Limits...
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.


PIWI proteins are conserved between mammals and birds.Phylogenetic tree of PIWI proteins, including four human PIWI proteins, three mouse PIWI proteins, and two chicken PIWI proteins.DOI:http://dx.doi.org/10.7554/eLife.24695.005
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC5383398&req=5

fig1s2: PIWI proteins are conserved between mammals and birds.Phylogenetic tree of PIWI proteins, including four human PIWI proteins, three mouse PIWI proteins, and two chicken PIWI proteins.DOI:http://dx.doi.org/10.7554/eLife.24695.005

Mentions: Active ERVs are transcribed and translated, and are able to transpose within the germ line. Comparison of RNA-seq data from 12 tissues (Brawand et al., 2011) indicated that chicken ERV families were ubiquitously expressed (Figure 1—figure supplement 1A). Because many insertions are truncated, detection of ERV RNAs does not necessarily indicate that they are translated or competent for transposition. It has been shown that chicken ERVs are transcribed and translated in somatic cells (Bolisetty et al., 2012). Because the highest expression was in testis and ovary—the only tissues where their expansion can become heritable (Figure 1—figure supplement 1A), we decided to perform polysome profile analysis to determine whether ERVs were also being translated in testis. Adult White Leghorn testis lysates were separated in 10–50% sucrose-density gradients by ultracentrifugation (Figure 1A). This fractionation separates non-translating ribonucleoproteins, small and large subunits of ribosomes, monosomes and polysomes, as shown by the distribution of rRNA. Actively translated β-ACTIN, CILI, and CIWI mRNAs co-sedimented with both monosome and polysome fractions, but the MALAT1 non-coding RNA did not co-sedimented with polysomes. CILI and CIWI are the two PIWI proteins in chickens (Figure 1—figure supplement 2). We tested the distribution of CR1-B and CR1-F families that belong to the CR1 superfamily, as well as the EAV-HP and ALVE that belong to ERV families. Although CR1 arose prior to the divergence of birds and reptiles and peaked ~45 million years ago (Vandergon and Reitman, 1994), CR1-F and CR1-B elements remain able to drive their own transcription (Wicker et al., 2005; Lee et al., 2009). CR1-B, CR1-F, EAV-HP, and ALVE transcripts co-sedimented with polysomes. These profiling results suggest that CR1-B, CR1-F, EAV and ALVE insertions are transcribed and translated in testis.10.7554/eLife.24695.003Figure 1.Active ERVs in White Leghorn testis.


Domestic chickens activate a piRNA defense against avian leukosis virus
PIWI proteins are conserved between mammals and birds.Phylogenetic tree of PIWI proteins, including four human PIWI proteins, three mouse PIWI proteins, and two chicken PIWI proteins.DOI:http://dx.doi.org/10.7554/eLife.24695.005
© Copyright Policy
Related In: Results  -  Collection

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

fig1s2: PIWI proteins are conserved between mammals and birds.Phylogenetic tree of PIWI proteins, including four human PIWI proteins, three mouse PIWI proteins, and two chicken PIWI proteins.DOI:http://dx.doi.org/10.7554/eLife.24695.005
Mentions: Active ERVs are transcribed and translated, and are able to transpose within the germ line. Comparison of RNA-seq data from 12 tissues (Brawand et al., 2011) indicated that chicken ERV families were ubiquitously expressed (Figure 1—figure supplement 1A). Because many insertions are truncated, detection of ERV RNAs does not necessarily indicate that they are translated or competent for transposition. It has been shown that chicken ERVs are transcribed and translated in somatic cells (Bolisetty et al., 2012). Because the highest expression was in testis and ovary—the only tissues where their expansion can become heritable (Figure 1—figure supplement 1A), we decided to perform polysome profile analysis to determine whether ERVs were also being translated in testis. Adult White Leghorn testis lysates were separated in 10–50% sucrose-density gradients by ultracentrifugation (Figure 1A). This fractionation separates non-translating ribonucleoproteins, small and large subunits of ribosomes, monosomes and polysomes, as shown by the distribution of rRNA. Actively translated β-ACTIN, CILI, and CIWI mRNAs co-sedimented with both monosome and polysome fractions, but the MALAT1 non-coding RNA did not co-sedimented with polysomes. CILI and CIWI are the two PIWI proteins in chickens (Figure 1—figure supplement 2). We tested the distribution of CR1-B and CR1-F families that belong to the CR1 superfamily, as well as the EAV-HP and ALVE that belong to ERV families. Although CR1 arose prior to the divergence of birds and reptiles and peaked ~45 million years ago (Vandergon and Reitman, 1994), CR1-F and CR1-B elements remain able to drive their own transcription (Wicker et al., 2005; Lee et al., 2009). CR1-B, CR1-F, EAV-HP, and ALVE transcripts co-sedimented with polysomes. These profiling results suggest that CR1-B, CR1-F, EAV and ALVE insertions are transcribed and translated in testis.10.7554/eLife.24695.003Figure 1.Active ERVs in White Leghorn testis.

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.