Biogenesis pathways of piRNAs loaded onto AGO3 in the Drosophila testis

Akihiro Nagao, Toutai Mituyama, Haidong Huang, Dahua Chen, Mikiko C. Siomi, Haruhiko Siomi

Research output: Contribution to journalArticle

66 Citations (Scopus)

Abstract

PIWI-interacting RNAs (piRNAs) silence transposable elements in animal germ cells. In Drosophila ovaries, piRNAs are produced by two distinct pathways: the "ping-pong" amplification cycle that operates in germ cells and a ping-pong-independent pathway termed the primary pathway that mainly operates in somatic cells. AGO3, one of three PIWI proteins in flies, is involved in the ping-pong cycle in ovaries. We characterized AGO3-associated piRNAs in fly testes and found that like in ovaries, AGO3 functions in the ping-pong cycle with Aubergine (Aub) for piRNA production from transposon transcripts. In contrast, most AGO3-associated piRNAs corresponding to Suppressor of Stellate [Su(Ste)] genes are antisense-oriented and bound to Aub. In addition, the vast majority of AGO3-bound piRNAs derived from the AT-chX locus on chromosome X are antisense-oriented and are also found among Aub-associated piRNAs. The presence of very few sense Su(Ste) and AT-chX piRNAs suggests that biogenesis of both Su(Ste) and AT-chX piRNAs by a ping-pong mechanism only is highly unlikely. Nevertheless, the mutual interdependence of AGO3 and Aub for the accumulation of these piRNAs shows that their production relies on both AGO3 and Aub. Analysis of piRNA pathway mutants revealed that although the requirements for piRNA factors for Su(Ste)- and AT-chX-piRNA levels mostly overlap and resemble those for the ping-pong mechanism in the ovaries, Armitage (armi) is not required for the accumulation of AT-chX-1 piRNA. These findings suggest that the impacts of armi mutants on the operation of the piRNA pathway are variable in germ cells of fly testes. Published by Cold Spring Harbor Laboratory Press.

Original languageEnglish
Pages (from-to)2503-2515
Number of pages13
JournalRNA
Volume16
Issue number12
DOIs
Publication statusPublished - 2010 Dec

Fingerprint

Drosophila
Testis
Solanum melongena
RNA
Small Interfering RNA
Ovary
Germ Cells
Diptera
Suppressor Genes
DNA Transposable Elements
X Chromosome

Keywords

  • AGO3
  • Aubergine
  • Drosophila
  • Germline
  • piRNA
  • RNA silencing

ASJC Scopus subject areas

  • Molecular Biology

Cite this

Nagao, A., Mituyama, T., Huang, H., Chen, D., Siomi, M. C., & Siomi, H. (2010). Biogenesis pathways of piRNAs loaded onto AGO3 in the Drosophila testis. RNA, 16(12), 2503-2515. https://doi.org/10.1261/rna.2270710

Biogenesis pathways of piRNAs loaded onto AGO3 in the Drosophila testis. / Nagao, Akihiro; Mituyama, Toutai; Huang, Haidong; Chen, Dahua; Siomi, Mikiko C.; Siomi, Haruhiko.

In: RNA, Vol. 16, No. 12, 12.2010, p. 2503-2515.

Research output: Contribution to journalArticle

Nagao, A, Mituyama, T, Huang, H, Chen, D, Siomi, MC & Siomi, H 2010, 'Biogenesis pathways of piRNAs loaded onto AGO3 in the Drosophila testis', RNA, vol. 16, no. 12, pp. 2503-2515. https://doi.org/10.1261/rna.2270710
Nagao A, Mituyama T, Huang H, Chen D, Siomi MC, Siomi H. Biogenesis pathways of piRNAs loaded onto AGO3 in the Drosophila testis. RNA. 2010 Dec;16(12):2503-2515. https://doi.org/10.1261/rna.2270710
Nagao, Akihiro ; Mituyama, Toutai ; Huang, Haidong ; Chen, Dahua ; Siomi, Mikiko C. ; Siomi, Haruhiko. / Biogenesis pathways of piRNAs loaded onto AGO3 in the Drosophila testis. In: RNA. 2010 ; Vol. 16, No. 12. pp. 2503-2515.
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