Fruitless and Doublesex Coordinate to Generate Male-Specific Neurons that Can Initiate Courtship

Kimura, Ken; Hachiya, Tomoaki; Koganezawa, Masayuki; Tazawa, Tatsunori; Yamamoto, Daisuke

doi:10.1016/j.neuron.2008.06.007

Cited by 288 publications

(277 citation statements)

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“…Male-specific and female-specific fru-P1 transcripts were detected at a similar level of expression in both the male and female CNS in a restricted subset of approximately 2000 cells out of the 10 5 cells constituting the CNS of Drosophila (Ryner et al 1996;Kimura et al 2008); however, FRU protein is not detected in the female CNS. Immunocytochemistry assays with a FRU antibody, specific for the common region of the protein, detected FRU protein only in the CNS of males Usui-Aoki et al 2000).…”

Section: Alternative Sex-specific Splicing Of Dmfrumentioning

confidence: 89%

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fruitless alternative splicing and sex behaviour in insects: an ancient and unforgettable love story?

Salvemini

Polito

Saccone

2010

J Genet

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Courtship behaviours are common features of animal species that reproduce sexually. Typically, males are involved in courting females. Insects display an astonishing variety of courtship strategies primarily based on innate stereotyped responses to various external stimuli. In Drosophila melanogaster, male courtship requires proteins encoded by the fruitless (fru) gene that are produced in different sex-specific isoforms via alternative splicing. Drosophila mutant flies with loss-of-function alleles of the fru gene exhibit blocked male courtship behaviour. However, various individual steps in the courtship ritual are disrupted in fly strains carrying different fru alleles. These findings suggest that fru is required for specific steps in courtship. In distantly related insect species, various fru paralogues were isolated, which shows conservation of sex-specific alternative splicing and protein expression in neural tissues and suggests an evolutionary functional conservation of fru in the control of male-specific courtship behaviour. In this review, we report the seminal findings regarding the fru gene, its splicing regulation and evolution in insects.

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Section: Alternative Sex-specific Splicing Of Dmfrumentioning

confidence: 89%

“…When near a female, Drosophila males vibrate one wing producing a species-specific song, which exerts an aphrodisiac effect on the female (Hall 1994;Greenspan and Ferveur 2000;Shirangi and McKeown 2007;Kimura et al 2008). In addition, mosquitoes can sing; males of most mosquito *For correspondence.…”

Section: Introductionmentioning

confidence: 99%

fruitless alternative splicing and sex behaviour in insects: an ancient and unforgettable love story?

Salvemini

Polito

Saccone

2010

J Genet

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“…Although the distribution and projection patterns of fru neurons are broadly similar between male and female Drosophila (30 -32), subpopulations of fru neurons have been shown to exhibit sexual dimorphism in both num- ber and wiring (33)(34)(35). We initially tested whether editing activity in fru neurons also showed sexual dimorphism by driving the two independent insertions of the syt-T reporter (Fig.…”

Section: Inhibition Of Rna Editing In a Small Subset Of Neurons Is Sumentioning

confidence: 99%

Engineered Alterations in RNA Editing Modulate Complex Behavior in Drosophila

Jepson¹,

Savva²,

Yokose

et al. 2011

Journal of Biological Chemistry

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Select proteins involved in electrical and chemical neurotransmission are re-coded at the RNA level via the deamination of particular adenosines to inosine by adenosine deaminases acting on RNA (ADARs). It has been hypothesized that this process, termed RNA editing, acts to "fine-tune" neurophysiological properties in animals and potentially downstream behavioral outputs. However, the extreme phenotypes resulting from deletions of adar loci have precluded investigations into the relationship between ADAR levels, target transcripts, and complex behaviors. Here, we engineer Drosophila hypomorphic for ADAR expression using homologous recombination. A substantial reduction in ADAR activity (>80%) leads to altered circadian motor patterns and abnormal male courtship, although surprisingly, general locomotor coordination is spared. The altered phenotypic landscape in our adar hypomorph is paralleled by an unexpected dichotomous response of ADAR target transcripts, i.e. certain adenosines are minimally affected by dramatic ADAR reduction, whereas editing of others is severely curtailed. Furthermore, we use a novel reporter to map RNA editing activity across the nervous system, and we demonstrate that knockdown of editing in fruitless-expressing neurons is sufficient to modify the male courtship song. Our data demonstrate that network-wide temporal and spatial regulation of ADAR activity can tune the complex system of RNA-editing sites and modulate multiple ethologically relevant behavioral modalities.Informational recoding of RNA by the catalytic deamination of adenosine to inosine proceeds through the action of ADARs 3 (1). Long double strand RNA duplexes exhibiting perfect complementarity can be modified extensively by promiscuous ADAR activity. However, mRNAs may also serve as site-specific substrates for ADARs via base pairing interactions that generate short imperfect duplexes that generally include the exon destined for editing and a cis-acting complementary sequence, usually found in a neighboring intron (2, 3). Because inosine is recognized by the translation machinery as guanosine (4), A-to-I editing in mRNAs can lead to the incorporation of amino acids differing from those specified by the literal genome.In Drosophila, the spectrum of ADAR substrates is peculiarly specific, consisting primarily of mRNAs encoding an array of voltage-and ligand-gated ion channels, as well as numerous pre-synaptic proteins involved in exo-and endocytosis of synaptic vesicles (5-8). Similarly, several mammalian ion channels and G-protein-coupled receptors are also subject to RNA editing (2, 7, 9 -11). In light of the ontological class and high sequence conservation of ADAR target genes, RNA editing has been invoked as an essential function in controlling synaptic transmission and neurophysiology. Correspondingly, deletion of the single Drosophila adar locus (dAdar) results in severe adult-stage behavioral abnormalities, including extreme uncoordination, seizures and a complete lack of courtship in dAdar null (dAdar 5g1 ) males (1...

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“…Previous studies have tended to focus on the magnitude of sea-level decline during the Last Glacial Maximum (LGM), rather than the timing of it, with the general consensus being that sea level was about 125-135 m lower than it is today 3,4 . Geological records that shed light on the detailed timing of sea-level change during this period are notoriously difficult to obtain, not least because they are often located about 100 m underwater.…”

Section: P I P Pa W H I T E H O U S Ementioning

confidence: 99%

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2018

Nature

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Fruitless and Doublesex Coordinate to Generate Male-Specific Neurons that Can Initiate Courtship

Cited by 288 publications

References 46 publications

fruitless alternative splicing and sex behaviour in insects: an ancient and unforgettable love story?

fruitless alternative splicing and sex behaviour in insects: an ancient and unforgettable love story?

Engineered Alterations in RNA Editing Modulate Complex Behavior in Drosophila

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