Data from: Evolution and dynamics of germline sex chromosome regulation in D. miranda
Data files
Jan 26, 2024 version files 110.25 MB
Abstract
Although sex chromosomes have evolved from autosomes, they often have unusual regulatory regimes that are sex- and cell-type-specific such as dosage compensation (DC) and meiotic sex chromosome inactivation (MSCI). The molecular mechanisms and evolutionary forces driving these unique transcriptional programs are critical for genome evolution but have been, in the case of MSCI in Drosophila, subject to continuous debate. Here, we take advantage of the younger sex chromosomes in D. miranda (XR and the neo-X) to infer how former autosomes acquire sex-chromosome specific regulatory programs using single-cell and bulk RNA sequencing and ribosome profiling, in a comparative evolutionary context. We show that contrary to mammals and worms, the X’s are downregulated through germline progression most consistent with a loss of DC instead of MSCI, resulting in half gene dosage at the end of meiosis for all three X’s. Moreover, lowly expressed germline and meiotic genes on the neo-X are ancestrally lowly expressed, instead of suppression after sex linkage. For the young neo-X, DC is incomplete across all tissue and cell types and this dosage imbalance is rescued by contributions from Y-linked gametologs which produce transcripts that are translated to compensate both gene and protein dosage. We find an excess of previously autosomal testis genes becoming Y-specific, showing that the neo-Y and its masculinization likely resolve sexual antagonism. Multicopy neo-sex genes are predominantly expressed during meiotic stages of spermatogenesis, consistent with their amplification being driven to interfere with Mendelian segregation. Altogether, this study reveals germline regulation of evolving sex chromosomes and elucidates the consequences these unique regulatory mechanisms have on the evolution sex chromosome architecture.
README: Evolution and dynamics of germline sex chromosome regulation in D. miranda
Although sex chromosomes have evolved from autosomes, they often have unusual regulatory regimes that are sex- and cell-type-specific such as dosage compensation (DC) and meiotic sex chromosome inactivation (MSCI). The molecular mechanisms and evolutionary forces driving these unique transcriptional programs are critical for genome evolution but have been, in the case of MSCI in Drosophila, subject to continuous debate. Here, we take advantage of the younger sex chromosomes in D. miranda (XR and the neo-X) to infer how former autosomes acquire sex-chromosome specific regulatory programs using single-cell and bulk RNA sequencing and ribosome profiling, in a comparative evolutionary context.
Description of the data and file structure
scRNAseq:
miranda.testes.alevin.tar.gz: Alevin mapping of scRNA-seq data.
aggregate_countsxcelltype.txt: Aggregated read counts for genes (row) in each cell type (column).
MSL ChIP-seq:
mir_MSE_peaks.narrowPeak: Output of MACS2 peak calling.
mir_MSE_summits.bed: Output of MACS2 peak calling.
Bulk tissue RNA-seq and ribo-seq:
Dmir.STARpri.CDS.fc: Read counts from D. miranda tissue dissection. (Mapped by STAR and annotated with featurecounts)
Dpse.STARpri.CDS.fc: Read counts from D. pseudoobscura tissue dissection. (Mapped by STAR and annotated with featurecounts)
Dmir.ribo.Starpri.fc: Read counts from D. miranda ribosome profiling. (Mapped by STAR and annotated with featurecounts)
Sequence homology:
RB.pse2mir.RBH.new.txt: Reciprocal best hit calls between D.pseudoobscura and D.miranda transcripts.
RB.pse2mir.RBH.noC.new.txt: Reciprocal best hit calls between D.pseudoobscura and D.miranda transcripts, but with neo-X linked genes removed in D. miranda.
RB.pse2mir.RBH.noY.new.txt: Reciprocal best hit calls between D.pseudoobscura and D.miranda transcripts, but with neo-Y linked genes removed in D. miranda.
usearch.clust.summary: results of homology based clustering to identify multicopy genes in D.miranda.
Sharing/Access information
Raw data for scRNA-seq can be found on the Sequenced Read Archive under BioProject: PRJNA907067
Code/Software
n/a