The centipede Strigamia maritima possesses a large complement of Wnt genes with diverse expression patterns

Abstract

The genes of the Wnt family play important roles in the development of many animals. In the arthropods, these genes are known to have multiple functions, including roles in posterior development and segmentation. Despite this, secondary loss of Wnt genes is common among the Arthropoda. Unlike many arthropods, Strigamia maritima, a geophilomorph centipede, possesses a large complement of Wnt ligands, with 11 Wnt genes present. In this study, the expression of each of these genes was examined across a range of stages during embryonic development. The expression of Wnt genes in Strigamia displays much variability. Most Wnt genes are expressed in segmental stripes in the trunk; near the proctodeum; and in the head region. However, despite this overall broad similarity, there are many differences between the various Wnt genes in their exact patterns of expression. These data should be considered in the context of different hypotheses regarding the functional relationships between the Wnt genes and the degree of redundancy present in this system. The findings of this study are consistent with one particular model of Wnt activity, the combinatorial model, whereby the combination of Wnt ligands present in a particular region defines its identity. These findings should also be useful in attempts to reconstruct the evolutionary history of Wnt signaling in arthropods.

Myriapoda

“…The genes Wnt5 , Wnt6, and Wnt10 in Strigamia according to Hayden and Arthur ( 2014 ) as well as the genes Wnt5 , Wnt6 , and Wnt16 in Glomeris according to and Janssen and Posnien ( 2014 ) appear to have comparable expression with wg , in the shape of transversal stripes mostly in the middle of each segment. They briefl y anticipate the appearance of the morphological segment, suggesting a possible role in segment formation.…”

“…Myriapods have a rather ancestral array of Wnt genes, having 11 out of the 12 ancestral arthropod Wnt . wg/Wnt1 , Wnt2 , Wnt 4-7 , Wnt9 , Wnt11 , and WntA are present in both studied myriapods, but Wnt8 is present only in Glomeris and Wnt10 only in Strigamia (Janssen et al 2004Hayden and Arthur 2014 ;Janssen and Posnien 2014 ). They almost all show a reiterated expression along the AP axis, mostly related to what may be mesodermal somites -although published works do not mention mesodermal expression.…”

“…Although in myriapods the fi rst appearing furrows are properly segmental (Hughes and Kaufman 2002b ;Chipman et al 2004a ) and not parasegmental as in Drosophila (Martinez-Arias and Lawrence 1985 ), in Lithobius (Hughes and Kaufman 2002b ), Strigamia (Chipman et al 2004a ;Hayden and Arthur 2014 ), and Glomeris , the expression patterns of en and wg and in Glomeris also of hh and ci (Janssen et al 2004 ) are very similar to Drosophila and other arthropods (e.g., Patel et al 1989 ;Martinez-Arias 1993 ;Nagy and Carroll 1994 ;Niwa et al 2000 ;Damen 2002 ). Transcripts of en and hh colocalise to posterior cells of each segment, whereas wg and ci are expressed in anteriorly adjacent cells, demonstrating the conservation of the parasegment boundary across arthropods (see below for peculiarity of dorsal patterning in diplopods).…”

“…6.9B and 6.14F ; Steinmetz et al 2010 ;Janssen et al 2011a ;Hunnekuhl 2013 ), dpp and hedgehog ( HH ) (Prpic 2004 ;Janssen 2012 ;Hunnekuhl 2013 ;C. Brena, unpublished data), dachshund , and homothorax (Prpic and Tautz 2003 ) and several Wnt genes (Janssen et al 2004Hayden and Arthur 2014 ;Janssen and Posnien 2014 ).…”

“…Early limb determinants are the morphogens dpp and Wnt , which are involved in determining the early gradients activating downstream limb genes: dpp is expressed in all limb buds in Glomeris (Prpic 2004 ) and Lithobius and Strigamia (C. Brena, unpublished data), and several Wnt genes are there expressed as well in Glomeris (Prpic 2004 ;Janssen and Posnien 2014 ) and Strigamia (Hayden and Arthur 2014 ), where they could operate in a redundant and/or in a combinatorial way, as they do in other arthropods (see discussion in Janssen and Posnien 2014 ). In particular, some of them, like Wnt5 in Glomeris , may be involved in limb dorso-(ventral) patterning, as are probably the dpp and the optomotor blind genes, in a conserved way as in Drosophila , while the role of H15 in ventral patterning is not as strongly supported by its expression (Prpic 2004 ;Prpic et al 2005 ;Janssen and Posnien 2014 ).…”