scholarly journals Rapid evolution and conserved function of the piRNA pathway

Open Biology ◽  
2019 ◽  
Vol 9 (1) ◽  
pp. 180181 ◽  
Author(s):  
Swapnil S. Parhad ◽  
William E. Theurkauf
Keyword(s):  
Phylogenetic Diversity ◽  
Gene Evolution ◽  
Rapid Evolution ◽  
Dna Breaks ◽  
Germline Development ◽  
Transposon Silencing ◽  
Core Function ◽  
Major Genome ◽  
Host Defence System ◽  
Pirna Pathway

Transposons are major genome constituents that can mobilize and trigger mutations, DNA breaks and chromosome rearrangements. Transposon silencing is particularly important in the germline, which is dedicated to transmission of the inherited genome. Piwi-interacting RNAs (piRNAs) guide a host defence system that transcriptionally and post-transcriptionally silences transposons during germline development. While germline control of transposons by the piRNA pathway is conserved, many piRNA pathway genes are evolving rapidly under positive selection, and the piRNA biogenesis machinery shows remarkable phylogenetic diversity. Conservation of core function combined with rapid gene evolution is characteristic of a host–pathogen arms race, suggesting that transposons and the piRNA pathway are engaged in an evolutionary tug of war that is driving divergence of the biogenesis machinery. Recent studies suggest that this process may produce biochemical incompatibilities that contribute to reproductive isolation and species divergence.

scholarly journals Assembly and Function of Gonad-Specific Non-Membranous Organelles in Drosophila piRNA Biogenesis

2019 ◽  
Vol 5 (4) ◽  
pp. 52 ◽  
Author(s):  
Shigeki Hirakata ◽  
Mikiko C. Siomi
Keyword(s):  
Dna Damage ◽  
Gonadal Development ◽  
Mitochondrial Membranes ◽  
Animal Life ◽  
Transposon Silencing ◽  
Dna Elements ◽  
Non Coding Rnas ◽  
And Function ◽  
Pirna Pathway

PIWI-interacting RNAs (piRNAs) are small non-coding RNAs that repress transposons in animal germlines. This protects the genome from the invasive DNA elements. piRNA pathway failures lead to DNA damage, gonadal development defects, and infertility. Thus, the piRNA pathway is indispensable for the continuation of animal life. piRNA-mediated transposon silencing occurs in both the nucleus and cytoplasm while piRNA biogenesis is a solely cytoplasmic event. piRNA production requires a number of proteins, the majority of which localize to non-membranous organelles that specifically appear in the gonads. Other piRNA factors are localized on outer mitochondrial membranes. In situ RNA hybridization experiments show that piRNA precursors are compartmentalized into other non-membranous organelles. In this review, we summarize recent findings about the function of these organelles in the Drosophila piRNA pathway by focusing on their assembly and function.

scholarly journals PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression

2014 ◽  
Vol 1 (2) ◽  
pp. 205-218 ◽  
Author(s):  
Hsueh-Yen Ku ◽  
Haifan Lin
Keyword(s):  
Translational Control ◽  
Mrna Turnover ◽  
Regulatory Function ◽  
Piwi Protein ◽  
Germline Development ◽  
Epigenetic Programming ◽  
Transposon Silencing ◽  
Tudor Domain ◽  
Argonaute Family ◽  
Non Coding Rnas

Abstract PIWI-interacting RNAs (piRNAs) are a complex class of small non-coding RNAs that are mostly 24–32 nucleotides in length and composed of at least hundreds of thousands of species that specifically interact with the PIWI protein subfamily of the ARGONAUTE family. Recent studies revealed that PIWI proteins interact with a number of proteins, especially the TUDOR-domain-containing proteins, to regulate piRNA biogenesis and regulatory function. Current research also provides evidence that PIWI proteins and piRNAs are not only crucial for transposon silencing in the germline, but also mediate novel mechanisms of epigenetic programming, DNA rearrangements, mRNA turnover, and translational control both in the germline and in the soma. These new discoveries begin to reveal an exciting new dimension of gene regulation in the cell.

