piRNA-mediated transgenerational inheritance of an acquired trait
Open accessAbstract
The maintenance of genome integrity is an essential trait to the successful transmission of genetic information. In animal germ cells, piRNAs guide PIWI proteins to silence transposable elements (TEs) in order to maintain genome integrity. In insects, most TE silencing in the germline is achieved by secondary piRNAs that are produced by a feed-forward loop (the ping-pong cycle), which requires the piRNA-directed cleavage of two types of RNAs: mRNAs of functional euchromatic TEs and heterochromatic transcripts that contain defective TE sequences. The first cleavage that initiates such an amplification loop remains poorly understood. Taking advantage of the existence of strains that are devoid of functional copies of the LINE-like I-element, we report here that in such Drosophila ovaries, the initiation of a ping-pong cycle is exclusively achieved by secondary I-element piRNAs that are produced in the ovary and deposited in the embryonic germline. This unusual secondary piRNA biogenesis, detected in the absence of functional I-element copies, results from the processing of sense and antisense transcripts of several different defective I-element. Once acquired, for instance after ancestor aging, this capacity to produce heterochromatic-only secondary piRNAs is partially transmitted through generations via maternal piRNAs. Furthermore, such piRNAs acting as ping-pong initiators in a chromatin-independent manner confer to the progeny a high capacity to repress the I-element mobility. Our study explains, at the molecular level, the basis for epigenetic memory of maternal immunity that protects females from hybrid dysgenesis caused by transposition of paternally inherited functional I-element.
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piRNAs are inherited maternally and can be amplified by a ping-pong system, helping the organism resist new invasions and adapt its genome to them.
“piRNAs are maternally heritable and can be amplified via a ping-pong system, effectively allowing the organism to resist new invasions and adapt their genome to them 69 .”
From Advances in epigenetics link genetics to the environment and disease (2019) · cites this paper as [69]
In Drosophila, piRNAs produce transgenerational epigenetic inheritance in response to transposable element activity.
“In Drosophila (Fig. 3c), heterochromatin components can induce TEI upon heat shock or osmotic stress 108 , whereas piRNAs produce TEI in response to transposable element activity 69 .”
From Advances in epigenetics link genetics to the environment and disease (2019) · cites this paper as [69]
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Research works printed but not linked: 1
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Advances in epigenetics link genetics to the environment and disease
Cavalli, G., & Heard, E. (2019) · Nature · doi:10.1038/s41586-019-1411-0 · Cited by 1,509 · see citing works
Gapp, K., von Ziegler, L., Tweedie‐Cullen, R. Y., & Mansuy, I. M. (2014) · BioEssays · doi:10.1002/bies.201300116 · Cited by 136 · see citing works
- Authors
- Grentzinger, T., Armenise, C., Brun, C., Mugat, B., Serrano, V., Pelisson, A., & Chambeyron, S.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Chambeyron, Séverine
- Venue
- Genome Research
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2012-05-03
- Volume
- 22
- Issue
- 10
- Pages
- 1877-1888
- ISSN
- 1088-9051 (ISSN-L)
- PMC
- PMC3460183
- OpenAlex
- W2157193551
- Cited by
- 162
- References
- 60
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 7 · 2023: 4 · 2022: 11 · 2021: 6 · 2020: 15 · 2019: 15 · 2018: 6 · 2017: 14 · 2016: 8 · 2015: 13 · 2014: 24 · 2013: 26 · 2012: 3
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genome Research (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by-nc)
- Funders
- Association pour la Recherche sur le Cancer
- Agence Nationale de la Recherche
- Centre National de la Recherche Scientifique
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- piRNA, transgenerational inheritance, ping-pong cycle, transposon silencing, Drosophila, epigenetic memory, hybrid dysgenesis, germline, transposon mobility
- MeSH terms
- Aging, Animals, Chromatin, DNA Transposable Elements, Drosophila, Female, Male, RNA Precursors, Transcription, Genetic, Quantitative Trait, Heritable, Gene Silencing, RNA, Small Interfering
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