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Transcriptome profiling of Nasonia vitripennis testis reveals novel transcripts expressed from the selfish B chromosome, paternal sex ratio.

Akbari OS, Antoshechkin I, Hay BA, Ferree PM - G3 (Bethesda) (2013)

Bottom Line: This results in the conversion of a fertilized embryo--normally a female--into a male, thereby insuring transmission of the "selfish" PSR chromosome, and simultaneously leading to wasp populations that are male-biased.We propose several different models for how these transcripts could facilitate PSR-dependent effects.Finally, we detected expression of multiple meiosis-related genes in the wasp testis, despite the lack of conventional meiosis in the male sex.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, MC156-29, California Institute of Technology, Pasadena, California 91125.

ABSTRACT
A widespread phenomenon in nature is sex ratio distortion of arthropod populations caused by microbial and genetic parasites. Currently little is known about how these agents alter host developmental processes to favor one sex or the other. The paternal sex ratio (PSR) chromosome is a nonessential, paternally transmitted centric fragment that segregates in natural populations of the jewel wasp, Nasonia vitripennis. To persist, PSR is thought to modify the hereditary material of the developing sperm, with the result that all nuclear DNA other than the PSR chromosome is destroyed shortly after fertilization. This results in the conversion of a fertilized embryo--normally a female--into a male, thereby insuring transmission of the "selfish" PSR chromosome, and simultaneously leading to wasp populations that are male-biased. To begin to understand this system at the mechanistic level, we carried out transcriptional profiling of testis from WT and PSR-carrying males. We identified a number of transcripts that are differentially expressed between these conditions. We also discovered nine transcripts that are uniquely expressed from the PSR chromosome. Four of these PSR-specific transcripts encode putative proteins, whereas the others have very short open reading frames and no homology to known proteins, suggesting that they are long noncoding RNAs. We propose several different models for how these transcripts could facilitate PSR-dependent effects. Our analyses also revealed 15.71 MB of novel transcribed regions in the N. vitripennis genome, thus increasing the current annotation of total transcribed regions by 53.4%. Finally, we detected expression of multiple meiosis-related genes in the wasp testis, despite the lack of conventional meiosis in the male sex.

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Scatter plot of PSR vs. WT testes with coefficient of determination. Scatter plot of fragments per kilobase of exon per million fragments mapped values for genes and NTRs comparing expression values for PSR (Y-axis) and WT (X-axis) testes. The coefficient of determination (R2) is displayed in top left.
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fig2: Scatter plot of PSR vs. WT testes with coefficient of determination. Scatter plot of fragments per kilobase of exon per million fragments mapped values for genes and NTRs comparing expression values for PSR (Y-axis) and WT (X-axis) testes. The coefficient of determination (R2) is displayed in top left.

Mentions: Another goal of this study was to identify any genes in the normal wasp genome that are misexpressed and to assess whether TEs become transcriptionally hyperactive, in the presence of PSR. First, using our comprehensive testis transcriptome, we calculated the expression levels for all previously annotated genes and our NTRs, and observed a strong correlation between the WT and PSR-containing testis samples (Pearson Correlation Coefficient 0.962; Figure 2, Table S8, and Table S9). Thus, expression of the vast majority of wasp genes in the testis is not affected by PSR. To further investigate the genes that were misexpressed in the presence of PSR, we performed an over/underrepresentation analysis, which revealed several patterns. First, we found a total of 199 previously annotated genes and NTRs that are overrepresented in the PSR testis and 345 previously annotated genes and NTRs that are underrepresented in the PSR testes compared with WT testes (P < 0.05; Table S10 and Table S11). A gene ontology analysis revealed that the majority of overexpressed genes are involved in cellular carbohydrate biosynthesis, protein polymerization, and cellular protein complex assembly. The majority of genes that were under-represented in the PSR testes are involved in chitin metabolism, aminoglycan metabolism, and polysaccharide metabolism. There were also smaller numbers of genes in other gene ontology categories that were also up- or down-regulated in PSR testes and these may also be important for the role PSR plays (Table S12 and Table S13).


