Abstract
Background Heterogametic species display a differential number of sex chromosomes resulting in imbalanced transcription levels for these chromosomes between males and females. To correct this disequilibrium, dosage compensation mechanisms involving gene expression and chromatin accessibility regulations have emerged throughout evolution. In insects, these mechanisms have been extensively characterized only in Drosophila but not in insects of agronomical importance. Aphids are indeed major pests of a wide range of crops. Their remarkable ability to switch from asexual to sexual reproduction during their life cycle largely explains the economic losses they can cause. As heterogametic insects, male aphids are X0, while females (asexual and sexual) are XX.ResultsHere, we analyzed transcriptomic and open chromatin data obtained from whole male and female individuals to evaluate the putative existence of a dosage compensation mechanism involving differential chromatin accessibility of the pea aphid’s X chromosome. Transcriptomic analyses first showed X/AA and XX/AA expression ratios for expressed genes close to 1 in males and females, respectively, suggesting dosage compensation in the pea aphid. Analyses of open chromatin data obtained by Formaldehyde-Assisted Isolation of Regulatory Elements (FAIRE-seq) revealed a X chromosome chromatin accessibility globally and significantly higher in males than in females, while autosomes’ chromatin accessibility is similar between sexes. Moreover, chromatin environment of X-linked genes displaying similar expression levels in males and females—and thus likely to be compensated—is significantly more accessible in males.ConclusionsOur results suggest the existence of an underlying epigenetic mechanism enhancing the X chromosome chromatin accessibility in males to allow X-linked gene dose correction between sexes in the pea aphid, similar to Drosophila. Our study gives new evidence into the comprehension of dosage compensation in link with chromatin biology in insects and newly in a major crop pest, taking benefits from both transcriptomic and open chromatin data.
Highlights
Heterogametic species display a differential number of sex chromosomes resulting in imbalanced transcription levels for these chromosomes between males and females
X-linked genes expressed at the same level in males and females and, likely to be compensated, have significantly higher chromatin accessibility in males than in females, notably in the transcription start sites (TSSs). These results suggest that a potential global regulation of chromatin accessibility might occur on the X chromosome of aphids to compensate for the gene dose in males
We reanalyzed previously published A. pisum RNA-seq data from wholeindividual males and parthenogenetic females [34] in regard to this new gene assignation to characterize the expression level of the 19,232 and 13,711 genes located on the X and autosomes, respectively
Summary
Heterogametic species display a differential number of sex chromosomes resulting in imbalanced transcription levels for these chromosomes between males and females To correct this disequilibrium, dosage com‐ pensation mechanisms involving gene expression and chromatin accessibility regulations have emerged throughout evolution. Dosage compensation mechanisms are thought to have evolved to correct such disequilibrium These mechanisms tend to generate equilibrated X-linked and autosomal transcript levels, often resulting in XX/AA and X/AA expression ratios equal to 1 in both the homogametic (XX) and the heterogametic (XY or X0) sexes, and of XX/X ratios equal to 1, as described in several model organisms such as Eutherian mammals [2, 6,7,8,9], Caenorhabditis elegans [9,10,11] and the insect model Drosophila melanogaster [12,13,14]. A partial dosage compensation was found in Strepsiptera [18], and no compensation was detectable in Teleopsis dalmanni [19]
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