Diversification of the expression patterns and developmental functions of the dishevelled gene family during chordate evolution

Abstract

Dishevelled (Dvl) proteins are key transducers of Wnt signaling encoded by members of a multi-gene family in vertebrates. We report here the divergent, tissue-specific expression patterns for all three Dvl genes in Xenopus embryos, which contrast dramatically with their expression patterns in mice. Moreover, we find that the expression patterns of Dvl genes in the chick diverge significantly from those of Xenopus. In addition, in hemichordates, an outgroup to chordates, we find that the one Dvl gene is dynamically expressed in a tissue-specific manner. Using knockdowns, we find that Dvl1 and Dvl2 are required for early neural crest specification and for somite segmentation in Xenopus. Most strikingly, we report a novel role for Dvl3 in the maintenance of gene expression in muscle and in the development of the Xenopus sclerotome. These data demonstrate that the expression patterns and developmental functions of specific Dvl genes have diverged significantly during chordate evolution.

The evolution of somatostatin in vertebrates

“…For the TP53 gene family, one common ancestral gene has been identified in the unduplicated ancestor B. floridae (Putnam et al, 2008) and three TP53 gene family members have been found in most vertebrates (Yang et al, 2002;Nedelcu and Tan 2007). In a similar way, a single DVL ancestral gene has been identified in C. intestinalis and three DVL gene family members has been reported in vertebrates (Gray et al, 2009). These data could be interpreted to mean that one ancestral gene gave rise to four paralogs after 2R, but one gene has been lost after the second duplication.…”

Distinct functionality of dishevelled isoforms on Ca2+/calmodulin-dependent protein kinase 2 (CamKII) inXenopusgastrulation

“…This does not exclude overlapping functions in CE movements or other developmental processes in general, as reported for Dvl2 and Dvl3 in CE movements (Tadjuidje et al. , 2011) and for Dvl1 and Dvl2 in neural crest migration (Gray et al. , 2009), since these morphogenetic processes are regulated by multiple interacting Wnt pathways.…”

Wnt-dependent assembly of supermolecular Dishevelled-3-based complexes

“…Although the fly displays only a single Dishevelled protein (Dsh), higher-order species express several isoforms of Dvl. Mammalian cells express three isoforms, Dvl1, Dvl2, and Dvl3; each isoform is expressed at varying levels (Sussman et al, 1994;Klingensmith et al, 1996;Gray et al, 2009). Targeted gene disruptions performed in mice (Lijam et al, 1997;Hamblet et al, 2002;Etheridge et al, 2008) as well as knockdown and rescue protocols performed in mouse F9 cells (Lee et al, 2008) demonstrate that mammalian Dvl proteins are not truly 'redundant' with respect to function.…”