Fruitless isoforms and target genes specify the sexually dimorphic nervous system underlying<i>Drosophila</i>reproductive behavior

Nojima, Tetsuya; Neville, Megan C; Goodwin, Stephen F.

doi:10.4161/fly.29132

Cited by 23 publications

(27 citation statements)

References 45 publications

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“…Although in recent years studies of neural and genetic mechanisms of sexual behavior in fruit flies indicate that Dmdsx M and Dmfru M are the master regulators of many sexually differentiated processes and behaviors [27, 28], how these master genes act to control neural development to build these complex behaviors by regulating downstream genes is still not fully understood [29]. Many studies have shown the fru gene to be conserved functionally with sex-specific splicing expression patterns among Diptera, including Anopheles gambiae , Ceratitis capitata , Aedes aegypti , Nasonia vitripennis , and Musca domestica , and a Blattodea, Blatella germanica [29–35]. However, the genetic regulatory mechanism of sexual behavior remains unclear in lepidopteran insects.…”

Section: Introductionmentioning

confidence: 99%

Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade

Liu

Yang

et al. 2020

Preprint

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25Insect courtship and mating depend on integration of olfactory, visual, and tactile cues. 26 Compared to other insects, Bombyx mori, the domesticated silkworm, has relatively 27 simple sexual behaviors as it cannot fly. Here by using CRISPR/Cas and 28 electrophysiological techniques we found that courtship and mating behaviors are 29 regulated in male silk moths by mutating genes in the sex determination cascade 30 belonging to two conserved pathways. Loss of Bmdsx gene expression significantly 31 reduced the peripheral perception of the major pheromone component bombykol by 32 reducing expression of the product of the BmOR1 gene which completely blocked 33 courtship in adult males. Interestingly, we found that mating behavior was regulated 34 independently by another sexual differentiation gene, Bmfru. Loss of Bmfru completely 35 blocked mating, but males displayed normal courtship behavior. Lack of Bmfru 36 expression significantly reduced the perception of the minor pheromone component 37 bombykal due to the down regulation of BmOR3 expression; further, functional analysis 38 revealed that loss of the product of BmOR3 played a key role in terminating male mating 39 behavior. Our results suggest that Bmdsx and Bmfru are at the base of the two primary 40 pathways that regulate olfactory-based sexual behavior. 41 42 genome editing 43 44 45 46 3 47 Author Summary 48 The fundamental insect sexual behaviors, courtship and mating, result from successful 49 integration of olfactory, vision, tactile and other complex innate behaviors. In the widely 50 used insect model, Drosophila melanogaster, the sex determination cascade genes 51 fruitless and doublesex are involved in the regulation of courtship and mating behaviors; 52 however, little is known about the function of these sexual differentiation genes in 53 regulating sex behaviors of Lepidoptera. Here we combine genetics and 54 electrophysiology to investigate regulation pathway of sexual behaviors in the model 55 lepidopteran insect, the domesticated silk moth, Bombyx mori. Our results support the 56 presence of two genetic pathways in B. mori, named Bmdsx-BmOR1-bombykol and 57 Bmfru-BmOR3-bombykal, which control distinct aspects of male sexual behavior that are 58 modulated by olfaction. This is the first comprehensive report about the role of sex 59 differentiation genes in the male sexual behavior in the silk moth.60 61 62 63 64 65 66 67 68 4 69 Introduction 70 Sex determination pathways control the sexually dimorphic traits of males and females, 71 including sexual differentiation and sexual behavior [1]. The genetic cascades of primary 72 signalling that underlie sex determination in insects have high diversity among species. In 73 the model insect Drosophila melanogaster, sex determination is controlled hierarchically 74 by X:A, Sex-lethal (Sxl), transformer or transformer 2 (tra/tra2), doublesex (dsx), and 75 fruitless (fru) [2, 3]. An X:A ratio of 1 promotes transcription of Sxl and results in 76 feminization, while an X:A ratio of 0.5 results in Sxl ...

