Abstract
ABSTRACTAxis specification is a fundamental developmental process. Despite this, the mechanisms by which it is controlled across insect taxa are strikingly different. An excellent example of this is terminal patterning, which in Diptera such as Drosophila melanogaster occurs via the localized activation of the receptor tyrosine kinase Torso. In Hymenoptera, however, the same process appears to be achieved via localized mRNA. How these mechanisms evolved and what they evolved from remains largely unexplored. Here, we show that torso-like, known for its role in Drosophila terminal patterning, is instead required for the integrity of the vitelline membrane in the hymenopteran wasp Nasonia vitripennis. We find that other genes known to be involved in Drosophila terminal patterning, such as torso and Ptth, also do not function in Nasonia embryonic development. These findings extended to orthologues of Drosophila vitelline membrane proteins known to play a role in localizing Torso-like in Drosophila; in Nasonia these are instead required for dorso–ventral patterning, gastrulation and potentially terminal patterning. Our data underscore the importance of the vitelline membrane in insect development, and implies phenotypes caused by knockdown of torso-like must be interpreted in light of its function in the vitelline membrane. In addition, our data imply that the signalling components of the Drosophila terminal patterning systems were co-opted from roles in regulating moulting, and co-option into terminal patterning involved the evolution of a novel interaction with the vitelline membrane protein Torso-like.This article has an associated First Person interview with the first author of the paper.
Highlights
Establishment of the major axes and termini are some of the first events to take place during insect embryonic development
Drosophila, the termini are patterned via the localized activation of the receptor tyrosine kinase Torso (Tor) by its ligand Trunk (Trk) which results in expression of the transcription factors Tailless (Tll) (Klingler et al, 1988; Strecker et al, 1989) and Huckebein (Bronner and Jackle, 1991, 1996) at the anterior and posterior of the embryo
To determine if Nv-tsl is expressed in a pattern related to axis formation we investigated the expression of Nv-tsl RNA in Nasonia ovaries and embryos
Summary
Establishment of the major axes and termini are some of the first events to take place during insect embryonic development. Drosophila, the termini are patterned via the localized activation of the receptor tyrosine kinase Torso (Tor) by its ligand Trunk (Trk) which results in expression of the transcription factors Tailless (Tll) (Klingler et al, 1988; Strecker et al, 1989) and Huckebein (Bronner and Jackle, 1991, 1996) at the anterior and posterior of the embryo. Localization of signalling is provided by torso-like (tsl) (Savant-Bhonsale and Montell, 1993; Stevens et al, 1990), which encodes a protein present only at the termini of the embryo (Stevens et al, 2003). The long-standing model is that Tsl localizes the activity of the Tor ligand (Trk) to the terminal regions, possibly via a mechanism involving the regulation of Trk secretion (Johnson et al, 2015), other models have been proposed (Amarnath et al, 2017; Mineo et al, 2018a,b)
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