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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

Genetic analysis of zygotic induction and maternal repression of gonadal atrophy.(A) Induction of sterility by 160 is broadly distributed across the genome, with the exception of chromosome 6 (the dot chromosome). Log odds ratios for probability of induction were estimated by crossing F1 males to strain 9, determining whether F2s had male gonadal atrophy and genotyping F2s to determine the chromosomes inherited from the father. Estimates were determined using a generalized linear model for logistic regression (binomial family with a logit link). Values in red are actual odds ratios. Whiskers are 95% confidence intervals. Chromosome 5 is significant at 0.1 level only. X chromosome is not scored because dysgenesis is scored in males and males do not inherit the X from their fathers (N = 92). (B) Scatterplot showing proportion of dysgenic testes (y axis) observed in the progeny of each F3 female individual (x axis). Red dots indicate F3 females that were selected for whole genome sequencing. (C) Single marker QTL analysis identified 3 putative QTLs: one flanking the centromeres of the 5th and X chromosomes and one of the tested euchromatic regions of the 4th chromosome. (D) Top row: Results from the genotyping assay. Colored rectangles represent the presence of strain 160 SNPs in individuals, ranked from top to bottom (most protective individuals on top). Scatterplots: sequencing results. Each dot represents the average number of base pairs that uniquely mapped to every 10kb of the 160 genome. Valleys indicate regions of strain 9 homozygosity. Black dots above scatterplots show the location of each SNP used for our genotyping assay. Grey background demonstrates that no region of the genome from 160 is necessary to protect against dysgenesis. Right-most columns: Number of piRNAs mapped to TART sequences, per million reads, for each F3 female individual. Color intensity is representative of TART piRNA abundance. Number of 21 nt endo-siRNAs mapped to Penelope sequences, per million 21 nt reads, for each F3 female individual. Color intensity is representative of Penelope endo-siRNA abundance. Red bar indicates position of one of several Penelope endo-siRNA loci on the X.
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pgen.1005332.g006: Genetic analysis of zygotic induction and maternal repression of gonadal atrophy.(A) Induction of sterility by 160 is broadly distributed across the genome, with the exception of chromosome 6 (the dot chromosome). Log odds ratios for probability of induction were estimated by crossing F1 males to strain 9, determining whether F2s had male gonadal atrophy and genotyping F2s to determine the chromosomes inherited from the father. Estimates were determined using a generalized linear model for logistic regression (binomial family with a logit link). Values in red are actual odds ratios. Whiskers are 95% confidence intervals. Chromosome 5 is significant at 0.1 level only. X chromosome is not scored because dysgenesis is scored in males and males do not inherit the X from their fathers (N = 92). (B) Scatterplot showing proportion of dysgenic testes (y axis) observed in the progeny of each F3 female individual (x axis). Red dots indicate F3 females that were selected for whole genome sequencing. (C) Single marker QTL analysis identified 3 putative QTLs: one flanking the centromeres of the 5th and X chromosomes and one of the tested euchromatic regions of the 4th chromosome. (D) Top row: Results from the genotyping assay. Colored rectangles represent the presence of strain 160 SNPs in individuals, ranked from top to bottom (most protective individuals on top). Scatterplots: sequencing results. Each dot represents the average number of base pairs that uniquely mapped to every 10kb of the 160 genome. Valleys indicate regions of strain 9 homozygosity. Black dots above scatterplots show the location of each SNP used for our genotyping assay. Grey background demonstrates that no region of the genome from 160 is necessary to protect against dysgenesis. Right-most columns: Number of piRNAs mapped to TART sequences, per million reads, for each F3 female individual. Color intensity is representative of TART piRNA abundance. Number of 21 nt endo-siRNAs mapped to Penelope sequences, per million 21 nt reads, for each F3 female individual. Color intensity is representative of Penelope endo-siRNA abundance. Red bar indicates position of one of several Penelope endo-siRNA loci on the X.

Mentions: We found that induction of dysgenesis is distributed across all chromosomes, with the exception of the dot sixth chromosome (Fig 6A). Therefore, strain 160 telomeres of the second and sixth chromosomes do not contribute uniquely to induction of dysgenesis. Using QTL analysis (Fig 6B) with special attention to telomeric and pericentric regions (motivated by the fact that these genomic compartments often contain TE-rich piRNA clusters[23,26]), we identified three genomic regions for which strain 160 variants at these positions significantly protected against F1 sterility when present in the mother (i.e., dysgenesis; Fig 6C). The genomic region with the most significant effect corresponded to the pericentric region of chromosome 5. The pericentric region of the X chromosome also explained a significant proportion of variation in protective ability, followed by a euchromatic region in the proximal arm region of chromosome 4. We tested for interactions between these loci and saw no evidence for synergism (p-value for all interactions >0.2). Our previous work also found chromosome 5 to be the most protective, followed by the X and then chromosome 4 [49]. Together with the results from this study, there is strong genetic evidence that pericentric, cluster-derived piRNAs play a role in the protection against dysgenesis in D. virilis. By contrast, variation in telomeric repeat abundance between strains does not explain variation in protection against dysgenesis. Thus, telomeric piRNA clusters and amplified TART elements are likely a result of TE destabilization in the inducer strain rather than a driver.


