Speedy A governs non-homologous XY chromosome desynapsis as a unique prerequisite for XY loop-axis organization
(2025) In EMBO Journal p.1-28- Abstract
In mouse early pachytene spermatocytes, the X and Y chromosomes undergo rapid non-homologous (NH) synapsis and desynapsis, but the functional significance remains unknown. Here, we report that pachynema-specific knockout of Speedy A (SpdyA) from telomeres caused persistent Y-X NH synapsis, with the entire Y axis synapsed onto the X axis. This persistent Y-X NH synapsis did not interrupt meiotic sex chromosome inactivation, recombination, or sex body formation, but it disrupted X-Y loop-axis organization and homologous X-Y desynapsis, leading to spermatocyte death. Similarly, persistent Y-X NH synapsis was also observed in pachytene spermatocytes lacking TRF1, where SpdyA was frequently lost from the X-Y non-pseudoautosomal region... (More)
In mouse early pachytene spermatocytes, the X and Y chromosomes undergo rapid non-homologous (NH) synapsis and desynapsis, but the functional significance remains unknown. Here, we report that pachynema-specific knockout of Speedy A (SpdyA) from telomeres caused persistent Y-X NH synapsis, with the entire Y axis synapsed onto the X axis. This persistent Y-X NH synapsis did not interrupt meiotic sex chromosome inactivation, recombination, or sex body formation, but it disrupted X-Y loop-axis organization and homologous X-Y desynapsis, leading to spermatocyte death. Similarly, persistent Y-X NH synapsis was also observed in pachytene spermatocytes lacking TRF1, where SpdyA was frequently lost from the X-Y non-pseudoautosomal region (non-PAR) telomeres. Mechanistic studies revealed that Serine 48 of SUN1 is a key SpdyA/CDK2 phosphorylation site required for Y-X NH desynapsis. We propose that SpdyA governs Y-X NH desynapsis by stabilizing the linkage between the X-Y non-PAR telomeres and their LINC complexes, and that this process is regulated independently from other aspects of pachynema progression. Our findings suggest a key role for Y-X NH desynapsis in establishing proper X-Y loop-axis organization.
(Less)
- author
- organization
- publishing date
- 2025-08-18
- type
- Contribution to journal
- publication status
- epub
- subject
- in
- EMBO Journal
- pages
- 1 - 28
- publisher
- Oxford University Press
- external identifiers
-
- pmid:40826181
- ISSN
- 1460-2075
- DOI
- 10.1038/s44318-025-00528-8
- language
- English
- LU publication?
- yes
- additional info
- © 2025. The Author(s).
- id
- 80548d02-079d-46df-bc23-6f589c7ebdab
- date added to LUP
- 2025-08-22 08:13:57
- date last changed
- 2025-08-25 08:13:58
@article{80548d02-079d-46df-bc23-6f589c7ebdab, abstract = {{<p>In mouse early pachytene spermatocytes, the X and Y chromosomes undergo rapid non-homologous (NH) synapsis and desynapsis, but the functional significance remains unknown. Here, we report that pachynema-specific knockout of Speedy A (SpdyA) from telomeres caused persistent Y-X NH synapsis, with the entire Y axis synapsed onto the X axis. This persistent Y-X NH synapsis did not interrupt meiotic sex chromosome inactivation, recombination, or sex body formation, but it disrupted X-Y loop-axis organization and homologous X-Y desynapsis, leading to spermatocyte death. Similarly, persistent Y-X NH synapsis was also observed in pachytene spermatocytes lacking TRF1, where SpdyA was frequently lost from the X-Y non-pseudoautosomal region (non-PAR) telomeres. Mechanistic studies revealed that Serine 48 of SUN1 is a key SpdyA/CDK2 phosphorylation site required for Y-X NH desynapsis. We propose that SpdyA governs Y-X NH desynapsis by stabilizing the linkage between the X-Y non-PAR telomeres and their LINC complexes, and that this process is regulated independently from other aspects of pachynema progression. Our findings suggest a key role for Y-X NH desynapsis in establishing proper X-Y loop-axis organization.</p>}}, author = {{Liu, Dongteng and Zhang, Yuxiang and Li, Dongliang and Jiang, Binjie and Zhao, Xudong and Li, Yanyan and Lin, Zexiong and Zhao, Yu and Hu, Zhe and Deng, Shuzi and Li, Zheng and Lu, Haonan and Chan, Karen K L and Yeung, William S B and Kaldis, Philipp and Yao, Chencheng and Wang, Hengbin and Chow, Louise T and Liu, Kui}}, issn = {{1460-2075}}, language = {{eng}}, month = {{08}}, pages = {{1--28}}, publisher = {{Oxford University Press}}, series = {{EMBO Journal}}, title = {{Speedy A governs non-homologous XY chromosome desynapsis as a unique prerequisite for XY loop-axis organization}}, url = {{http://dx.doi.org/10.1038/s44318-025-00528-8}}, doi = {{10.1038/s44318-025-00528-8}}, year = {{2025}}, }