Transcriptome profiling of Nasonia vitripennis testis reveals novel transcripts expressed from the selfish B chromosome, paternal sex ratio.

Akbari OS, Antoshechkin I, Hay BA, Ferree PM - G3 (Bethesda) (2013)

Scatter plot of PSR vs. WT testes with coefficient of determination. Scatter plot of fragments per kilobase of exon per million fragments mapped values for genes and NTRs comparing expression values for PSR (Y-axis) and WT (X-axis) testes. The coefficient of determination (R2) is displayed in top left.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3755920&req=5

fig2: Scatter plot of PSR vs. WT testes with coefficient of determination. Scatter plot of fragments per kilobase of exon per million fragments mapped values for genes and NTRs comparing expression values for PSR (Y-axis) and WT (X-axis) testes. The coefficient of determination (R2) is displayed in top left.
Mentions: Another goal of this study was to identify any genes in the normal wasp genome that are misexpressed and to assess whether TEs become transcriptionally hyperactive, in the presence of PSR. First, using our comprehensive testis transcriptome, we calculated the expression levels for all previously annotated genes and our NTRs, and observed a strong correlation between the WT and PSR-containing testis samples (Pearson Correlation Coefficient 0.962; Figure 2, Table S8, and Table S9). Thus, expression of the vast majority of wasp genes in the testis is not affected by PSR. To further investigate the genes that were misexpressed in the presence of PSR, we performed an over/underrepresentation analysis, which revealed several patterns. First, we found a total of 199 previously annotated genes and NTRs that are overrepresented in the PSR testis and 345 previously annotated genes and NTRs that are underrepresented in the PSR testes compared with WT testes (P < 0.05; Table S10 and Table S11). A gene ontology analysis revealed that the majority of overexpressed genes are involved in cellular carbohydrate biosynthesis, protein polymerization, and cellular protein complex assembly. The majority of genes that were under-represented in the PSR testes are involved in chitin metabolism, aminoglycan metabolism, and polysaccharide metabolism. There were also smaller numbers of genes in other gene ontology categories that were also up- or down-regulated in PSR testes and these may also be important for the role PSR plays (Table S12 and Table S13).

Bottom Line: This results in the conversion of a fertilized embryo--normally a female--into a male, thereby insuring transmission of the "selfish" PSR chromosome, and simultaneously leading to wasp populations that are male-biased.We propose several different models for how these transcripts could facilitate PSR-dependent effects.Finally, we detected expression of multiple meiosis-related genes in the wasp testis, despite the lack of conventional meiosis in the male sex.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, MC156-29, California Institute of Technology, Pasadena, California 91125.

ABSTRACT
A widespread phenomenon in nature is sex ratio distortion of arthropod populations caused by microbial and genetic parasites. Currently little is known about how these agents alter host developmental processes to favor one sex or the other. The paternal sex ratio (PSR) chromosome is a nonessential, paternally transmitted centric fragment that segregates in natural populations of the jewel wasp, Nasonia vitripennis. To persist, PSR is thought to modify the hereditary material of the developing sperm, with the result that all nuclear DNA other than the PSR chromosome is destroyed shortly after fertilization. This results in the conversion of a fertilized embryo--normally a female--into a male, thereby insuring transmission of the "selfish" PSR chromosome, and simultaneously leading to wasp populations that are male-biased. To begin to understand this system at the mechanistic level, we carried out transcriptional profiling of testis from WT and PSR-carrying males. We identified a number of transcripts that are differentially expressed between these conditions. We also discovered nine transcripts that are uniquely expressed from the PSR chromosome. Four of these PSR-specific transcripts encode putative proteins, whereas the others have very short open reading frames and no homology to known proteins, suggesting that they are long noncoding RNAs. We propose several different models for how these transcripts could facilitate PSR-dependent effects. Our analyses also revealed 15.71 MB of novel transcribed regions in the N. vitripennis genome, thus increasing the current annotation of total transcribed regions by 53.4%. Finally, we detected expression of multiple meiosis-related genes in the wasp testis, despite the lack of conventional meiosis in the male sex.

Show MeSH
Related in: MedlinePlus