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Molecular insights into female hybrid sterility in interspecific crosses between Drosophila melanogaster and Drosophila simulans (RNA-Seq)

ABSTRACT: Species of the genus Drosophila have served as favorite models in speciation studies, however genetic factors of the interspecific hybrid sterility are underinvestigated to date. Here we performed the analysis of reproductive incompatibilities of hybrid females in crossing Drosophila melanogaster females and Drosophila simulans males. Using transcriptomic data analysis, molecular, cellular and genetic approaches we analyzed differential gene expression, transposable element (TE) activity, piRNA biogenesis and functional defects of oogenesis in hybrids. A premature GSC loss was a most prominent defect of oogenesis in hybrid ovaries. Owing differential expression of genes encoding components of the piRNA pathway rhino and deadlock, functional RDCmel complex in hybrid ovaries was not assembled. At the same time the activity of RDCsim complex was maintained in hybrids, independently from the genomic origin of piRNA clusters. Despite identification of a cohort of overexpressed TEs in hybrid ovaries we found no evidences that their activity can be considered as the main cause of hybrid sterility. We revealed complex pattern of Vasa protein expression in hybrid germline, including partial AT-chX piRNA targeting of vasasim allele and significant developmental delay of vasamel expression. We came to the conclusions that complex multi-locus genetic changes between the species were responsible for hybrid sterility phenotype.

ORGANISM(S): Drosophila simulans Drosophila melanogaster x Drosophila simulans Drosophila melanogaster

PROVIDER: GSE263982 | GEO | 2024/05/30

REPOSITORIES: GEO

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Molecular insights into female hybrid sterility in interspecific crosses between Drosophila melanogaster and Drosophila simulans (small RNA-Seq)

Project description:Species of the genus Drosophila have served as favorite models in speciation studies, however genetic factors of the interspecific hybrid sterility are underinvestigated to date. Here we performed the analysis of reproductive incompatibilities of hybrid females in crossing Drosophila melanogaster females and Drosophila simulans males. Using transcriptomic data analysis, molecular, cellular and genetic approaches we analyzed differential gene expression, transposable element (TE) activity, piRNA biogenesis and functional defects of oogenesis in hybrids. A premature GSC loss was a most prominent defect of oogenesis in hybrid ovaries. Owing differential expression of genes encoding components of the piRNA pathway rhino and deadlock, functional RDCmel complex in hybrid ovaries was not assembled. At the same time the activity of RDCsim complex was maintained in hybrids, independently from the genomic origin of piRNA clusters. Despite identification of a cohort of overexpressed TEs in hybrid ovaries we found no evidences that their activity can be considered as the main cause of hybrid sterility. We revealed complex pattern of Vasa protein expression in hybrid germline, including partial AT-chX piRNA targeting of vasasim allele and significant developmental delay of vasamel expression. We came to the conclusions that complex multi-locus genetic changes between the species were responsible for hybrid sterility phenotype.

2024-05-30 | GSE263983 | GEO

piRNA silencing contributes to interspecies hybrid sterility and reproductive isolation in Drosophila

Project description:The piRNA pathway is an adaptive mechanism for maintaining the stability of the genome by repression selfish genomic elements such as transposons. As a host defense mechanism the piRNA pathway is rapidly evolving with different sets of piRNA silencing different targets in closely-related species. In male germline of D.melanogaster, repression of Stellate genes by piRNA generated from Supressor of Stellate, Su(Ste), locus is required for male fertility, but both Su(Ste) piRNA and their targets are absent in other Drosophila species. Here we showed that D.melanogaster genome contain non-coding genomic repeats that have sequence similarity to vasa, protein-coding host gene essential for germline development. In male germline Vasa Related (Varel) repeats produce abundant piRNA that are anti-sense to vasa, however, vasa mRNA escape silencing due to imperfect complementarity between piRNA and vasa sequences. Unexpectedly, we found that Varel piRNA of D.melanogaster target vasa of closely related D. mauritana species in interspecies hybrids. The same hybrids show derepression of harmful Stellate locus due to the absence of Su(Ste) piRNA. Thus, the piRNA pathway contributes to the reproductive isolation between Drosophila species, causing hybrid male sterility via misregulation of two different host factors.

