Role of the male BmDSX protein in the sexual differentiation of <i>Bombyx mori</i>

Suzuki, Masataka; Funaguma, Shunsuke; Kanda, Toshio; Tamura, Toshiki; Shimada, Toru

doi:10.1111/j.1525-142x.2005.05007.x

Cited by 106 publications

(103 citation statements)

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“…Sexually mosaic individuals have been observed in a wide variety of butterflies and moths (27). In B. mori, a homolog of doublesex, a sex-related gene of D. melanogaster located downstream of the sex determination cascade, is certainly transcribed in a sex-specific manner (36,46). Hence, although the mechanism is unknown, lepidopteran sex determination is probably completed very early in embryogenesis, as in many other insects and animals (7,52).…”

Section: Vol 73 2007 Wolbachia-induced Feminization In a Butterfly mentioning

confidence: 99%

Unexpected Mechanism of Symbiont-Induced Reversal of Insect Sex: Feminizing Wolbachia Continuously Acts on the Butterfly Eurema hecabe during Larval Development

Narita

Kageyama

Nomura

et al. 2007

Appl Environ Microbiol

127

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When the butterfly Eurema hecabe is infected with two different strains (wHecCI2 and wHecFem2) of the bacterial endosymbiont Wolbachia, genetic males are transformed into functional females, resulting in production of all-female broods. In an attempt to understand how and when the Wolbachia endosymbiont feminizes genetically male insects, larval insects were fed an antibiotic-containing diet beginning at different developmental stages until pupation. When the adult insects emerged, strikingly, many of them exhibited sexually intermediate traits in their wings, reproductive organs, and genitalia. The expression of intersexual phenotypes was strong in the insects treated from first instar, moderate in the insects treated from third instar, and weak in the insects treated from fourth instar. The insects treated from early larval instar grew and pupated normally but frequently failed to emerge and died in the pupal case. The dead insects in the pupal case contained lower densities of the feminizing Wolbachia endosymbiont than the successfully emerged insects, although none of them were completely cured of the symbiont infection. These results suggest the following: (i) the antibiotic treatment suppressed the population of feminizing Wolbachia endosymbionts; (ii) the suppression probably resulted in attenuated feminizing activity of the symbiont, leading to expression of intersexual host traits; (iii) many of the insects suffered pupal mortality, possibly due to either intersexual defects or Wolbachia-mediated addiction; and hence (iv) the feminizing Wolbachia endosymbiont continuously acts on the host insects during larval development for expression of female phenotypes under a male genotype. Our finding may prompt reconsideration of the notion that Wolbachia-induced reproductive manipulations are already complete before the early embryonic stage and provide insights into the mechanism underlying the symbiontinduced reversal of insect sex.

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Section: Vol 73 2007 Wolbachia-induced Feminization In a Butterfly mentioning

confidence: 99%

Unexpected Mechanism of Symbiont-Induced Reversal of Insect Sex: Feminizing Wolbachia Continuously Acts on the Butterfly Eurema hecabe during Larval Development

Narita

Kageyama

Nomura

et al. 2007

Appl Environ Microbiol

127

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“…Also a tra homolog has not been found in the Bombyx genome (Mita et al, 2009). Despite these differences, a B. mori dsx homolog (Bmdsx) has been implicated in sex determination (Suzuki et al, 2005). Bmdsx produces alternatively spliced mRNA isoforms that encode sex specific transcription factors as observed in dsx (Suzuki et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

Effect of RNAi-mediated knockdown of the Bombyx mori transformer-2 gene on the sex-specific splicing of Bmdsx pre-mRNA

Suzuki¹,

Suzuki²,

Aoki³

et al. 2012

Int. J. Dev. Biol.

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In Drosophila melanogaster, transformer-2 (tra-2) is essential for female differentiation and is known to induce female-specific splicing of doublesex (dsx). The function of Bmtra-2, the Bombyx mori homolog of tra-2, on the other hand remains to be elucidated. As an initial step to learn about the biological function of Bmtra-2, we determined whether Bmtra-2 is capable of inducing the female-specific splicing of Drosophila dsx. RNAi-mediated knockdown of Bmtra-2 using Bombyx cultured cells transiently transfected with a dsx minigene revealed that Bmtra-2 can induce female-specific splicing of Drosophila dsx. To examine the role Bmtra-2 plays in regulating sex-specific splicing of Bmdsx pre-mRNA, we used an RNAi approach to reduce BmTra-2 expression in the early embryo. Embryos injected with dsRNAs or siRNAs targeted to Bmtra-2 showed no variation in the sex-specific splicing pattern of Bmdsx pre-mRNA. RNAi knockdown of Bmtra-2 in the early embryo caused abnormal testis formation. Taken together, these results indicate that Bmtra-2 is required for normal testis development, but is not involved in regulating the sex-specific splicing of Bmdsx pre-mRNA, even though it is capable of inducing the female-specific splicing of Drosophila dsx.

