Richard Gautier, Legeai Fabrice, Prunier-Leterme Nathalie, Bretaudeau Anthony, Tagu Denis, Jaquiéry Julie, Le Trionnaire Gaël
EGI, UMR 1349, INRA, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Domaine de la Motte, BP 35327, Le Rheu, France.
BIPAA, UMR 1349, INRA, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Campus Beaulieu, Rennes, France.
Epigenetics Chromatin. 2017 Jun 15;10:30. doi: 10.1186/s13072-017-0137-1. eCollection 2017.
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.
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.
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.
异配性别物种的性染色体数量不同，导致这些染色体在雄性和雌性之间的转录水平不均衡。为了纠正这种失衡，在整个进化过程中出现了涉及基因表达和染色质可及性调控的剂量补偿机制。在昆虫中，这些机制仅在果蝇中得到了广泛的表征，而在具有农业重要性的昆虫中尚未得到充分研究。蚜虫确实是多种作物的主要害虫。它们在生命周期中从无性繁殖转变为有性繁殖的显著能力在很大程度上解释了它们可能造成的经济损失。作为异配性别昆虫，雄性蚜虫为X0，而雌性（无性和有性）为XX。
在这里，我们分析了从整个雄性和雌性个体获得的转录组和开放染色质数据，以评估豌豆蚜X染色体上是否存在涉及染色质可及性差异的剂量补偿机制。转录组分析首先表明，雄性和雌性中表达基因的X/AA和XX/AA表达比率分别接近1，这表明豌豆蚜存在剂量补偿。通过甲醛辅助调控元件分离（FAIRE-seq）获得的开放染色质数据分析显示，X染色体的染色质可及性总体上在雄性中显著高于雌性，而常染色体的染色质可及性在两性之间相似。此外，在雄性和雌性中表达水平相似且因此可能得到补偿的X连锁基因的染色质环境在雄性中显著更易接近。
我们的结果表明，存在一种潜在的表观遗传机制，可增强雄性中X染色体的染色质可及性，从而在豌豆蚜中实现两性之间X连锁基因剂量的校正，这与果蝇类似。我们的研究为理解昆虫中与染色质生物学相关的剂量补偿提供了新的证据，并且首次在一种主要作物害虫中提供了此类证据，这得益于转录组和开放染色质数据。
