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Sex-lethal is a target of Bruno-mediated translational repression in promoting the differentiation of stem cell progeny during Drosophila oogenesis.

ABSTRACT: The RNA Recognition Motif (RRM) type RNA binding protein Bruno is required for the differentiation of cystoblasts, the committed daughters of germline stem cells in the Drosophila ovary. To understand how Bruno controls cystoblast differentiation, we used a bioinformatics approach to identify potential mRNA targets of Bruno. One such target is the Sex-lethal (Sxl) transcript MS11, which contains four Bruno Response Elements (BREs) in its 3' untranslated region. Electrophoresis mobility shift assays demonstrated that Bruno specifically binds to the BREs of Sxl MS11 mRNA. Tagged transgenic Sxl MS11 cDNA constructs were used to show that Bruno represses the translation of the Sxl MS11 mRNA via the BRE-containing region in the 3'UTR. The lack of either Bruno or the BRE-containing region leads to overexpression of SXL, which in turn causes defects in cystoblast differentiation similar to the Bruno mutant phenotype. Therefore, Sxl MS11 represents a novel target of Bruno-mediated translational repression required for cystoblast differentiation.

SUBMITTER: Wang Z

PROVIDER: S-EPMC1904479 | biostudies-literature | 2007 Feb

REPOSITORIES: biostudies-literature

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Sex-lethal is a target of Bruno-mediated translational repression in promoting the differentiation of stem cell progeny during Drosophila oogenesis.

Wang Zhong Z Lin Haifan H

Developmental biology 20060915 1

The RNA Recognition Motif (RRM) type RNA binding protein Bruno is required for the differentiation of cystoblasts, the committed daughters of germline stem cells in the Drosophila ovary. To understand how Bruno controls cystoblast differentiation, we used a bioinformatics approach to identify potential mRNA targets of Bruno. One such target is the Sex-lethal (Sxl) transcript MS11, which contains four Bruno Response Elements (BREs) in its 3' untranslated region. Electrophoresis mobility shift ass ...[more]

PMID: 17067567

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Project description:BACKGROUND: Sex determining mechanisms are evolutionarily labile and related species often use different primary signals and gene regulatory networks. This is well illustrated by the sex determining cascade of Drosophila fruitflies, which have recruited Sex-lethal as the master switch and cellular memory of sexual identity, a role performed in other insects by the gene transformer. Here we investigate the evolutionary change in the coding sequences of sex determining genes associated with the recruitment of Sex-lethal. We analyze sequences of Sex-lethal itself, its Drosophila paralogue sister-or-Sex-lethal and downstream targets transformer and doublesex. RESULTS: We find that the recruitment of sister-or-Sex-lethal was associated with a number of adaptive amino acid substitutions, followed by a tightening of purifying selection within the Drosophila clade. Sequences of the paralogue sister-or-Sex-lethal, in contrast, show a signature of rampant positive selection and relaxation of purifying selection. The recruitment of Sex-lethal as top regulator and memory gene is associated with a significant release from purifying selection in transformer throughout the Drosophila clade. In addition, doublesex shows a signature of positive selection and relaxation of purifying selection in the Drosophila clade. A similar pattern is seen in sequences from the sister Tephritidae clade. CONCLUSIONS: The pattern of molecular evolution we observe for Sex-lethal and its paralogue sister-or-Sex-lethal is not characteristic of a duplication followed by neo-functionalization. Rather, evidence suggests a sub-functionalization scenario achieved through the evolution of sophisticated splicing. As expected, we find that transformer evolves under relaxed purifying selection after the recruitment of Sex-lethal in Drosophila. Finally, the observation of doublesex adaptation in both Drosophila and Tephritidae suggests that these changes are due to ongoing adaptation of downstream sex-specific regulation, rather than being associated the recruitment of Sex-lethal and the resulting change in the topology of the sex determining cascade.

Dataset Information

Sex-lethal is a target of Bruno-mediated translational repression in promoting the differentiation of stem cell progeny during Drosophila oogenesis.

Publications

Sex-lethal is a target of Bruno-mediated translational repression in promoting the differentiation of stem cell progeny during Drosophila oogenesis.

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