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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

Medium TE piRNAs are authentic piRNAs.(A) Length distributions of testis small RNAs that map to young TEs (left) and medium TEs (right). (B) Sequence logo showing the nucleotide composition of Young TE piRNA species (left) and Medium TE piRNA species (right); Top, sense mapping TE piRNAs; Bottom, anti-sense mapping TE piRNAs.DOI:http://dx.doi.org/10.7554/eLife.24695.010
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fig2s2: Medium TE piRNAs are authentic piRNAs.(A) Length distributions of testis small RNAs that map to young TEs (left) and medium TEs (right). (B) Sequence logo showing the nucleotide composition of Young TE piRNA species (left) and Medium TE piRNA species (right); Top, sense mapping TE piRNAs; Bottom, anti-sense mapping TE piRNAs.DOI:http://dx.doi.org/10.7554/eLife.24695.010

Mentions: The expression of piRNAs that target each TE family correlated with overall TE expression (ρ = 0.81, p<2.2 × 10−16, Figure 2A; the two events were significantly associated: Fisher's exact test, p<2.2 × 10−16, Figure 2B), although there were exceptions. All the 73 actively expressed TE families were targeted by piRNAs. The presence of this piRNA activity explains why expression of the TEs can be tolerated in White Leghorn. Most inactive TEs (108 families) are not targeted by piRNAs; interestingly, 19 inactive TEs are targeted by piRNAs. Those piRNAs that target inactive TEs exhibit the authentic piRNA length distribution, resistance to oxidation, and first position (1st) U bias (Figure 2—figure supplement 2A,B), but they are less abundant than the piRNAs that target active TEs (p<2.2×10−16) (Figure 2C). piRNAs that target active TEs display a robust Ping-Pong amplification with a median Z score of 12.2; whereas, the piRNAs that target the inactive TEs do not show significant Ping-Pong amplification (median Z score of 0.41) (Figure 2C; Z-score >3.3 corresponds to p<0.01), although both sense and antisense TE piRNAs are produced in equal abundance (Figure 2—figure supplement 1B). The lack of a Ping-Pong signature for piRNAs targeting inactive TEs supports the function of Ping-Pong amplification as an adaptive response to TE activation rather than merely a consequence of piRNA production.10.7554/eLife.24695.008Figure 2.Three groups of TEs based on TE expression and piRNA expression.


Domestic chickens activate a piRNA defense against avian leukosis virus
Medium TE piRNAs are authentic piRNAs.(A) Length distributions of testis small RNAs that map to young TEs (left) and medium TEs (right). (B) Sequence logo showing the nucleotide composition of Young TE piRNA species (left) and Medium TE piRNA species (right); Top, sense mapping TE piRNAs; Bottom, anti-sense mapping TE piRNAs.DOI:http://dx.doi.org/10.7554/eLife.24695.010
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5383398&req=5

fig2s2: Medium TE piRNAs are authentic piRNAs.(A) Length distributions of testis small RNAs that map to young TEs (left) and medium TEs (right). (B) Sequence logo showing the nucleotide composition of Young TE piRNA species (left) and Medium TE piRNA species (right); Top, sense mapping TE piRNAs; Bottom, anti-sense mapping TE piRNAs.DOI:http://dx.doi.org/10.7554/eLife.24695.010
Mentions: The expression of piRNAs that target each TE family correlated with overall TE expression (ρ = 0.81, p<2.2 × 10−16, Figure 2A; the two events were significantly associated: Fisher's exact test, p<2.2 × 10−16, Figure 2B), although there were exceptions. All the 73 actively expressed TE families were targeted by piRNAs. The presence of this piRNA activity explains why expression of the TEs can be tolerated in White Leghorn. Most inactive TEs (108 families) are not targeted by piRNAs; interestingly, 19 inactive TEs are targeted by piRNAs. Those piRNAs that target inactive TEs exhibit the authentic piRNA length distribution, resistance to oxidation, and first position (1st) U bias (Figure 2—figure supplement 2A,B), but they are less abundant than the piRNAs that target active TEs (p<2.2×10−16) (Figure 2C). piRNAs that target active TEs display a robust Ping-Pong amplification with a median Z score of 12.2; whereas, the piRNAs that target the inactive TEs do not show significant Ping-Pong amplification (median Z score of 0.41) (Figure 2C; Z-score >3.3 corresponds to p<0.01), although both sense and antisense TE piRNAs are produced in equal abundance (Figure 2—figure supplement 1B). The lack of a Ping-Pong signature for piRNAs targeting inactive TEs supports the function of Ping-Pong amplification as an adaptive response to TE activation rather than merely a consequence of piRNA production.10.7554/eLife.24695.008Figure 2.Three groups of TEs based on TE expression and piRNA expression.

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