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Section: Introductionmentioning

confidence: 99%

Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade

Liu

Yang

et al. 2020

Preprint

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“…For example, female-specific isoforms promote expression of yolk proteins in the fat body of females but not males. Work is underway to identify specific genes regulated by sex-specific isoforms of Fru Nojima et al 2014;Vernes 2014) and Dsx (Clough et al 2014;Luo and Baker 2015). For a review on sex determination in Drosophila, see Salz and Erickson (2010).…”

Section: Sex Determinationmentioning

confidence: 99%

Genetics on the Fly: A Primer on theDrosophilaModel System

et al. 2015

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Fruit flies of the genus Drosophila have been an attractive and effective genetic model organism since Thomas Hunt Morgan and colleagues made seminal discoveries with them a century ago. Work with Drosophila has enabled dramatic advances in cell and developmental biology, neurobiology and behavior, molecular biology, evolutionary and population genetics, and other fields. With more tissue types and observable behaviors than in other short-generation model organisms, and with vast genome data available for many species within the genus, the fly's tractable complexity will continue to enable exciting opportunities to explore mechanisms of complex developmental programs, behaviors, and broader evolutionary questions. This primer describes the organism's natural history, the features of sequenced genomes within the genus, the wide range of available genetic tools and online resources, the types of biological questions Drosophila can help address, and historical milestones.

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“…Interestingly, our data also support the idea that different isoforms of Fru also can have very different functions. In the CNS, Fru A , Fru B , and Fru C have mostly overlapping expression, but play distinct roles: Fru B is required for all steps of courtship behaviors; FruC controls specific steps; and Fru A is dispensable for courtship behaviors [42,43]. In the gonad, we also detected all C-terminal isoforms of fru at the mRNA level ( Figure S3B).…”

Section: Fru Function Outside the Nervous Systemmentioning

confidence: 86%

fruitlessfunctions downstream ofdoublesexto promote sexual dimorphism of the gonad stem cell niche

Zhou

Whitworth

Pozmanter

et al. 2018

Preprint

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Background: doublesex (dsx) and fruitless (fru) are the two downstream transcription factors that actuate Drosophila sex determination. While dsx assists fru to regulate sexspecific behavior, whether fru collaborates with dsx in regulating other aspects of sexual dimorphism remains unknown. One important aspect of sexual dimorphism is found in the gonad stem cell (GSC) niches, where male and female GSCs are regulated to create large numbers of sperm and eggs. Results: Here we report that Fru is expressed male-specifically in the GSC niche and plays important roles in the development and maintenance of these cells. Unlike previously studied regulation of sex-specific Fru expression, which is regulated by alternative splicing by Transformer (Tra), we show that male-specific expression of fru is regulated downstream of dsx, and is independent of Tra. Regulation of fru by dsx also occurs in the nervous system. fru genetically interacts with dsx to support maintenance of the hub throughout development. Ectopic expression of fru inhibited female niche formation and partially masculinized the ovary. fru is also required autonomously for cyst stem cell maintenance and cyst cell survival. Finally, we identified a conserved Dsx binding site upstream of fru promoter P4 that regulates fru expression in the hub, indicating that fru is likely a direct target for transcriptional regulation by Dsx. Conclusions: These findings demonstrate that fru acts outside the nervous system to influence sexual dimorphism and reveal a new mechanism for regulating sex-specific expression of fru that is regulated at the transcriptional level by Dsx, rather than by alternative splicing by Tra.Summary word count: 254 words Main text: 6127 words including citation

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Fruitless isoforms and target genes specify the sexually dimorphic nervous system underlyingDrosophilareproductive behavior

Cited by 23 publications

References 45 publications

Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade

Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade

Genetics on the Fly: A Primer on theDrosophilaModel System

fruitlessfunctions downstream ofdoublesexto promote sexual dimorphism of the gonad stem cell niche

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