Doublesex and GATAβ4 synergistically regulate the sex-dimorphic expression of storage protein 1 in Bombyx mori.

Sexually dimorphic traits are widespread in organisms and are crucial for reproduction and behavior. These traits are typically controlled by sex-specific genes. However, their regulatory mechanisms are complex and incompletely understood. In Bombyx mori, a group of sex-differential storage proteins...

Full description

Saved in:
Bibliographic Details
Main Authors: Jiamin Yan, Haonan Dong, Tingting Tian, Chunxia Xiao, Yuanyuan Sun, Jing Gong, Qingyou Xia, Yong Hou
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-07-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1011762
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849715069439442944
author Jiamin Yan
Haonan Dong
Tingting Tian
Chunxia Xiao
Yuanyuan Sun
Jing Gong
Qingyou Xia
Yong Hou
author_facet Jiamin Yan
Haonan Dong
Tingting Tian
Chunxia Xiao
Yuanyuan Sun
Jing Gong
Qingyou Xia
Yong Hou
author_sort Jiamin Yan
collection DOAJ
description Sexually dimorphic traits are widespread in organisms and are crucial for reproduction and behavior. These traits are typically controlled by sex-specific genes. However, their regulatory mechanisms are complex and incompletely understood. In Bombyx mori, a group of sex-differential storage proteins (SPs) exists, with storage protein 1 (SP1) expressed exclusively in females. In this study, we used the CRISPR/Cas9 system to knock out the doublesex gene and found that SP1 expression was sharply upregulated in male doublesex mutants and downregulated in female doublesex mutants, which suggests that doublesex is a key factor in the sex-differential expression of SP1. Then, we revealed that the female-specific doublesex isoform (dsxF) bound to and activated the SP1 promoter more strongly than the male-specific isoform (dsxM). Meanwhile, a transcription factor named GATAβ4 was found to be involved in the regulation by doublesex. Overexpression of GATAβ4 in Bombyx mori larvae affected adult reproductive behavior and dramatically upregulated SP1 expression in males. Furthermore, GATAβ4 interacted with both dsxF and dsxM, promoting nuclear translocation of dsxM, which in turn inhibited GATAβ4 binding to the SP1 promoter. In total, we found that dsxM did not directly repress SP1 expression in males but instead cooperated with other transcription factors to regulate downstream gene expression. These findings provide new insights into the regulation of sex-specific genes and the mechanisms controlling dimorphic traits.
format Article
id doaj-art-abe07cae0f7142659fd8779f1c57b2a4
institution DOAJ
issn 1553-7390
1553-7404
language English
publishDate 2025-07-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Genetics
spelling doaj-art-abe07cae0f7142659fd8779f1c57b2a42025-08-20T03:13:30ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042025-07-01217e101176210.1371/journal.pgen.1011762Doublesex and GATAβ4 synergistically regulate the sex-dimorphic expression of storage protein 1 in Bombyx mori.Jiamin YanHaonan DongTingting TianChunxia XiaoYuanyuan SunJing GongQingyou XiaYong HouSexually dimorphic traits are widespread in organisms and are crucial for reproduction and behavior. These traits are typically controlled by sex-specific genes. However, their regulatory mechanisms are complex and incompletely understood. In Bombyx mori, a group of sex-differential storage proteins (SPs) exists, with storage protein 1 (SP1) expressed exclusively in females. In this study, we used the CRISPR/Cas9 system to knock out the doublesex gene and found that SP1 expression was sharply upregulated in male doublesex mutants and downregulated in female doublesex mutants, which suggests that doublesex is a key factor in the sex-differential expression of SP1. Then, we revealed that the female-specific doublesex isoform (dsxF) bound to and activated the SP1 promoter more strongly than the male-specific isoform (dsxM). Meanwhile, a transcription factor named GATAβ4 was found to be involved in the regulation by doublesex. Overexpression of GATAβ4 in Bombyx mori larvae affected adult reproductive behavior and dramatically upregulated SP1 expression in males. Furthermore, GATAβ4 interacted with both dsxF and dsxM, promoting nuclear translocation of dsxM, which in turn inhibited GATAβ4 binding to the SP1 promoter. In total, we found that dsxM did not directly repress SP1 expression in males but instead cooperated with other transcription factors to regulate downstream gene expression. These findings provide new insights into the regulation of sex-specific genes and the mechanisms controlling dimorphic traits.https://doi.org/10.1371/journal.pgen.1011762
spellingShingle Jiamin Yan
Haonan Dong
Tingting Tian
Chunxia Xiao
Yuanyuan Sun
Jing Gong
Qingyou Xia
Yong Hou
Doublesex and GATAβ4 synergistically regulate the sex-dimorphic expression of storage protein 1 in Bombyx mori.
PLoS Genetics
title Doublesex and GATAβ4 synergistically regulate the sex-dimorphic expression of storage protein 1 in Bombyx mori.
title_full Doublesex and GATAβ4 synergistically regulate the sex-dimorphic expression of storage protein 1 in Bombyx mori.
title_fullStr Doublesex and GATAβ4 synergistically regulate the sex-dimorphic expression of storage protein 1 in Bombyx mori.
title_full_unstemmed Doublesex and GATAβ4 synergistically regulate the sex-dimorphic expression of storage protein 1 in Bombyx mori.
title_short Doublesex and GATAβ4 synergistically regulate the sex-dimorphic expression of storage protein 1 in Bombyx mori.
title_sort doublesex and gataβ4 synergistically regulate the sex dimorphic expression of storage protein 1 in bombyx mori
url https://doi.org/10.1371/journal.pgen.1011762
work_keys_str_mv AT jiaminyan doublesexandgatab4synergisticallyregulatethesexdimorphicexpressionofstorageprotein1inbombyxmori
AT haonandong doublesexandgatab4synergisticallyregulatethesexdimorphicexpressionofstorageprotein1inbombyxmori
AT tingtingtian doublesexandgatab4synergisticallyregulatethesexdimorphicexpressionofstorageprotein1inbombyxmori
AT chunxiaxiao doublesexandgatab4synergisticallyregulatethesexdimorphicexpressionofstorageprotein1inbombyxmori
AT yuanyuansun doublesexandgatab4synergisticallyregulatethesexdimorphicexpressionofstorageprotein1inbombyxmori
AT jinggong doublesexandgatab4synergisticallyregulatethesexdimorphicexpressionofstorageprotein1inbombyxmori
AT qingyouxia doublesexandgatab4synergisticallyregulatethesexdimorphicexpressionofstorageprotein1inbombyxmori
AT yonghou doublesexandgatab4synergisticallyregulatethesexdimorphicexpressionofstorageprotein1inbombyxmori