A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila

Zsolt G Venkei; Ildar Gainetdinov; Ayca Bagci; Margaret R Starostik; Charlotte P Choi; Jaclyn M Fingerhut; Peiwei Chen; Chiraag Balsara; Troy W Whitfield; George W Bell; Suhua Feng; Steven E Jacobsen; Alexei A Aravin; John K Kim; Phillip D Zamore; Yukiko M Yamashita

doi:10.1038/s41556-023-01227-4

A maternally programmed intergenerational mechanism enables male offspring to make piRNAs from Y-linked precursor RNAs in Drosophila

Nat Cell Biol. 2023 Oct;25(10):1495-1505. doi: 10.1038/s41556-023-01227-4. Epub 2023 Sep 18.

Authors

Zsolt G Venkei^#¹, Ildar Gainetdinov^#², Ayca Bagci², Margaret R Starostik³, Charlotte P Choi³, Jaclyn M Fingerhut^{1

4}, Peiwei Chen⁵, Chiraag Balsara⁶, Troy W Whitfield¹, George W Bell¹, Suhua Feng^{7

8}, Steven E Jacobsen^{7

8

9}, Alexei A Aravin⁵, John K Kim³, Phillip D Zamore^{10

11}, Yukiko M Yamashita^{12

13}

Affiliations

¹ Whitehead Institute for Biomedical Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA.
² RNA Therapeutics Institute, University of Massachusetts Chan Medical School, Worcester, MA, USA.
³ Department of Biology, Johns Hopkins University, Baltimore, MD, USA.
⁴ Howard Hughes Medical Institute, Whitehead Institute, Massachusetts Institute of Technology, Cambridge, MA, USA.
⁵ Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA.
⁶ Life Sciences Institute, University of Michigan, Ann Arbor, MI, USA.
⁷ Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, CA, USA.
⁸ Eli and Edyth Broad Center of Regenerative Medicine and Stem Cell Research, University of California, Los Angeles, CA, USA.
⁹ Howard Hughes Medical Institute, University of California Los Angeles, Los Angeles, CA, USA.
¹⁰ RNA Therapeutics Institute, University of Massachusetts Chan Medical School, Worcester, MA, USA. phillip.zamore@umassmed.edu.
¹¹ Howard Hughes Medical Institute, University of Massachusetts Chan Medical School, Worcester, MA, USA. phillip.zamore@umassmed.edu.
¹² Whitehead Institute for Biomedical Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA. yukikomy@wi.mit.edu.
¹³ Howard Hughes Medical Institute, Whitehead Institute, Massachusetts Institute of Technology, Cambridge, MA, USA. yukikomy@wi.mit.edu.

^# Contributed equally.

Abstract

In animals, PIWI-interacting RNAs (piRNAs) direct PIWI proteins to silence complementary targets such as transposons. In Drosophila and other species with a maternally specified germline, piRNAs deposited in the egg initiate piRNA biogenesis in the progeny. However, Y chromosome loci cannot participate in such a chain of intergenerational inheritance. How then can the biogenesis of Y-linked piRNAs be initiated? Here, using Suppressor of Stellate (Su(Ste)), a Y-linked Drosophila melanogaster piRNA locus as a model, we show that Su(Ste) piRNAs are made in the early male germline via 5'-to-3' phased piRNA biogenesis initiated by maternally deposited 1360/Hoppel transposon piRNAs. Notably, deposition of Su(Ste) piRNAs from XXY mothers obviates the need for phased piRNA biogenesis in sons. Together, our study uncovers a developmentally programmed, intergenerational mechanism that allows fly mothers to protect their sons using a Y-linked piRNA locus.

MeSH terms

Animals
Argonaute Proteins / genetics
Drosophila Proteins* / genetics
Drosophila Proteins* / metabolism
Drosophila melanogaster / genetics
Drosophila melanogaster / metabolism
Drosophila* / metabolism
Piwi-Interacting RNA
RNA, Small Interfering / genetics
RNA, Small Interfering / metabolism

Substances

Piwi-Interacting RNA
Drosophila Proteins
RNA, Small Interfering
Argonaute Proteins

Abstract

MeSH terms

Substances

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