Bmovo-1 Regulates Ovary Size in the Silkworm, Bombyx mori

Xue, Renyu; Hu, Xiaolong; Cao, Guangwen; Huang, Moli; Xue, Gaoxu; Qian, Ying; Song, Zuowei; Gong, Chengliang

doi:10.1371/journal.pone.0104928

Cited by 20 publications

(29 citation statements)

References 26 publications

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“…To get more insight into the gene expression profile in the gonads of Masc-R /+, Bmdsx MΔ7 / MΔ7 females, we performed qRT-PCR to quantify expression levels of Bmovo-1 and Bm-nosO , both of which are important for oogenesis in the silkworm [ 24 , 25 ]. While Masc-R expression in females suppressed the expression of these two genes (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Transgenic and knockout analyses of Masculinizer and doublesex illuminated the unique functions of doublesex in germ cell sexual development of the silkworm, Bombyx mori

et al. 2020

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Background Masculinizer (Masc) plays a pivotal role in male sex determination in the silkworm, Bombyx mori. Masc is required for male-specific splicing of B. mori doublesex (Bmdsx) transcripts. The male isoform of Bmdsx (BmdsxM) induces male differentiation in somatic cells, while females express the female isoform of Bmdsx (BmdsxF), which promotes female differentiation in somatic cells. Our previous findings suggest that Masc could direct the differentiation of genetically female (ZW) germ cells into sperms. However, it remains unclear whether Masc directly induces spermatogenesis or if it promotes male differentiation in germ cells indirectly by inducing the expression of BmdsxM. Results In this study, we performed genetic analyses using the transgenic line that expressed Masc, as well as various Bmdsx knockout lines. We found that Masc-expressing females with a homozygous mutation in BmdsxM showed normal development in ovaries. The formation of testis-like tissues was abolished in these females. On the other hand, Masc-expressing females carrying a homozygous mutation in BmdsxF exhibited almost complete male-specific development in gonads and germ cells. These results suggest that BmdsxM has an ability to induce male development in germ cells as well as internal genital organs, while BmdsxF inhibits BmdsxM activity and represses male differentiation. To investigate whether MASC directly controls male-specific splicing of Bmdsx and identify RNAs that form complexes with MASC in testes, we performed RNA immunoprecipitation (RIP) using an anti-MASC antibody. We found that MASC formed a complex with AS1 lncRNA, which is a testis-specific factor involved in the male-specific splicing of Bmdsx pre-mRNA. Conclusions Taken together, our findings suggest that Masc induces male differentiation in germ cells by enhancing the production of BmdsxM. Physical interaction between MASC and AS1 lncRNA may be important for the BmdsxM expression in the testis. Unlike in the Drosophila dsx, BmdsxM was able to induce spermatogenesis in genetically female (ZW) germ cells. To the best of our knowledge, this is the first report that the role of dsx in germ cell sexual development is different between insect species.

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Section: Resultsmentioning

confidence: 99%

“…Bmovo-1 protein is primarily found in the nuclei of ovarian cells and has been implicated in oogenesis. Bmovo-1 knockdown resulted in degenerated ovaries and markedly fewer oocytes [ 24 ]. Bm-nosO is required for the arrangement of eggs in the ovariole and normal morphogenesis of eggs [ 25 ].…”

Section: Discussionmentioning

confidence: 99%

Transgenic and knockout analyses of Masculinizer and doublesex illuminated the unique functions of doublesex in germ cell sexual development of the silkworm, Bombyx mori

et al. 2020

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“…Bmovo-1 protein is primarily found in the nuclei of ovarian cells and has been implicated in oogenesis. Bmovo-1 knockdown resulted in degenerated ovaries and markedly fewer oocytes [24]. Bm-nosO is required for the arrangement of eggs in the ovariole and normal morphogenesis of eggs [25].…”

Section: Discussionmentioning

confidence: 99%

“…To get more insight into the gene expression pro le in the gonads of Masc-R/+, Bmdsx MD7/ MD7 females, we performed qRT-PCR to quantify expression levels of Bmovo-1 and Bm-nosO, both of which are important for oogenesis in the silkworm [24,25]. While Masc-R expression in females suppressed the expression of these two genes (Fig.…”

Section: Bmdsxm Knockout In Masc-r Females Induces the Expression Of mentioning

confidence: 99%

Transgenic and knockout analyses of Masculinizer and doublesex illuminated the unique functions of doublesex in germ cell sexual development of the silkworm, Bombyx mori