piRNA identification based on motif discovery

2014 ◽  
Vol 10 (12) ◽  
pp. 3075-3080 ◽  
Author(s):  
Xiuqin Liu ◽  
Jun Ding ◽  
Fuzhou Gong
Keyword(s):  
Epigenetic Regulation ◽  
Motif Discovery ◽  
Germline Development ◽  
Transposon Silencing ◽  
Non Coding Rnas

Piwi-interacting RNA (piRNA) is a class of small non-coding RNAs about 24 to 32 nucleotides long, associated with PIWI proteins, which are involved in germline development, transposon silencing, and epigenetic regulation.

scholarly journals Specialization of the Drosophila nuclear export family protein, Nxf3, for piRNA precursor export

2019 ◽  
Author(s):  
Emma Kneuss ◽  
Marzia Munafò ◽  
Evelyn L. Eastwood ◽  
Undine-Sophie Deumer ◽  
Jonathan B. Preall ◽  
...  
Keyword(s):  
Rna Polymerase Ii ◽  
Small Rna ◽  
Nuclear Export ◽  
Mrna Export ◽  
Transposon Silencing ◽  
Family Protein ◽  
Pirna Pathway ◽  
Harmful Effects ◽  
Shed Light ◽  
Mature Mrnas

AbstractThe piRNA pathway is a conserved, small RNA-based immune system that protects animal germ cell genomes from the harmful effects of transposon mobilisation. In Drosophila ovaries, most piRNAs originate from dual-strand clusters, which generate piRNAs from both genomic strands. Dual-strand clusters use non-canonical transcription mechanisms. Although transcribed by RNA polymerase II, cluster transcripts lack splicing signatures and poly(A) tails. mRNA processing is important for general mRNA export mediated by Nuclear export factor 1. Although UAP56, a component of the transcription and export complex, has been implicated in piRNA precursor export, it remains unknown how dual-strand cluster transcripts are specifically targeted for piRNA biogenesis by export from the nucleus to cytoplasmic processing centers. Here we report that dual-strand cluster transcript export requires CG13741/Bootlegger and the Drosophila Nuclear export factor family protein, Nxf3. Bootlegger is specifically recruited to piRNA clusters and in turn brings Nxf3. We find that Nxf3 specifically binds to piRNA precursors and is essential for their export to piRNA biogenesis sites, a process that is critical for germline transposon silencing. Our data shed light on how dual-strand clusters compensate for a lack of canonical features of mature mRNAs to be specifically exported via Nxf3, ensuring proper piRNA production.

scholarly journals Maternal Piwi Regulates Primordial Germ Cell Development to Ensure the Fertility of Female Progeny in Drosophila

Genetics ◽  
2021 ◽  
Author(s):  
Lauren E Gonzalez ◽  
Xiongzhuo Tang ◽  
Haifan Lin
Keyword(s):  
Germ Cell ◽  
Primordial Germ Cell ◽  
Early Embryo ◽  
Null Alleles ◽  
Germline Stem Cell ◽  
Germline Development ◽  
Female Progeny ◽  
Adult Ovary ◽  
Pirna Pathway ◽  
Germline Sex Determination

