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Domestic chickens activate a piRNA defense against avian leukosis virus

View Article: PubMed Central - PubMed

ABSTRACT

PIWI-interacting RNAs (piRNAs) protect the germ line by targeting transposable elements (TEs) through the base-pair complementarity. We do not know how piRNAs co-evolve with TEs in chickens. Here we reported that all active TEs in the chicken germ line are targeted by piRNAs, and as TEs lose their activity, the corresponding piRNAs erode away. We observed de novo piRNA birth as host responds to a recent retroviral invasion. Avian leukosis virus (ALV) has endogenized prior to chicken domestication, remains infectious, and threatens poultry industry. Domestic fowl produce piRNAs targeting ALV from one ALV provirus that was known to render its host ALV resistant. This proviral locus does not produce piRNAs in undomesticated wild chickens. Our findings uncover rapid piRNA evolution reflecting contemporary TE activity, identify a new piRNA acquisition modality by activating a pre-existing genomic locus, and extend piRNA defense roles to include the period when endogenous retroviruses are still infectious.

Doi:: http://dx.doi.org/10.7554/eLife.24695.001

No MeSH data available.


Related in: MedlinePlus

piRNA-mediated TE suppression in rooster testes.(A) Length distributions of testis small RNAs that map to TE regions. Blue represents sense mapping piRNAs; Red represents anti-sense mapping piRNAs. (B) Scatter plots of piRNA abundance in total small RNA library and oxidized small RNA library. Each filled circle represents a TE family. Color identifies young, medium, or old TE as in Figure 2. (C) Sequence logo showing the nucleotide composition of TE piRNA species; Top, sense mapping TE piRNAs; Bottom, anti-sense mapping TE piRNAs. (D) Scatter plots of sense piRNA abundance versus anti-sense piRNA abundance. Each filled circle represents a TE family. Color identifies young, medium, or old TE. (E) The 5´−5´ overlap between TE piRNAs from opposite strands was analyzed.DOI:http://dx.doi.org/10.7554/eLife.24695.009
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fig2s1: piRNA-mediated TE suppression in rooster testes.(A) Length distributions of testis small RNAs that map to TE regions. Blue represents sense mapping piRNAs; Red represents anti-sense mapping piRNAs. (B) Scatter plots of piRNA abundance in total small RNA library and oxidized small RNA library. Each filled circle represents a TE family. Color identifies young, medium, or old TE as in Figure 2. (C) Sequence logo showing the nucleotide composition of TE piRNA species; Top, sense mapping TE piRNAs; Bottom, anti-sense mapping TE piRNAs. (D) Scatter plots of sense piRNA abundance versus anti-sense piRNA abundance. Each filled circle represents a TE family. Color identifies young, medium, or old TE. (E) The 5´−5´ overlap between TE piRNAs from opposite strands was analyzed.DOI:http://dx.doi.org/10.7554/eLife.24695.009

Mentions: Active TEs must be tightly controlled in germ cells. Using small RNA-seq data from the adult testis of White Leghorn (Li et al., 2013), we detected abundant TE piRNAs, which accounted for 7.8% of total piRNAs, and exhibited a size range peaking at 24–25 nt. These small RNAs were resistant to oxidation (Figure 2—figure supplement 1A,B). Oxidation by sodium periodate makes most small RNA species non-accessible for cloning into libraries, but 2´-O-methyl-modified 3´ termini protect piRNAs from oxidation (Ghildiyal et al., 2008). Like piRNAs in other species, these TE piRNAs typically began with uracil (61.6% of species and 66.7% of reads, Figure 2—figure supplement 1C). Almost equal numbers of piRNAs mapped to sense versus antisense strands (median ratio of sense to antisense piRNAs was 1.2) (Figure 2—figure supplement 1D), and there was an adenine bias at the 10th position (Figure 2—figure supplement 1C), indicating that secondary piRNAs are generated (Brennecke et al., 2007; Gunawardane et al., 2007). To test whether the anti-sense TE piRNAs were able to guide the PIWI proteins to cleave TE transcripts, we plotted the distance between the 5´ends of anti-sense piRNAs and the 5´ends of sense piRNAs from TE loci. We detected a significant Z score at a distance of 10 nt, a signature of robust Ping-Pong amplification (Figure 2—figure supplement 1E) (Brennecke et al., 2007; Gunawardane et al., 2007). These findings indicate that a piRNA mediated silencing pathway against TEs is active in the chicken germ line.