Yuzawa¹,

Matsuoka

Sumitani

et al. 2020

Preprint

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Background: Masculinizer (Masc) plays a pivotal role in male sex determination in the silkworm, Bombyx mori. Masc is required for male-specific splicing of B. mori doublesex (Bmdsx) transcripts. The male isoform of Bmdsx (BmdsxM) induces male differentiation in somatic cells, while females express the female isoform of Bmdsx (BmdsxF), which promotes female differentiation in somatic cells. Our previous findings suggest that Masc could direct the differentiation of genetically female (ZW) germ cells into sperms. However, it remains unclear whether Masc directly induces spermatogenesis of if it promotes male differentiation in germ cells indirectly by inducing the expression of BmdsxM. Results: In this study, we performed genetic analyses using a transgenic line that expressed Masc, as well as various Bmdsx knockout lines. Masc-expressing females express both BmdsxF and BmdsxM and have degenerated ovaries combined with testis-like tissues, which produce sperm. We found that Masc-expressing females with a homozygous mutation in BmdsxM showed normal development in ovaries. The formation of testis-like tissues was abolished in these females. In comparison, Masc-expressing females carrying a homozygous mutation in BmdsxF exhibited almost complete male-specific development in gonads and germ cells. These results suggest that BmdsxM can induce male development in germ cells and internal genital organs, while BmdsxF inhibits BmdsxM activity and represses male differentiation. To investigate whether MASC directly controls male-specific splicing of Bmdsx and identify RNAs that form complexes with MASC in testes, we performed RNA immunoprecipitation (RIP) using an anti-MASC antibody. We found that MASC formed a complex with AS1 lncRNA , which is a testis-specific factor involved in the male-specific splicing of Bmdsx pre-mRNA . Conclusions: Taken together, our findings suggest that Masc induces male differentiation in gonads and germ cells by enhancing the production of BmdsxM. Physical interaction between MASC and AS1 lncRNA may be important for the BmdsxM expression in the testis. Unlike Drosophila dsx, BmdsxM was able to induce spermatogenesis in genetically female (ZW) germ cells. To the best of our knowledge, this is the first report that the role of dsx in germ cell sexual development is different between insect species.

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“…Many genes related to growth, development, metamorphosis, immunologic response and fibroin synthesis have been well studied. Control of organ size is very important in sericulture; the ability to regulate the size of the silk gland and ovary could improve the silk yield and oviposition number, respectively [ 14 , 15 ]. Hippo signalling represents a cell proliferation and organ-size control pathway; however, little is known about the genes related to the Hippo pathway.…”

Section: Introductionmentioning

confidence: 99%

Cultured cells and wing disc size of silkworm can be controlled by the Hippo pathway

Liang

Qian

et al. 2018

Open Biol.

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Hippo signalling represents a cell proliferation and organ-size control pathway. Yorki (Yki), a component of the Hippo pathway, induces the transcription of a number of targets that promote cell proliferation and survival. The functions of Yki have been characterized in Drosophila and mammals, while there are few reports on silkworm, Bombyx mori. In the present study, we found that BmYki3 facilitates cell migration and cell division, and enlarges the cultured cell and wing disc size. Co-immunoprecipitation results indicated that BmYki3 may interact with thymosin, E3 ubiquitin-protein ligase, protein kinase ASK1, dedicator of cytokinesis protein 1, calcium-independent phospholipase A2 and beta-spectrin. RNA-seq results indicated that 4444 genes were upregulated and 10 291 genes were downregulated after BmYki3 was overexpressed in the cultured cells. GO annotation indicated that the up/downregulated genes were enriched in 268/382 GO terms (p < 0.01); KEGG analysis showed that the up/downregulated genes were enriched in 49/101 pathways. These findings provided novel information to understand the functions of BmYki3 in a cell proliferation and organ-size control pathway.

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Bmovo-1 Regulates Ovary Size in the Silkworm, Bombyx mori

Cited by 20 publications

References 26 publications

Transgenic and knockout analyses of Masculinizer and doublesex illuminated the unique functions of doublesex in germ cell sexual development of the silkworm, Bombyx mori

Transgenic and knockout analyses of Masculinizer and doublesex illuminated the unique functions of doublesex in germ cell sexual development of the silkworm, Bombyx mori

Transgenic and knockout analyses of Masculinizer and doublesex illuminated the unique functions of doublesex in germ cell sexual development of the silkworm, Bombyx mori

Cultured cells and wing disc size of silkworm can be controlled by the Hippo pathway

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