Transcriptomic Evidence for Cell-Autonomous Sex Differentiation of the Gynandromorphic Fat Body in the Silkworm, <i>Bombyx mori</i>

The classic model of sex determination in insects suggests that they do not have sex hormones and that sex is determined in a cell-autonomous manner. On the other hand, there is accumulating evidence that the development of secondary sexual traits is controlled in a non-cell-autonomous manner throug...

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Main Authors: Fumiko Yamamoto, Takeshi Yokoyama, Yan Su, Masataka G. Suzuki
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Journal of Developmental Biology
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Online Access:https://www.mdpi.com/2221-3759/12/4/31
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author Fumiko Yamamoto
Takeshi Yokoyama
Yan Su
Masataka G. Suzuki
author_facet Fumiko Yamamoto
Takeshi Yokoyama
Yan Su
Masataka G. Suzuki
author_sort Fumiko Yamamoto
collection DOAJ
description The classic model of sex determination in insects suggests that they do not have sex hormones and that sex is determined in a cell-autonomous manner. On the other hand, there is accumulating evidence that the development of secondary sexual traits is controlled in a non-cell-autonomous manner through external factors. To evaluate the degrees of the cell-autonomous and non-cell-autonomous regulation of secondary sexual trait development, we analyzed the dynamics of the sexually dimorphic transcriptome in gynandromorphic individuals of the <i>mo</i> mutant strain in the silkworm <i>Bombyx mori</i>. The silkworm possesses a female heterogametic sex-determination system (ZZ = male/ZW = female), where the master regulatory gene for femaleness, <i>Feminizer</i> (<i>Fem</i>), is located in the W chromosome. As a secondary sexual trait, we focused on the fat body, which shows remarkable differences between the sexes during the last instar larval stage. A comparison of the transcriptomes between the fat bodies of male and female larvae identified 232 sex-differentially expressed genes (S-DEGs). The proportions of ZZ and ZW cells constituting the fat body of the gynandromorphic larvae were calculated according to the expression level of the <i>Fem</i>. Based on the obtained values, the expression level of each S-DEG was estimated, assuming that the levels of S-DEG expression were determined according to the proportion of ZZ and ZW cells. The estimated expression levels of 207 out of 232 S-DEGs were strongly correlated with the corresponding S-DEG expression level of the gynandromorphic fat body, determined by RNA-seq. These results strongly suggest that most of the sexually dimorphic transcriptome in the fat body is regulated in a cell-autonomous manner.
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spelling doaj-art-ce323d2ab34f4e83ad437fa1fbb62a2e2025-08-20T02:53:34ZengMDPI AGJournal of Developmental Biology2221-37592024-11-011243110.3390/jdb12040031Transcriptomic Evidence for Cell-Autonomous Sex Differentiation of the Gynandromorphic Fat Body in the Silkworm, <i>Bombyx mori</i>Fumiko Yamamoto0Takeshi Yokoyama1Yan Su2Masataka G. Suzuki3Anicom Pafe, Inc., Sumitomo Fudosan, 8-17-1, Shinjyuku, Shinjyuku-ku 160-0023, Tokyo, JapanDepartment of Biological Production, Faculty of Agriculture, Tokyo University of Agriculture and Technology, 3-8-1, Harumi-cho, Fuchu 183-8538, Tokyo, JapanDepartment of Physiology, Graduate School of Medicine, Juntendo University, 2-1-1 Hongo, Bunkyo-ku 113-8421, Tokyo, JapanDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa 277-8562, Chiba, JapanThe classic model of sex determination in insects suggests that they do not have sex hormones and that sex is determined in a cell-autonomous manner. On the other hand, there is accumulating evidence that the development of secondary sexual traits is controlled in a non-cell-autonomous manner through external factors. To evaluate the degrees of the cell-autonomous and non-cell-autonomous regulation of secondary sexual trait development, we analyzed the dynamics of the sexually dimorphic transcriptome in gynandromorphic individuals of the <i>mo</i> mutant strain in the silkworm <i>Bombyx mori</i>. The silkworm possesses a female heterogametic sex-determination system (ZZ = male/ZW = female), where the master regulatory gene for femaleness, <i>Feminizer</i> (<i>Fem</i>), is located in the W chromosome. As a secondary sexual trait, we focused on the fat body, which shows remarkable differences between the sexes during the last instar larval stage. A comparison of the transcriptomes between the fat bodies of male and female larvae identified 232 sex-differentially expressed genes (S-DEGs). The proportions of ZZ and ZW cells constituting the fat body of the gynandromorphic larvae were calculated according to the expression level of the <i>Fem</i>. Based on the obtained values, the expression level of each S-DEG was estimated, assuming that the levels of S-DEG expression were determined according to the proportion of ZZ and ZW cells. The estimated expression levels of 207 out of 232 S-DEGs were strongly correlated with the corresponding S-DEG expression level of the gynandromorphic fat body, determined by RNA-seq. These results strongly suggest that most of the sexually dimorphic transcriptome in the fat body is regulated in a cell-autonomous manner.https://www.mdpi.com/2221-3759/12/4/31sex determinationcell-autonomous regulationsecondary sexual traits<i>Feminizer</i>fat body
spellingShingle Fumiko Yamamoto
Takeshi Yokoyama
Yan Su
Masataka G. Suzuki
Transcriptomic Evidence for Cell-Autonomous Sex Differentiation of the Gynandromorphic Fat Body in the Silkworm, <i>Bombyx mori</i>
Journal of Developmental Biology
sex determination
cell-autonomous regulation
secondary sexual traits
<i>Feminizer</i>
fat body
title Transcriptomic Evidence for Cell-Autonomous Sex Differentiation of the Gynandromorphic Fat Body in the Silkworm, <i>Bombyx mori</i>
title_full Transcriptomic Evidence for Cell-Autonomous Sex Differentiation of the Gynandromorphic Fat Body in the Silkworm, <i>Bombyx mori</i>
title_fullStr Transcriptomic Evidence for Cell-Autonomous Sex Differentiation of the Gynandromorphic Fat Body in the Silkworm, <i>Bombyx mori</i>
title_full_unstemmed Transcriptomic Evidence for Cell-Autonomous Sex Differentiation of the Gynandromorphic Fat Body in the Silkworm, <i>Bombyx mori</i>
title_short Transcriptomic Evidence for Cell-Autonomous Sex Differentiation of the Gynandromorphic Fat Body in the Silkworm, <i>Bombyx mori</i>
title_sort transcriptomic evidence for cell autonomous sex differentiation of the gynandromorphic fat body in the silkworm i bombyx mori i
topic sex determination
cell-autonomous regulation
secondary sexual traits
<i>Feminizer</i>
fat body
url https://www.mdpi.com/2221-3759/12/4/31
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