Evolutionary Dynamics of the wnt Gene Family: A Lophotrochozoan Perspective

Abstract

The wnt gene family encodes a set of secreted glycoproteins involved in key developmental processes, including cell fate specification and regulation of posterior growth (Cadigan KM, Nusse R. 1997 . To obtain a more comprehensive scenario of the evolutionary dynamics of this gene family, we exhaustively mined wnt gene sequences from the whole genome assemblies of a mollusk (Lottia gigantea) and two annelids (Capitella teleta and Helobdella robusta) and examined them by phylogenetic, genetic linkage, intron-exon structure, and embryonic expression analyses. The 36 wnt genes obtained represent 11, 12, and 9 distinct wnt subfamilies in Lottia, Capitella, and Helobdella, respectively. Thus, two of the three analyzed lophotrochozoan genomes retained an almost complete ancestral complement of wnt genes emphasizing the importance and complexity of this gene family across metazoans. The genome of the leech Helobdella reflects significantly more dynamism than those of Lottia and Capitella, as judged by gene duplications and losses, branch length, and changes in genetic linkage. Finally, we performed a detailed expression analysis for all the Helobdella wnt genes during embryonic development. We find that, although the patterns show substantial overlap during early cleavage stages, each wnt gene has a unique expression pattern in the germinal plate and during tissue morphogenesis. Comparisons of the embryonic expression patterns of the duplicated wnt genes in Helobdella with their orthologs in Capitella reveal extensive regulatory diversification of the duplicated leech wnt genes.

The Evolution of the Wnt Pathway

“…Lottia gigantea shows a similar organization of these Wnt genes and therefore reflects the ancient cluster of Wnt genes in eumetazoans (Nusse 2001;Sullivan et al 2007;Cho et al 2010;Janssen et al 2010). These two Wnt clusters are also supported by recent molecular phylogenies on Wnt genes (Cho et al 2010;Janssen et al 2010). How the interacting Wnt ligands are regulated is rather unknown so far, but it is tempting to speculate that there is a regulative hierarchy of Wnt gene expression similar to that described for Hydra (Nakamura et al 2011) or Drosophila (van de Wetering et al 1997Lessing and Nusse 1998).…”

“…This indicates that basal protostomes also had an almost complete set of Wnt genes (Cho et al 2010). Other annelids and mollusks have lost several Wnt gene subfamilies, that is, Wnt8, -9, and -A in Helobdella robusta or Wnt4, -5, -6, -7, -8, -9, -11, and -16 in Patella vulgata (Prud'homme et al 2002;Cho et al 2010;Janssen et al 2010;Riddiford and Olson 2011). The Wnt genes of P. dumerilii show blastoporal and posterior expression in the growth zone (segment addition zone) of trochophoran larvae, and at the posterior side of each segment (Janssen et al 2010), reminiscent to arthropods (see below).…”

“…New data on the arrangement of Wnt genes in the Daphnia genome revealed two syntenic clusters of these genes: Wnt9 -Wnt1 -Wnt6 -Wnt10 and Wnt5 -Wnt7 (Janssen et al 2010). Lottia gigantea shows a similar organization of these Wnt genes and therefore reflects the ancient cluster of Wnt genes in eumetazoans (Nusse 2001;Sullivan et al 2007;Cho et al 2010;Janssen et al 2010). These two Wnt clusters are also supported by recent molecular phylogenies on Wnt genes (Cho et al 2010;Janssen et al 2010).…”

“…Twelve Wnt subfamilies have been reported for annelids (Capitella teleta and Platynereis dumerlii), a major lophotrochozoan group. This indicates that basal protostomes also had an almost complete set of Wnt genes (Cho et al 2010). Other annelids and mollusks have lost several Wnt gene subfamilies, that is, Wnt8, -9, and -A in Helobdella robusta or Wnt4, -5, -6, -7, -8, -9, -11, and -16 in Patella vulgata (Prud'homme et al 2002;Cho et al 2010;Janssen et al 2010;Riddiford and Olson 2011).…”

“…Cho et al [2010], and Janssen et al [2010].) Note that there are more Wnts for a given species that are not clustered (see Table 1).…”