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Abstract
RNA interference (RNAi) related pathways are essential for germline development and fertility in metazoa and can contribute to inter- and trans-generational inheritance. In the nematode Caenorhabditis elegans, environmental double-stranded RNA provided by feeding can lead to heritable changes in phenotype and gene expression. Notably, transmission efficiency differs between the male and female germline, yet the underlying mechanisms remain elusive. Here we use high-throughput sequencing of dissected gonads to quantify sex-specific endogenous piRNAs, miRNAs and siRNAs in the C. elegans germline and the somatic gonad. We identify genes with exceptionally high levels of secondary 22G RNAs that are associated with low mRNA expression, a signature compatible with silencing. We further demonstrate that contrary to the hermaphrodite germline, the male germline, but not male soma, is resistant to environmental RNAi triggers provided by feeding, in line with previous work. This sex-difference in silencing efficacy is associated with lower levels of gonadal RNAi amplification products. Moreover, this tissue- and sex-specific RNAi resistance is regulated by the germline, since mutant males with a feminized germline are RNAi sensitive. This study provides important sex- and tissue-specific expression data of miRNA, piRNA and siRNA as well as mechanistic insights into sex-differences of gene regulation in response to environmental cues.
Highlights
The environment can induce changes in phenotype and gene expression that persist across multiple generations [reviewed in 1]
We describe the naturally occurring small RNA populations of female and male gonads and use genetic mutants to assign small RNAs to the two tissues of the gonad, namely the somatic gonad or the germline
These sex-and tissue-specific small RNA expression data provide an important resource for future research
Summary
The environment can induce changes in phenotype and gene expression that persist across multiple generations [reviewed in 1]. Thereafter, exogenous dsRNAs are processed by the conserved nuclease Dicer into ~22 nucleotide (nt) primary small interfering RNAs (siRNA) and incorporated into Argonaute proteins to form the RNA-induced silencing complex (RISC) [15,16]. This protein-RNA complex binds complementary mRNA sequences and initiates the production of secondary siRNA by RNA-dependent RNA polymerases (RdRP) (Fig 1A) [17,18,19]. Phenotypic changes induced by exogenous dsRNA can be transmitted over multiple generations [10,12,23,24]
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