2019-02-19 | GSE120802 | GEO

Adaptation to transposon invasion in Drosophila melanogaster

Project description:Transposons evolve rapidly and can mobilize and trigger genetic instability. piRNAs silence these genome pathogens, but it is unclear how the piRNA pathway adapts to new transposons. In Drosophila piRNAs, encoded by heterochromatic clusters are maternally deposited in the embryo. Paternally inherited P-element transposons thus escape silencing and trigger a genetic instability and sterility. We show that this syndrome, termed P-M hybrid dysgenesis, also disrupts the piRNA biogenesis machinery and activates resident transposons. As dysgenic hybrids age, however, fertility is restored, P-elements are silenced, and P-element piRNAs are produced de novo. In addition, the piRNA biogenesis machinery is restored and resident elements are silenced. Significantly, new resident transposons insertions accumulate in piRNA clusters, and these new insertions are transmitted to progeny with high fidelity, produce novel piRNAs, and are associated with reduced transposition. P-M hybrid dysgenesis thus leads to heritable changes in chromosome structure that appear to enhance transposon silencing. 3 replicates of each sample (Har 2-4 days, w1 x Har 2-4 days, w1 x Har 21 days), total RNA samples hybridized to tiling array.

2011-12-23 | E-GEOD-31813 | biostudies-arrayexpress

Adaptation to transposon invasion in Drosophila melanogaster

2011-12-23 | GSE31813 | GEO

A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway [smallRNA-Seq]

Project description:The Drosophila piRNA pathway provides an RNA-based immune system that defends the germline genome against selfish genetic elements. Two inter-related branches of the piRNA system exist: somatic cells that support oogenesis only employ Piwi, whereas germ cells utilize a more elaborated pathway centered on the three gonad-specific Argonaute proteins Piwi, Aubergine, and Argonaute3. While several key factors of each branch have been identified, our current knowledge is insufficient to explain the complex workings of the piRNA machinery. Here, we report a reverse genetic screen spanning the ovarian transcriptome in an attempt to uncover the full repertoire of genes required for piRNA-mediated transposon silencing in the female germline. Our screen reveals new key factors of piRNA-mediated transposon silencing, including the novel piRNA biogenesis factors, CG2183 (GASZ) and Deadlock. Last, our data uncovers a previously unanticipated set of factors preferentially required for repression of different transposons types. Examination of small RNA levels from nos-GAL4 or tj-GAL4 driven UAS-dsRNA knockdowns of control genes and piRNA pathway components in ovaries of Drosophila melanogaster by deep sequencing (using Illumina HiSeq2000).

2013-05-10 | E-GEOD-46099 | biostudies-arrayexpress

A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway [RNA-Seq]

Project description:The Drosophila piRNA pathway provides an RNA-based immune system that defends the germline genome against selfish genetic elements. Two inter-related branches of the piRNA system exist: somatic cells that support oogenesis only employ Piwi, whereas germ cells utilize a more elaborated pathway centered on the three gonad-specific Argonaute proteins Piwi, Aubergine, and Argonaute3. While several key factors of each branch have been identified, our current knowledge is insufficient to explain the complex workings of the piRNA machinery. Here, we report a reverse genetic screen spanning the ovarian transcriptome in an attempt to uncover the full repertoire of genes required for piRNA-mediated transposon silencing in the female germline. Our screen reveals new key factors of piRNA-mediated transposon silencing, including the novel piRNA biogenesis factors, CG2183 (GASZ) and Deadlock. Last, our data uncovers a previously unanticipated set of factors preferentially required for repression of different transposons types. Examination of total RNA levels from nos-GAL4 or tj-GAL4 driven UAS-dsRNA knockdowns of control genes and piRNA pathway components in ovaries of Drosophila melanogaster by deep sequencing (using Illumina HiSeq2000).

