Abstract
Heterochromatin is made of repetitive sequences, mainly transposable elements (TEs), the regulation of which is critical for genome stability. We have analyzed the role of the heterochromatin-associated Su(var)3–7 protein in Drosophila ovaries. We present evidences that Su(var)3–7 is required for correct oogenesis and female fertility. It accumulates in heterochromatic domains of ovarian germline and somatic cells nuclei, where it co-localizes with HP1. Homozygous mutant females display ovaries with frequent degenerating egg-chambers. Absence of Su(var)3–7 in embryos leads to defects in meiosis and first mitotic divisions due to chromatin fragmentation or chromosome loss, showing that Su(var)3–7 is required for genome integrity. Females homozygous for Su(var)3–7 mutations strongly impair repression of P-transposable element induced gonadal dysgenesis but have minor effects on other TEs. Su(var)3–7 mutations reduce piRNA cluster transcription and slightly impact ovarian piRNA production. However, this modest piRNA reduction does not correlate with transposon de-silencing, suggesting that the moderate effect of Su(var)3–7 on some TE repression is not linked to piRNA production. Strikingly, Su(var)3–7 genetically interacts with the piwi and aubergine genes, key components of the piRNA pathway, by strongly impacting female fertility without impairing transposon silencing. These results lead us to propose that the interaction between Su(var)3–7 and piwi or aubergine controls important developmental processes independently of transposon silencing.
Highlights
IntroductionHeterochromatic regions are late replicating, more condensed, predominantly located near centromeres and telomeres, and contain only a few genes
Constitutive heterochromatin is a nearly universal component of eukaryotic genomes
Among Su(var)3–7 euchromatic sites, 73% are bound by HP1 and 58% are shared by the three partners of constitutive heterochromatin, Su(var)3–9, HP1 and Su(var)3–7 (Table S1)
Summary
Heterochromatic regions are late replicating, more condensed, predominantly located near centromeres and telomeres, and contain only a few genes. They are associated with specific proteins as, in Drosophila, methylated H3K9, HP1, a chromo domain protein, Su(var), a histone-methyltransferase responsible for H3K9 methylation and Su(var). Genomic sites containing full-length or defective copies of TEs can establish a complete repression of the other copies of the same family scattered throughout the genome [8]. This repression was shown to occur via small RNAs mediated silencing. In Drosophila gonads, small RNAs of 23–30 nucleotides in length, called piRNAs, are derived from transposons and repetitive elements dispersed in the genome [9]. piRNAs bind proteins of the Piwi subfamily of Argonaute proteins, and serve as guide to silence their targets through complementary base-pairing [10,11]
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