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)

Genetic analysis of zygotic induction and maternal repression of gonadal atrophy.(A) Induction of sterility by 160 is broadly distributed across the genome, with the exception of chromosome 6 (the dot chromosome). Log odds ratios for probability of induction were estimated by crossing F1 males to strain 9, determining whether F2s had male gonadal atrophy and genotyping F2s to determine the chromosomes inherited from the father. Estimates were determined using a generalized linear model for logistic regression (binomial family with a logit link). Values in red are actual odds ratios. Whiskers are 95% confidence intervals. Chromosome 5 is significant at 0.1 level only. X chromosome is not scored because dysgenesis is scored in males and males do not inherit the X from their fathers (N = 92). (B) Scatterplot showing proportion of dysgenic testes (y axis) observed in the progeny of each F3 female individual (x axis). Red dots indicate F3 females that were selected for whole genome sequencing. (C) Single marker QTL analysis identified 3 putative QTLs: one flanking the centromeres of the 5th and X chromosomes and one of the tested euchromatic regions of the 4th chromosome. (D) Top row: Results from the genotyping assay. Colored rectangles represent the presence of strain 160 SNPs in individuals, ranked from top to bottom (most protective individuals on top). Scatterplots: sequencing results. Each dot represents the average number of base pairs that uniquely mapped to every 10kb of the 160 genome. Valleys indicate regions of strain 9 homozygosity. Black dots above scatterplots show the location of each SNP used for our genotyping assay. Grey background demonstrates that no region of the genome from 160 is necessary to protect against dysgenesis. Right-most columns: Number of piRNAs mapped to TART sequences, per million reads, for each F3 female individual. Color intensity is representative of TART piRNA abundance. Number of 21 nt endo-siRNAs mapped to Penelope sequences, per million 21 nt reads, for each F3 female individual. Color intensity is representative of Penelope endo-siRNA abundance. Red bar indicates position of one of several Penelope endo-siRNA loci on the X.
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Related In: Results  -  Collection

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pgen.1005332.g006: Genetic analysis of zygotic induction and maternal repression of gonadal atrophy.(A) Induction of sterility by 160 is broadly distributed across the genome, with the exception of chromosome 6 (the dot chromosome). Log odds ratios for probability of induction were estimated by crossing F1 males to strain 9, determining whether F2s had male gonadal atrophy and genotyping F2s to determine the chromosomes inherited from the father. Estimates were determined using a generalized linear model for logistic regression (binomial family with a logit link). Values in red are actual odds ratios. Whiskers are 95% confidence intervals. Chromosome 5 is significant at 0.1 level only. X chromosome is not scored because dysgenesis is scored in males and males do not inherit the X from their fathers (N = 92). (B) Scatterplot showing proportion of dysgenic testes (y axis) observed in the progeny of each F3 female individual (x axis). Red dots indicate F3 females that were selected for whole genome sequencing. (C) Single marker QTL analysis identified 3 putative QTLs: one flanking the centromeres of the 5th and X chromosomes and one of the tested euchromatic regions of the 4th chromosome. (D) Top row: Results from the genotyping assay. Colored rectangles represent the presence of strain 160 SNPs in individuals, ranked from top to bottom (most protective individuals on top). Scatterplots: sequencing results. Each dot represents the average number of base pairs that uniquely mapped to every 10kb of the 160 genome. Valleys indicate regions of strain 9 homozygosity. Black dots above scatterplots show the location of each SNP used for our genotyping assay. Grey background demonstrates that no region of the genome from 160 is necessary to protect against dysgenesis. Right-most columns: Number of piRNAs mapped to TART sequences, per million reads, for each F3 female individual. Color intensity is representative of TART piRNA abundance. Number of 21 nt endo-siRNAs mapped to Penelope sequences, per million 21 nt reads, for each F3 female individual. Color intensity is representative of Penelope endo-siRNA abundance. Red bar indicates position of one of several Penelope endo-siRNA loci on the X.
Mentions: We found that induction of dysgenesis is distributed across all chromosomes, with the exception of the dot sixth chromosome (Fig 6A). Therefore, strain 160 telomeres of the second and sixth chromosomes do not contribute uniquely to induction of dysgenesis. Using QTL analysis (Fig 6B) with special attention to telomeric and pericentric regions (motivated by the fact that these genomic compartments often contain TE-rich piRNA clusters[23,26]), we identified three genomic regions for which strain 160 variants at these positions significantly protected against F1 sterility when present in the mother (i.e., dysgenesis; Fig 6C). The genomic region with the most significant effect corresponded to the pericentric region of chromosome 5. The pericentric region of the X chromosome also explained a significant proportion of variation in protective ability, followed by a euchromatic region in the proximal arm region of chromosome 4. We tested for interactions between these loci and saw no evidence for synergism (p-value for all interactions >0.2). Our previous work also found chromosome 5 to be the most protective, followed by the X and then chromosome 4 [49]. Together with the results from this study, there is strong genetic evidence that pericentric, cluster-derived piRNAs play a role in the protection against dysgenesis in D. virilis. By contrast, variation in telomeric repeat abundance between strains does not explain variation in protection against dysgenesis. Thus, telomeric piRNA clusters and amplified TART elements are likely a result of TE destabilization in the inducer strain rather than a driver.

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