The organizing role of Wnt signaling pathway during arthropod posterior growth

Abstract

Wnt signaling pathways are recognized for having major roles in tissue patterning and cell proliferation. In the last years, remarkable progress has been made in elucidating the molecular and cellular mechanisms that underlie sequential segmentation and axial elongation in various arthropods, and the canonical Wnt pathway has emerged as an essential factor in these processes. Here we review, with a comparative perspective, the current evidence concerning the participation of this pathway during posterior growth, its degree of conservation among the different subphyla within Arthropoda and its relationship with the rest of the gene regulatory network involved. Furthermore, we discuss how this signaling pathway could regulate segmentation to establish this repetitive pattern and, at the same time, probably modulate different cellular processes precisely coupled to axial elongation. Based on the information collected, we suggest that this pathway plays an organizing role in the formation of the body segments through the regulation of the dynamic expression of segmentation genes, via controlling the caudal gene, at the posterior region of the embryo/larva, that is necessary for the correct sequential formation of body segments in most arthropods and possibly in their common segmented ancestor. On the other hand, there is insufficient evidence to link this pathway to axial elongation by controlling its main cellular processes, such as convergent extension and cell proliferation. However, conclusions are premature until more studies incorporating diverse arthropods are carried out.

Keywords: axial elongation; body segmentation; segment addition zone; signaling pathway; wnt signaling.

FIGURE 1

Updated repertoire and phylogenetic relationship of Wnt ligands among panarthropods. Insects are shown in purple rectangles (Dearden et al., 2006; Bolognesi et al., 2008a; Murat et al., 2010; Shigenobu et al., 2010; Yin et al., 2015; Ding et al., 2019; Holzem et al., 2019; Panfilio et al., 2019; Vosburg et al., 2020), crustaceans in pale blue (Janssen et al., 2010; Constantinou et al., 2016; Jaramillo et al., 2016; Kao et al., 2016; Du et al., 2018), myriapods in green (Janssen et al., 2010; Hayden and Arthur, 2014; Janssen and Posnien, 2014), chelicerates in yellow (Janssen et al., 2010; Pace et al., 2014; Posnien et al., 2014; Harper et al., 2021; Janssen et al., 2021; Janssen and Eriksson, 2022), onychophoran in brown (Hogvall et al., 2014) and tardigrades in red (Chavarria et al., 2021). An asterisk in the name indicates more organisms having the same repertoire. *B. mori also includes Bicyclus anynana, Amyelois transitella, Calycopis cecrops, Danaus plexippus, Heliconius melpomene, Operophtera brumata and Papilio xuthus. *P. tepidariorum includes Pholcus phalangioides and *P. amentata includes Marpissa muscosa and Stegodyphus dumicola. Filled and no-filled boxes represent the presence and the absence of the ligand, respectively. Dotted boxes represent the presence/absence of the ligand in doubt (genome not fully sequenced) and white/black numbers inside the boxes represent ligand numbers. The Wnt ligand family is indicated at the top as well as the total (To) number of ligand families. The source of the sequences (Ss) is showed as Genome (G), Transcriptome (T) or Proteome (P). Phylogenetic positions based on Koenemann et al., 2010, Misof et al., 2014, Giribet and Edgecombe, 2019, Lozano-Fernandez et al., 2019 and Ballesteros et al., 2022.

FIGURE 2

Representative expression patterns of Wnt ligands in panarthropods. Expression patterns of Wnt ligands in representative organisms of Insecta, Crustacea, Myriapoda, Chelicerata, Onychophora and Tardigrada. Each color represents one Wnt ligand as is indicated at the top. 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).

FIGURE 3

Wnt ligands expression domains within panarthropod germbands. Blues boxes represent the expression of the corresponding Wnt ligand in the posterior zone, red boxes indicate segmental expression, and white boxes show the absence of expression. Double red and blue boxes indicate Wnt ligand expression at the posterior zone and within segments. Insects are shown in purple rectangles, crustaceans in pale blue, myriapods in green, chelicerates in yellow, onychophoran in brown and tardigrades in red. The Wnt ligand families are indicated at the top, in gray boxes. D. melanogaster (Murat et al., 2010); B. anynana (Holzem et al., 2019); T. castaneum (Bolognesi et al., 2008a); T. platyurus (Constantinou et al., 2016); S. marítima (Hayden and Arthur, 2014); G. marginata (Janssen et al., 2010; Janssen and Posnien, 2014); chelicerates (Janssen et al., 2021; Janssen and Eriksson, 2022); E. kanangrensis (Hogvall et al., 2014); H. exemplaris (Chavarria et al., 2021).

FIGURE 4

Segmentation patterning phenotypes after Wnt signaling functional analysis. (M) Loss of segment boundaries. (T) Truncated embryo due to loss of abdominal segments. (N) No effect on the segmentation patterning. Down arrow indicates inhibition, up arrow indicates activation. cWnt indicates the full canonical pathway. An empty rectangle points out the absence of the corresponding functional studies in this organism. Insects are shown in purple rectangles (Miyawaki et al., 2004; Angelini and Kaufman, 2005; Bolognesi et al., 2008b; Chesebro et al., 2013; Liu et al., 2017; Nakao, 2018; Setton and Sharma, 2021); myriapods in green (Hayden et al., 2015); chelicerates in yellow (McGregor et al., 2008; Setton and Sharma, 2021).

FIGURE 5

Wnt pathway role on the segmentation gene network at the SAZ. Regulatory relationships of the Wnt signaling pathway with the Notch pathway, the caudal gene and the dynamic/oscillatory genes (belonging to the Notch pathway or to the Pair-Rule gene family) in the SAZ, based on current evidence in chelicerates (orange letters) and insects (purple letters). Genes with a dynamic/oscillatory behavior at the SAZ in different arthropods are shown at the bottom. C. salei (Cs); D. pulex (Dp); G. bimaculatus (Gb); O. fasciatus (Of); P. americana (Pa); P. tepidariorum (Pt); S. maritima (Sm); T. castaneum (Tc).