Domestic chickens activate a piRNA defense against avian leukosis virus
piRNA-mediated TE suppression in rooster testes.(A) Length distributions of testis small RNAs that map to TE regions. Blue represents sense mapping piRNAs; Red represents anti-sense mapping piRNAs. (B) Scatter plots of piRNA abundance in total small RNA library and oxidized small RNA library. Each filled circle represents a TE family. Color identifies young, medium, or old TE as in Figure 2. (C) Sequence logo showing the nucleotide composition of TE piRNA species; Top, sense mapping TE piRNAs; Bottom, anti-sense mapping TE piRNAs. (D) Scatter plots of sense piRNA abundance versus anti-sense piRNA abundance. Each filled circle represents a TE family. Color identifies young, medium, or old TE. (E) The 5´−5´ overlap between TE piRNAs from opposite strands was analyzed.DOI:http://dx.doi.org/10.7554/eLife.24695.009
© Copyright Policy
Related In: Results  -  Collection

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fig2s1: piRNA-mediated TE suppression in rooster testes.(A) Length distributions of testis small RNAs that map to TE regions. Blue represents sense mapping piRNAs; Red represents anti-sense mapping piRNAs. (B) Scatter plots of piRNA abundance in total small RNA library and oxidized small RNA library. Each filled circle represents a TE family. Color identifies young, medium, or old TE as in Figure 2. (C) Sequence logo showing the nucleotide composition of TE piRNA species; Top, sense mapping TE piRNAs; Bottom, anti-sense mapping TE piRNAs. (D) Scatter plots of sense piRNA abundance versus anti-sense piRNA abundance. Each filled circle represents a TE family. Color identifies young, medium, or old TE. (E) The 5´−5´ overlap between TE piRNAs from opposite strands was analyzed.DOI:http://dx.doi.org/10.7554/eLife.24695.009
Mentions: Active TEs must be tightly controlled in germ cells. Using small RNA-seq data from the adult testis of White Leghorn (Li et al., 2013), we detected abundant TE piRNAs, which accounted for 7.8% of total piRNAs, and exhibited a size range peaking at 24–25 nt. These small RNAs were resistant to oxidation (Figure 2—figure supplement 1A,B). Oxidation by sodium periodate makes most small RNA species non-accessible for cloning into libraries, but 2´-O-methyl-modified 3´ termini protect piRNAs from oxidation (Ghildiyal et al., 2008). Like piRNAs in other species, these TE piRNAs typically began with uracil (61.6% of species and 66.7% of reads, Figure 2—figure supplement 1C). Almost equal numbers of piRNAs mapped to sense versus antisense strands (median ratio of sense to antisense piRNAs was 1.2) (Figure 2—figure supplement 1D), and there was an adenine bias at the 10th position (Figure 2—figure supplement 1C), indicating that secondary piRNAs are generated (Brennecke et al., 2007; Gunawardane et al., 2007). To test whether the anti-sense TE piRNAs were able to guide the PIWI proteins to cleave TE transcripts, we plotted the distance between the 5´ends of anti-sense piRNAs and the 5´ends of sense piRNAs from TE loci. We detected a significant Z score at a distance of 10 nt, a signature of robust Ping-Pong amplification (Figure 2—figure supplement 1E) (Brennecke et al., 2007; Gunawardane et al., 2007). These findings indicate that a piRNA mediated silencing pathway against TEs is active in the chicken germ line.

View Article: PubMed Central - PubMed

ABSTRACT

PIWI-interacting RNAs (piRNAs) protect the germ line by targeting transposable elements (TEs) through the base-pair complementarity. We do not know how piRNAs co-evolve with TEs in chickens. Here we reported that all active TEs in the chicken germ line are targeted by piRNAs, and as TEs lose their activity, the corresponding piRNAs erode away. We observed de novo piRNA birth as host responds to a recent retroviral invasion. Avian leukosis virus (ALV) has endogenized prior to chicken domestication, remains infectious, and threatens poultry industry. Domestic fowl produce piRNAs targeting ALV from one ALV provirus that was known to render its host ALV resistant. This proviral locus does not produce piRNAs in undomesticated wild chickens. Our findings uncover rapid piRNA evolution reflecting contemporary TE activity, identify a new piRNA acquisition modality by activating a pre-existing genomic locus, and extend piRNA defense roles to include the period when endogenous retroviruses are still infectious.

Doi:: http://dx.doi.org/10.7554/eLife.24695.001

No MeSH data available.


Related in: MedlinePlus