Small-RNA-mediated transgenerational silencing of histone genes impairs fertility in piRNA mutants

PIWI-interacting RNAs (piRNAs) promote fertility in many animals. However, whether this is due to their conserved role in repressing repetitive elements (REs) remains unclear. Here, we show that the progressive loss of fertility in Caenorhabditis elegans lacking piRNAs is not caused by derepression...

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Published in:Nature cell biology Vol. 22; no. 2; pp. 235 - 245
Main Authors: Barucci, Giorgia, Cornes, Eric, Singh, Meetali, Li, Blaise, Ugolini, Martino, Samolygo, Aleksei, Didier, Celine, Dingli, Florent, Loew, Damarys, Quarato, Piergiuseppe, Cecere, Germano
Format: Journal Article
Language:English
Published: England Nature Publishing Group 01.02.2020
Subjects:
Animals
Animals, Genetically Modified
Antisense RNA
Argonaute Proteins - deficiency
Argonaute Proteins - genetics
Argonaute Proteins - metabolism
Biological Evolution
Caenorhabditis elegans
Caenorhabditis elegans - genetics
Caenorhabditis elegans - metabolism
Caenorhabditis elegans Proteins - genetics
Caenorhabditis elegans Proteins - metabolism
CRISPR-Cas Systems
Derepression
Epigenetics
Fertility
Fertility - genetics
Gene Editing
Gene expression
Gene Silencing
Genes
Heredity
Histones
Histones - genetics
Histones - metabolism
Inheritance Patterns
Mutation
Nematodes
Repetitive Sequences, Nucleic Acid
RNA, Antisense - genetics
RNA, Antisense - metabolism
RNA, Messenger - genetics
RNA, Messenger - metabolism
RNA, Small Interfering - genetics
RNA, Small Interfering - metabolism
RNA-mediated interference
Worms
ISSN:1465-7392, 1476-4679, 1476-4679
Online Access:Get full text
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Summary:PIWI-interacting RNAs (piRNAs) promote fertility in many animals. However, whether this is due to their conserved role in repressing repetitive elements (REs) remains unclear. Here, we show that the progressive loss of fertility in Caenorhabditis elegans lacking piRNAs is not caused by derepression of REs or other piRNA targets but, rather, is mediated by epigenetic silencing of all of the replicative histone genes. In the absence of piRNAs, downstream components of the piRNA pathway relocalize from germ granules and piRNA targets to histone mRNAs to synthesize antisense small RNAs (sRNAs) and induce transgenerational silencing. Removal of the downstream components of the piRNA pathway restores histone mRNA expression and fertility in piRNA mutants, and the inheritance of histone sRNAs in wild-type worms adversely affects their fertility for multiple generations. We conclude that sRNA-mediated silencing of histone genes impairs the fertility of piRNA mutants and may serve to maintain piRNAs across evolution.
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ISSN:1465-7392
1476-4679
1476-4679
DOI:10.1038/s41556-020-0462-7