Regulatory logic of endogenous RNAi in silencing de novo genomic conflicts.
Although the biological utilities of endogenous RNAi (endo-RNAi) have been largely elusive, recent studies reveal its critical role in the non-model fruitfly Drosophila simulans to suppress selfish genes, whose unchecked activities can severely impair spermatogenesis. In particular, hairpin RNA (hpR...
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| Format: | Article |
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Public Library of Science (PLoS)
2023-06-01
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| Series: | PLoS Genetics |
| Online Access: | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1010787&type=printable |
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| author | Jeffrey Vedanayagam Ching-Jung Lin Ranjith Papareddy Michael Nodine Alex S Flynt Jiayu Wen Eric C Lai |
| author_facet | Jeffrey Vedanayagam Ching-Jung Lin Ranjith Papareddy Michael Nodine Alex S Flynt Jiayu Wen Eric C Lai |
| author_sort | Jeffrey Vedanayagam |
| collection | DOAJ |
| description | Although the biological utilities of endogenous RNAi (endo-RNAi) have been largely elusive, recent studies reveal its critical role in the non-model fruitfly Drosophila simulans to suppress selfish genes, whose unchecked activities can severely impair spermatogenesis. In particular, hairpin RNA (hpRNA) loci generate endo-siRNAs that suppress evolutionary novel, X-linked, meiotic drive loci. The consequences of deleting even a single hpRNA (Nmy) in males are profound, as such individuals are nearly incapable of siring male progeny. Here, comparative genomic analyses of D. simulans and D. melanogaster mutants of the core RNAi factor dcr-2 reveal a substantially expanded network of recently-emerged hpRNA-target interactions in the former species. The de novo hpRNA regulatory network in D. simulans provides insight into molecular strategies that underlie hpRNA emergence and their potential roles in sex chromosome conflict. In particular, our data support the existence of ongoing rapid evolution of Nmy/Dox-related networks, and recurrent targeting of testis HMG-box loci by hpRNAs. Importantly, the impact of the endo-RNAi network on gene expression flips the convention for regulatory networks, since we observe strong derepression of targets of the youngest hpRNAs, but only mild effects on the targets of the oldest hpRNAs. These data suggest that endo-RNAi are especially critical during incipient stages of intrinsic sex chromosome conflicts, and that continual cycles of distortion and resolution may contribute to speciation. |
| format | Article |
| id | doaj-art-db4ee86ff50b4aa0a98d0a5cb4b1bb1b |
| institution | Kabale University |
| issn | 1553-7390 1553-7404 |
| language | English |
| publishDate | 2023-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj-art-db4ee86ff50b4aa0a98d0a5cb4b1bb1b2025-01-16T05:31:14ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042023-06-01196e101078710.1371/journal.pgen.1010787Regulatory logic of endogenous RNAi in silencing de novo genomic conflicts.Jeffrey VedanayagamChing-Jung LinRanjith PapareddyMichael NodineAlex S FlyntJiayu WenEric C LaiAlthough the biological utilities of endogenous RNAi (endo-RNAi) have been largely elusive, recent studies reveal its critical role in the non-model fruitfly Drosophila simulans to suppress selfish genes, whose unchecked activities can severely impair spermatogenesis. In particular, hairpin RNA (hpRNA) loci generate endo-siRNAs that suppress evolutionary novel, X-linked, meiotic drive loci. The consequences of deleting even a single hpRNA (Nmy) in males are profound, as such individuals are nearly incapable of siring male progeny. Here, comparative genomic analyses of D. simulans and D. melanogaster mutants of the core RNAi factor dcr-2 reveal a substantially expanded network of recently-emerged hpRNA-target interactions in the former species. The de novo hpRNA regulatory network in D. simulans provides insight into molecular strategies that underlie hpRNA emergence and their potential roles in sex chromosome conflict. In particular, our data support the existence of ongoing rapid evolution of Nmy/Dox-related networks, and recurrent targeting of testis HMG-box loci by hpRNAs. Importantly, the impact of the endo-RNAi network on gene expression flips the convention for regulatory networks, since we observe strong derepression of targets of the youngest hpRNAs, but only mild effects on the targets of the oldest hpRNAs. These data suggest that endo-RNAi are especially critical during incipient stages of intrinsic sex chromosome conflicts, and that continual cycles of distortion and resolution may contribute to speciation.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1010787&type=printable |
| spellingShingle | Jeffrey Vedanayagam Ching-Jung Lin Ranjith Papareddy Michael Nodine Alex S Flynt Jiayu Wen Eric C Lai Regulatory logic of endogenous RNAi in silencing de novo genomic conflicts. PLoS Genetics |
| title | Regulatory logic of endogenous RNAi in silencing de novo genomic conflicts. |
| title_full | Regulatory logic of endogenous RNAi in silencing de novo genomic conflicts. |
| title_fullStr | Regulatory logic of endogenous RNAi in silencing de novo genomic conflicts. |
| title_full_unstemmed | Regulatory logic of endogenous RNAi in silencing de novo genomic conflicts. |
| title_short | Regulatory logic of endogenous RNAi in silencing de novo genomic conflicts. |
| title_sort | regulatory logic of endogenous rnai in silencing de novo genomic conflicts |
| url | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1010787&type=printable |
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