Abstract
XY systems usually show chromosome-wide compensation of X-linked genes, while in many ZW systems, compensation is restricted to a minority of dosage-sensitive genes. Why such differences arose is still unclear. Here, we combine comparative genomics, transcriptomics and proteomics to obtain a complete overview of the evolution of gene dosage on the Z-chromosome of Schistosoma parasites. We compare the Z-chromosome gene content of African (Schistosoma mansoni and S. haematobium) and Asian (S. japonicum) schistosomes and describe lineage-specific evolutionary strata. We use these to assess gene expression evolution following sex-linkage. The resulting patterns suggest a reduction in expression of Z-linked genes in females, combined with upregulation of the Z in both sexes, in line with the first step of Ohno's classic model of dosage compensation evolution. Quantitative proteomics suggest that post-transcriptional mechanisms do not play a major role in balancing the expression of Z-linked genes.
Highlights
In species with separate sexes, genetic sex determination is often present in the form of differentiated sex chromosomes [1]
The loss of one gene copy on the Y/W is predicted to result in a two-fold reduction of expression in the heterogametic sex, as gene expression is correlated to gene copy number [12]
Available raw reads were used for S. mansoni and S. haematobium (Wellcome Trust Sanger Institute Bioprojects PREJB2320 and PREJB2425), while male and female S. japonicum were sequenced for this study
Summary
In species with separate sexes, genetic sex determination is often present in the form of differentiated sex chromosomes [1]. Similar to what was observed using RNA-seq, the expression of Z-specific genes was strongly male-biased compared to that of autosomal genes in both heads (F:M of 0.68 for the Z chromosome versus 0.92 for the autosomes; Figure 4A, Supplementary File 1) and gonads (F:M of 0.78 versus 0.99; Figure 4B, Supplementary File 1) These F:M ratios are closer to each other than in our RNA-seq analysis (Figure 2, Supplementary File 1), or than the microarray data (Supplementary File 1), which could suggest a potential contribution of post-transcriptional regulation to dosage equalization. This similarity between Z-linked and autosomal genes holds when only genes with male-biased expression in the microarray data are considered (Figure 4-figure supplement 3), and when the transcript and protein dosage of Z-linked autosomal genes are compared within each sex (Figure 4-figure supplement 1 and 2)
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