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The sex-specific factor SOA establishes X chromosome dosage compensation in Anopheles mosquitos [SOAR-RNA-seq]

ABSTRACT: The Anopheles mosquito is one of thousands of species in which sex differences play a central role in their biology, as only females need a blood meal in order to produce eggs. Sex differentiation is regulated by sex chromosomes, but their presence creates a dosage imbalance between males (XY) and females (XX). Dosage compensation (DC) can re-equilibrate the expression of sex-chromosomal genes, but because DC mechanisms have only been fully characterized in a few model organisms, key questions about its evolutionary diversity and functional necessity remain unresolved. Here we report the discovery of a previously uncharacterized gene (SOA) as a master regulator of DC in the malaria mosquito Anopheles gambiae. Sex-specific alternative splicing prevents functional SOA protein expression in females. The male isoform encodes a DNA-binding protein that binds the promoters of active X chromosomal genes. Expressing male SOA is sufficient to induce DC in female cells. Male mosquitoes lacking SOA or female mosquitos ectopically expressing the male isoform exhibit X chromosome misregulation, which is compatible with viability but causes developmental delay. Thus, our molecular analysis of the first DC master regulator in a non-model organism elucidates the evolutionary steps leading to the establishment of a chromosome-specific fine-tuning mechanism.

ORGANISM(S): Anopheles gambiae

PROVIDER: GSE233473 | GEO | 2023/07/25

REPOSITORIES: GEO

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The sex-specific factor SOA establishes X chromosome dosage compensation in Anopheles mosquitos

Project description:The Anopheles mosquito is one of thousands of species in which sex differences play a central role in their biology, as only females need a blood meal in order to produce eggs. Sex differentiation is regulated by sex chromosomes, but their presence creates a dosage imbalance between males (XY) and females (XX). Dosage compensation (DC) can re-equilibrate the expression of sex-chromosomal genes, but because the molecular mechanisms providing DC have only been studied in a few model organisms, key questions about its evolutionary diversity and functional necessity remain unresolved. Here, we reveal the DC pathway in the malaria mosquito Anopheles gambiae. We identified SOA, a previously uncharacterized gene, whose expression is sufficient to induce a global upregulation of X-linked genes. Sex-specific alternative splicing prevents the production of a functional SOA protein in females. The male SOA isoform encodes a DNA-binding protein that recognizes the promoters of X chromosomal genes through a CA repeat sequence. Male mosquitos lacking SOA exhibit a chromosome-wide downregulation of the X, which is compatible with viability, but causes a developmental delay. Thus, our molecular analysis of the first DC master regulator in a non-model organism elucidates the evolutionary steps leading to the establishment of a chromosome-specific fine-tuning mechanism.

2023-07-13 | PXD042353 | Pride

The sex-specific factor SOA establishes X chromosome dosage compensation in Anopheles mosquitos [SOAR-CUTnTag]

Project description:The Anopheles mosquito is one of thousands of species in which sex differences play a central role in their biology, as only females need a blood meal in order to produce eggs. Sex differentiation is regulated by sex chromosomes, but their presence creates a dosage imbalance between males (XY) and females (XX). Dosage compensation (DC) can re-equilibrate the expression of sex-chromosomal genes, but because DC mechanisms have only been fully characterized in a few model organisms, key questions about its evolutionary diversity and functional necessity remain unresolved. Here we report the discovery of a previously uncharacterized gene (SOA) as a master regulator of DC in the malaria mosquito Anopheles gambiae. Sex-specific alternative splicing prevents functional SOA protein expression in females. The male isoform encodes a DNA-binding protein that binds the promoters of active X chromosomal genes. Expressing male SOA is sufficient to induce DC in female cells. Male mosquitoes lacking SOA or female mosquitos ectopically expressing the male isoform exhibit X chromosome misregulation, which is compatible with viability but causes developmental delay. Thus, our molecular analysis of the first DC master regulator in a non-model organism elucidates the evolutionary steps leading to the establishment of a chromosome-specific fine-tuning mechanism.

