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Transgenerational inheritance of diet-induced genome rearrangements in Drosophila.

Aldrich JC, Maggert KA - PLoS Genet. (2015)

Bottom Line: Pursuing the relationship between rDNA expression and stability, we have discovered that increased dietary yeast concentration, emulating periods of dietary excess during life, results in somatic rDNA instability and copy number reduction.Modulation of Insulin/TOR signaling produces similar results, indicating a role for known nutrient sensing signaling pathways in this process.Furthermore, adults fed elevated dietary yeast concentrations produce offspring with fewer rDNA copies demonstrating that these effects also occur in the germline, and are transgenerationally heritable.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, College of Science, Texas A&M University, College Station, Texas, United States of America.

ABSTRACT
Ribosomal RNA gene (rDNA) copy number variation modulates heterochromatin formation and influences the expression of a large fraction of the Drosophila genome. This discovery, along with the link between rDNA, aging, and disease, high-lights the importance of understanding how natural rDNA copy number variation arises. Pursuing the relationship between rDNA expression and stability, we have discovered that increased dietary yeast concentration, emulating periods of dietary excess during life, results in somatic rDNA instability and copy number reduction. Modulation of Insulin/TOR signaling produces similar results, indicating a role for known nutrient sensing signaling pathways in this process. Furthermore, adults fed elevated dietary yeast concentrations produce offspring with fewer rDNA copies demonstrating that these effects also occur in the germline, and are transgenerationally heritable. This finding explains one source of natural rDNA copy number variation revealing a clear long-term consequence of diet.

No MeSH data available.


Related in: MedlinePlus

Copy number and RNA expression of R1 and R2 retrotransposable elements are not discordant.(A) Reverse Transcriptase Real-time PCR of expression of R1 and R2 transcripts from flies raised on Standard, SY10, or SY30 food sources. Values are normalized to rho1 mRNA and relative to R1 and R2 RNA levels in flies raised on Standard food, errors indicate standard error of the mean and capture increases in pooled populations raised on different food sources. Expression levels do not differ significantly from each other (only P-values less than 0.25 are shown). (B) Copy number determination of R1 and R2 elements in the Y-linked rDNA loci of flies raised on SY10, raised on SY30, or a rDNA deletion allele from a previous study with I-CreI-mediated rDNA loss (bb-183). “R1” detects unique R1-rDNA junctions, while “noR1” detects the rDNA flanking the stereotyped R1 insertion site in the rDNA. “R2” and “noR2” similarly detect R2-inserted 35S rDNA and 35S without R2 insertion, respectively. Note that each reaction uses separate primers, so comparisons between primers (“R1,” “noR1,” “R2,” “noR2”) are not valid, while comparisons between treatments (SY10, SY30, bb-183) are.
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pgen.1005148.g002: Copy number and RNA expression of R1 and R2 retrotransposable elements are not discordant.(A) Reverse Transcriptase Real-time PCR of expression of R1 and R2 transcripts from flies raised on Standard, SY10, or SY30 food sources. Values are normalized to rho1 mRNA and relative to R1 and R2 RNA levels in flies raised on Standard food, errors indicate standard error of the mean and capture increases in pooled populations raised on different food sources. Expression levels do not differ significantly from each other (only P-values less than 0.25 are shown). (B) Copy number determination of R1 and R2 elements in the Y-linked rDNA loci of flies raised on SY10, raised on SY30, or a rDNA deletion allele from a previous study with I-CreI-mediated rDNA loss (bb-183). “R1” detects unique R1-rDNA junctions, while “noR1” detects the rDNA flanking the stereotyped R1 insertion site in the rDNA. “R2” and “noR2” similarly detect R2-inserted 35S rDNA and 35S without R2 insertion, respectively. Note that each reaction uses separate primers, so comparisons between primers (“R1,” “noR1,” “R2,” “noR2”) are not valid, while comparisons between treatments (SY10, SY30, bb-183) are.

Mentions: First, we investigated whether consumption of SY30 lead to pronounced derepression of R1 or R2, the retrotransposable elements resident in the Drosophila rDNA. We could not detect significant increases in expression of either when raised on SY10 or SY30 (Fig 2A). Second, we investigated whether R1- or R2-interrupted 35S rRNA genes were preferentially lost after growth on SY30. We observed decreased R1-interrupted and R2-interrupted rDNA copies, as well as loss of uninterrupted 35S rDNA copies, but neither R1 nor R2 reductions were strongly biased over decreases as a result of I-CreI-induced damage (Fig 2B) [55].


