The roles of wingless and decapentaplegic in axis and appendage development in the red flour beetle, Tribolium castaneum

Abstract

Axis patterning and appendage development have been well studied in Drosophila melanogaster, a species in which both limb and segment morphogenesis are derived. In Drosophila, positional information from genes important in anteroposterior and dorsoventral axis formation, including wingless (wg) and decapentaplegic (dpp), is required for allocating and patterning the appendage primordia. We used RNA interference to characterize the functions of wg and dpp in the red flour beetle, Tribolium castaneum, which retains more ancestral modes of limb and segment morphogenesis. We also characterized the expression of potential targets of the WG and DPP signaling pathways in these embryos. Tribolium embryos in which dpp had been downregulated had defects in the dorsalmost body wall, but did not appear to have been globally repatterned and had normal appendages. Downregulation of wg led to the loss of segment boundaries, gnathal and thoracic appendages, and lateral head lobes, and to changes in the expression of dpp, Distal-less, and Engrailed. The functions of wg varied along both the anteroposterior and dorsoventral axes of the embryo. Phylogenetic comparisons indicate that the role of WNT signaling in segment boundary formation is evolutionarily old, but that its role in appendage allocation originated in the common ancestor of holometabolous insects.

Hexapoda: Comparative Aspects of Later Embryogenesis and Metamorphosis

“…In Tribolium , wg RNAi leads to complete loss of legs during embryogenesis (Ober and Jockusch 2006 ;Grossmann et al 2009 ). Additional appendagepatterning functions of Wg signaling are also conserved in Tribolium , including regulation of PD axis development and ventral patterning (Grossmann et al 2009 ).…”

“…In Oncopeltus , strong defects in early embryogenesis prevented diagnosis of later functions (Angelini and Kaufman 2005 ). Tribolium embryos in which dpp transcripts are almost undetectable by in situ hybridization form normal appendages (Ober and Jockusch 2006 ). However, these specimens were generated by maternal RNAi, and earlier functions of dpp are required for fertility as well as DV axis patterning (van der Zee et al 2006 ), indicating that these embryos must have retained some dpp function during early embryogenesis.…”

A context-dependent combination of Wnt receptors controls axis elongation and leg development in a short germ insect

“…Tc-fz1 single RNAi leads to specific defects in the distal leg In Drosophila and Tribolium, wingless is required for segmentation as well as for distalisation and dorso-ventral patterning of the appendages (Cohen and Jürgens, 1989;Grossmann et al, 2009;Ober and Jockusch, 2006). For Tribolium, it was argued that the leg patterning function of wingless is only required during later embryonic stages (Grossmann et al, 2009).…”

Sog/Chordin is required for ventral-to-dorsal Dpp/BMP transport and head formation in a short germ insect

“…The remaining embryos were classified as WT-like but lacked detectable Tc-dpp transcription as well; these embryos may represent the weaker phenotypes described in ref. 30. In subsequent RNAi experiments, only embryos with strong phenotypes were analyzed.…”