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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0.5 0.4 0.3 0.2 0.1 0 0.6 0.7 0.8 0.9 1fru P1-GAL4 UAS-FruMAUAS-FruMBUAS-FruMC+ + + + + + + + + +Courtship Index (Time Courting/Total Time)UAS-GAL4+ + + + 0.5 0.4 0.3 0.2 0.1 0Wing Extension Index (Time Wing Extending/Total Time)fru P1-GAL4 UAS-FruMAUAS-FruMBUAS-FruMC+ + + + + + + + + +UAS-GAL4+ + + +A. B.Male to Female Courtship Male to Female Courtship Additional Figure 3 Additional Figure 3: Courtship analysis of males over-expressing FruMA,B or C Courtship index (A-B) and wing extension index (C-D) for male-female (A and C) and male-male (B and D) courtship behavior of corresponding experimental or control males (grey and white boxes, respectively). Males over-expressing FruMA, FruMB, or FruMCin fru P1-expressing neurons (grey lled purple, pink or cyan), single transgene FruMA, FruMB, or FruMCmales (white lled purple, pink, or cyan), UAS-GAL4/+; fru P1-GAL4/+ single transgene males, and Canton S males (no transgenes indicated) are indicated. Dashed grey box indicates statistically signicance dierence of experimental males from all three controls (Canton S, UAS-GAL4/+;fru P1-GAL4/+, and respective FruMA,B or C single transgene males ) at p-value < 0.05 (Wilcoxon rank sum test, two sided). Median is indicated by horizontal line in box, boxes cover 25th to 75th percentiles of the samples, whiskers represent data not considered an outlier, and outliers are dened as values greater than or less than 1.5 times the interquartile range (red cross).