Transgenerational inheritance of diet-induced genome rearrangements in Drosophila.

Aldrich JC, Maggert KA - PLoS Genet. (2015)

Copy number and RNA expression of R1 and R2 retrotransposable elements are not discordant.(A) Reverse Transcriptase Real-time PCR of expression of R1 and R2 transcripts from flies raised on Standard, SY10, or SY30 food sources. Values are normalized to rho1 mRNA and relative to R1 and R2 RNA levels in flies raised on Standard food, errors indicate standard error of the mean and capture increases in pooled populations raised on different food sources. Expression levels do not differ significantly from each other (only P-values less than 0.25 are shown). (B) Copy number determination of R1 and R2 elements in the Y-linked rDNA loci of flies raised on SY10, raised on SY30, or a rDNA deletion allele from a previous study with I-CreI-mediated rDNA loss (bb-183). “R1” detects unique R1-rDNA junctions, while “noR1” detects the rDNA flanking the stereotyped R1 insertion site in the rDNA. “R2” and “noR2” similarly detect R2-inserted 35S rDNA and 35S without R2 insertion, respectively. Note that each reaction uses separate primers, so comparisons between primers (“R1,” “noR1,” “R2,” “noR2”) are not valid, while comparisons between treatments (SY10, SY30, bb-183) are.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4401788&req=5

pgen.1005148.g002: Copy number and RNA expression of R1 and R2 retrotransposable elements are not discordant.(A) Reverse Transcriptase Real-time PCR of expression of R1 and R2 transcripts from flies raised on Standard, SY10, or SY30 food sources. Values are normalized to rho1 mRNA and relative to R1 and R2 RNA levels in flies raised on Standard food, errors indicate standard error of the mean and capture increases in pooled populations raised on different food sources. Expression levels do not differ significantly from each other (only P-values less than 0.25 are shown). (B) Copy number determination of R1 and R2 elements in the Y-linked rDNA loci of flies raised on SY10, raised on SY30, or a rDNA deletion allele from a previous study with I-CreI-mediated rDNA loss (bb-183). “R1” detects unique R1-rDNA junctions, while “noR1” detects the rDNA flanking the stereotyped R1 insertion site in the rDNA. “R2” and “noR2” similarly detect R2-inserted 35S rDNA and 35S without R2 insertion, respectively. Note that each reaction uses separate primers, so comparisons between primers (“R1,” “noR1,” “R2,” “noR2”) are not valid, while comparisons between treatments (SY10, SY30, bb-183) are.
Mentions: First, we investigated whether consumption of SY30 lead to pronounced derepression of R1 or R2, the retrotransposable elements resident in the Drosophila rDNA. We could not detect significant increases in expression of either when raised on SY10 or SY30 (Fig 2A). Second, we investigated whether R1- or R2-interrupted 35S rRNA genes were preferentially lost after growth on SY30. We observed decreased R1-interrupted and R2-interrupted rDNA copies, as well as loss of uninterrupted 35S rDNA copies, but neither R1 nor R2 reductions were strongly biased over decreases as a result of I-CreI-induced damage (Fig 2B) [55].

Bottom Line: Pursuing the relationship between rDNA expression and stability, we have discovered that increased dietary yeast concentration, emulating periods of dietary excess during life, results in somatic rDNA instability and copy number reduction.Modulation of Insulin/TOR signaling produces similar results, indicating a role for known nutrient sensing signaling pathways in this process.Furthermore, adults fed elevated dietary yeast concentrations produce offspring with fewer rDNA copies demonstrating that these effects also occur in the germline, and are transgenerationally heritable.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, College of Science, Texas A&M University, College Station, Texas, United States of America.

ABSTRACT
Ribosomal RNA gene (rDNA) copy number variation modulates heterochromatin formation and influences the expression of a large fraction of the Drosophila genome. This discovery, along with the link between rDNA, aging, and disease, high-lights the importance of understanding how natural rDNA copy number variation arises. Pursuing the relationship between rDNA expression and stability, we have discovered that increased dietary yeast concentration, emulating periods of dietary excess during life, results in somatic rDNA instability and copy number reduction. Modulation of Insulin/TOR signaling produces similar results, indicating a role for known nutrient sensing signaling pathways in this process. Furthermore, adults fed elevated dietary yeast concentrations produce offspring with fewer rDNA copies demonstrating that these effects also occur in the germline, and are transgenerationally heritable. This finding explains one source of natural rDNA copy number variation revealing a clear long-term consequence of diet.

No MeSH data available.


Related in: MedlinePlus