Male-specific Fruitless isoforms have different regulatory roles conferred by distinct zinc finger DNA binding domains


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Male-specific Fruitless isoforms have different regulatory roles conferred by distinct zinc finger DNA binding domains
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Dalton, Justin E.
Fear, Justin M.
Knott, Simon
Baker, Bruce S.
McIntyre, Lauren M.
Arbeitman, Michelle N.
Bio-Med Central (BMC Genomics)
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Background: Drosophila melanogaster adult males perform an elaborate courtship ritual to entice females to mate. fruitless (fru), a gene that is one of the key regulators of male courtship behavior, encodes multiple male-specific isoforms (FruM). These isoforms vary in their carboxy-terminal zinc finger domains, which are predicted to facilitate DNA binding. Results: By over-expressing individual FruM isoforms in fru-expressing neurons in either males or females and assaying the global transcriptional response by RNA-sequencing, we show that three FruM isoforms have different regulatory activities that depend on the sex of the fly. We identified several sets of genes regulated downstream of FruM isoforms, including many annotated with neuronal functions. By determining the binding sites of individual FruM isoforms using SELEX we demonstrate that the distinct zinc finger domain of each FruM isoforms confers different DNA binding specificities. A genome-wide search for these binding site sequences finds that the gene sets identified as induced by over-expression of FruM isoforms in males are enriched for genes that contain the binding sites. An analysis of the chromosomal distribution of genes downstream of FruM shows that those that are induced and repressed in males are highly enriched and depleted on the X chromosome, respectively. Conclusions: This study elucidates the different regulatory and DNA binding activities of three FruM isoforms on a genome-wide scale and identifies genes regulated by these isoforms. These results add to our understanding of sex chromosome biology and further support the hypothesis that in some cell-types genes with male-biased expression are enriched on the X chromosome. Keywords: Fruitless, Sex hierarchy, Drosophila, Behavior, Genomics, RNA-seq
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Dalton et al. BMC Genomics 2013, 14:659; Pages 1-15
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doi:10.1186/1471-2164-14-659 Cite this article as: Dalton et al.: Male-specific Fruitless isoforms have different regulatory roles conferred by distinct zinc finger DNA binding domains. BMC Genomics 2013 14:659.

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A.FruMA Induced Male and FemaleB.FruMB Induced Male and FemaleC. D. E. F. G.Induced in MaleH. 70844 67Male Female 692 47 70 Male FemaleFruMC Induced Male and Female863 64 103 Male FemaleFruMA Repressed Male and Female FruMB Repressed Male and Female FruMC Repressed Male and Female147 57 126 207 52 185 245 50 148 Male Female Male Female Male Female 497 206 35 11 87 20 16 124 90 113 103 10 347 4 51 FruNullFruMCFruMBFruMA 417 163 5 5 23 2 1 101 129 4 46 2 51 0 22 FruNullFruMCFruMBFruMARepressed in MaleAdditional Figure 1Additional Figure 1: Venn diagrams of comparisons from various sets of genes. (A-H) Venn diagrams displaying number of distinct and mutual genes between dierent sets of dierentially expressed genes. (A-F) Numbers of genes induced or repressed in males and females by over-expression of FruMA, FruMB or FruMC in fru P1-expressing neurons of the head. (G-H) Numbers of genes induced or repressed by FruM as determined by FruM loss of function analysis, and induced or repressed by over-expression of FruMA, FruMB, or FruMC isoforms.