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Cross-species incompatibility between a DNA satellite and the Drosophila Spartan homolog poisons germline genome integrity

Brand, Cara L. ; Levine, Mia T.

Current biology, 2022-07, Vol.32 (13), p.2962-2971.e4 [Periódico revisado por pares]

England: Elsevier Inc

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  • Título:
    Cross-species incompatibility between a DNA satellite and the Drosophila Spartan homolog poisons germline genome integrity
  • Autor: Brand, Cara L. ; Levine, Mia T.
  • Assuntos: 359bp ; Animals ; coevolution ; DNA satellite ; DNA, Satellite - genetics ; Drosophila ; Drosophila - genetics ; Drosophila melanogaster - genetics ; Drosophila melanogaster - metabolism ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Female ; Germ Cells - metabolism ; maternal haploid ; Poisons ; Spartan ; topoisomerase II
  • É parte de: Current biology, 2022-07, Vol.32 (13), p.2962-2971.e4
  • Notas: AUTHOR CONTRIBUTIONS
    Conceptualization, M.T.L and C.L.B.; Methodology, M.T.L and C.L.B.; Investigation, M.T.L and C.L.B; Writing M.T.L and C.L.B; Funding Acquisition, M.T.L and C.L.B.
  • Descrição: Satellite DNA spans megabases of eukaryotic sequence and evolves rapidly.1–6 Paradoxically, satellite-rich genomic regions mediate strictly conserved, essential processes such as chromosome segregation and nuclear structure.7–10 A leading resolution to this paradox posits that satellite DNA and satellite-associated chromosomal proteins coevolve to preserve these essential functions.11 We experimentally test this model of intragenomic coevolution by conducting the first evolution-guided manipulation of both chromosomal protein and DNA satellite. The 359bp satellite spans an 11 Mb array in Drosophila melanogaster that is absent from its sister species, Drosophila simulans.12–14 This species-specific DNA satellite colocalizes with the adaptively evolving, ovary-enriched protein, maternal haploid (MH), the Drosophila homolog of Spartan.15 To determine if MH and 359bp coevolve, we swapped the D. simulans version of MH (“MH[sim]”) into D. melanogaster. MH[sim] triggers ovarian cell death, reduced ovary size, and loss of mature eggs. Surprisingly, the D. melanogaster mh-null mutant has no such ovary phenotypes,15 suggesting that MH[sim] is toxic in a D. melanogaster background. Using both cell biology and genetics, we discovered that MH[sim] poisons oogenesis through a DNA-damage pathway. Remarkably, deleting the D. melanogaster-specific 359bp satellite array completely restores mh[sim] germline genome integrity and fertility, consistent with a history of coevolution between these two fast-evolving loci. Germline genome integrity and fertility are also restored by overexpressing topoisomerase II (Top2), suggesting that MH[sim] interferes with Top2-mediated processing of 359bp. The observed 359bp-MH[sim] cross-species incompatibility supports a model under which seemingly inert repetitive DNA and essential chromosomal proteins must coevolve to preserve germline genome integrity. [Display omitted] •The Drosophila homolog of Spartan, maternal haploid (MH), evolves adaptively•The D. simulans version of MH is toxic to oogenesis in its sister species, D. melanogaster•D. simulans MH toxicity depends on the presence of a D. melanogaster-specific satellite array•Overexpression of Top2 mitigates this D. melanogaster-D. simulans incompatibility Rapid evolution of DNA repeats is thought to trigger rapid evolution of proteins that package and process DNA repeats. Brand and Levine genetically manipulate both protein and DNA satellite to reveal the molecular players and the chromosome biology shaped by this intragenomic coevolution.
  • Editor: England: Elsevier Inc
  • Idioma: Inglês
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  • Realização: ABCD-USP USP   Logos de Redes Sociais: Freepik

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