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piRNAs Are Associated with Diverse Transgenerational Effects on Gene and Transposon Expression in a Hybrid Dysgenic Syndrome of D. virilis.

Erwin AA, Galdos MA, Wickersheim ML, Harrison CC, Marr KD, Colicchio JM, Blumenstiel JP - PLoS Genet. (2015)

Bottom Line: Moreover, chronic and persisting TE expression coincides with increased levels of genic piRNAs associated with reduced gene expression.Combined with these effects, we further demonstrate that gene expression is idiosyncratically influenced by differences in the genic piRNA profile of the parents that arise though polymorphic TE insertions.This work demonstrates that divergence in the TE profile is associated with diverse piRNA-mediated transgenerational effects on gene expression within populations.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas, United States of America.

ABSTRACT
Sexual reproduction allows transposable elements (TEs) to proliferate, leading to rapid divergence between populations and species. A significant outcome of divergence in the TE landscape is evident in hybrid dysgenic syndromes, a strong form of genomic incompatibility that can arise when (TE) family abundance differs between two parents. When TEs inherited from the father are absent in the mother's genome, TEs can become activated in the progeny, causing germline damage and sterility. Studies in Drosophila indicate that dysgenesis can occur when TEs inherited paternally are not matched with a pool of corresponding TE silencing PIWI-interacting RNAs (piRNAs) provisioned by the female germline. Using the D. virilis syndrome of hybrid dysgenesis as a model, we characterize the effects that divergence in TE profile between parents has on offspring. Overall, we show that divergence in the TE landscape is associated with persisting differences in germline TE expression when comparing genetically identical females of reciprocal crosses and these differences are transmitted to the next generation. Moreover, chronic and persisting TE expression coincides with increased levels of genic piRNAs associated with reduced gene expression. Combined with these effects, we further demonstrate that gene expression is idiosyncratically influenced by differences in the genic piRNA profile of the parents that arise though polymorphic TE insertions. Overall, these results support a model in which early germline events in dysgenesis establish a chronic, stable state of both TE and gene expression in the germline that is maintained through adulthood and transmitted to the next generation. This work demonstrates that divergence in the TE profile is associated with diverse piRNA-mediated transgenerational effects on gene expression within populations.

No MeSH data available.


Related in: MedlinePlus

Genic piRNA targeting is increased in the dysgenic germline.(A) log10 Z-score heat map of genic (CDS) piRNA density for D. melanogaster orthologs (above a threshold of 5 piRNAs per CDS per 1 million mapped in at least one of four columns). Of these 105 genes, there is an excess of genic piRNAs in the dysgenic germline (89 genes with greatest genic targeting in dysgenesis, P<0.001) (B) Sense vs. Anti-sense abundance for piRNAs in genic piRNA class for one library (Sample 1). Some CDS regions are predominantly the source of anti-sense piRNAs, but the majority are biased as a source of sense strand piRNA (C) Distribution of expression levels (log 10 RPKM+0.01) for all genes in the genome and piRNA target genes (expression levels from non-dysgenic germline). Genic piRNA targets are derived from more highly expressed genes (p < 0.001). (D) Of 105 genes, the 89 that show excess genic piRNA in dysgenesis are also more lowly expressed in dysgenesis. Shown is the distribution of expression ratios (dysgenic:non-dysgenic) for all genes and genes that are increased as a source of genic piRNAs in dysgenesis (p < 0.001).
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pgen.1005332.g005: Genic piRNA targeting is increased in the dysgenic germline.(A) log10 Z-score heat map of genic (CDS) piRNA density for D. melanogaster orthologs (above a threshold of 5 piRNAs per CDS per 1 million mapped in at least one of four columns). Of these 105 genes, there is an excess of genic piRNAs in the dysgenic germline (89 genes with greatest genic targeting in dysgenesis, P<0.001) (B) Sense vs. Anti-sense abundance for piRNAs in genic piRNA class for one library (Sample 1). Some CDS regions are predominantly the source of anti-sense piRNAs, but the majority are biased as a source of sense strand piRNA (C) Distribution of expression levels (log 10 RPKM+0.01) for all genes in the genome and piRNA target genes (expression levels from non-dysgenic germline). Genic piRNA targets are derived from more highly expressed genes (p < 0.001). (D) Of 105 genes, the 89 that show excess genic piRNA in dysgenesis are also more lowly expressed in dysgenesis. Shown is the distribution of expression ratios (dysgenic:non-dysgenic) for all genes and genes that are increased as a source of genic piRNAs in dysgenesis (p < 0.001).