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The sex-specific factor SOA establishes X chromosome dosage compensation in Anopheles mosquitos [Mybless-CUTnTag]

Project description:The Anopheles mosquito is one of thousands of species in which sex differences play a central role in their biology, as only females need a blood meal in order to produce eggs. Sex differentiation is regulated by sex chromosomes, but their presence creates a dosage imbalance between males (XY) and females (XX). Dosage compensation (DC) can re-equilibrate the expression of sex-chromosomal genes, but because DC mechanisms have only been fully characterized in a few model organisms, key questions about its evolutionary diversity and functional necessity remain unresolved. Here we report the discovery of a previously uncharacterized gene (SOA) as a master regulator of DC in the malaria mosquito Anopheles gambiae. Sex-specific alternative splicing prevents functional SOA protein expression in females. The male isoform encodes a DNA-binding protein that binds the promoters of active X chromosomal genes. Expressing male SOA is sufficient to induce DC in female cells. Male mosquitoes lacking SOA or female mosquitos ectopically expressing the male isoform exhibit X chromosome misregulation, which is compatible with viability but causes developmental delay. Thus, our molecular analysis of the first DC master regulator in a non-model organism elucidates the evolutionary steps leading to the establishment of a chromosome-specific fine-tuning mechanism.

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SOA confers X chromosome dosage compensation in Anopheles gambiae mosquitoes (RNA-Seq II)

Project description:Differences between males and females are central to the biology of thousands of species across the tree of life. Sex chromosomes play a key role, but despite their their evolutionary diversity, the regulatory mechanisms have been mostly elucidated in the three model species Mammals, D. melanogaster and C. elegans. Here we present the characterization of the first X chromosome dosage compensation (DC) pathway in a non-model organism, the malaria mosquito Anopheles gambiae. In mosquitos, DC corrects the imbalance in gene expression between sexes by approximately two-fold upregulation of male X-linked genes. We have identified SOA, a previously uncharacterized gene, which is specific to Anophelinae and activated concomitantly with the onset of DC. SOA displays sex-specific alternative splicing, where only males express full-length protein. SOA is a DNA-binding protein, specifically localizes to an X chromosome territory and binds promoters of active X-linked genes. Expression of the male, but not female isoform, is sufficient to induce DC. SOA knock-out mosquitos display a male-specific developmental delay, which is associated with a global downregulation of the X chromosome. Thus, SOA is the first DC factor discovered in Anopheles and provides only the fourth DC pathway ever identified to date. Since only females are blood-feeding and able to transmit malaria, identification of this sex-specific pathway is highly relevant and an important progress for malaria control programs.

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Sex-specific transcriptome dynamics of Anopheles gambiae during embryonic development [CUT&Tag]

Project description:Malaria-transmitting mosquitoes are extremely sexually dimorphic in their anatomy and behaviour. Sex-specific gene expression in Anopheles gambiae is well-studied in adult stages, but its onset during embryogenesis, apart from sex-determination factors like Yob, remains largely unknown. Here, we report a comprehensive single-embryo transcriptome atlas of A. gambiae males and females to understand the earliest stages of establishing the sex-specific expression networks. Our dataset reveals embryonic RNA isoform diversity including a global shift towards distal alternative polyadenylation (APA) events sites during the maternal-to-zygotic genome transition. Sex-biased gene expression and alternative splicing are limited during embryogenesis, with most sex-specific patterns emerging post-embryonically. X chromosome dosage compensation is established shortly after zygotic genome activation concomitant with direct binding of the master regulator protein SOA to X-linked promoters. Unlike the dosage compensation regulators in Drosophila or mammals, SOA operates in a one-step fashion, directly binding CA-rich promoter motifs without prioritizing certain gene groups over others. We propose that the Anopheles dosage compensation system represents an evolutionary endpoint of a gene-by-gene regulatory mechanism that evolved to a chromosome-wide scale.

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