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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

Divergent transcription of piRNA clusters.(A) Scatter plots of Watson-strand piRNA abundance versus Crick-strand piRNA abundance (left); scatter plots of Watson-strand piRNA precursor abundance versus Crick-strand piRNA precursor abundance (right). Each filled circle represents a conserved piRNA cluster and each open circle represent a divergent piRNA cluster. (B) Length distributions of testis small RNAs from conserved piRNA clusters (left) and divergent piRNA clusters (right). (C) Sequence logo showing the nucleotide composition of piRNA species from conserved piRNA clusters (left) and from divergent piRNA clusters (right).DOI:http://dx.doi.org/10.7554/eLife.24695.013
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fig4s1: Divergent transcription of piRNA clusters.(A) Scatter plots of Watson-strand piRNA abundance versus Crick-strand piRNA abundance (left); scatter plots of Watson-strand piRNA precursor abundance versus Crick-strand piRNA precursor abundance (right). Each filled circle represents a conserved piRNA cluster and each open circle represent a divergent piRNA cluster. (B) Length distributions of testis small RNAs from conserved piRNA clusters (left) and divergent piRNA clusters (right). (C) Sequence logo showing the nucleotide composition of piRNA species from conserved piRNA clusters (left) and from divergent piRNA clusters (right).DOI:http://dx.doi.org/10.7554/eLife.24695.013

Mentions: The ability of chickens to produce piRNAs against a new ERV provides a rare opportunity to study where new piRNAs are acquired. To identify the genomic source of the ALVE piRNAs, we defined all piRNA-producing loci, so-called piRNA clusters, in White Leghorn. Using our previously developed dynamic programming algorithm (Li et al., 2013), in total, we identified 1633 piRNA clusters that accounted for 0.88% of the chicken genome, and explained 87.3% of total piRNA reads and 81.1% of uniquely mapping piRNAs (Figure 4A). These piRNA clusters were distributed on most autosomes and the Z chromosome (Figure 1D). Unlike divergently and uni-directionally transcribed mouse piRNA-producing loci, we observed that chicken piRNAs were produced from both strands of piRNA clusters (Figure 4B, Figure 4—figure supplement 1A) as reported previously (Li et al., 2013; Chirn et al., 2015), and were derived from convergently transcribed precursors detected by our RNA-seq data (Figure 4B, Figure 4—figure supplement 1A). Over 70% of clusters (1173 out of 1633) included uniquely mapping piRNAs transcribed from either strand at a level of greater than 10% of total uniquely mapping piRNAs from that cluster. Based on these findings, we conclude that most chicken piRNA-producing loci are transcribed from both strands, and both transcripts are processed into piRNAs.10.7554/eLife.24695.012Figure 4.ALVE6 is the primary piRNA-producing locus for viral piRNAs.


Domestic chickens activate a piRNA defense against avian leukosis virus
Divergent transcription of piRNA clusters.(A) Scatter plots of Watson-strand piRNA abundance versus Crick-strand piRNA abundance (left); scatter plots of Watson-strand piRNA precursor abundance versus Crick-strand piRNA precursor abundance (right). Each filled circle represents a conserved piRNA cluster and each open circle represent a divergent piRNA cluster. (B) Length distributions of testis small RNAs from conserved piRNA clusters (left) and divergent piRNA clusters (right). (C) Sequence logo showing the nucleotide composition of piRNA species from conserved piRNA clusters (left) and from divergent piRNA clusters (right).DOI:http://dx.doi.org/10.7554/eLife.24695.013
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5383398&req=5

fig4s1: Divergent transcription of piRNA clusters.(A) Scatter plots of Watson-strand piRNA abundance versus Crick-strand piRNA abundance (left); scatter plots of Watson-strand piRNA precursor abundance versus Crick-strand piRNA precursor abundance (right). Each filled circle represents a conserved piRNA cluster and each open circle represent a divergent piRNA cluster. (B) Length distributions of testis small RNAs from conserved piRNA clusters (left) and divergent piRNA clusters (right). (C) Sequence logo showing the nucleotide composition of piRNA species from conserved piRNA clusters (left) and from divergent piRNA clusters (right).DOI:http://dx.doi.org/10.7554/eLife.24695.013
Mentions: The ability of chickens to produce piRNAs against a new ERV provides a rare opportunity to study where new piRNAs are acquired. To identify the genomic source of the ALVE piRNAs, we defined all piRNA-producing loci, so-called piRNA clusters, in White Leghorn. Using our previously developed dynamic programming algorithm (Li et al., 2013), in total, we identified 1633 piRNA clusters that accounted for 0.88% of the chicken genome, and explained 87.3% of total piRNA reads and 81.1% of uniquely mapping piRNAs (Figure 4A). These piRNA clusters were distributed on most autosomes and the Z chromosome (Figure 1D). Unlike divergently and uni-directionally transcribed mouse piRNA-producing loci, we observed that chicken piRNAs were produced from both strands of piRNA clusters (Figure 4B, Figure 4—figure supplement 1A) as reported previously (Li et al., 2013; Chirn et al., 2015), and were derived from convergently transcribed precursors detected by our RNA-seq data (Figure 4B, Figure 4—figure supplement 1A). Over 70% of clusters (1173 out of 1633) included uniquely mapping piRNAs transcribed from either strand at a level of greater than 10% of total uniquely mapping piRNAs from that cluster. Based on these findings, we conclude that most chicken piRNA-producing loci are transcribed from both strands, and both transcripts are processed into piRNAs.10.7554/eLife.24695.012Figure 4.ALVE6 is the primary piRNA-producing locus for viral piRNAs.

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