Vitellogenin receptor mediates heat adaptability of oocyte development in mud crabs and zebrafish
Abstract Climate-driven warming affects the reproduction of oviparous ectotherms. However, whether oviparous ectotherms possess a protection mechanism against heat stress for oocyte development, which is essential for maintaining the continuity of animal populations, is largely unknown. Under high t...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2025-04-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-59035-3 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850181113923764224 |
|---|---|
| author | Long Zhang Kun Wu Haoyang Li Minwen Zhan Sheng Wang Enhui Song Qi Zhang Jian He Xinyi He Menghuang Xu Hengwei Deng Yingchun Su Ziwei Liu Zhuyue Yan Peipei Tan Mengyun He Shaoping Weng Wei Ge Jianguo He Muhua Wang |
| author_facet | Long Zhang Kun Wu Haoyang Li Minwen Zhan Sheng Wang Enhui Song Qi Zhang Jian He Xinyi He Menghuang Xu Hengwei Deng Yingchun Su Ziwei Liu Zhuyue Yan Peipei Tan Mengyun He Shaoping Weng Wei Ge Jianguo He Muhua Wang |
| author_sort | Long Zhang |
| collection | DOAJ |
| description | Abstract Climate-driven warming affects the reproduction of oviparous ectotherms. However, whether oviparous ectotherms possess a protection mechanism against heat stress for oocyte development, which is essential for maintaining the continuity of animal populations, is largely unknown. Under high temperatures, female mud crabs (Scylla paramamosain) typically have well-formed ovaries, while a few crabs were found to experience oocyte development failure. To investigate the heat stress protection mechanism of oocyte development in mud crabs, we construct a chromosome-level genome of this species and identify an enhancer of the vitellogenin receptor (VtgR) that stimulates its expression under high temperatures. Lacking this enhancer due to an intronic deletion leads to low VtgR expression in abnormal crabs, resulting in abnormal vitellogenic oocyte formation in these individuals when exposed to high temperatures. Furthermore, we identify a similar heat stress protection mechanism in zebrafish. Disruption of Lrp13, a VtgR-like protein in zebrafish, results in impaired vitellogenin absorption and ovarian degeneration in zebrafish exposed to high temperatures. Our results reveal a VtgR-mediated mechanism that protects vitellogenic oocyte formation against heat stress in mud crabs and zebrafish, contributing to their heat adaptability during oocyte development. |
| format | Article |
| id | doaj-art-2c9bcabc2fbb45759662d18dc1002ac1 |
| institution | OA Journals |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-04-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-2c9bcabc2fbb45759662d18dc1002ac12025-08-20T02:17:58ZengNature PortfolioNature Communications2041-17232025-04-0116111710.1038/s41467-025-59035-3Vitellogenin receptor mediates heat adaptability of oocyte development in mud crabs and zebrafishLong Zhang0Kun Wu1Haoyang Li2Minwen Zhan3Sheng Wang4Enhui Song5Qi Zhang6Jian He7Xinyi He8Menghuang Xu9Hengwei Deng10Yingchun Su11Ziwei Liu12Zhuyue Yan13Peipei Tan14Mengyun He15Shaoping Weng16Wei Ge17Jianguo He18Muhua Wang19School of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversitySchool of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversitySchool of Life Sciences, China-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangdong Provincial Key Laboratory of Aquatic Economic Animals, Sun Yat-sen UniversitySchool of Life Sciences, China-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangdong Provincial Key Laboratory of Aquatic Economic Animals, Sun Yat-sen UniversitySchool of Life Sciences, China-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangdong Provincial Key Laboratory of Aquatic Economic Animals, Sun Yat-sen UniversitySchool of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversitySchool of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversitySchool of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversitySchool of Life Sciences, China-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangdong Provincial Key Laboratory of Aquatic Economic Animals, Sun Yat-sen UniversitySchool of Life Sciences, China-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangdong Provincial Key Laboratory of Aquatic Economic Animals, Sun Yat-sen UniversitySchool of Life Sciences, China-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangdong Provincial Key Laboratory of Aquatic Economic Animals, Sun Yat-sen UniversitySchool of Life Sciences, China-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangdong Provincial Key Laboratory of Aquatic Economic Animals, Sun Yat-sen UniversitySchool of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversitySchool of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversitySchool of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversitySchool of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversitySchool of Life Sciences, China-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangdong Provincial Key Laboratory of Aquatic Economic Animals, Sun Yat-sen UniversityDepartment of Biomedical Sciences and Centre of Reproduction, Development and Aging (CRDA), Faculty of Health Sciences, University of MacauSchool of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversitySchool of Marine Sciences, State Key Laboratory for Biocontrol, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen UniversityAbstract Climate-driven warming affects the reproduction of oviparous ectotherms. However, whether oviparous ectotherms possess a protection mechanism against heat stress for oocyte development, which is essential for maintaining the continuity of animal populations, is largely unknown. Under high temperatures, female mud crabs (Scylla paramamosain) typically have well-formed ovaries, while a few crabs were found to experience oocyte development failure. To investigate the heat stress protection mechanism of oocyte development in mud crabs, we construct a chromosome-level genome of this species and identify an enhancer of the vitellogenin receptor (VtgR) that stimulates its expression under high temperatures. Lacking this enhancer due to an intronic deletion leads to low VtgR expression in abnormal crabs, resulting in abnormal vitellogenic oocyte formation in these individuals when exposed to high temperatures. Furthermore, we identify a similar heat stress protection mechanism in zebrafish. Disruption of Lrp13, a VtgR-like protein in zebrafish, results in impaired vitellogenin absorption and ovarian degeneration in zebrafish exposed to high temperatures. Our results reveal a VtgR-mediated mechanism that protects vitellogenic oocyte formation against heat stress in mud crabs and zebrafish, contributing to their heat adaptability during oocyte development.https://doi.org/10.1038/s41467-025-59035-3 |
| spellingShingle | Long Zhang Kun Wu Haoyang Li Minwen Zhan Sheng Wang Enhui Song Qi Zhang Jian He Xinyi He Menghuang Xu Hengwei Deng Yingchun Su Ziwei Liu Zhuyue Yan Peipei Tan Mengyun He Shaoping Weng Wei Ge Jianguo He Muhua Wang Vitellogenin receptor mediates heat adaptability of oocyte development in mud crabs and zebrafish Nature Communications |
| title | Vitellogenin receptor mediates heat adaptability of oocyte development in mud crabs and zebrafish |
| title_full | Vitellogenin receptor mediates heat adaptability of oocyte development in mud crabs and zebrafish |
| title_fullStr | Vitellogenin receptor mediates heat adaptability of oocyte development in mud crabs and zebrafish |
| title_full_unstemmed | Vitellogenin receptor mediates heat adaptability of oocyte development in mud crabs and zebrafish |
| title_short | Vitellogenin receptor mediates heat adaptability of oocyte development in mud crabs and zebrafish |
| title_sort | vitellogenin receptor mediates heat adaptability of oocyte development in mud crabs and zebrafish |
| url | https://doi.org/10.1038/s41467-025-59035-3 |
| work_keys_str_mv | AT longzhang vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT kunwu vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT haoyangli vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT minwenzhan vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT shengwang vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT enhuisong vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT qizhang vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT jianhe vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT xinyihe vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT menghuangxu vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT hengweideng vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT yingchunsu vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT ziweiliu vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT zhuyueyan vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT peipeitan vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT mengyunhe vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT shaopingweng vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT weige vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT jianguohe vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish AT muhuawang vitellogeninreceptormediatesheatadaptabilityofoocytedevelopmentinmudcrabsandzebrafish |