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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

ALVE6 existed in chicken genome prior domestication.(A) From top to bottom, the genomic location of Cluster719, White Leghorn genomic re-sequencing signals mapping to Crick strand and Watson strand, Ref-Seq track showing depletion of annotated gene, RepeatMasker track showing the annotated ALVE region, the position of primers used for genomic PCRs, and genomic PCR sequences. Separation of genomic PCR products is shown on the agarose gel, and the primers used for genomic PCRs are labeled in each lane. The sequences of these PCR products were blasted against Red Jungle Fowl with complete alignment. A red tick-mark represents a base substitution; an orange tick-mark represents an insertion. (B) Sequence logo showing the nucleotide composition of ALVE piRNA species from ALVE6 locus (top) and from new ALVE insertions (bottom).DOI:http://dx.doi.org/10.7554/eLife.24695.014
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fig4s2: ALVE6 existed in chicken genome prior domestication.(A) From top to bottom, the genomic location of Cluster719, White Leghorn genomic re-sequencing signals mapping to Crick strand and Watson strand, Ref-Seq track showing depletion of annotated gene, RepeatMasker track showing the annotated ALVE region, the position of primers used for genomic PCRs, and genomic PCR sequences. Separation of genomic PCR products is shown on the agarose gel, and the primers used for genomic PCRs are labeled in each lane. The sequences of these PCR products were blasted against Red Jungle Fowl with complete alignment. A red tick-mark represents a base substitution; an orange tick-mark represents an insertion. (B) Sequence logo showing the nucleotide composition of ALVE piRNA species from ALVE6 locus (top) and from new ALVE insertions (bottom).DOI:http://dx.doi.org/10.7554/eLife.24695.014

Mentions: One divergent piRNA-producing locus (cluster 719) contains the truncated ALVE provirus (Figure 4E), ALVE6. Cluster 719 produces abundant piRNAs (147 ppm) in White Leghorn, but in Red Jungle Fowl produces few piRNAs (Figure 4E). ALVE6 has lost its 5´LTR, gag, and half of pol, eliminating its transcriptional promoter (Tereba, 1981). The gene structure matches the distributions of piRNAs on ALVE, which starts in the middle of the pol gene (Figure 1C). This defective provirus has been associated with ALVE resistance (Robinson et al., 1981). The wide distribution of ALVE6 in commercial egg-laying breeds has been believed to reflect selection of nonshedders (Hayward et al., 1980; Kuhnlein et al., 1989; Smith et al., 1990b). ALVE6 is the only known ALVE provirus that is present in both White Leghorn and Red Jungle Fowl (Levin et al., 1994). In addition to the resequencing analysis of White Leghorn, we used the longer sequencing reads of Sanger sequencing to confirm that although sequence polymorphisms exist, the genomic structure of the ALVE6 locus surrounding regions was remains the same as the reference locus in Red Jungle Fowl (Figure 4—figure supplement 2A). These results indicate that ALVE6 existed in the chicken genome prior to domestication.


Domestic chickens activate a piRNA defense against avian leukosis virus
ALVE6 existed in chicken genome prior domestication.(A) From top to bottom, the genomic location of Cluster719, White Leghorn genomic re-sequencing signals mapping to Crick strand and Watson strand, Ref-Seq track showing depletion of annotated gene, RepeatMasker track showing the annotated ALVE region, the position of primers used for genomic PCRs, and genomic PCR sequences. Separation of genomic PCR products is shown on the agarose gel, and the primers used for genomic PCRs are labeled in each lane. The sequences of these PCR products were blasted against Red Jungle Fowl with complete alignment. A red tick-mark represents a base substitution; an orange tick-mark represents an insertion. (B) Sequence logo showing the nucleotide composition of ALVE piRNA species from ALVE6 locus (top) and from new ALVE insertions (bottom).DOI:http://dx.doi.org/10.7554/eLife.24695.014
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Related In: Results  -  Collection

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fig4s2: ALVE6 existed in chicken genome prior domestication.(A) From top to bottom, the genomic location of Cluster719, White Leghorn genomic re-sequencing signals mapping to Crick strand and Watson strand, Ref-Seq track showing depletion of annotated gene, RepeatMasker track showing the annotated ALVE region, the position of primers used for genomic PCRs, and genomic PCR sequences. Separation of genomic PCR products is shown on the agarose gel, and the primers used for genomic PCRs are labeled in each lane. The sequences of these PCR products were blasted against Red Jungle Fowl with complete alignment. A red tick-mark represents a base substitution; an orange tick-mark represents an insertion. (B) Sequence logo showing the nucleotide composition of ALVE piRNA species from ALVE6 locus (top) and from new ALVE insertions (bottom).DOI:http://dx.doi.org/10.7554/eLife.24695.014
Mentions: One divergent piRNA-producing locus (cluster 719) contains the truncated ALVE provirus (Figure 4E), ALVE6. Cluster 719 produces abundant piRNAs (147 ppm) in White Leghorn, but in Red Jungle Fowl produces few piRNAs (Figure 4E). ALVE6 has lost its 5´LTR, gag, and half of pol, eliminating its transcriptional promoter (Tereba, 1981). The gene structure matches the distributions of piRNAs on ALVE, which starts in the middle of the pol gene (Figure 1C). This defective provirus has been associated with ALVE resistance (Robinson et al., 1981). The wide distribution of ALVE6 in commercial egg-laying breeds has been believed to reflect selection of nonshedders (Hayward et al., 1980; Kuhnlein et al., 1989; Smith et al., 1990b). ALVE6 is the only known ALVE provirus that is present in both White Leghorn and Red Jungle Fowl (Levin et al., 1994). In addition to the resequencing analysis of White Leghorn, we used the longer sequencing reads of Sanger sequencing to confirm that although sequence polymorphisms exist, the genomic structure of the ALVE6 locus surrounding regions was remains the same as the reference locus in Red Jungle Fowl (Figure 4—figure supplement 2A). These results indicate that ALVE6 existed in the chicken genome prior to domestication.

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