Expression of the wnt gene complement in a spiral-cleaving embryo and trochophore larva

Abstract

The highly conserved wnt gene family has roles in developmental processes ranging from axis formation to cell fate determination. The polychaete Platynereis dumerilii has retained 12 of the 13 ancient wnt subfamilies and is a good model system to study the roles of the wnt ligands in spiralian development. While it has been shown that Platynereis uses a global b-cateninmediated binary cell fate specification module in development, the early roles of the 12 wnt genes present in Platynereis are unknown. Transcriptional profiling by RNA-Seq during early development and whole-mount in situ hybridization of embryo and larval stages were used to determine the temporal and spatial regulation of the wnt complement in Platynereis. None of the 12 wnt transcripts were maternally provided at significant levels. In pregastrula embryos, zygotic wntA, wnt4, and wnt5 transcripts exhibited distinctive patterns of differential gene expression. In contrast, in trochophore larvae, all 12 wnt ligands were expressed and each had a distinct expression pattern. While three wnt ligands were expressed in early development, none were expressed in the right place for a widespread role in b-catenin-mediated binary specification in early Platynereis development. However, the expression patterns of the wnt ligands suggest the presence of numerous wnt signaling centers, with the most prominent being a bias for staggered posterior wnt expression in trochophore larvae. The similarity to wnt expression domains in cnidarians around the blastopore and the tail organizer in chordates supports a hypothesis of a common evolutionary origin of posterior organizing centers.

Spiralian model systems

“…This is in contrast with another annelid, Hydroides, where MAPK appears to be activated only in the 4d cell, though the function of MAPK in that system has not been determined (Lambert and Nagy, 2003). We are just beginning to understand the molecular level events that control the processes of cell fate and axis specification during spiralian development (see papers by Gharbiah et al, 2014, Pruitt et al, 2014 …”

β‐catenin‐driven binary cell fate decisions in animal development

“…Whether localized extracellular Wnt ligands and polarized intracellular cortical components also play a role is currently unknown. A recent analysis of the expression patterns of the Wnt ligands in the embryo of Platynereis revealed that none of them seem expressed in the right place at the right time to act as a global regulator of β‐catenin asymmetries, suggesting a possible Wnt ligand independent mechanism in this organism …”

Expression of vasa, piwi, and nanos during gametogenesis in Typosyllis antoni (Annelida, Syllidae)

“…(Irvine & Martindale, ), Helobdella sp. (Kourakis & Martindale, ; Kourakis et al, ), and Tubifex tubifex (Endo, Sakai, & Shimizu, ); the Wnt gene family, which has been studied in annelids in the context of body plan evolution (Cho, Vallès, Giani, Seaver, & Weisblat, ; Prud'homme, Lartillot, Balavoine, Adoutte, & Vervoort, ) and development (Demilly, Steinmetz, Gazave, Marchand, & Vervoort, ; Pruitt, Letcher, Chou, Bastin, & Schneider, ), particularly in relation to segmentation (Janssen et al, ; Prud'homme et al, ; Seaver & Kaneshige, ); and a set of genes used as putative stem‐cell markers in the germ line which includes, among others, vasa , piwi , and nanos (Ewen‐Campen, Schwager, & Extavour, ). Briefly, vasa encodes an ATP‐dependent RNA helicase that acts, among others, on nanos , which suppresses somatic differentiation, and piwi encodes a regulatory protein with RNase H endonuclease activity that plays an important role in cell stemness (Extavour & Akam, ; Gustafson & Wessel, ; Rebscher, ; van Wolfswinkel, ).…”

“…Nevertheless, other annelids have been also subjected to molecular developmental studies in order to address questions such as the development of body plans, the regeneration of lost parts, the differentiation of Primordial Germ Cells (PGCs), the establishment of gonads, and the proliferation of somatic tissues. Among the most widely investigated genes related to these questions are the Hox genes, for which whole-body expression patterns have been characterized for body plan evolution (Cho, Vallès, Giani, Seaver, & Weisblat, 2010;Prud'homme, Lartillot, Balavoine, Adoutte, & Vervoort, 2002) and development (Demilly, Steinmetz, Gazave, Marchand, & Vervoort, 2013;Pruitt, Letcher, Chou, Bastin, & Schneider, 2014), particularly in relation to segmentation (Janssen et al, 2010;Prud'homme et al, 2003;Seaver & Kaneshige, 2006); and a set of genes used as putative stem-cell markers in the germ line which includes, among others, vasa, piwi, and nanos (Ewen-Campen, Schwager, & Extavour, 2010). Briefly, vasa encodes an ATP-dependent RNA helicase that acts, among others, on nanos, which suppresses somatic differentiation, and piwi encodes a regulatory protein with RNase H endonuclease activity that plays an important role in cell stemness (Extavour & Akam, 2003;Gustafson & Wessel, 2010;Rebscher, 2014;van Wolfswinkel, 2014).…”