Programmed genome rearrangements in ciliates
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Institut de Biologie de l’Ecole Normale Supérieure (IBENS), CNRS UMR 8197, Inserm U1024
46, rue d’Ulm
75005 Paris
France
Scientific Interest
Ciliates are unicellular eukaryotes that control transposable elements (TEs) in a radical manner, intimately connected to their characterisic nuclear dimorphism. In the germline micronuclei, which only serve to undergo meiosis during sexual events, TEs are safely kept inactive by the complete lack of any gene expression. During development of the polyploid somatic macronucleus, where genes are expressed, programmed genome rearrangements reproducibly remove all TE copies, and numerous single-copy remnants of ancient insertions are precisely excised from cellular genes. Our team uses the model species Paramecium tetraurelia to study the mechanisms of developmental DNA elimination and the epigenetic pathways ensuring its specificity. These include piRNA-like small RNAs that mediate a genomic subtraction between germline and somatic genomes during meiosis, thus allowing the zygote to later reproduce the same deletions as in the parental clone. While these homology-dependent processes are essential for elimination of TEs and the most recently derived single-copy insertions, they are no longer required for excision of the oldest, suggesting a transition to other, still elusive recognition mechanisms. The latter are a focus of current research in collaboration with other teams, which uses comparative genomics of a set of sibling species to reconstruct the evolutionary history of TE insertions in the Paramecium germline, their progressive decay into single-copy remnants, and the associated transitions in defence mechanisms that together maintain continuous recognition of non-self DNA insertions as they age. The comparative genomics data also support studies of (i) the domestication of TE genes by the host, in particular to serve in DNA elimination, and (ii) the co-optation of the excision machinery to target cellular genes, instead of TEs or derived sequences, for regulatory purposes: such is the case of genes involved in mating-type determination, where similar alternative rearrangements evolved independently in sibling species.
Ciliates are unicellular eukaryotes that control transposable elements (TEs) in a radical manner, intimately connected to their characterisic nuclear dimorphism. In the germline micronuclei, which only serve to undergo meiosis during sexual events, TEs are safely kept inactive by the complete lack of any gene expression. During development of the polyploid somatic macronucleus, where genes are expressed, programmed genome rearrangements reproducibly remove all TE copies, and numerous single-copy remnants of ancient insertions are precisely excised from cellular genes. Our team uses the model species Paramecium tetraurelia to study the mechanisms of developmental DNA elimination and the epigenetic pathways ensuring its specificity. These include piRNA-like small RNAs that mediate a genomic subtraction between germline and somatic genomes during meiosis, thus allowing the zygote to later reproduce the same deletions as in the parental clone. While these homology-dependent processes are essential for elimination of TEs and the most recently derived single-copy insertions, they are no longer required for excision of the oldest, suggesting a transition to other, still elusive recognition mechanisms. The latter are a focus of current research in collaboration with other teams, which uses comparative genomics of a set of sibling species to reconstruct the evolutionary history of TE insertions in the Paramecium germline, their progressive decay into single-copy remnants, and the associated transitions in defence mechanisms that together maintain continuous recognition of non-self DNA insertions as they age. The comparative genomics data also support studies of (i) the domestication of TE genes by the host, in particular to serve in DNA elimination, and (ii) the co-optation of the excision machinery to target cellular genes, instead of TEs or derived sequences, for regulatory purposes: such is the case of genes involved in mating-type determination, where similar alternative rearrangements evolved independently in sibling species.