2013-05-10 | E-GEOD-46100 | biostudies-arrayexpress

Comparison of testes gene expression of D. melanogaster species and their hybrids

Project description:Males hybrids from the crosses between species of the D. simulans clade are steriles as the females are fertiles. Hybrid male sterility is due to severe defects in spermatogenesis and phenotypic differences are observed between the different hybrids involving D. simulans, D. sechellia and D. mauritiana. In this study we are comparing gene expression in the testes of hybrids involving the female D. simulans and the males D. melanogaster, D. mauritiana, or D. sechellia to the gene expression in species testes. Keywords: Comparative genomic hybridization

2006-06-12 | GSE3673 | GEO

Expression data from testes and abdomen in fertile and sterile introgression males

Project description:Postmating reproductive isolation is often manifested as hybrid male sterility, for which X-linked genes are over-represented. In contrast, X-linked gene are significantly under-represented among testis-expressing gene.This seeming contradiction may be germane to the X:autosome imbalance hypothesis on hybrid sterility ,in which the X-linked effect is mediated mainly through the misexpression of autosomal genes. We compared gene expression in fertile and sterile males in the hybrids between two Drosophila species. These hybrid males differ only in a small region of the X chromosome containing the OdsH locus of hybrid sterility. Of genes expressed in the testis, autosomal genes were indeed more likely to be misexpressed than X-linked genes under the steriizing action of OdsH.

2010-05-19 | GSE21734 | GEO

Next-generation sequencing analysis of Piwi-interacting RNAs (piRNAs) in Drosophila wild-type and bel mutant ovaries

Project description:Belle has been known to be co-localized with piRNA-related proteins at the nuage of germline cells during Drosophila oogenesis. However, its role in piRNA biogenesis remains unclear. To reveal whether Belle is involved in regulating piRNA expression, we performed next-generation sequencing analysis of small non-coding RNAs on ovaries harvested from the wild type (W1118) and trans-heterozygous bel[74407/neo30] mutant. Small RNA-seq experiments were performed on three individual ovary samples with the same genotype. For piRNA expression analysis, we performed mapping of three sets of small RNA sequencing reads for each genotype to previously identified eight distinct piRNA clusters located in four different Drosophila chromosomes (from X to 4). Analysis of the piRNA expression profiling from these piRNA cluster loci indicates that some specific piRNA populations were either upregulated or downregulated in bel mutant ovaries compared with wild-type ovaries. Furthermore, we performed systematic analysis by mapping piRNA sequencing reads to sequences of all identified Drosophila transposable elements (TEs) to classify and measure piRNA reads based on their TE targets. Among 124 TE-classified piRNA populations, 9 and 20 of them were upregulated and downregulated (≥2 folds), respectively, in bel74407/neo30 mutant ovaries compared with those from wild-type ovaries. To examine the effect of the bel[74407/neo30] mutation on the ping-pong cycle for secondary piRNA biogenesis, analysis of the ping-pong signature of piRNAs specifically mapped to the retro-element Burdock was performed. The ping-pong signature for the generation of secondary piRNAs was not significantly altered in bel mutants compared with the wild type. These results, taken together, indicate that Bel is not required for primary and secondary piRNA biogenesis, but it is involved in regulating expression of specific subsets of piRNA populations.

2017-09-01 | GSE65565 | GEO

Comparison of D. simulans/D. sechellia F1 male hybrid genome-wide expression values to pure-species parents

Project description:Species often produce sterile hybrids early in their evolutionary divergence, and some evidence suggests that hybrid sterility may be associated with deviations or disruptions in gene expression. In support of this idea, many studies have shown that a high proportion of male-biased genes are underexpressed compared to non-sex-biased genes in sterile F1 male hybrids of Drosophila species. In this study, we examined and compared patterns of misexpression in 4 day old sterile male F1 hybrids of Drosophila simulans and its sibling species, D. sechellia. We analyzed hybrids using genome-wide D. melanogaster arrays from the Drosophila Genome Resource Center (DGRC). The results from a custom array (GPL4022) for this species pair, from the custom array and the genome-wide array for the D. simulans-D. mauritiana species pair, and from the larvae of these two species pairs using the custom array, are presented separately. Keywords: Comparison of pure-species Drosophila expression to hybrid expression

2006-09-13 | GSE5607 | GEO

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