Abstract
BackgroundThe Drosophila miranda neo-sex chromosome system is a useful resource for studying recently evolved sex chromosomes. However, the neo-Y genomic assembly is fragmented due to the accumulation of repetitive sequence. Furthermore, the separate assembly of the neo-X and neo-Y chromosomes into genomic scaffolds has proven to be difficult, due to their low level of sequence divergence, which in coding regions is about 1.5%. Here, we de novo assemble the transcriptome of D. miranda using RNA-seq data from several male and female tissues, and develop a bioinformatic pipeline to separately reconstruct neo-X and neo-Y transcripts.ResultsWe obtain 2,141 transcripts from the neo-X and 1,863 from the neo-Y. Neo-Y transcripts are generally shorter than their homologous neo-X transcripts (N50 of 2,048-bp vs. 2,775-bp) and expressed at lower levels. We find that 24% of expressed neo-Y transcripts harbor nonsense mutation within their open reading frames, yet most non-functional neo-Y genes are expressed throughout all of their length. We find evidence of gene loss of male-specific genes on the neo-X chromosome, and transcriptional silencing of testis-specific genes from the neo-X.ConclusionsNonsense mediated decay (NMD) has been implicated to degrade transcripts containing pre-mature termination codons (PTC) in Drosophila, but rampant description of neo-Y genes with pre-mature stop codons suggests that it does not play a major role in down-regulating transcripts from the neo-Y. Loss or transcriptional down-regulation of genes from the neo-X with male-biased function provides evidence for beginning demasculinization of the neo-X. Thus, evolving sex chromosomes can rapidly shift their gene content or patterns of gene expression in response to their sex-biased transmission, supporting the idea that sex-specific or sexually antagonistic selection plays a major role in the evolution of heteromorphic sex chromosomes.
Highlights
The Drosophila miranda neo-sex chromosome system is a useful resource for studying recently evolved sex chromosomes
The final D. miranda transcriptome assembly, which has been submitted to NCBI under the accession number GALP00000000, contained 12,522 protein-coding genes, including 2,141 from the neo-X, 1,863 from the neo-Y and 8,500 from the autosomes/ ancestral sex chromosomes
Our de novo transcriptome captures a large fraction of genes present on the neo-sex chromosomes, with 1,754 protein-coding genes being expressed from both the neo-X and neo-Y, 387 transcripts only being detected from the neo-X, and 109 transcripts only from the neo-Y
Summary
The Drosophila miranda neo-sex chromosome system is a useful resource for studying recently evolved sex chromosomes. The separate assembly of the neo-X and neo-Y chromosomes into genomic scaffolds has proven to be difficult, due to their low level of sequence divergence, which in coding regions is about 1.5%. The Drosophila miranda neo-sex chromosome system is emerging as a useful resource to study the evolution of young sex chromosomes [7,8,9]. The genome sequence of D. miranda has recently been published, including a draft assembly of the neo-Y chromosome [9]. The use of diagnostic SNPs for expression analysis will lead to an inherent mapping bias towards higher neo-X expression, since RNA-Seq reads can overlap with parts of transcripts that differ structurally between the neo-X and neo-Y. There is considerable interest to study the neo-sex transcriptome directly, which we do here
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