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Journal Articles Seminars in Cell and Developmental Biology Year : 2015

Paramutation phenomena in non-vertebrate animals


Paramutation was initially described in maize and was defined as an epigenetic interaction between two alleles of a locus, through which one allele induces a heritable modification of the other allele without modifying the DNA sequence [1] and [2]. Thus it implies that the paramutated allele conserves its new properties on the long term over generations even in the absence of the paramutagenic allele and that it turns paramutagenic itself, without undergoing any changes in the DNA sequence. Some epigenetic interactions have been described in two non-vertebrate animal models, which appear to exhibit similar properties. Both systems are linked to trans-generational transmission of non-coding small RNAs. In Drosophila melanogaster, paramutation is correlated with transmission of PIWI-Interacting RNAs (piRNAs), a class of small non-coding RNAs that repress mobile DNA in the germline. A tandem repeated transgenic locus producing abundant ovarian piRNAs can activate piRNA production and associated homology-dependent silencing at a locus that was previously stably devoid of such capacities. The newly converted locus is then perfectly stable in absence of the inducer locus (>100 generations) and becomes fully paramutagenic. In Caenorhabditis elegans, paramutation is correlated with transmission of siRNAs, which are produced by transgenes targeted by piRNAs in the germline. Indeed, a transgenic locus, targeted by the piRNA machinery, produces siRNAs that can induce silencing of homologous transgenes, which can be further transmitted in a repressed state over generations despite the absence of the inducer transgenic locus. As in fly, the paramutated locus can become fully paramutagenic, and paramutation can be mediated by cytoplasmic inheritance without transmission of the paramutagenic locus itself. Nevertheless, in contrast to flies where the induction is only maternally inherited, both parents can transmit it in worms. In addition, a reciprocal phenomenon – (from off toward on) – appears to be also possible in worms as some activated transgenes can reactivate silent transgenes in the germline, and this modification can also be transmitted to next generations, even so it appears to be only partially stable. Thus, in a given system, opposite paramutation-like phenomena could exist, mediated by antagonist active pathways. As in plants, paramutation in flies and worms correlates with chromatin structure modification of the paramutated locus. In flies, inheritance of small RNAs from one generation to the next transmits a memory mainly targeting loci for repression whereas in worms, small RNAs can target loci either for repression or expression. Nevertheless, in the two species, paramutation can play an important role in the epigenome establishment.
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hal-01204543 , version 1 (28-09-2015)



Stéphane Ronsseray. Paramutation phenomena in non-vertebrate animals. Seminars in Cell and Developmental Biology, 2015, 44, pp.39-46. ⟨10.1016/j.semcdb.2015.08.009⟩. ⟨hal-01204543⟩
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