Dataset Information

Female Sex Determination Factors in Ceratitis capitata: Molecular and Structural Basis of TRA and TRA2 Recognition.

ABSTRACT: In the model system for genetics, Drosophila melanogaster, sexual differentiation and male courtship behavior are controlled by sex-specific splicing of doublesex (dsx) and fruitless (fru). In vitro and in vivo studies showed that female-specific Transformer (TRA) and the non-sex-specific Transformer 2 (TRA2) splicing factors interact, forming a complex promoting dsx and fru female-specific splicing. TRA/TRA2 complex binds to 13 nt long sequence repeats in their pre-mRNAs. In the Mediterranean fruitfly Ceratitis capitata (Medfly), a major agricultural pest, which shares with Drosophila a ~120 million years old ancestor, Cctra and Cctra2 genes seem to promote female-specific splicing of Ccdsx and Ccfru, which contain conserved TRA/TRA2 binding repeats. Unlike Drosophila tra, Cctra autoregulates its female-specific splicing through these putative regulatory repeats. Here, a yeast two-hybrid assay shows that CcTRA interacts with CcTRA2, despite its high amino acid divergence compared to Drosophila TRA. Interestingly, CcTRA2 interacts with itself, as also observed for Drosophila TRA2. We also generated a three-dimensional model of the complex formed by CcTRA and CcTRA2 using predictive approaches based on Artificial Intelligence. This structure also identified an evolutionary and highly conserved putative TRA2 recognition motif in the TRA sequence. The Y2H approach, combined with powerful predictive tools of three-dimensional protein structures, could use helpful also in this and other insect species to understand the potential links between different upstream proteins acting as primary sex-determining signals and the conserved TRA and TRA2 transducers.

SUBMITTER: Perrotta MM

PROVIDER: S-EPMC10380613 | biostudies-literature | 2023 Jul

REPOSITORIES: biostudies-literature

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Female Sex Determination Factors in Ceratitis capitata: Molecular and Structural Basis of TRA and TRA2 Recognition.

Perrotta Maryanna Martina MM Lucibelli Francesca F Mazzucchiello Sarah Maria SM Fucci Nicole N Hay Mele Bruno B Giordano Ennio E Salvemini Marco M Ruggiero Alessia A Vitagliano Luigi L Aceto Serena S Saccone Giuseppe G

Insects 20230704 7

In the model system for genetics, Drosophila melanogaster, sexual differentiation and male courtship behavior are controlled by sex-specific splicing of doublesex (dsx) and fruitless (fru). In vitro and in vivo studies showed that female-specific Transformer (TRA) and the non-sex-specific Transformer 2 (TRA2) splicing factors interact, forming a complex promoting dsx and fru female-specific splicing. TRA/TRA2 complex binds to 13 nt long sequence r ...[more]

PMID: 37504611

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Project description:BACKGROUND: In embryos the maternal-to-zygotic transition (MTZ) integrates post-transcriptional regulation of maternal transcripts with transcriptional activation of the zygotic genome. Although the molecular mechanisms underlying this event are being clarified in Drosophila melanogaster, little is know about the embryogenic processes in other insect species. The recent publication of expressed sequence tags (ESTs) from embryos of the global pest species Ceratitis capitata (medfly) has enabled the investigation of embryogenesis in this species and has allowed a comparison of the embryogenic processes in these two related dipteran species, C. capitata and D. melanogaster, that shared a common ancestor 80-100 mya. RESULTS: Using a novel PCR-based sexing method, which takes advantage of a putative LTR retrotransposon MITE insertion on the medfly Y chromosome, the transcriptomes of individual early male and female embryos were analysed using RT-PCR. This study is focused on two crucial aspects of the onset of embryonic development: sex determination and cellular blastoderm formation. Together with the three known medfly genes (Cctransformer, Cctransformer2 and Ccdoublesex), the expression patterns of other medfly genes that are similar to the D. melanogaster sex-determination genes (sisterlessA, groucho, deadpan, Sex-lethal, female lethal d, sans fille and intersex) and four cellular blastoderm formation genes (Rho1, spaghetti squash, slow-as-molasses and serendipity-alpha) were analyzed, allowing us to sketch a preliminary outline of the embryonic process in the medfly. Furthermore, a putative homologue of the Zelda gene has been considered, which in D. melanogaster encodes a DNA-binding factor responsible for the maternal-to-zygotic transition. CONCLUSIONS: Our novel sexing method facilitates the study of i) when the MTZ transition occurs in males and females of C. capitata, ii) when and how the maternal information of "female-development" is reprogrammed in the embryos and iii) similarities and differences in the regulation of gene expression in C. capitata and D. melanogaster. We suggest a new model for the onset of the sex determination cascade in the medfly: the maternally inherited Cctra transcripts in the female embryos are insufficient to produce enough active protein to inhibit the male mode of Cctra splicing. The slow rate of development and the inefficiency of the splicing mechanism in the pre-cellular blastoderm facilitates the male-determining factor (M) activity, which probably acts by inhibiting CcTRA protein activity.

Project description:The Mediterranean fruit fly (medfly), Ceratitis capitata (Wiedemann), is a key pest of fruit crops in many tropical, subtropical and mild temperate areas worldwide. The economic importance of this fruit fly is increasing due to its invasion of new geographical areas. Efficient control and eradication efforts require adequate information regarding C. capitata adults in relation to environmental and physiological cues. This would allow effective characterisation of the population spatio-temporal dynamic of the C. capitata population at both the orchard level and the area-wide landscape. The aim of this study was to analyse population patterns of adult medflies caught using two trapping systems in a peach orchard located in central Italy. They were differentiated by adult sex (males or females) and mating status of females (unmated or mated females) to determine the spatio-temporal dynamic and evaluate the effect of cultivar and chemical treatments on trap catches. Female mating status was assessed by spermathecal dissection and a blind test was carried out to evaluate the reliability of the technique. Geostatistical methods, variogram and kriging, were used to produce distributional maps. Results showed a strong correlation between the distribution of males and unmated females, whereas males versus mated females and unmated females versus mated females showed a lower correlation. Both cultivar and chemical treatments had significant effects on trap catches, showing associations with sex and female mating status. Medfly adults showed aggregated distributions in the experimental field, but hot spots locations varied. The spatial pattern of unmated females reflected that of males, whereas mated females were largely distributed around ripening or ripe fruit. The results give relevant insights into pest management. Mated females may be distributed differently to unmated females and the identification of male hot spots through monitoring would allow localisation of virgin female populations. Based on our results, a more precise IPM strategy, coupled with effective sanitation practices, could represent a more effective approach to medfly control.

Dataset Information

Female Sex Determination Factors in Ceratitis capitata: Molecular and Structural Basis of TRA and TRA2 Recognition.

Publications

Female Sex Determination Factors in <i>Ceratitis capitata</i>: Molecular and Structural Basis of TRA and TRA2 Recognition.

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