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Biol Open. 2019 Sep 25;8(9). pii: bio046284. doi: 10.1242/bio.046284.

The torso-like gene functions to maintain the structure of the vitelline membrane in Nasonia vitripennis, implying its co-option into Drosophila axis formation.

Author information

1
Genomics Aotearoa and Biochemistry Department, University of Otago, P.O. Box 56, Dunedin, Aotearoa-New Zealand.
2
School of Biological Sciences, Monash University, 18 Innovation Walk, Clayton VIC 3800, Australia.
3
Otago Micro- and Nano- scale Imaging, University of Otago, PO Box 913, Dunedin, New Zealand, Aotearoa-New Zealand.
4
School of Medicine, University of Tasmania, 17 Liverpool St Hobart, TAS 7000, Australia.
5
Genomics Aotearoa and Biochemistry Department, University of Otago, P.O. Box 56, Dunedin, Aotearoa-New Zealand peter.dearden@otago.ac.nz.

Abstract

Axis 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.

KEYWORDS:

Axis formation; Drosophila; Evolution of development; Nasonia; Terminal patterning; Vitelline membrane

Conflict of interest statement

Competing interestsThe authors declare no competing or financial interests.

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