Mentions: In the dysgenic germline we found significant enrichment of piRNAs derived from genes. We identified 105 genes that had at least 5 piRNA per million mapping to genic CDS regions in either the parental strains or reciprocal F1 progeny. For these 105 genes, there was a significant excess of piRNAs in the dysgenic germline (Fig 5A; p-value < 0.0001, Wilcoxon-signed rank test). Genic piRNA production, relative to parental strains, is also higher in non-dysgenic progeny, indicating that this may arise from crosses between strains with divergent piRNA profiles. For some genes, the genic piRNAs were predominantly anti-sense, but the majority of genes were associated with primarily sense strand piRNAs (Fig 5B). Comparing genic piRNA density across introns and exons, we found that piRNAs from these genes are enriched on exons (Paired T-test across genes contrasting intronic and exonic density: Library 1: p = 0.0046, Library 2: p = 0.0024). This suggests that genic piRNA processing may occur in the cytoplasm. We examined genic piRNAs for piRNA biogenesis signatures: first position U bias and 10th position A bias. Results indicate that the genic piRNAs are primary piRNAs (S2 Table). From the entire set of 105 genes, focusing on 80 genes that primarily produce sense piRNAs, we found a signature of primary piRNA biogenesis and a very weak signature of secondary piRNA biogenesis (Library 1: U first position: 0.33, background U: 0.21, A 10th position: 0.25, background A: 0.22; Library 2: U first position: 0.33, background U: 0.21, A 10th position: 0.24, background A: 0.23).


piRNAs Are Associated with Diverse Transgenerational Effects on Gene and Transposon Expression in a Hybrid Dysgenic Syndrome of D. virilis.

Erwin AA, Galdos MA, Wickersheim ML, Harrison CC, Marr KD, Colicchio JM, Blumenstiel JP - PLoS Genet. (2015)

Genic piRNA targeting is increased in the dysgenic germline.(A) log10 Z-score heat map of genic (CDS) piRNA density for D. melanogaster orthologs (above a threshold of 5 piRNAs per CDS per 1 million mapped in at least one of four columns). Of these 105 genes, there is an excess of genic piRNAs in the dysgenic germline (89 genes with greatest genic targeting in dysgenesis, P<0.001) (B) Sense vs. Anti-sense abundance for piRNAs in genic piRNA class for one library (Sample 1). Some CDS regions are predominantly the source of anti-sense piRNAs, but the majority are biased as a source of sense strand piRNA (C) Distribution of expression levels (log 10 RPKM+0.01) for all genes in the genome and piRNA target genes (expression levels from non-dysgenic germline). Genic piRNA targets are derived from more highly expressed genes (p < 0.001). (D) Of 105 genes, the 89 that show excess genic piRNA in dysgenesis are also more lowly expressed in dysgenesis. Shown is the distribution of expression ratios (dysgenic:non-dysgenic) for all genes and genes that are increased as a source of genic piRNAs in dysgenesis (p < 0.001).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4524669&req=5

