Abstract
BackgroundWnt signaling pathways are highly conserved signal transduction pathways important for axis formation, cell fate specification, and organogenesis throughout metazoan development. Within the various Wnt pathways, the frizzled transmembrane receptors (Fzs) and secreted frizzled-related proteins (sFRPs) play central roles in receiving and antagonizing Wnt signals, respectively. Despite their importance, very little is known about the frizzled-related gene family (fzs & sfrps) in lophotrochozoans, especially during early stages of spiralian development. Here we ascertain the frizzled-related gene complement in six lophotrochozoan species, and determine their spatial and temporal expression pattern during early embryogenesis and larval stages of the marine annelid Platynereis dumerilii.ResultsPhylogenetic analyses confirm conserved homologs for four frizzled receptors (Fz1/2/7, Fz4, Fz5/8, Fz9/10) and sFRP1/2/5 in five of six lophotrochozoan species. The sfrp3/4 gene is conserved in one, divergent in two, and evidently lost in three lophotrochozoan species. Three novel fz-related genes (fzCRD1-3) are unique to Platynereis. Transcriptional profiling and in situ hybridization identified high maternal expression of fz1/2/7, expression of fz9/10 and fz1/2/7 within animal and dorsal cell lineages after the 32-cell stage, localization of fz5/8, sfrp1/2/5, and fzCRD-1 to animal-pole cell lineages after the 80-cell stage, and no expression for fz4, sfrp3/4, and fzCRD-2, and -3 in early Platynereis embryos. In later larval stages, all frizzled-related genes are expressed in distinct patterns preferentially in the anterior hemisphere and less in the developing trunk.ConclusionsLophotrochozoans have retained a generally conserved ancestral bilaterian frizzled-related gene complement (four Fzs and two sFRPs). Maternal expression of fz1/2/7, and animal lineage-specific expression of fz5/8 and sfrp1/2/5 in early embryos of Platynereis suggest evolutionary conserved roles of these genes to perform Wnt pathway functions during early cleavage stages, and the early establishment of a Wnt inhibitory center at the animal pole, respectively. Numerous frizzled receptor-expressing cells and embryonic territories were identified that might indicate competence to receive Wnt signals during annelid development. An anterior bias for frizzled-related gene expression in embryos and larvae might point to a polarity of Wnt patterning systems along the anterior–posterior axis of this annelid.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0032-4) contains supplementary material, which is available to authorized users.
Highlights
Wnt signaling pathways are highly conserved signal transduction pathways important for axis forma‐ tion, cell fate specification, and organogenesis throughout metazoan development
In addition to frizzled receptors, a second class of frizzled family genes, the secreted frizzledrelated proteins, have been identified as modifiers of Wnt signaling. These sFRPs consist of an N-terminal cysteine-rich domain (CRD) that is evolutionarily related to the CRD of frizzled receptors, and a C-terminal Netrin domain [14, 15]. sFRPs are thought to inhibit Wnt signaling by competitively binding Wnt ligands [16]
De novo transcriptome assembly using Trinity software [56] and subsequent annotation by various Basic Local Alignment Search Tool (BLAST)-based bioinformatics pipelines identified nine gene models encoding Fz-related cysteine-rich domains (CRDs). These gene models corresponded to four frizzled transmembrane receptors, two sfrps, and three novel frizzled-related genes coding for proteins consisting of a frizzled-like CRD domain only, named Frizzled-related CRD 1, 2, and 3 (FzCRD-1, -2, -3)
Summary
Wnt signaling pathways are highly conserved signal transduction pathways important for axis forma‐ tion, cell fate specification, and organogenesis throughout metazoan development. Within the various Wnt pathways, the frizzled transmembrane receptors (Fzs) and secreted frizzled-related proteins (sFRPs) play central roles in receiving and antagonizing Wnt signals, respectively Despite their importance, very little is known about the frizzled-related gene family (fzs & sfrps) in lophotrochozoans, especially during early stages of spiralian development. First identified in Drosophila melanogaster as factors involved in planar cell polarity [13], are 7-pass transmembrane receptors with an extracellular cysteine-rich domain (CRD) that binds secreted Wnt ligands. This Wnt ligandfrizzled receptor interaction activates the Wnt pathway by transmitting the signal via structural changes to the receptor’s cytoplasmic domain. These sFRPs consist of an N-terminal CRD that is evolutionarily related to the CRD of frizzled receptors, and a C-terminal Netrin domain [14, 15]. sFRPs are thought to inhibit Wnt signaling by competitively binding Wnt ligands [16]
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