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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

Signatures of piRNA biogenesis in the dysgenic germline show only modest defects.(A) Size distributions of small RNAs are similar between dysgenic and non-dysgenic germlines. Distribution of all small RNAs (not normalized) from four germline libraries (2 dysgenic, 2 non-dysgenic) filtered for tRNA, rRNA and snoRNA. (B) piRNA biogenesis signature heatmaps. TEs upregulated in the dysgenic germline (a difference of 5 RPKM or higher) are indicated with red bars. TEs upregulated in the non-dysgenic germline (a difference of 5 RPKM or higher) are indicated with purple. On the left are heatmaps for raw measures of abundance, the density of ping-pong pairs and percent ping-pong. On the right are heatmaps for the same metrics, but by row z-score. For raw measures, there are no globally discernible effects of dysgenesis on piRNA biogenesis. Row z-scores in dysgenesis do show lower values for abundance measures (abundance and ping-pong pair density), but not percent ping-pong (see text). (C) Fold excess in expression in dysgenesis vs. the difference in percent ping-pong Z-score between dysgenic and non-dysgenic germline. Of the top eight that are most differently expressed in dysgenesis, all have lower ping-pong z-scores in dysgenesis.
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pgen.1005332.g004: Signatures of piRNA biogenesis in the dysgenic germline show only modest defects.(A) Size distributions of small RNAs are similar between dysgenic and non-dysgenic germlines. Distribution of all small RNAs (not normalized) from four germline libraries (2 dysgenic, 2 non-dysgenic) filtered for tRNA, rRNA and snoRNA. (B) piRNA biogenesis signature heatmaps. TEs upregulated in the dysgenic germline (a difference of 5 RPKM or higher) are indicated with red bars. TEs upregulated in the non-dysgenic germline (a difference of 5 RPKM or higher) are indicated with purple. On the left are heatmaps for raw measures of abundance, the density of ping-pong pairs and percent ping-pong. On the right are heatmaps for the same metrics, but by row z-score. For raw measures, there are no globally discernible effects of dysgenesis on piRNA biogenesis. Row z-scores in dysgenesis do show lower values for abundance measures (abundance and ping-pong pair density), but not percent ping-pong (see text). (C) Fold excess in expression in dysgenesis vs. the difference in percent ping-pong Z-score between dysgenic and non-dysgenic germline. Of the top eight that are most differently expressed in dysgenesis, all have lower ping-pong z-scores in dysgenesis.

Mentions: Raw abundance measures of piRNAs ignore critical aspects of their biogenesis and recent studies have demonstrated that globally reduced signatures of robust piRNA biogenesis likely contribute to the mobilization of diverse TEs [15,28]. In contrast to interspecific crosses that show near complete collapse of the 23–30 nt small RNA pool, we found no evidence that piRNA biogenesis is skewed away from the 23–30 nt expectation based on the size distribution of small RNA reads (Fig 4A). For each TE, we estimated the percent ping-pong [24] as well as the normalized density of ping-pong pairs in the dysgenic and non-dysgenic germline. When we compared metrics directly (first column of heatmaps, Fig 4B) we found little evidence that piRNA biogenesis is grossly perturbed in the dysgenic cross, though a more sensitive comparison using normalized Z-scores indicated a modest reduction in piRNA abundance and density of ping-pong pairs (Fig 4B). This is observed in the Z-score heat maps (Fig 4B, second column of heatmaps) for abundance and ping-pong pair density. Both showed an excess of negative Z-scores for dysgenesis (p<0.0001, Wilcoxon Signed-Rank Test). Importantly, both ping-pong abundance and ping-pong pair density are normalized, proportional measures of abundance that are likely influenced by increases in the abundance of non-TE, genic piRNAs in the same library (see below).


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)

Signatures of piRNA biogenesis in the dysgenic germline show only modest defects.(A) Size distributions of small RNAs are similar between dysgenic and non-dysgenic germlines. Distribution of all small RNAs (not normalized) from four germline libraries (2 dysgenic, 2 non-dysgenic) filtered for tRNA, rRNA and snoRNA. (B) piRNA biogenesis signature heatmaps. TEs upregulated in the dysgenic germline (a difference of 5 RPKM or higher) are indicated with red bars. TEs upregulated in the non-dysgenic germline (a difference of 5 RPKM or higher) are indicated with purple. On the left are heatmaps for raw measures of abundance, the density of ping-pong pairs and percent ping-pong. On the right are heatmaps for the same metrics, but by row z-score. For raw measures, there are no globally discernible effects of dysgenesis on piRNA biogenesis. Row z-scores in dysgenesis do show lower values for abundance measures (abundance and ping-pong pair density), but not percent ping-pong (see text). (C) Fold excess in expression in dysgenesis vs. the difference in percent ping-pong Z-score between dysgenic and non-dysgenic germline. Of the top eight that are most differently expressed in dysgenesis, all have lower ping-pong z-scores in dysgenesis.
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pgen.1005332.g004: Signatures of piRNA biogenesis in the dysgenic germline show only modest defects.(A) Size distributions of small RNAs are similar between dysgenic and non-dysgenic germlines. Distribution of all small RNAs (not normalized) from four germline libraries (2 dysgenic, 2 non-dysgenic) filtered for tRNA, rRNA and snoRNA. (B) piRNA biogenesis signature heatmaps. TEs upregulated in the dysgenic germline (a difference of 5 RPKM or higher) are indicated with red bars. TEs upregulated in the non-dysgenic germline (a difference of 5 RPKM or higher) are indicated with purple. On the left are heatmaps for raw measures of abundance, the density of ping-pong pairs and percent ping-pong. On the right are heatmaps for the same metrics, but by row z-score. For raw measures, there are no globally discernible effects of dysgenesis on piRNA biogenesis. Row z-scores in dysgenesis do show lower values for abundance measures (abundance and ping-pong pair density), but not percent ping-pong (see text). (C) Fold excess in expression in dysgenesis vs. the difference in percent ping-pong Z-score between dysgenic and non-dysgenic germline. Of the top eight that are most differently expressed in dysgenesis, all have lower ping-pong z-scores in dysgenesis.
Mentions: Raw abundance measures of piRNAs ignore critical aspects of their biogenesis and recent studies have demonstrated that globally reduced signatures of robust piRNA biogenesis likely contribute to the mobilization of diverse TEs [15,28]. In contrast to interspecific crosses that show near complete collapse of the 23–30 nt small RNA pool, we found no evidence that piRNA biogenesis is skewed away from the 23–30 nt expectation based on the size distribution of small RNA reads (Fig 4A). For each TE, we estimated the percent ping-pong [24] as well as the normalized density of ping-pong pairs in the dysgenic and non-dysgenic germline. When we compared metrics directly (first column of heatmaps, Fig 4B) we found little evidence that piRNA biogenesis is grossly perturbed in the dysgenic cross, though a more sensitive comparison using normalized Z-scores indicated a modest reduction in piRNA abundance and density of ping-pong pairs (Fig 4B). This is observed in the Z-score heat maps (Fig 4B, second column of heatmaps) for abundance and ping-pong pair density. Both showed an excess of negative Z-scores for dysgenesis (p<0.0001, Wilcoxon Signed-Rank Test). Importantly, both ping-pong abundance and ping-pong pair density are normalized, proportional measures of abundance that are likely influenced by increases in the abundance of non-TE, genic piRNAs in the same library (see below).

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