Abstract:
Genomic imprinting-the non-equivalence of maternal and paternal genomes-is a critical process that has evolved independently in many plant and mammalian species1,2. According to kinship theory, imprinting is the inevitable consequence of conflictive selective forces acting on differentially expressed parental alleles3,4. Yet, how these epigenetic differences evolve in the first place is poorly understood3,5,6. Here we report the identification and molecular dissection of a parent-of-origin effect on gene expression that might help to clarify this fundamental question. Toxin-antidote elements (TAs) are selfish elements that spread in populations by poisoning non-carrier individuals7-9. In reciprocal crosses between two Caenorhabditis tropicalis wild isolates, we found that the slow-1/grow-1 TA is specifically inactive when paternally inherited. This parent-of-origin effect stems from transcriptional repression of the slow-1 toxin by the PIWI-interacting RNA (piRNA) host defence pathway. The repression requires PIWI Argonaute and SET-32 histone methyltransferase activities and is transgenerationally inherited via small RNAs. Remarkably, when slow-1/grow-1 is maternally inherited, slow-1 repression is halted by a translation-independent role of its maternal mRNA. That is, slow-1 transcripts loaded into eggs-but not SLOW-1 protein-are necessary and sufficient to counteract piRNA-mediated repression. Our findings show that parent-of-origin effects can evolve by co-option of the piRNA pathway and hinder the spread of selfish genes that require sex for their propagation.
摘要:
基因组印记-母本和父本基因组的非等效性-是在许多植物和哺乳动物物种中独立进化的关键过程1,2。根据亲属关系理论,印记是冲突选择力作用于差异表达的亲本等位基因3,4的必然结果。然而,这些表观遗传差异首先是如何进化的,人们对此知之甚少3,5,6。在这里,我们报告了亲本对基因表达的影响的鉴定和分子解剖,这可能有助于澄清这一基本问题。毒素解毒剂元素(TA)是通过毒害非携带者个体在人群中传播的自私元素7-9。在两个热带秀丽隐杆线虫野生分离株之间的相互杂交中,我们发现,当父系遗传时,慢1/grow-1TA特别不活跃。这种亲本起源效应源于PIWI相互作用RNA(piRNA)宿主防御途径对慢速1毒素的转录抑制。抑制需要PIWIArgonaute和SET-32组蛋白甲基转移酶活性,并且通过小RNA进行转代遗传。值得注意的是,当slow-1/grow-1是母系遗传时,slow-1抑制通过其母体mRNA的翻译独立作用而停止。也就是说,加载到卵中的slow-1转录物-而不是SLOW-1蛋白-是必需的并且足以抵消piRNA介导的抑制。我们的发现表明,亲本效应可以通过piRNA途径的共同选择而进化,并阻碍需要性别才能繁殖的自私基因的传播。