderm are specified from a bipotential precursor (endomesoderm) that is argued to be homologous across bilaterians. Spiralians also generate mesoderm from ectodermal precursors (ectomesoderm), which arises near the blastopore. While a conserved gene regulatory network controls specification of endomesoderm in deuterostomes and ecdysozoans, little is known about genes controlling specification or behavior of either source of spiralian mesoderm or the digestive tract. Results: Using the mollusc Crepidula, we examined conserved regulatory factors and compared their expression to fate maps to score expression in the germ layers, blastopore lip, and digestive tract. Many genes were expressed in both ecto-and endomesoderm, but only five were expressed in ectomesoderm exclusively. The latter may contribute to epithelial-to-mesenchymal transition seen in ectomesoderm. Conclusions: We present the first comparison of genes expressed during spiralian gastrulation in the context of high-resolution fate maps. We found variation of genes expressed in the blastopore lip, mouth, and cells that will form the anus. Shared expression of many genes in both mesodermal sources suggests that components of the conserved endomesoderm program were either co-opted for ectomesoderm formation or that ecto-and endomesoderm are derived from a common mesodermal precursor that became subdivided into distinct domains during evolution.

Cleavage modification did not alter blastomere fates during bryozoan evolution

“…The anterior/foregut markers nk2.1 , foxa , and gsc are expressed in a region opposed to posterior/hindgut markers bra , cdx , evx , and wnt1 , which are generally restricted to the D quadrant. Transcripts of nk2.1 are restricted to the B quadrant in a comparable position, in relation to the cyphonautes anteroposterior axis, to the anterior/ventral expression found in other bilaterians [62, 71, 122, 129, 130]. In a similar fashion, transcripts of wnt1 , a gene commonly expressed at the posterior end of bilaterians [131–134], occur at the posterior region of the vegetal ectoderm of M. membranacea (see also Additional file 18: Table S2 for a comparison of spiralian-specific gene expression patterns).…”

“…six3/6 and dlx are expressed at the animal end, while otx is expressed in the vegetal-most progeny of the first quartet. Other spiralian embryos display a similar arrangement of these transcripts [63, 68, 69, 71, 117–122] (Additional file 18: Table S2). Therefore, the region derived from the first quartet of M. membranacea match the pretroch region of spiral-cleaving embryos.…”

Brain regionalization genes are co-opted into shell field patterning in Mollusca

“…Pax2/5/8 and Otx are both expressed in the region of the developing cerebral ganglia in solenogasters 31 (Redl et al ., unpublished results). In the gastropod Crepidula fornicata Otx is expressed in the anterior CNS of trochophore and veliger larvae 40 , in contrast to trochophore larvae of the patellogastropod Patella vulgata that lack Otx -expression in this region 41 . As in other bilaterians Six3/6 is expressed in the anteriormost region of the CNS in gastropods, cephalopods, polyplacophorans, and solenogasters 13, 28, 40 (Redl et al ., unpublished results).…”

Early Activation of MAPK and Apoptosis in Nutritive Embryos of Calyptraeid Gastropods

“…The patterns of MAPK activation in C. navicella and C. lichen are more variable than previously reported for C. fornicata (Henry and Perry, ) and other spiralians (see next). Development of C. fornicata has been well characterized (Conklin, , Henry et al., , Hejnol et al., , Lyons et al., , Lyons et al., , Perry et al., ), and all embryos develop into normal veliger larvae. In contrast, more than 90% of embryos produced by C. navicella will become nutritive embryos (Lesoway et al., ).…”