Nutrient status alters developmental fates via a switch in mitochondrial homeodynamics
Abstract Steroid hormones are powerful endocrine regulators, but little is known about how environmental conditions modulate steroidogenesis to reprogram developmental fates. Here, we use the Drosophila prothoracic gland (PG) to investigate how a nutrient restriction checkpoint (NRC) ensures or bloc...
Saved in:
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2025-02-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-56528-z |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1832571524788256768 |
|---|---|
| author | Jie Zhang Suning Liu Yang Li Guanfeng Xu Huimin Deng Kirst King-Jones Sheng Li |
| author_facet | Jie Zhang Suning Liu Yang Li Guanfeng Xu Huimin Deng Kirst King-Jones Sheng Li |
| author_sort | Jie Zhang |
| collection | DOAJ |
| description | Abstract Steroid hormones are powerful endocrine regulators, but little is known about how environmental conditions modulate steroidogenesis to reprogram developmental fates. Here, we use the Drosophila prothoracic gland (PG) to investigate how a nutrient restriction checkpoint (NRC) ensures or blocks developmental progression and sexual maturation via regulating steroidogenesis. Extensive transcriptome analysis of the PG reveals that pre-NRC starvation significantly downregulates mitochondria-associated genes. Pre-NRC starvation reduces prothoracicotropic neuropeptide hormone signaling, insulin signaling, and TORC1 activity in PG cells, which prevent mitochondrial fragmentation and import of Disembodied, a key steroidogenic enzyme. Ultimately, pre-NRC starvation causes severe mitophagy and proteasome dysfunction, blocking steroidogenesis and metamorphosis. By contrast, post-NRC starvation does not impair mitochondrial homeostasis in PG cells but reduces sit expression and induces moderate autophagy to promote steroidogenesis, leading to precocious metamorphosis. This study constitutes a paradigm for exploring how steroid hormone levels are controlled in response to environmental stress during developmental checkpoints. |
| format | Article |
| id | doaj-art-7c2d481d53084a88b94fdeb1f83f57e8 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-7c2d481d53084a88b94fdeb1f83f57e82025-02-02T12:32:27ZengNature PortfolioNature Communications2041-17232025-02-0116111610.1038/s41467-025-56528-zNutrient status alters developmental fates via a switch in mitochondrial homeodynamicsJie Zhang0Suning Liu1Yang Li2Guanfeng Xu3Huimin Deng4Kirst King-Jones5Sheng Li6Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityDepartment of Biological Sciences, University of AlbertaGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology & School of Life Sciences, South China Normal UniversityAbstract Steroid hormones are powerful endocrine regulators, but little is known about how environmental conditions modulate steroidogenesis to reprogram developmental fates. Here, we use the Drosophila prothoracic gland (PG) to investigate how a nutrient restriction checkpoint (NRC) ensures or blocks developmental progression and sexual maturation via regulating steroidogenesis. Extensive transcriptome analysis of the PG reveals that pre-NRC starvation significantly downregulates mitochondria-associated genes. Pre-NRC starvation reduces prothoracicotropic neuropeptide hormone signaling, insulin signaling, and TORC1 activity in PG cells, which prevent mitochondrial fragmentation and import of Disembodied, a key steroidogenic enzyme. Ultimately, pre-NRC starvation causes severe mitophagy and proteasome dysfunction, blocking steroidogenesis and metamorphosis. By contrast, post-NRC starvation does not impair mitochondrial homeostasis in PG cells but reduces sit expression and induces moderate autophagy to promote steroidogenesis, leading to precocious metamorphosis. This study constitutes a paradigm for exploring how steroid hormone levels are controlled in response to environmental stress during developmental checkpoints.https://doi.org/10.1038/s41467-025-56528-z |
| spellingShingle | Jie Zhang Suning Liu Yang Li Guanfeng Xu Huimin Deng Kirst King-Jones Sheng Li Nutrient status alters developmental fates via a switch in mitochondrial homeodynamics Nature Communications |
| title | Nutrient status alters developmental fates via a switch in mitochondrial homeodynamics |
| title_full | Nutrient status alters developmental fates via a switch in mitochondrial homeodynamics |
| title_fullStr | Nutrient status alters developmental fates via a switch in mitochondrial homeodynamics |
| title_full_unstemmed | Nutrient status alters developmental fates via a switch in mitochondrial homeodynamics |
| title_short | Nutrient status alters developmental fates via a switch in mitochondrial homeodynamics |
| title_sort | nutrient status alters developmental fates via a switch in mitochondrial homeodynamics |
| url | https://doi.org/10.1038/s41467-025-56528-z |
| work_keys_str_mv | AT jiezhang nutrientstatusaltersdevelopmentalfatesviaaswitchinmitochondrialhomeodynamics AT suningliu nutrientstatusaltersdevelopmentalfatesviaaswitchinmitochondrialhomeodynamics AT yangli nutrientstatusaltersdevelopmentalfatesviaaswitchinmitochondrialhomeodynamics AT guanfengxu nutrientstatusaltersdevelopmentalfatesviaaswitchinmitochondrialhomeodynamics AT huimindeng nutrientstatusaltersdevelopmentalfatesviaaswitchinmitochondrialhomeodynamics AT kirstkingjones nutrientstatusaltersdevelopmentalfatesviaaswitchinmitochondrialhomeodynamics AT shengli nutrientstatusaltersdevelopmentalfatesviaaswitchinmitochondrialhomeodynamics |