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Epigenetics Chromatin. 2017 Jun 15;10:30. doi: 10.1186/s13072-017-0137-1. eCollection 2017.

Dosage compensation and sex-specific epigenetic landscape of the X chromosome in the pea aphid.

Author information

1
EGI, UMR 1349, INRA, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Domaine de la Motte, BP 35327, Le Rheu, France.
2
BIPAA, UMR 1349, INRA, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Campus Beaulieu, Rennes, France.
3
Genscale, INRIA, IRISA, Campus Beaulieu, Rennes, France.
4
Genouest, INRIA, IRISA, Campus Beaulieu, Rennes, France.
5
CNRS, UMR 6553, EcoBio, University of Rennes 1, 35042 Rennes, France.
#
Contributed equally

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.

RESULTS:

Here, 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.

CONCLUSIONS:

Our 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.

KEYWORDS:

Acyrthosiphon pisum; Dosage compensation; Formaldehyde-Assisted Isolation of Regulatory Elements (FAIRE); Non-model organism; Open chromatin; Pea aphid; Transcriptomics; X chromosome

PMID:
28638443
PMCID:
PMC5471693
DOI:
10.1186/s13072-017-0137-1
[Indexed for MEDLINE]
Free PMC Article

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