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Expression analysis of Drosophila yakuba, D. santomea and hybrids to evaluate the large-X effect using Nimblegen 60-mer custom made arrays

ABSTRACT: The X chromosome has a large effect on hybrid dysfunction, particularly hybrid male sterility. Although the evidence for this so-called large-X effect is clear, its molecular causes are not yet fully understood. One possibility is that, under certain conditions, evolution proceeds faster in X-linked loci than in their autosomal counterparts due to both natural selection and their hemizygosity in males (i.e. Faster-X effect), an effect that is expected to be greatest in genes with male-biased expression. Here I studied variation in transcript abundance within and between species in Drosophila yakuba, D. santomea and their hybrid males to evaluate both the faster-X and large-X effects at the level of genome-wide gene expression. I found that expression in X-linked male-biased genes evolves faster than in their autosomal counterparts, an effect that is accompanied by a unique reduction in gene expression polymorphism. Although we do not know the precise relationship between nucleotide and gene expression changes, elevated divergence to polymorphism ratios are consistent with Darwinian selection driving expression differences between species in X-linked male-biased genes, likely enhanced by male hemizygosity. Abundant changes in both cis- and trans-regulatory elements underlie regulatory gene expression divergence in the majority of the genes analyzed despite the recent split of the two sister species. I detected a large-X effect on regulation of expression in hybrid males, affecting mostly male-biased genes but also, to a lesser degree, nonsex-biased genes. Interestingly this misexpression is concentrated mostly in autosomal genes, likely facilitated by the rapid evolution of sex-linked trans-acting factors. I conclude that the faster evolution of X-linked male-biased genes, at both protein and expression levels, can contribute to explain the large effect of the X chromosome on hybrid male sterility, possibly mediating autosomal misexpression through cis-trans interactions.

OTHER RELATED OMICS DATASETS IN: PRJNA168637

ORGANISM(S): Drosophila santomea Drosophila yakuba Drosophila yakuba x Drosophila santomea

PROVIDER: GSE38793 | GEO | 2012/09/05

SECONDARY ACCESSION(S): PRJNA168637

REPOSITORIES: GEO

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Project description:Stalk-eyed flies (family Diopsidae) are a model system for studying sexual selection due to the elongated and sexually dimorphic eye-stalks found in many species. These flies are of additional interest because their X chromosome is derived largely from an autosomal arm in other flies. To identify candidate genes required for development of dimorphic eyestalks and investigate how sex-biased expression arose on the novel X we compared gene expression between males and females using oligonucleotide microarrays and RNA from developing eyestalk tissue or adult heads in the dimorphic diopsid, Teleopsis dalmanni. Microarray analysis revealed sex-biased expression for 26% of 3,748 genes expressed in eye-antennal imaginal discs and concordant sex-biased expression for 86 genes in adult heads. Overall, 415 female-biased and 482 male-biased genes were associated with dimorphic eyestalk development but not differential expression in the adult head. Functional analysis revealed that male-biased genes are disproportionately associated with growth and mitochondrial function while female-biased genes are associated with cell differentiation and patterning or are novel transcripts. With regard to chromosomal effects, dosage compensation occurs by elevated expression of X-linked genes in males. Genes with female-biased expression were more common on the X and less common on autosomes than expected, while male-biased genes exhibited no chromosomal pattern. Rates of protein evolution were lower for female-biased genes but higher for genes that moved on or off the novel X chromosome. These findings cannot be due to meiotic sex chromosome inactivation or by constraints associated with dosage compensation. Instead, they could be consistent with sexual conflict in which female-biased genes on the novel X act primarily to reduce eyespan in females while other genes increase eyespan in both sexes. Additional information on sex-biased gene expression in other tissues and related sexually monomorphic species could confirm this interpretation.

Project description:Drosophila males double transcription of their single X chromosome to equalize X-linked gene expression with females, which carry two X chromosomes. Increased transcription requires the Male-Specific Lethal (MSL) complex. One of the primary functions of the MSL complex is thought to be enrichment of H4Ac16 on the male X chromosome, a modification linked to elevated transcription. The roX1 and roX2 RNAs are essential but redundant components of the MSL complex. Simultaneous removal of both roX RNAs reduces MSL X-localization and leads to ectopic binding of these proteins at autosomal sites and to the chromocenter. Some H4Ac16 accumulates at these ectopic sites in roX1- roX2- males, suggesting the possibility of increased expression. The global effect of roX mutations on gene expression was measured by microarray analysis. We found that expression of the X chromosome was decreased by 26% in roX1- roX2- male larvae, supporting the involvement of roX RNAs in the up-regulation of X-linked genes. This finding is broadly comparable to reports of reduced X chromosome expression following msl2 RNAi knockdown in S2 cells. In spite of strong MSL binding and H4Ac16 accumulation at autosomal sites in roX1- roX2- males, enhanced gene expression could not be detected at these sites by microarray analysis or reverse northern blotting. Thus, failure to compensate X-linked genes, rather than inappropriate up-regulation of autosomal genes at ectopic sites of MSL binding, appears to cause male lethality upon loss of roX RNAs. Experiment Overall Design: Total RNA was prepared from groups of 50 third instar larvae by TRIzol (Invitrogen) extraction and purified using the RNeasy kit (Qiagen). Three independent RNA preparations for each genotype served as templates for probe synthesis. Affymetrix Drosophila Genome 2.0 chips were hybridized to these probes (Santa Clara, CA). The affymertrix Drosophila annotation of December 2004 was used to map genes to their cytological locations. Genes were filtered for present/absent calls by a PM-MM (Perfect match- Mismatch) comparison. Autosomal transcripts were normalized on a chip-by-chip basis to bring their median values to 100. The identical degree of adjustment was used to normalize X-linked transcripts. Changes in gene expression were determined by comparing the mean signal intensities of genes on arrays hybridized with roX1SMC17A roX2- probes to those hybridized with roX1+ roX2- probes.

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Expression analysis of Drosophila yakuba, D. santomea and hybrids to evaluate the large-X effect using Nimblegen 60-mer custom made arrays

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