Abstract In many animals, germline development is initiated by proteins and RNAs that are expressed maternally. PIWI proteins and their associated small noncoding PIWI-interacting RNAs (piRNAs), which guide PIWI to target RNAs by base-pairing, are among the maternal components deposited into the germline of the Drosophila early embryo. Piwi has been extensively studied in the adult ovary and testis, where it is required for transposon suppression, germline stem cell self-renewal, and fertility. Consequently, loss of Piwi in the adult ovary using piwi-null alleles or knockdown from early oogenesis results in complete sterility, limiting investigation into possible embryonic functions of maternal Piwi. In this study, we show that the maternal Piwi protein persists in the embryonic germline through gonad coalescence, suggesting that maternal Piwi can regulate germline development beyond early embryogenesis. Using a maternal knockdown strategy, we find that maternal Piwi is required for the fertility and normal gonad morphology of female, but not male, progeny. Following maternal piwi knockdown, transposons were mildly derepressed in the early embryo but were fully repressed in the ovaries of adult progeny. Furthermore, the maternal piRNA pool was diminished, reducing the capacity of the PIWI/piRNA complex to target zygotic genes during embryogenesis. Examination of embryonic germ cell proliferation and ovarian gene expression showed that the germline of female progeny was partially masculinized by maternal piwi knockdown. Our study reveals a novel role for maternal Piwi in the germline development of female progeny and suggests that the PIWI/piRNA pathway is involved in germline sex determination in Drosophila.

scholarly journals Dimerisation of the PICTS complex via LC8/Cut-up drives co-transcriptional transposon silencing in Drosophila

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Evelyn L Eastwood ◽  
Kayla A Jara ◽  
Susanne Bornelöv ◽  
Marzia Munafò ◽  
Vasileios Frantzis ◽  
...  
Keyword(s):  
Genome Integrity ◽  
Transcriptional Gene Silencing ◽  
Dynein Light Chain ◽  
Heterochromatin Formation ◽  
Transposon Silencing ◽  
Cellular Machinery ◽  
Transposon Insertions ◽  
Pirna Pathway ◽  
Fundamental Requirement ◽  
Rna And Dna

In animal gonads, the PIWI-interacting RNA (piRNA) pathway guards genome integrity in part through the co-transcriptional gene silencing of transposon insertions. In Drosophila ovaries, piRNA-loaded Piwi detects nascent transposon transcripts and instructs heterochromatin formation through the Panoramix-induced co-transcriptional silencing (PICTS) complex, containing Panoramix, Nxf2 and Nxt1. Here, we report that the highly conserved dynein light chain LC8/Cut-up (Ctp) is an essential component of the PICTS complex. Loss of Ctp results in transposon de-repression and a reduction in repressive chromatin marks specifically at transposon loci. In turn, Ctp can enforce transcriptional silencing when artificially recruited to RNA and DNA reporters. We show that Ctp drives dimerisation of the PICTS complex through its interaction with conserved motifs within Panoramix. Artificial dimerisation of Panoramix bypasses the necessity for its interaction with Ctp, demonstrating that conscription of a protein from a ubiquitous cellular machinery has fulfilled a fundamental requirement for a transposon silencing complex.

scholarly journals Somatic piRNAs and Transposons are Differentially Expressed Coincident with Skeletal Muscle Atrophy and Programmed Cell Death

2021 ◽  
Vol 12 ◽  
Author(s):  
Junko Tsuji ◽  
Travis Thomson ◽  
Christine Brown ◽  
Subhanita Ghosh ◽  
William E. Theurkauf ◽  
...  
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Skeletal Muscle Atrophy ◽  
Rna Seq ◽  
Developmentally Regulated ◽  
Transposon Silencing ◽  
Ping Pong ◽  
Somatic Tissues ◽  
Oxidation Resistant ◽  
Pirna Pathway