pgen.1005332.g005: Genic piRNA targeting is increased in the dysgenic germline.(A) log10 Z-score heat map of genic (CDS) piRNA density for D. melanogaster orthologs (above a threshold of 5 piRNAs per CDS per 1 million mapped in at least one of four columns). Of these 105 genes, there is an excess of genic piRNAs in the dysgenic germline (89 genes with greatest genic targeting in dysgenesis, P<0.001) (B) Sense vs. Anti-sense abundance for piRNAs in genic piRNA class for one library (Sample 1). Some CDS regions are predominantly the source of anti-sense piRNAs, but the majority are biased as a source of sense strand piRNA (C) Distribution of expression levels (log 10 RPKM+0.01) for all genes in the genome and piRNA target genes (expression levels from non-dysgenic germline). Genic piRNA targets are derived from more highly expressed genes (p < 0.001). (D) Of 105 genes, the 89 that show excess genic piRNA in dysgenesis are also more lowly expressed in dysgenesis. Shown is the distribution of expression ratios (dysgenic:non-dysgenic) for all genes and genes that are increased as a source of genic piRNAs in dysgenesis (p < 0.001).
Mentions: In the dysgenic germline we found significant enrichment of piRNAs derived from genes. We identified 105 genes that had at least 5 piRNA per million mapping to genic CDS regions in either the parental strains or reciprocal F1 progeny. For these 105 genes, there was a significant excess of piRNAs in the dysgenic germline (Fig 5A; p-value < 0.0001, Wilcoxon-signed rank test). Genic piRNA production, relative to parental strains, is also higher in non-dysgenic progeny, indicating that this may arise from crosses between strains with divergent piRNA profiles. For some genes, the genic piRNAs were predominantly anti-sense, but the majority of genes were associated with primarily sense strand piRNAs (Fig 5B). Comparing genic piRNA density across introns and exons, we found that piRNAs from these genes are enriched on exons (Paired T-test across genes contrasting intronic and exonic density: Library 1: p = 0.0046, Library 2: p = 0.0024). This suggests that genic piRNA processing may occur in the cytoplasm. We examined genic piRNAs for piRNA biogenesis signatures: first position U bias and 10th position A bias. Results indicate that the genic piRNAs are primary piRNAs (S2 Table). From the entire set of 105 genes, focusing on 80 genes that primarily produce sense piRNAs, we found a signature of primary piRNA biogenesis and a very weak signature of secondary piRNA biogenesis (Library 1: U first position: 0.33, background U: 0.21, A 10th position: 0.25, background A: 0.22; Library 2: U first position: 0.33, background U: 0.21, A 10th position: 0.24, background A: 0.23).

Bottom Line: Moreover, chronic and persisting TE expression coincides with increased levels of genic piRNAs associated with reduced gene expression.Combined with these effects, we further demonstrate that gene expression is idiosyncratically influenced by differences in the genic piRNA profile of the parents that arise though polymorphic TE insertions.This work demonstrates that divergence in the TE profile is associated with diverse piRNA-mediated transgenerational effects on gene expression within populations.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas, United States of America.

ABSTRACT
Sexual reproduction allows transposable elements (TEs) to proliferate, leading to rapid divergence between populations and species. A significant outcome of divergence in the TE landscape is evident in hybrid dysgenic syndromes, a strong form of genomic incompatibility that can arise when (TE) family abundance differs between two parents. When TEs inherited from the father are absent in the mother's genome, TEs can become activated in the progeny, causing germline damage and sterility. Studies in Drosophila indicate that dysgenesis can occur when TEs inherited paternally are not matched with a pool of corresponding TE silencing PIWI-interacting RNAs (piRNAs) provisioned by the female germline. Using the D. virilis syndrome of hybrid dysgenesis as a model, we characterize the effects that divergence in TE profile between parents has on offspring. Overall, we show that divergence in the TE landscape is associated with persisting differences in germline TE expression when comparing genetically identical females of reciprocal crosses and these differences are transmitted to the next generation. Moreover, chronic and persisting TE expression coincides with increased levels of genic piRNAs associated with reduced gene expression. Combined with these effects, we further demonstrate that gene expression is idiosyncratically influenced by differences in the genic piRNA profile of the parents that arise though polymorphic TE insertions. Overall, these results support a model in which early germline events in dysgenesis establish a chronic, stable state of both TE and gene expression in the germline that is maintained through adulthood and transmitted to the next generation. This work demonstrates that divergence in the TE profile is associated with diverse piRNA-mediated transgenerational effects on gene expression within populations.

No MeSH data available.


Related in: MedlinePlus