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Sex-specific adaptation and genomic responses to Y chromosome presence in female reproductive and neural tissues.

ABSTRACT: Y chromosomes typically harbour a small number of genes and an abundance of repetitive sequences. In Drosophila, the Y chromosome comprises multimegabase long segments of repetitive DNA and a handful of protein-coding genes. In mammals, the Y chromosome also harbours a disproportionally high abundance of repeats. Here, we built on a Drosophila melanogaster model in which the Y chromosome is decoupled from sexual determination. Genotypes were genetically identical for the autosomes, X chromosome, and mitochondria, but differ by the presence or dose of the Y chromosome. Addition of an extra Y chromosome had limited impact in males. However, the presence of a Y chromosome in females induced a disproportionate response in genes expressed in the ovaries as well as genes encoded by the mitochondrial genome. Furthermore, the data revealed significant consequences of Y chromosome presence in larvae neuronal tissue. This included the repression of genes implicated in reproductive behaviour, courtship, mating and synaptic function. Our findings exhibit the Y chromosome as a hotspot for sex-specific adaptation. They suggest roles for natural selection on Y-linked genetic elements exerting impact on sex-specific tissues as well as somatic tissues shared by males and females.

SUBMITTER: Branco AT

PROVIDER: S-EPMC5745411 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Sex-specific adaptation and genomic responses to Y chromosome presence in female reproductive and neural tissues.

Branco Alan T AT Brito Rute M RM Lemos Bernardo B

Proceedings. Biological sciences 20171201 1869

Y chromosomes typically harbour a small number of genes and an abundance of repetitive sequences. In <i>Drosophila,</i> the Y chromosome comprises multimegabase long segments of repetitive DNA and a handful of protein-coding genes. In mammals, the Y chromosome also harbours a disproportionally high abundance of repeats. Here, we built on a <i>Drosophila melanogaster</i> model in which the Y chromosome is decoupled from sexual determination. Genotypes were genetically identical for the autosomes, ...[more]

PMID: 29237855

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Project description:BackgroundAscaris lumbricoides causes human ascariasis, the most prevalent helminth disease, infecting approximately 1 billion individuals globally. In 2019 the global disease burden was estimated to be 754,000 DALYs and resulted in 2090 deaths. In the absence of a vaccination strategy, treatment of ascariasis has relied on anthelminthic chemotherapy, but drug resistance is a concern. The propensity for reinfection is also a major challenge to disease control; female worms lay up to 200,000 eggs daily, which contaminate surrounding environments and remain viable for years, resulting in high transmission rates. Understanding the molecular mechanisms of reproductive processes, including control of egg production, spermatogenesis, oogenesis and embryogenesis, will drive the development of new drugs and/or vaccine targets for future ascariasis control.MethodsTranscriptome profiles of discrete reproductive and somatic tissue samples were generated from adult male and female worms using Illumina HiSeq with 2 × 150 bp paired-end sequencing. Male tissues included: testis germinal zone, testis part of vas deferens, seminal vesicle and somatic tissue. Female tissues included: ovary germinal zone, ovary part of the oviduct, uterus and somatic tissue. Differentially expressed genes (DEGs) were identified from the fragments per kilobases per million reads (FPKM) profiles. Hierarchical analysis was performed to identify tissue-specific genes. Furthermore, Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were employed to identify significant terms and pathways for the DEGs.ResultsDEGs involved in protein phosphorylation and adhesion molecules were indicated to play a crucial role in spermatogenesis and fertilization, respectively. Those genes associated with the G-protein-coupled receptor (GPCR) signaling pathway and small GTPase-mediated signal transduction pathway play an essential role in cytoskeleton organization during oogenesis. Additionally, DEGs associated with the SMA genes and TGF-β signaling pathway are crucial in adult female embryogenesis. Some genes associated with particular biological processes and pathways that were identified in this study have been linked to defects in germline development, embryogenesis and reproductive behavior. In the enriched KEGG pathway analysis, Hippo signaling, oxytocin signaling and tight junction pathways were identified to play a role in Ascaris male and female reproductive systems.ConclusionsThis study has provided comprehensive transcriptome profiles of discrete A. lumbricoides reproductive tissue samples, revealing the molecular basis of these functionally important tissues. The data generated from this study will provide fundamental knowledge on the reproductive biology of Ascaris and will inform future target identification for anti-ascariasis drugs and/or vaccines.

Project description:BackgroundSex differences in pituitary growth hormone (GH) are well documented and coordinate maturation and growth. GH and its receptor are also produced in the brain where they may impact cognitive function and synaptic plasticity, and estradiol produces Gh sex differences in rat hippocampus. In mice, circulating estradiol increases Gh mRNA in female but not in male medial preoptic area (mPOA); therefore, additional factors regulate sexually dimorphic Gh expression in the brain. Thus, we hypothesized that sex chromosomes interact with estradiol to promote sex differences in GH. Here, we assessed the contributions of both estradiol and sex chromosome complement on Gh mRNA levels in three large brain regions: the hippocampus, hypothalamus, and cerebellum.MethodsWe used the four core genotypes (FCG) mice, which uncouple effects of sex chromosomes and gonadal sex. The FCG model has a deletion of the sex-determining region on the Y chromosome (Sry) and transgenic insertion of Sry on an autosome. Adult FCG mice were gonadectomized and given either a blank Silastic implant or an implant containing 17β-estradiol. Significant differences in GH protein and mRNA were attributed to estradiol replacement, gonadal sex, sex chromosome complement, and their interactions, which were assessed by ANOVA and planned comparisons.ResultsEstradiol increased Gh mRNA in the cerebellum and hippocampus, regardless of sex chromosome complement or gonadal sex. In contrast, in the hypothalamus, females had higher Gh mRNA than males, and XY females had more Gh mRNA than XY males and XX females. This same pattern was observed for GH protein. Because the differences in Gh mRNA in the hypothalamus did not replicate prior studies using other mouse models and tissue from mPOA or arcuate nucleus, we examined GH protein in the arcuate, a subdivision of the hypothalamus. Like the previous reports, and in contrast to the entire hypothalamus, a sex chromosome complement effect showed that XX mice had more GH than XY in the arcuate.ConclusionsSex chromosome complement regulates GH in some but not all brain areas, and within the hypothalamus, sex chromosomes have cell-specific actions on GH. Thus, sex chromosome complement and estradiol both contribute to GH sex differences in the brain.

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Sex-specific adaptation and genomic responses to Y chromosome presence in female reproductive and neural tissues.

Publications

Sex-specific adaptation and genomic responses to Y chromosome presence in female reproductive and neural tissues.

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