Striking parallels between dorsoventral patterning in Drosophila and Gryllus reveal a complex evolutionary history behind a model gene regulatory network.

Matthias Pechmann,Thomas Buchta,Orhan Özüak,Laura Pott,Siegfried Roth,Jeremy Lynch,Peter Heger,Yen-Ta Chen,Nathan James Kenny

doi:10.7554/elife.68287

Matthias Pechmann, Thomas Buchta + Show 7 more

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https://doi.org/10.7554/elife.68287

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Abstract

Dorsoventral pattering relies on Toll and BMP signalling in all insects studied so far, with variations in the relative contributions of both pathways. Drosophila and the beetle Tribolium share extensive dependence on Toll, while representatives of more distantly related lineages like the wasp Nasonia and bug Oncopeltus rely more strongly on BMP signalling. Here, we show that in the cricket Gryllus bimaculatus, an evolutionarily distant outgroup, Toll has, like in Drosophila, a direct patterning role for the ventral half of the embryo. In addition, Toll polarises BMP signalling, although this does not involve the conserved BMP inhibitor Sog/Chordin. Finally, Toll activation relies on ovarian patterning mechanisms with striking similarity to Drosophila. Our data suggest two surprising hypotheses: (1) that Toll's patterning function in Gryllus and Drosophila is the result of convergent evolution or (2) a Drosophila-like system arose early in insect evolution and was extensively altered in multiple independent lineages.

Highlights

In all insects studied so far, Toll and BMP signalling are essential for establishing the dorsoventral (DV) body axis of the embryo (Lynch and Roth, 2011; Ozuak et al, 2014b; Sachs et al, 2015)
To better analyse embryonic development and search for components that could be required to pattern the DV body axis of G. bimaculatus, we sequenced the transcriptomes of ovaries and embryonic egg stages 1–12
Our assembly results are similar in some metrics to those obtained by Fisher et al, 2018, our slightly better N50 and mean length figures, coupled to a lower number of transcripts (328,616 cf. 511,724) and a much higher number of bases contained in our assembly (301,016,284 cf. 237,416,984), suggest that our assembly is more contiguous

Summary

Introduction

In all insects studied so far, Toll and BMP signalling are essential for establishing the dorsoventral (DV) body axis of the embryo (Lynch and Roth, 2011; Ozuak et al, 2014b; Sachs et al, 2015). Toll signalling acts ventrally and is involved in specifying the mesoderm and neurogenic (ventral) ectoderm. BMP signalling acts dorsally and is required for specifying the extraembryonic tissues and the non-neurogenic (dorsal) ectoderm. Provided eggshell cues, which depend on the ventral expression of pipe in the ovarian cells producing the eggshell (so-called follicle cells), determine the shape of a steep, long-range Toll signalling gradient (Figure 1). This gradient acts as a morphogen that provides precise spatial information along the entire DV axis (Moussian and Roth, 2005; Schloop et al, 2020; Stein and Stevens, 2014). Toll signalling regulates the expression of more than 50 target genes in a concentration-dependent manner (Hong et al, 2008; Reeves and Stathopoulos, 2009)

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