Conserved piRNA expression from a distinct set of piRNA cluster loci in Eutherian mammals

Gung-wei Chirn, Reazur Rahman, Yuliya A. Sytnikova, Jessica A. Matts, Mei Zeng, Daniel Gerlach, Michael Yu, Bonnie Berger, Mayumi Naramura, Benjamin T. Kile, Nelson C. Lau

Research output: Contribution to journalArticleResearchpeer-review

Abstract

The Piwi pathway is deeply conserved amongst animals because one of its essential functions is to repress transposons. However, many Piwi-interacting RNAs (piRNAs) do not base-pair to transposons and remain mysterious in their targeting function. The sheer number of piRNA cluster (piC) loci in animal genomes and infrequent piRNA sequence conservation also present challenges in determining which piC loci are most important for development. To address this question, we determined the piRNA expression patterns of piC loci across a wide phylogenetic spectrum of animals, and reveal that most genic and intergenic piC loci evolve rapidly in their capacity to generate piRNAs, regardless of known transposon silencing function. Surprisingly, we also uncovered a distinct set of piC loci with piRNA expression conserved deeply in Eutherian mammals. We name these loci Eutherian-Conserved piRNA cluster (ECpiC) loci. Supporting the hypothesis that conservation of piRNA expression across ~100 million years of Eutherian evolution implies function, we determined that one ECpiC locus generates abundant piRNAs antisense to the STOX1 transcript, a gene clinically associated with preeclampsia. Furthermore, we confirmed reduced piRNAs in existing mouse mutations at ECpiC-Asb1 and -Cbl, which also display spermatogenic defects. The Asb1 mutant testes with strongly reduced Asb1 piRNAs also exhibit up-regulated gene expression profiles. These data indicate ECpiC loci may be specially adapted to support Eutherian reproduction.

Original languageEnglish
Article numbere1005652
Number of pages26
JournalPLoS Genetics
Volume11
Issue number11
DOIs
Publication statusPublished - 20 Nov 2015
Externally publishedYes

Keywords

  • genetic loci
  • testes
  • gene expression
  • chickens
  • mammalian genomics
  • mammals
  • genomic libraries
  • sequence motif analysis

Cite this

Chirn, G., Rahman, R., Sytnikova, Y. A., Matts, J. A., Zeng, M., Gerlach, D., ... Lau, N. C. (2015). Conserved piRNA expression from a distinct set of piRNA cluster loci in Eutherian mammals. PLoS Genetics, 11(11), [e1005652]. https://doi.org/10.1371/journal.pgen.1005652
Chirn, Gung-wei ; Rahman, Reazur ; Sytnikova, Yuliya A. ; Matts, Jessica A. ; Zeng, Mei ; Gerlach, Daniel ; Yu, Michael ; Berger, Bonnie ; Naramura, Mayumi ; Kile, Benjamin T. ; Lau, Nelson C. / Conserved piRNA expression from a distinct set of piRNA cluster loci in Eutherian mammals. In: PLoS Genetics. 2015 ; Vol. 11, No. 11.
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Chirn, G, Rahman, R, Sytnikova, YA, Matts, JA, Zeng, M, Gerlach, D, Yu, M, Berger, B, Naramura, M, Kile, BT & Lau, NC 2015, 'Conserved piRNA expression from a distinct set of piRNA cluster loci in Eutherian mammals' PLoS Genetics, vol. 11, no. 11, e1005652. https://doi.org/10.1371/journal.pgen.1005652

Conserved piRNA expression from a distinct set of piRNA cluster loci in Eutherian mammals. / Chirn, Gung-wei; Rahman, Reazur; Sytnikova, Yuliya A. ; Matts, Jessica A.; Zeng, Mei; Gerlach, Daniel; Yu, Michael; Berger, Bonnie; Naramura, Mayumi; Kile, Benjamin T.; Lau, Nelson C.

In: PLoS Genetics, Vol. 11, No. 11, e1005652, 20.11.2015.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Chirn, Gung-wei

AU - Rahman, Reazur

AU - Sytnikova, Yuliya A.

AU - Matts, Jessica A.

AU - Zeng, Mei

AU - Gerlach, Daniel

AU - Yu, Michael

AU - Berger, Bonnie

AU - Naramura, Mayumi

AU - Kile, Benjamin T.

AU - Lau, Nelson C.

PY - 2015/11/20

Y1 - 2015/11/20

N2 - The Piwi pathway is deeply conserved amongst animals because one of its essential functions is to repress transposons. However, many Piwi-interacting RNAs (piRNAs) do not base-pair to transposons and remain mysterious in their targeting function. The sheer number of piRNA cluster (piC) loci in animal genomes and infrequent piRNA sequence conservation also present challenges in determining which piC loci are most important for development. To address this question, we determined the piRNA expression patterns of piC loci across a wide phylogenetic spectrum of animals, and reveal that most genic and intergenic piC loci evolve rapidly in their capacity to generate piRNAs, regardless of known transposon silencing function. Surprisingly, we also uncovered a distinct set of piC loci with piRNA expression conserved deeply in Eutherian mammals. We name these loci Eutherian-Conserved piRNA cluster (ECpiC) loci. Supporting the hypothesis that conservation of piRNA expression across ~100 million years of Eutherian evolution implies function, we determined that one ECpiC locus generates abundant piRNAs antisense to the STOX1 transcript, a gene clinically associated with preeclampsia. Furthermore, we confirmed reduced piRNAs in existing mouse mutations at ECpiC-Asb1 and -Cbl, which also display spermatogenic defects. The Asb1 mutant testes with strongly reduced Asb1 piRNAs also exhibit up-regulated gene expression profiles. These data indicate ECpiC loci may be specially adapted to support Eutherian reproduction.

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KW - genetic loci

KW - testes

KW - gene expression

KW - chickens

KW - mammalian genomics

KW - mammals

KW - genomic libraries

KW - sequence motif analysis

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Chirn G, Rahman R, Sytnikova YA, Matts JA, Zeng M, Gerlach D et al. Conserved piRNA expression from a distinct set of piRNA cluster loci in Eutherian mammals. PLoS Genetics. 2015 Nov 20;11(11). e1005652. https://doi.org/10.1371/journal.pgen.1005652