Embryo polarity in moth flies and mosquitoes relies on distinct old genes with localized transcript isoforms.

Yoseop Yoon,Frank Criscione,Jose Ribeiro,Ines Martin-Martin,Jeff Klomp,Eric Calvo,Urs Schmidt-Ott

doi:10.7554/elife.46711

Yoseop Yoon, Frank Criscione + Show 5 more

Open Access

https://doi.org/10.7554/elife.46711

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Abstract

Unrelated genes establish head-to-tail polarity in embryos of different fly species, raising the question of how they evolve this function. We show that in moth flies (Clogmia, Lutzomyia), a maternal transcript isoform of odd-paired (Zic) is localized in the anterior egg and adopted the role of anterior determinant without essential protein change. Additionally, Clogmia lost maternal germ plasm, which contributes to embryo polarity in fruit flies (Drosophila). In culicine (Culex, Aedes) and anopheline mosquitoes (Anopheles), embryo polarity rests on a previously unnamed zinc finger gene (cucoid), or pangolin (dTcf), respectively. These genes also localize an alternative transcript isoform at the anterior egg pole. Basal-branching crane flies (Nephrotoma) also enrich maternal pangolin transcript at the anterior egg pole, suggesting that pangolin functioned as ancestral axis determinant in flies. In conclusion, flies evolved an unexpected diversity of anterior determinants, and alternative transcript isoforms with distinct expression can adopt fundamentally distinct developmental roles.

Highlights

The specification of the primary axis in embryos of flies (Diptera) offers important advantages for studying how new essential gene functions evolve in early development
Using RNA-seq data from preblastoderm and blastoderm embryos and Rapid Amplication of Complementary DNA (cDNA) Ends (RACE), we identified maternal and zygotic contains a single odd-paired locus (Cal-opa) transcripts with alternative first exons that we mapped onto a 54 kb genomic scaffold (Figure 1C)
We have identified three unrelated old genes that encode the anterior determinant in moth flies, culicine mosquitoes, and anopheline mosquitoes, respectively (Figure 7)

Summary

Introduction

The specification of the primary axis (head-to-tail) in embryos of flies (Diptera) offers important advantages for studying how new essential gene functions evolve in early development This process rests on lineage-specific maternal mRNAs that are localized at the anterior egg pole (‘anterior determinants’), which, surprisingly, have changed during the evolution of flies. Yoon et al identified three unrelated genes that perform similar roles to bicoid and panish in the embryos of several different moth flies and mosquitoes These genes appear to have acquired their activity because one of their alternative transcripts accumulated at the future head end, rather than through mutations in the protein-coding sequences. Studying multiple species made it clear that panish inherited its function from a localized alternative transcript of an old gene that duplicated and diverged These findings suggest that alternative transcription may provide opportunities for genes to evolve new roles in fundamental processes in flies.

Results

A4 Md Mx Lb T1 T2 T3 A1 A2 A3

Discussion

Materials and methods

Funding Funder National Science Foundation