RDC complex executes a dynamic piRNA program during Drosophila spermatogenesis to safeguard male fertility.
piRNAs are small non-coding RNAs that guide the silencing of transposons and other targets in animal gonads. In Drosophila female germline, many piRNA source loci dubbed "piRNA clusters" lack hallmarks of active genes and exploit an alternative path for transcription, which relies on the R...
| Main Authors: | , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2021-09-01
|
| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1009591 |
| _version_ | 1798032610122792960 |
|---|---|
| author | Peiwei Chen Yicheng Luo Alexei A Aravin |
| author_facet | Peiwei Chen Yicheng Luo Alexei A Aravin |
| author_sort | Peiwei Chen |
| collection | DOAJ |
| description | piRNAs are small non-coding RNAs that guide the silencing of transposons and other targets in animal gonads. In Drosophila female germline, many piRNA source loci dubbed "piRNA clusters" lack hallmarks of active genes and exploit an alternative path for transcription, which relies on the Rhino-Deadlock-Cutoff (RDC) complex. RDC was thought to be absent in testis, so it remains to date unknown how piRNA cluster transcription is regulated in the male germline. We found that components of RDC complex are expressed in male germ cells during early spermatogenesis, from germline stem cells (GSCs) to early spermatocytes. RDC is essential for expression of dual-strand piRNA clusters and transposon silencing in testis; however, it is dispensable for expression of Y-linked Suppressor of Stellate piRNAs and therefore Stellate silencing. Despite intact Stellate repression, males lacking RDC exhibited compromised fertility accompanied by germline DNA damage and GSC loss. Thus, piRNA-guided repression is essential for normal spermatogenesis beyond Stellate silencing. While RDC associates with multiple piRNA clusters in GSCs and early spermatogonia, its localization changes in later stages as RDC concentrates on a single X-linked locus, AT-chX. Dynamic RDC localization is paralleled by changes in piRNA cluster expression, indicating that RDC executes a fluid piRNA program during different stages of spermatogenesis. These results disprove the common belief that RDC is dispensable for piRNA biogenesis in testis and uncover the unexpected, sexually dimorphic and dynamic behavior of a core piRNA pathway machinery. |
| first_indexed | 2024-04-11T20:16:45Z |
| format | Article |
| id | doaj.art-2c2e651adb0b49688d2d8e481302d5f6 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-04-11T20:16:45Z |
| publishDate | 2021-09-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-2c2e651adb0b49688d2d8e481302d5f62022-12-22T04:04:57ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-09-01179e100959110.1371/journal.pgen.1009591RDC complex executes a dynamic piRNA program during Drosophila spermatogenesis to safeguard male fertility.Peiwei ChenYicheng LuoAlexei A AravinpiRNAs are small non-coding RNAs that guide the silencing of transposons and other targets in animal gonads. In Drosophila female germline, many piRNA source loci dubbed "piRNA clusters" lack hallmarks of active genes and exploit an alternative path for transcription, which relies on the Rhino-Deadlock-Cutoff (RDC) complex. RDC was thought to be absent in testis, so it remains to date unknown how piRNA cluster transcription is regulated in the male germline. We found that components of RDC complex are expressed in male germ cells during early spermatogenesis, from germline stem cells (GSCs) to early spermatocytes. RDC is essential for expression of dual-strand piRNA clusters and transposon silencing in testis; however, it is dispensable for expression of Y-linked Suppressor of Stellate piRNAs and therefore Stellate silencing. Despite intact Stellate repression, males lacking RDC exhibited compromised fertility accompanied by germline DNA damage and GSC loss. Thus, piRNA-guided repression is essential for normal spermatogenesis beyond Stellate silencing. While RDC associates with multiple piRNA clusters in GSCs and early spermatogonia, its localization changes in later stages as RDC concentrates on a single X-linked locus, AT-chX. Dynamic RDC localization is paralleled by changes in piRNA cluster expression, indicating that RDC executes a fluid piRNA program during different stages of spermatogenesis. These results disprove the common belief that RDC is dispensable for piRNA biogenesis in testis and uncover the unexpected, sexually dimorphic and dynamic behavior of a core piRNA pathway machinery.https://doi.org/10.1371/journal.pgen.1009591 |
| spellingShingle | Peiwei Chen Yicheng Luo Alexei A Aravin RDC complex executes a dynamic piRNA program during Drosophila spermatogenesis to safeguard male fertility. PLoS Genetics |
| title | RDC complex executes a dynamic piRNA program during Drosophila spermatogenesis to safeguard male fertility. |
| title_full | RDC complex executes a dynamic piRNA program during Drosophila spermatogenesis to safeguard male fertility. |
| title_fullStr | RDC complex executes a dynamic piRNA program during Drosophila spermatogenesis to safeguard male fertility. |
| title_full_unstemmed | RDC complex executes a dynamic piRNA program during Drosophila spermatogenesis to safeguard male fertility. |
| title_short | RDC complex executes a dynamic piRNA program during Drosophila spermatogenesis to safeguard male fertility. |
| title_sort | rdc complex executes a dynamic pirna program during drosophila spermatogenesis to safeguard male fertility |
| url | https://doi.org/10.1371/journal.pgen.1009591 |
| work_keys_str_mv | AT peiweichen rdccomplexexecutesadynamicpirnaprogramduringdrosophilaspermatogenesistosafeguardmalefertility AT yichengluo rdccomplexexecutesadynamicpirnaprogramduringdrosophilaspermatogenesistosafeguardmalefertility AT alexeiaaravin rdccomplexexecutesadynamicpirnaprogramduringdrosophilaspermatogenesistosafeguardmalefertility |