Ryazansky Sergei, Radion Elizaveta, Mironova Anastasia, Akulenko Natalia, Abramov Yuri, Morgunova Valeriya, Kordyukova Maria Y, Olovnikov Ivan, Kalmykova Alla
Institute of Molecular Genetics, Russian Academy of Sciences, Moscow, Russia.
PLoS Genet. 2017 Apr 27;13(4):e1006731. doi: 10.1371/journal.pgen.1006731. eCollection 2017 Apr.
In the Drosophila germline, transposable elements (TEs) are silenced by PIWI-interacting RNA (piRNA) that originate from distinct genomic regions termed piRNA clusters and are processed by PIWI-subfamily Argonaute proteins. Here, we explore the variation in the ability to restrain an alien TE in different Drosophila strains. The I-element is a retrotransposon involved in the phenomenon of I-R hybrid dysgenesis in Drosophila melanogaster. Genomes of R strains do not contain active I-elements, but harbour remnants of ancestral I-related elements. The permissivity to I-element activity of R females, called reactivity, varies considerably in natural R populations, indicating the existence of a strong natural polymorphism in defense systems targeting transposons. To reveal the nature of such polymorphisms, we compared ovarian small RNAs between R strains with low and high reactivity and show that reactivity negatively correlates with the ancestral I-element-specific piRNA content. Analysis of piRNA clusters containing remnants of I-elements shows increased expression of the piRNA precursors and enrichment by the Heterochromatin Protein 1 homolog, Rhino, in weak R strains, which is in accordance with stronger piRNA expression by these regions. To explore the nature of the differences in piRNA production, we focused on two R strains, weak and strong, and showed that the efficiency of maternal inheritance of piRNAs as well as the I-element copy number are very similar in both strains. At the same time, germline and somatic uni-strand piRNA clusters generate more piRNAs in strains with low reactivity, suggesting the relationship between the efficiency of primary piRNA production and variable response to TE invasions. The strength of adaptive genome defense is likely driven by naturally occurring polymorphisms in the rapidly evolving piRNA pathway proteins. We hypothesize that hyper-efficient piRNA production is contributing to elimination of a telomeric retrotransposon HeT-A, which we have observed in one particular transposon-resistant R strain.
在果蝇生殖系中，转座元件（TEs）被与PIWI相互作用的RNA（piRNA）沉默，这些piRNA起源于称为piRNA簇的不同基因组区域，并由PIWI亚家族的AGO蛋白加工处理。在此，我们探究了不同果蝇品系抑制外来TE能力的差异。I元件是一种逆转座子，参与黑腹果蝇的I-R杂种不育现象。R品系的基因组不包含活跃的I元件，但含有祖先I相关元件的残余。R雌性对I元件活性的易感性，即反应性，在天然R种群中差异很大，这表明在针对转座子的防御系统中存在强烈的自然多态性。为了揭示这种多态性的本质，我们比较了反应性低和高的R品系之间的卵巢小RNA，结果表明反应性与祖先I元件特异性piRNA含量呈负相关。对含有I元件残余的piRNA簇的分析表明，在反应性弱的R品系中，piRNA前体的表达增加，异染色质蛋白1同源物Rhino富集，这与这些区域更强的piRNA表达一致。为了探究piRNA产生差异的本质，我们聚焦于两个R品系，即反应性弱和强的品系，结果表明piRNA的母系遗传效率以及I元件拷贝数在这两个品系中非常相似。同时，生殖系和体细胞单链piRNA簇在反应性低的品系中产生更多的piRNA，这表明初级piRNA产生效率与对TE入侵的可变反应之间存在关联。适应性基因组防御的强度可能由快速进化的piRNA途径蛋白中的自然多态性驱动。我们推测，高效的piRNA产生有助于消除端粒逆转座子HeT-A，我们在一个特定的抗转座子R品系中观察到了这一现象。