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“…Like dsx, the primary transcript of the Bmdsx gene is alternatively spliced in males and females to yield sex-specific mRNAs that encode male-specific (BmDSXM) and femalespecific (BmDSXF) polypeptides (36,42). Transgenic analysis of Bmdsx revealed that Bmdsx functions as a double-switch gene at the final step in the B. mori sex determination cascade (43,44). Despite these similarities between dsx and Bmdsx, the underlying mechanism for sex-specific splicing is clearly different.…”

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Establishment of a Novel In Vivo Sex-Specific Splicing Assay System To Identify a trans-Acting Factor That Negatively Regulates Splicing of Bombyx mori dsx Female Exons

Suzuki

Imanishi

Dohmae

et al. 2008

Molecular and Cellular Biology

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101

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The Bombyx mori homolog of doublesex, Bmdsx, plays an essential role in silkworm sexual development. Exons 3 and 4 of Bmdsx pre-mRNA are specifically excluded in males. To explore how this occurs, we developed a novel in vivo sex-specific splicing assay system using sexually differentiated cultured cells. A series of mutation analyses using a Bmdsx minigene with this in vivo splicing assay system identified three distinct sequences (CE1, CE2, and CE3) positioned in exon 4 as exonic splicing silencers responsible for male-specific splicing. Gel shift analysis showed that CE1 binds to a nuclear protein from male cells but not that from female cells. Mutation of UAA repeats within CE1 inhibited the binding of the nuclear protein to the RNA and caused female-specific splicing in male cells. We have identified BmPSI, a Bombyx homolog of P-element somatic inhibitor (PSI), as the nuclear factor that specifically binds CE1. Down-regulation of endogenous BmPSI by RNA interference significantly increased female-specific splicing in male cells. This is the first report of a PSI homolog implicated in the regulated sex-specific splicing of dsx pre-mRNA.Sexual reproduction is the primary means to maintain variation for evolutionary survival. Sex determination cascades that drive the differentiation of dimorphic gonads, however, are some of the most rapidly evolved developmental events (28). Genetic and environmental cues direct the generation of two distinct sexual phenotypes via several key molecular signals. In Drosophila melanogaster and Caenorhabditis elegans, the ratio of X chromosomes to autosomes (X/A) is the primary signal for sex determination (19,23). In mammals, however, maleness is determined by the Y-linked gene SRY (17,41). Nevertheless, recent studies indicate some downstream sex determination genes are functionally similar in diverse species. Of these, DM domain (Doublesex/Mab-3 DNA-binding motif) genes have been shown in the past several years to regulate sexual development in multiple metazoan phyla, including arthropods, nematodes, and vertebrates, and thus this gene family may represent the first example of widespread conservation of sexual regulatory genes (20,46). The DM domain is a cysteine-rich DNA-binding motif first recognized in proteins encoded by the Drosophila sex determination gene doublesex (10, 48). As the name doublesex (dsx) suggests, this gene functions in both sexes: the primary transcript of dsx undergoes sex-specific alternative splicing, producing either a male-specific isoform, DSXM, or a female-specific isoform, DSXF (3, 6). Throughout most of the somatic tissues of the fruit fly, DSXM directs male development and DSXF directs female development.The mechanism of sex-specific dsx splicing has been well studied. Female-specific splicing of dsx requires TRA, TRA-2, and an exonic splicing enhancer (ESE) element located within the untranslated region of the fourth exon (29,34,35). Both TRA and TRA-2 contain Arg/Ser-rich (RS) domains, protein interaction domains characteristic of the Ser/Ar...

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Role of the male BmDSX protein in the sexual differentiation of Bombyx mori

Cited by 106 publications

References 50 publications

Unexpected Mechanism of Symbiont-Induced Reversal of Insect Sex: Feminizing Wolbachia Continuously Acts on the Butterfly Eurema hecabe during Larval Development

Unexpected Mechanism of Symbiont-Induced Reversal of Insect Sex: Feminizing Wolbachia Continuously Acts on the Butterfly Eurema hecabe during Larval Development

Effect of RNAi-mediated knockdown of the Bombyx mori transformer-2 gene on the sex-specific splicing of Bmdsx pre-mRNA

Establishment of a Novel In Vivo Sex-Specific Splicing Assay System To Identify a trans-Acting Factor That Negatively Regulates Splicing of Bombyx mori dsx Female Exons

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