A noncanonical role of roX RNAs in autosomal epigenetic repression
Abstract Long noncoding RNAs known as roX (RNA on the X) are crucial for male development in Drosophila, as their loss leads to male lethality from the late larval stages. While roX RNAs are recognized for their role in sex-chromosome dosage compensation, ensuring balanced expression of X-linked gen...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2025-01-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-55711-y |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1841559258585366528 |
|---|---|
| author | Jianjian Li Shuyang Xu Zicong Liu Liuyi Yang Zhe Ming Rui Zhang Wenjuan Zhao Huipai Peng Jeffrey J. Quinn Manyin Wu Yushan Geng Yuying Zhang Jiazhi He Minghai Chen Nan Li Ning-Yi Shao Qing Ma |
| author_facet | Jianjian Li Shuyang Xu Zicong Liu Liuyi Yang Zhe Ming Rui Zhang Wenjuan Zhao Huipai Peng Jeffrey J. Quinn Manyin Wu Yushan Geng Yuying Zhang Jiazhi He Minghai Chen Nan Li Ning-Yi Shao Qing Ma |
| author_sort | Jianjian Li |
| collection | DOAJ |
| description | Abstract Long noncoding RNAs known as roX (RNA on the X) are crucial for male development in Drosophila, as their loss leads to male lethality from the late larval stages. While roX RNAs are recognized for their role in sex-chromosome dosage compensation, ensuring balanced expression of X-linked genes in both sexes, their potential influence on autosomal gene regulation remains unexplored. Here, using an integrative multi-omics approach, we show that roX RNAs not only govern the X chromosome but also target genes on autosomes that lack male-specific lethal (MSL) complex occupancy, together with Polycomb repressive complexes (PRCs). We observed that roX RNAs colocalize with MSL proteins on the X chromosome and PRC components on autosomes. Intriguingly, loss of roX function reduces X-chromosomal H4K16ac levels and autosomal H3K27me3 levels. Correspondingly, X-linked genes display reduced expression, whereas many autosomal genes exhibit elevated expression upon roX loss. Our findings propose a dual role for roX RNAs: activators of X-linked genes and repressors of autosomal genes, achieved through interactions with MSL and PRC complexes, respectively. This study uncovers the unconventional epigenetic repressive function of roX RNAs with PRC interaction. |
| format | Article |
| id | doaj-art-fc53f6a9209d4c4ca9a238cdc5189d22 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-fc53f6a9209d4c4ca9a238cdc5189d222025-01-05T12:41:09ZengNature PortfolioNature Communications2041-17232025-01-0116111410.1038/s41467-024-55711-yA noncanonical role of roX RNAs in autosomal epigenetic repressionJianjian Li0Shuyang Xu1Zicong Liu2Liuyi Yang3Zhe Ming4Rui Zhang5Wenjuan Zhao6Huipai Peng7Jeffrey J. Quinn8Manyin Wu9Yushan Geng10Yuying Zhang11Jiazhi He12Minghai Chen13Nan Li14Ning-Yi Shao15Qing Ma16Shenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesCenter for Personal Dynamic Regulomes and Program in Epithelial Biology, Stanford University School of MedicineShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesFaculty of Health Sciences, University of MacauShenzhen Key Laboratory of Synthetic Genomics, Guangdong Provincial Key Laboratory of Synthetic Genomics, Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of SciencesAbstract Long noncoding RNAs known as roX (RNA on the X) are crucial for male development in Drosophila, as their loss leads to male lethality from the late larval stages. While roX RNAs are recognized for their role in sex-chromosome dosage compensation, ensuring balanced expression of X-linked genes in both sexes, their potential influence on autosomal gene regulation remains unexplored. Here, using an integrative multi-omics approach, we show that roX RNAs not only govern the X chromosome but also target genes on autosomes that lack male-specific lethal (MSL) complex occupancy, together with Polycomb repressive complexes (PRCs). We observed that roX RNAs colocalize with MSL proteins on the X chromosome and PRC components on autosomes. Intriguingly, loss of roX function reduces X-chromosomal H4K16ac levels and autosomal H3K27me3 levels. Correspondingly, X-linked genes display reduced expression, whereas many autosomal genes exhibit elevated expression upon roX loss. Our findings propose a dual role for roX RNAs: activators of X-linked genes and repressors of autosomal genes, achieved through interactions with MSL and PRC complexes, respectively. This study uncovers the unconventional epigenetic repressive function of roX RNAs with PRC interaction.https://doi.org/10.1038/s41467-024-55711-y |
| spellingShingle | Jianjian Li Shuyang Xu Zicong Liu Liuyi Yang Zhe Ming Rui Zhang Wenjuan Zhao Huipai Peng Jeffrey J. Quinn Manyin Wu Yushan Geng Yuying Zhang Jiazhi He Minghai Chen Nan Li Ning-Yi Shao Qing Ma A noncanonical role of roX RNAs in autosomal epigenetic repression Nature Communications |
| title | A noncanonical role of roX RNAs in autosomal epigenetic repression |
| title_full | A noncanonical role of roX RNAs in autosomal epigenetic repression |
| title_fullStr | A noncanonical role of roX RNAs in autosomal epigenetic repression |
| title_full_unstemmed | A noncanonical role of roX RNAs in autosomal epigenetic repression |
| title_short | A noncanonical role of roX RNAs in autosomal epigenetic repression |
| title_sort | noncanonical role of rox rnas in autosomal epigenetic repression |
| url | https://doi.org/10.1038/s41467-024-55711-y |
| work_keys_str_mv | AT jianjianli anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT shuyangxu anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT zicongliu anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT liuyiyang anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT zheming anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT ruizhang anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT wenjuanzhao anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT huipaipeng anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT jeffreyjquinn anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT manyinwu anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT yushangeng anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT yuyingzhang anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT jiazhihe anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT minghaichen anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT nanli anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT ningyishao anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT qingma anoncanonicalroleofroxrnasinautosomalepigeneticrepression AT jianjianli noncanonicalroleofroxrnasinautosomalepigeneticrepression AT shuyangxu noncanonicalroleofroxrnasinautosomalepigeneticrepression AT zicongliu noncanonicalroleofroxrnasinautosomalepigeneticrepression AT liuyiyang noncanonicalroleofroxrnasinautosomalepigeneticrepression AT zheming noncanonicalroleofroxrnasinautosomalepigeneticrepression AT ruizhang noncanonicalroleofroxrnasinautosomalepigeneticrepression AT wenjuanzhao noncanonicalroleofroxrnasinautosomalepigeneticrepression AT huipaipeng noncanonicalroleofroxrnasinautosomalepigeneticrepression AT jeffreyjquinn noncanonicalroleofroxrnasinautosomalepigeneticrepression AT manyinwu noncanonicalroleofroxrnasinautosomalepigeneticrepression AT yushangeng noncanonicalroleofroxrnasinautosomalepigeneticrepression AT yuyingzhang noncanonicalroleofroxrnasinautosomalepigeneticrepression AT jiazhihe noncanonicalroleofroxrnasinautosomalepigeneticrepression AT minghaichen noncanonicalroleofroxrnasinautosomalepigeneticrepression AT nanli noncanonicalroleofroxrnasinautosomalepigeneticrepression AT ningyishao noncanonicalroleofroxrnasinautosomalepigeneticrepression AT qingma noncanonicalroleofroxrnasinautosomalepigeneticrepression |