PIWI-interacting RNAs (piRNAs) are small single-stranded RNAs that can repress transposon expression via epigenetic silencing and transcript degradation. They have been identified predominantly in the ovary and testis, where they serve essential roles in transposon silencing in order to protect the integrity of the genome in the germline. The potential expression of piRNAs in somatic cells has been controversial. In the present study we demonstrate the expression of piRNAs derived from both genic and transposon RNAs in the intersegmental muscles (ISMs) from the tobacco hawkmoth Manduca sexta. These piRNAs are abundantly expressed, ∼27 nt long, map antisense to transposons, are oxidation resistant, exhibit a 5’ uridine bias, and amplify via the canonical ping-pong pathway. An RNA-seq analysis demonstrated that 19 piRNA pathway genes are expressed in the ISMs and are developmentally regulated. The abundance of piRNAs does not change when the muscles initiate developmentally-regulated atrophy, but are repressed coincident with the commitment of the muscles undergo programmed cell death at the end of metamorphosis. This change in piRNA expression is correlated with the repression of several retrotransposons and the induction of specific DNA transposons. The developmentally-regulated changes in the expression of piRNAs, piRNA pathway genes, and transposons are all regulated by 20-hydroxyecdysone, the steroid hormone that controls the timing of ISM death. Taken together, these data provide compelling evidence for the existence of piRNA in somatic tissues and suggest that they may play roles in developmental processes such as programmed cell death.

scholarly journals Channel Nuclear Pore Complex subunits are required for transposon silencing in Drosophila

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Marzia Munafò ◽  
Victoria R Lawless ◽  
Alessandro Passera ◽  
Serena MacMillan ◽  
Susanne Bornelöv ◽  
...  
Keyword(s):  
Nuclear Pore Complex ◽  
Selective Pressure ◽  
Ovarian Follicle ◽  
Follicle Cells ◽  
Nuclear Pore ◽  
Tissue Specific ◽  
Transposon Silencing ◽  
Multiple Copies ◽  
Pirna Pathway ◽  
Inner Channel

The Nuclear Pore Complex (NPC) is the principal gateway between nucleus and cytoplasm that enables exchange of macromolecular cargo. Composed of multiple copies of ~30 different nucleoporins (Nups), the NPC acts as a selective portal, interacting with factors which individually license passage of specific cargo classes. Here we show that two Nups of the inner channel, Nup54 and Nup58, are essential for transposon silencing via the PIWI-interacting RNA (piRNA) pathway in the Drosophila ovary. In ovarian follicle cells, loss of Nup54 and Nup58 results in compromised piRNA biogenesis exclusively from the flamenco locus, whereas knockdowns of other NPC subunits have widespread consequences. This provides evidence that some nucleoporins can acquire specialised roles in tissue-specific contexts. Our findings consolidate the idea that the NPC has functions beyond simply constituting a barrier to nuclear/cytoplasmic exchange, as genomic loci subjected to strong selective pressure can exploit NPC subunits to facilitate their expression.

scholarly journals Transposon silencing in the Drosophila female germline ensures genome stability in progeny embryos

2018 ◽  
Author(s):  
Zeljko Durdevic ◽  
Ramesh S. Pillai ◽  
Anne Ephrussi
Keyword(s):  
Dna Damage ◽  
Genome Stability ◽  
Egg Production ◽  
Germ Line ◽  
Selfish Genetic Elements ◽  
Dna Damage Signaling ◽  
Transposon Silencing ◽  
Transient Loss ◽  
Pirna Pathway ◽  
Female Germline

AbstractThe piRNA pathway functions in transposon control in the germ line of metazoans. The conserved RNA helicase Vasa is an essential piRNA pathway component, but has additional important developmental functions. Here we address the importance of Vasa-dependent transposon control in the Drosophila female germline and early embryos. We find that transient loss of vasa expression during early oogenesis leads to transposon up-regulation in supporting nurse cells of the fly egg-chamber. We show that elevated transposon levels have dramatic consequences, as de-repressed transposons accumulate in the oocyte where they cause DNA damage. We find that suppression of Chk2-mediated DNA damage signaling in vasa mutant females restores oogenesis and egg production. Damaged DNA and up-regulated transposons are transmitted from the mother to the embryos, which sustain severe nuclear defects and arrest development. Our findings reveal that the Vasa-dependent protection against selfish genetic elements in the nuage of nurse cell is essential to prevent DNA damage-induced arrest of embryonic development.

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