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Doublesex and the regulation of sexual dimorphism in Drosophila melanogaster: structure, function, and mutagenesis of a female-specific domain.

Yang Y, Zhang W, Bayrer JR, Weiss MA
J Biol Chem 283 7280-92 (2008)
Cited: 15 times
EuropePMC logo PMID: 18184648

Abstract

The DSX (Doublesex) transcription factor regulates somatic sexual differentiation in Drosophila. Female and male isoforms (DSX F and DSX M) are formed due to sex-specific RNA splicing. DNA recognition, mediated by a shared N-terminal zinc module (the DM domain), is enhanced by a C-terminal dimerization element. Sex-specific extension of this element in DSX F and DSX M leads to assembly of distinct transcriptional preinitiation complexes. Here, we describe the structure of the extended C-terminal dimerization domain of DSX F as determined by multidimensional NMR spectroscopy. The core dimerization element is well ordered, giving rise to a dense network of interresidue nuclear Overhauser enhancements. The structure contains dimer-related UBA folds similar to those defined by x-ray crystallographic studies of a truncated domain. Whereas the proximal portion of the female tail extends helix 3 of the UBA fold, the distal tail is disordered. Ala substitutions in the proximal tail disrupt the sex-specific binding of IX (Intersex), an obligatory partner protein and putative transcriptional coactivator; IX-DSX F interaction is, by contrast, not disrupted by truncation of the distal tail. Mutagenesis of the UBA-like dimer of DSX F highlights the importance of steric and electrostatic complementarity across the interface. Two temperature-sensitive mutations at this interface have been characterized in yeast model systems. One weakens a network of solvated salt bridges, whereas the other perturbs the underlying nonpolar interface. These mutations confer graded gene-regulatory activity in yeast within a physiological temperature range and so may provide novel probes for genetic analysis of a sex-specific transcriptional program in Drosophila development.

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Articles citing this publication (14)

  1. Sex- and tissue-specific functions of Drosophila doublesex transcription factor target genes. Clough E, Jimenez E, Kim YA, Whitworth C, Neville MC, Hempel LU, Pavlou HJ, Chen ZX, Sturgill D, Dale RK, Smith HE, Przytycka TM, Goodwin SF, Goodwin SF, Van Doren M, Oliver B. Dev Cell 31 761-773 (2014)
  2. Modular tissue-specific regulation of doublesex underpins sexually dimorphic development in Drosophila. Rice GR, Barmina O, Luecke D, Hu K, Arbeitman M, Kopp A. Development 146 dev178285 (2019)
  3. Developmental expression of "germline"- and "sex determination"-related genes in the ctenophore Mnemiopsis leidyi. Reitzel AM, Pang K, Martindale MQ. Evodevo 7 17 (2016)
  4. Isolation and characterization of Doublesex homologues in the Bactrocera species: B. dorsalis (Hendel) and B. correcta (Bezzi) and their putative promoter regulatory regions. Permpoon R, Aketarawong N, Thanaphum S. Genetica 139 113-127 (2011)
  5. Novel Doublesex Duplication Associated with Sexually Dimorphic Development of Dogface Butterfly Wings. Rodriguez-Caro F, Fenner J, Bhardwaj S, Cole J, Benson C, Colombara AM, Papa R, Brown MW, Martin A, Range RC, Counterman BA. Mol Biol Evol 38 5021-5033 (2021)
  6. Sex-specific and developmental expression of Dmrt genes in the starlet sea anemone, Nematostella vectensis. Traylor-Knowles NG, Kane EG, Sombatsaphay V, Finnerty JR, Reitzel AM. Evodevo 6 13 (2015)
  7. The study of the transformer gene from Bactrocera dorsalis and B. correcta with putative core promoter regions. Laohakieat K, Aketarawong N, Isasawin S, Thitamadee S, Thanaphum S. BMC Genet 17 34 (2016)
  8. Drosophila intersex orthologue in the silkworm, Bombyx mori and related species. Arunkumar KP, Nagaraju J. Genetica 139 141-147 (2011)
  9. Evolutionary History of Sexual Differentiation Mechanism in Insects. Chikami Y, Okuno M, Toyoda A, Itoh T, Niimi T. Mol Biol Evol 39 msac145 (2022)
  10. CRISPR/Cas9-based split homing gene drive targeting doublesex for population suppression of the global fruit pest Drosophila suzukii. Yadav AK, Butler C, Yamamoto A, Patil AA, Lloyd AL, Scott MJ. Proc Natl Acad Sci U S A 120 e2301525120 (2023)
  11. Pleiotropic Roles of the Orthologue of the Drosophila melanogaster Intersex Gene in the Brown Planthopper. Zhang HH, Xie YC, Li HJ, Zhuo JC, Zhang CX. Genes (Basel) 12 379 (2021)
  12. Characteristic and Functional Study of Intersex, a Gene Related to Female Fertility in Bemisia tabaci. Liu Y, Yang J, Huo Z, Wang S, Wu Q, Zhou X, Xie W, Zhang Y. Front Physiol 11 55 (2020)
  13. Intersex (ix) mutations of Drosophila melanogaster cause nonrandom cell death in genital disc and can induce tumours in genitals in response to decapentaplegic (dpp(disk)) mutations. Chatterjee RN, Chatterjee P, Kuthe S, Acharyya-Ari M, Chatterjee R. J Genet 94 207-220 (2015)
  14. Nucleoporin107 mediates female sexual differentiation via Dsx. Shore T, Levi T, Kalifa R, Dreifuss A, Rekler D, Weinberg-Shukron A, Nevo Y, Bialistoky T, Moyal V, Gold MY, Leebhoff S, Zangen D, Deshpande G, Gerlitz O. Elife 11 e72632 (2022)


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