A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning

Abstract

The Wnt genes represent a large family of secreted glycoprotein ligands that date back to early animal evolution. Multiple duplication events generated a set of 13 Wnt families of which 12 are preserved in protostomes. Embryonic Wnt expression patterns (Wnt-patterning) are complex, representing the plentitude of functions these genes play during development. Here, we comprehensively investigated the embryonic expression patterns of Wnt genes from three species of spiders covering both main groups of true spiders, Haplogynae and Entelegynae, a mygalomorph species (tarantula), as well as a distantly related chelicerate outgroup species, the harvestman Phalangium opilio. All spiders possess the same ten classes of Wnt genes, but retained partially different sets of duplicated Wnt genes after whole genome duplication, some of which representing impressive examples of sub- and neo-functionalization. The harvestman, however, possesses a more complete set of 11 Wnt genes but with no duplicates. Our comprehensive data-analysis suggests a high degree of complexity and evolutionary flexibility of Wnt-patterning likely providing a firm network of mutational protection. We discuss the new data on Wnt gene expression in terms of their potential function in segmentation, posterior elongation, and appendage development and critically review previous research on these topics. We conclude that earlier research may have suffered from the absence of comprehensive gene expression data leading to partial misconceptions about the roles of Wnt genes in development and evolution.

Regulation of Eye Determination and Regionalization in the Spider Parasteatoda tepidariorum

“…Theoretically, differences in the size and position of spider eyes could be achieved through changes in Wnt gene expression patterns. Consistent with this, evidence of divergence in Wnt gene expression was found in a recent study of three species of spiders, including P. tepidariorum [ 58 ]. Furthermore, the regulation of each eye type appears to be mechanistically different, reminiscent of D. melanogaster ( Figure 9 ).…”

An atlas of spider development at single-cell resolution provides new insights into arthropod embryogenesis

“…Given the wealth of genes previously known to be expressed in the SAZ and involved in posterior segmentation, we first examined whether they were markers of these two clusters. We found that Wnt8 [g19404], Wnt11b-2 [aug3.g1356], hh , even-skipped ( eve ) [g21109], runt [g18815], noto1 [g13049], bcl11 [g25539], were all markers of cluster 3 (Fig 5A, 5B) [38, 41, 42, 44, 50, 79]. We also repeated ISH for markers AP2 [aug3.g23531] and g30822 [aug3.g27670] and corroborated their expression in the SAZ (Fig 5C, S9 Fig) [44].…”

The organizing role of Wnt signaling pathway during arthropod posterior growth

“…The spatiotemporal analysis of wnt genes expression in the beetle Tribolium castaneum showed that several ligands overlap in the posterior zone, segments/parasegments, and head lobes, suggesting functional redundancy (Bolognesi et al, 2008a). However, when we compiled wnt genes expression patterns including the other panarthropods (Janssen et al, 2010;Hogvall et al, 2014;Janssen and Posnien, 2014;Constantinou et al, 2016;Holzem et al, 2019;Chavarria et al, 2021;Janssen et al, 2021), we found that overlapping is common, although diverse patterns are still observed (Figure 2). Based on the degree of patterning conservation, we were able to classify the expression of Wnt ligands as highly (Wnt1, Wnt5, Wnt6, Wnt7, and Wnt11), moderately (Wnt8, Wnt10, Wnt16, and WntA), and poorly (Wnt2, Wnt4, and Wnt9) conserved, which might suggest that the function of some of these ligands-and not others-would be essential for posterior growth in most panarthropods.…”

“…The Wnt7 ligand in P. tepidariorum presents duplication, therefore double expression is shown in the scheme (Wnt7.1 is pale brown in the posterior, Wnt7.2 is dark brown in the head). T. castaneum (Bolognesi et al, 2008a); T. platyurus (Constantinou et al, 2016); G. marginata (Janssen et al, 2010;Janssen and Posnien, 2014); P. opilio (Janssen et al, 2021); P. tepidariorum (Janssen et al, 2010;Janssen et al, 2021); E. kanangrensis (Hogvall et al, 2014); H. exemplaris (Chavarria et al, 2021).…”

“…Frontiers in Cell and Developmental Biology frontiersin.org hindgut of Parasteatoda-without expression in the SAZ-and in the SAZ of Pholcus and Phalangium, with no expression in the hindgut primordium (Janssen et al, 2021). Specialized functions for wnt1 and wnt5 are suggested by their expression patterns within the posterior region of the Tribolium germband (Nagy and Carroll 1994;Bolognesi et al, 2008a).…”