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Pleiotropic fitness effects of the Tre1/Gr5a region in Drosophila

ABSTRACT: The abundance of transposable elements and DNA repeat sequences in mammalian genomes raises the question whether such insertions represent passive evolutionary baggage or may influence the expression of complex traits. We addressed this question in Drosophila melanogaster where the effects of single transposable elements on complex traits can be assessed in genetically identical individuals reared in controlled environments. Here we demonstrate that single P-element insertions in the intergenic region between the Gustatory receptor 5a (Gr5a) and Trapped in endoderm 1 (Tre1), which encodes an orphan receptor, exert complex pleiotropic effects on fitness traits, including selective nutrient intake, resistance to starvation and heat stress, and life span. Mutations in this region interact epistatically with downstream components of the insulin signaling pathway. Transposon-induced sex-specific and sex-antagonistic effects further accentuate the complex influences intergenic transposable elements can contribute to complex phenotypes. Keywords: Transcriptional profiles of P-element insertion lines in the Tre1/GR5a region of Drosophila

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE4789 | GEO | 2006/05/31

SECONDARY ACCESSION(S): PRJNA95727

REPOSITORIES: GEO

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Project description:The abundance of transposable elements and DNA repeat sequences in mammalian genomes raises the question whether such insertions represent passive evolutionary baggage or may influence the expression of complex traits. We addressed this question in Drosophila melanogaster where the effects of single transposable elements on complex traits can be assessed in genetically identical individuals reared in controlled environments. Here we demonstrate that single P-element insertions in the intergenic region between the Gustatory receptor 5a (Gr5a) and Trapped in endoderm 1 (Tre1), which encodes an orphan receptor, exert complex pleiotropic effects on fitness traits, including selective nutrient intake, resistance to starvation and heat stress, and life span. Mutations in this region interact epistatically with downstream components of the insulin signaling pathway. Transposon-induced sex-specific and sex-antagonistic effects further accentuate the complex influences intergenic transposable elements can contribute to complex phenotypes. SUBMITTER_CITATION: Rollmann SM, Magwire MM, Morgan TJ, Ozsoy ED, Yamamoto A, Mackay TF, Anholt RR. Pleiotropic fitness effects of the Tre1-Gr5a region in Drosophila melanogaster. Nat Genet. 2006 Jul;38(7):824-9. Experiment Overall Design: BG02514, BG02257 and Canton S (B) lines were reared simultaneously at 25 C under a 12 h light/dark cycle and 70% humidity. At 5-7 days post-eclosion, we removed the heads of two replicate groups of 100 males and 100 females for each line. Total RNA was isolated from each replicate and biotinylated cRNA probes were hybridized to high density oligonucleotide microarrays (Affymetrix, Inc.) and visualized with a streptavidin-phycoerythrin conjugate, as described in the Affymetrix GeneChip Expression Analysis Technical Manual (2000), using internal references for quantification. The quantitative estimate of expression of each probe set is the Signal (Sig) metric, as described in the Affymetrix Microarray Suite, Version 5.0. Sig values were analyzed by two-way ANOVA according to the model Y = Î¼ + L + S + LxS + E, where L is the effect of line, S is the effect of sex and E the error variance

Project description:Transposable elements have the potential to act as controlling elements to influence the expression of genes. The current paradigm suggests that heterochromatic silencing can spread beyond the borders of the transposable element and influence the chromatin state of neighboring low-copy sequences. This would allow transposable elements to condition obligatory or facilitated epialleles and act as controlling elements. The maize genome contains numerous families of class I transposable elements (retrotransposons) that are present in moderate to high copy numbers and many are found in regions near genes which provides an opportunity to test whether the spreading of heterochromatin from retrotransposons is prevalent. We have investigated the extent of heterochromatin spreading into flanking DNA around each family of retrotransposons through profiling of DNA methylation and di-methylation of lysine 9 of histone 3 (H3K9me2) in low-copy regions of the maize genome. The effects of different retrotransposon families on local chromatin are highly variable. Some LTR families exhibit enrichment of heterochromatic marks within 800-1200 base pairs of the insertion site while other families have very little evidence for spreading of heterochromatic marks. The analysis of chromatin state in genotypes that lack specific insertions suggests that the adjacent heterochromatin results from spreading of silencing rather than insertion-site preferences. Genes that are located near elements that exhibit spreading of heterochromatin tend to be expressed at lower levels than other genes. Our findings suggest that a subset of LTR retrotransposon families may act as controlling elements influencing neighboring sequences while the majority of elements have little effect on flanking sequences Transposable elements comprise a substantial portion of many eukaryotic genomes. These mobile fragments of DNA can result in mutations through insertions into genes but may also affect the regulation of genes they insert near. There is evidence that the majority of transposable elements are epigenetically silenced and in some cases this silencing may affect neighboring sequences. However, evolutionary theory would predict that there would be selective pressures for transposable elements to limit their effects on neighboring genes. The maize genome has a complex organization with many genes flanked by retrotransposons. We profiled the spread of heterochromatin from the retrotransposons into nearby low copy sequences for 150 high copy retrotransposon families. While the manymajority of retrotransposons exhibit little to no spreading of heterochromatin there are a small number ofsome retrotransposon families that influence the chromatin state of surrounding regions. The families may represent bad “neighbors” that spread heterochromatin and influence nearby genes. 6 total samples: 3 replicates of B73 H3k9 and 3 replicates of Mo17 H3k9 3 total samples: mop1 mutant, b73.zmet2 (zmet2.m1 mutant in B73 background) and mo17.zmet2 (zmet2.m1 mutant in Mo17 background)

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Pleiotropic fitness effects of the Tre1/Gr5a region in Drosophila

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