Abstract
Transformer (TRA) promotes female development in several dipteran species including the Australian sheep blowfly Lucilia cuprina, the Mediterranean fruit fly, housefly and Drosophila melanogaster. tra transcripts are sex-specifically spliced such that only the female form encodes full length functional protein. The presence of six predicted TRA/TRA2 binding sites in the sex-specific female intron of the L. cuprina gene suggested that tra splicing is auto-regulated as in medfly and housefly. With the aim of identifying conserved motifs that may play a role in tra sex-specific splicing, here we have isolated and characterized the tra gene from three additional blowfly species, L. sericata, Cochliomyia hominivorax and C. macellaria. The blowfly adult male and female transcripts differ in the choice of splice donor site in the first intron, with males using a site downstream of the site used in females. The tra genes all contain a single TRA/TRA2 site in the male exon and a cluster of four to five sites in the male intron. However, overall the sex-specific intron sequences are poorly conserved in closely related blowflies. The most conserved regions are around the exon/intron junctions, the 3′ end of the intron and near the cluster of TRA/TRA2 sites. We propose a model for sex specific regulation of tra splicing that incorporates the conserved features identified in this study. In L. sericata embryos, the male tra transcript was first detected at around the time of cellular blastoderm formation. RNAi experiments showed that tra is required for female development in L. sericata and C. macellaria. The isolation of the tra gene from the New World screwworm fly C. hominivorax, a major livestock pest, will facilitate the development of a “male-only” strain for genetic control programs.
Highlights
A Y-linked male determining gene (M) determines sex in the Australian sheep blowfly Lucilia cuprina [1]
In the honeybee Apis mellifera, the apparent tra ortholog feminizer is regulated by heterozygosity of the complementary sex determiner gene [8,9]. csd heterozygotes are females, whereas homozygotes and hemizygotes develop as males. fem transcripts are sex- spliced with only the female transcript coding for FEM protein. fem RNA could be directly regulated by CSD, which is a putative splicing factor [10]
We previously suggested that tra alternative splicing in L. sericata (Ls). cuprina is likely to be autoregulated as 5 motifs that matched a TRA/TRA2 consensus sequence (U/AC/ AA/UA/UCAAUCAACA) were identified in the intron and one TRA/TRA2 site was in male exon M2
Summary
A Y-linked male determining gene (M) determines sex in the Australian sheep blowfly Lucilia cuprina [1]. A likely target of M is the transformer (tra) gene, which is required for female development in L. cuprina [2]. The L. cuprina tra gene is sex- spliced such that only the female transcript encodes a full-length functional protein. In Drosophila melanogaster, tra is required for female development but tra RNA splicing is regulated by the female-specific RNA binding protein SXL [7]. In the honeybee Apis mellifera, the apparent tra ortholog feminizer (fem) is regulated by heterozygosity of the complementary sex determiner gene (csd) [8,9]. An ortholog of tra is required for female development in the hymenopteran Nasonia vitripennis, but tra gene expression appears to be controlled by a maternal imprinting mechanism rather than a male-determining gene [11]
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