Drosophila Interspecific Hybrids Phenocopy piRNA-Pathway Mutants

Kelleher, Erin S.; Edelman, Nathaniel B.; Barbash, Daniel A.

doi:10.1371/journal.pbio.1001428

Cited by 92 publications

(130 citation statements)

References 85 publications

(153 reference statements)

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“…2A, 3B). Finally, the activity of endogenous clusters in D. melanogaster also seems to require a maternally inherited factor: Our analysis of previously published piRNA profiles in interspecies hybrids between D. melanogaster females and Drosophila simulans males (Kelleher et al 2012) showed that only D. melanogaster piRNA clusters generated piRNAs, while D. simulans piRNA clusters were inactive (Supplemental Fig. S12).…”

Section: Discussionmentioning

confidence: 92%

“…Libraries were sequenced on the Illumina HiSeq 2000 (50-bp reads) platform. Data sets for piRNAs were extracted from available Gene Expression Omnibus (GEO) data (Kelleher et al 2012): D. melanogaster, SRX205641; D. simulans, SRX205642; and F1, SRX205643. The resulting sequencing reads were mapped against the genome using Bowtie 0.12.7 (Langmead et al 2009) with the following settings: ''-v 0-best-strata,'' retaining only uniquely mappable reads with zero mismatches.…”

Section: Chip and Chip-qpcrmentioning

confidence: 99%

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Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing

et al. 2014

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Small noncoding RNAs that associate with Piwi proteins, called piRNAs, serve as guides for repression of diverse transposable elements in germ cells of metazoa. In Drosophila, the genomic regions that give rise to piRNAs, the socalled piRNA clusters, are transcribed to generate long precursor molecules that are processed into mature piRNAs. How genomic regions that give rise to piRNA precursor transcripts are differentiated from the rest of the genome and how these transcripts are specifically channeled into the piRNA biogenesis pathway are not known. We found that transgenerationally inherited piRNAs provide the critical trigger for piRNA production from homologous genomic regions in the next generation by two different mechanisms. First, inherited piRNAs enhance processing of homologous transcripts into mature piRNAs by initiating the ping-pong cycle in the cytoplasm. Second, inherited piRNAs induce installment of the histone 3 Lys9 trimethylation (H3K9me3) mark on genomic piRNA cluster sequences. The heterochromatin protein 1 (HP1) homolog Rhino binds to the H3K9me3 mark through its chromodomain and is enriched over piRNA clusters. Rhino recruits the piRNA biogenesis factor Cutoff to piRNA clusters and is required for efficient transcription of piRNA precursors. We propose that transgenerationally inherited piRNAs act as an epigenetic memory for identification of substrates for piRNA biogenesis on two levels: by inducing a permissive chromatin environment for piRNA precursor synthesis and by enhancing processing of these precursors.

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Section: Discussionmentioning

confidence: 92%

Section: Chip and Chip-qpcrmentioning

confidence: 99%

Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing

et al. 2014

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“…These phenotypes, including fertility and YRV, may emerge from nongenic elements on the Y chromosome heterochromatin and may be under selection Francisco and Lemos, 2014). The piRNA pathway is a candidate to mediate Y chromosome effects in hybrids (Castillo et al, 2011;Kelleher et al, 2012) and could reconcile the low polymorphism in Y-linked protein-coding sequences (Zurovcova and Eanes, 1999;Larracuente and Clark, 2013) with YRV. Differences in the extensive blocks of heterochromatin are given by the kinds and quantities of satellite DNA and transposable elements.…”

Section: Discussionmentioning

confidence: 99%

Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

Araripe

Tao

Lemos³

2016

Heredity

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Y chromosomes display population variation within and between species. Co-evolution within populations is expected to produce adaptive interactions between Y chromosomes and the rest of the genome. One consequence is that Y chromosomes from disparate populations could disrupt harmonious interactions between co-evolved genetic elements and result in reduced male fertility, sterility or inviability. Here we address the contribution of 'heterospecific Y chromosomes' to fertility in hybrid males carrying a homozygous region of Drosophila mauritiana introgressed in the Drosophila simulans background. In order to detect Y chromosome-autosome interactions, which may go unnoticed in a single-species background of autosomes, we constructed hybrid genotypes involving three sister species: Drosophila simulans, D. mauritiana, and D. sechellia. These engineered strains varied due to: (i) species origin of the Y chromosome (D. simulans or D. sechellia); (ii) location of the introgressed D. mauritiana segment on the D. simulans third chromosome, and (iii) grandparental genomic background (three genotypes of D. simulans). We find complex interactions between the species origin of the Y chromosome, the identity of the D. mauritiana segment and the grandparental genetic background donating the chromosomes. Unexpectedly, the interaction of the Y chromosome and one segment of D. mauritiana drastically reduced fertility in the presence of Ysim, whereas the fertility is partially rescued by the Y chromosome of D. sechellia when it descends from a specific grandparental genotype. The restoration of fertility occurs in spite of an autosomal and X-linked genome that is mostly of D. simulans origin. These results illustrate the multifactorial basis of genetic interactions involving the Y chromosome. Our study supports the hypothesis that the Y chromosome can contribute significantly to the evolution of reproductive isolation and highlights the conditional manifestation of infertility in specific genotypic combinations.

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“…At the initiation of differentiation, declining levels of Oct4 allow miR-145 to be expressed, which further suppresses Oct4 and reinforces differentiation. (Rozhkov et al 2010;Kelleher et al 2012). piRNAs are derived from distinct genomic regions called piRNA clusters, which are enriched in transposon sequences.…”

Section: Pirnas Provide Long-term Genetic Memory Of Transposon Invasionsmentioning

confidence: 99%

Small but sturdy: small RNAs in cellular memory and epigenetics

2014

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Cells in multicellular organisms have distinct identities characterized by their profiles of expressed genes. Cell identities can be stable over a long time and through multiple cellular divisions but are also responsive to extracellular signals. Since the DNA sequence is identical in all cells, a “cellular memory” of expression profiles is achieved by what are defined as epigenetic mechanisms. Two major molecular principles—networks of transcription factors and maintenance of cis-chromatin modifications—have been implicated in maintaining cellular memory. Here we describe recent studies demonstrating that short noncoding RNAs can also provide molecular signals that define epigenetic states of cells. Small RNAs can act independently or cooperate with chromatin modifications to achieve long-lasting effects necessary for cellular memory and transgenerational inheritance.

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Drosophila Interspecific Hybrids Phenocopy piRNA-Pathway Mutants

Abstract: Hybrids of two Drosophila species show transposable element derepression and piRNA pathway malfunction, revealing adaptive evolution of piRNA pathway components.

Cited by 92 publications

References 85 publications

Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing

Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing

Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

Small but sturdy: small RNAs in cellular memory and epigenetics

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