GRAS-1 is a novel regulator of early meiotic chromosome dynamics in C. elegans.
Chromosome movements and licensing of synapsis must be tightly regulated during early meiosis to ensure accurate chromosome segregation and avoid aneuploidy, although how these steps are coordinated is not fully understood. Here we show that GRAS-1, the worm homolog of mammalian GRASP/Tamalin and CY...
| Main Authors: | , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2023-02-01
|
| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1010666 |
| _version_ | 1797736600220729344 |
|---|---|
| author | Marina Martinez-Garcia Pedro Robles Naharro Marnie W Skinner Kerstin A Baran Laura I Lascarez-Lagunas Saravanapriah Nadarajan Nara Shin Carlos G Silva-García Takamune T Saito Sara Beese-Sims Brianna N Diaz-Pacheco Elizaveta Berson Ana B Castañer Sarai Pacheco Enrique Martinez-Perez Philip W Jordan Monica P Colaiácovo |
| author_facet | Marina Martinez-Garcia Pedro Robles Naharro Marnie W Skinner Kerstin A Baran Laura I Lascarez-Lagunas Saravanapriah Nadarajan Nara Shin Carlos G Silva-García Takamune T Saito Sara Beese-Sims Brianna N Diaz-Pacheco Elizaveta Berson Ana B Castañer Sarai Pacheco Enrique Martinez-Perez Philip W Jordan Monica P Colaiácovo |
| author_sort | Marina Martinez-Garcia |
| collection | DOAJ |
| description | Chromosome movements and licensing of synapsis must be tightly regulated during early meiosis to ensure accurate chromosome segregation and avoid aneuploidy, although how these steps are coordinated is not fully understood. Here we show that GRAS-1, the worm homolog of mammalian GRASP/Tamalin and CYTIP, coordinates early meiotic events with cytoskeletal forces outside the nucleus. GRAS-1 localizes close to the nuclear envelope (NE) in early prophase I and interacts with NE and cytoskeleton proteins. Delayed homologous chromosome pairing, synaptonemal complex (SC) assembly, and DNA double-strand break repair progression are partially rescued by the expression of human CYTIP in gras-1 mutants, supporting functional conservation. However, Tamalin, Cytip double knockout mice do not exhibit obvious fertility or meiotic defects, suggesting evolutionary differences between mammals. gras-1 mutants show accelerated chromosome movement during early prophase I, implicating GRAS-1 in regulating chromosome dynamics. GRAS-1-mediated regulation of chromosome movement is DHC-1-dependent, placing it acting within the LINC-controlled pathway, and depends on GRAS-1 phosphorylation at a C-terminal S/T cluster. We propose that GRAS-1 coordinates the early steps of homology search and licensing of SC assembly by regulating the pace of chromosome movement in early prophase I. |
| first_indexed | 2024-03-12T13:16:15Z |
| format | Article |
| id | doaj.art-256d8d7b5f334b59810c1d4d8aae4a05 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-03-12T13:16:15Z |
| publishDate | 2023-02-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-256d8d7b5f334b59810c1d4d8aae4a052023-08-27T05:31:47ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042023-02-01192e101066610.1371/journal.pgen.1010666GRAS-1 is a novel regulator of early meiotic chromosome dynamics in C. elegans.Marina Martinez-GarciaPedro Robles NaharroMarnie W SkinnerKerstin A BaranLaura I Lascarez-LagunasSaravanapriah NadarajanNara ShinCarlos G Silva-GarcíaTakamune T SaitoSara Beese-SimsBrianna N Diaz-PachecoElizaveta BersonAna B CastañerSarai PachecoEnrique Martinez-PerezPhilip W JordanMonica P ColaiácovoChromosome movements and licensing of synapsis must be tightly regulated during early meiosis to ensure accurate chromosome segregation and avoid aneuploidy, although how these steps are coordinated is not fully understood. Here we show that GRAS-1, the worm homolog of mammalian GRASP/Tamalin and CYTIP, coordinates early meiotic events with cytoskeletal forces outside the nucleus. GRAS-1 localizes close to the nuclear envelope (NE) in early prophase I and interacts with NE and cytoskeleton proteins. Delayed homologous chromosome pairing, synaptonemal complex (SC) assembly, and DNA double-strand break repair progression are partially rescued by the expression of human CYTIP in gras-1 mutants, supporting functional conservation. However, Tamalin, Cytip double knockout mice do not exhibit obvious fertility or meiotic defects, suggesting evolutionary differences between mammals. gras-1 mutants show accelerated chromosome movement during early prophase I, implicating GRAS-1 in regulating chromosome dynamics. GRAS-1-mediated regulation of chromosome movement is DHC-1-dependent, placing it acting within the LINC-controlled pathway, and depends on GRAS-1 phosphorylation at a C-terminal S/T cluster. We propose that GRAS-1 coordinates the early steps of homology search and licensing of SC assembly by regulating the pace of chromosome movement in early prophase I.https://doi.org/10.1371/journal.pgen.1010666 |
| spellingShingle | Marina Martinez-Garcia Pedro Robles Naharro Marnie W Skinner Kerstin A Baran Laura I Lascarez-Lagunas Saravanapriah Nadarajan Nara Shin Carlos G Silva-García Takamune T Saito Sara Beese-Sims Brianna N Diaz-Pacheco Elizaveta Berson Ana B Castañer Sarai Pacheco Enrique Martinez-Perez Philip W Jordan Monica P Colaiácovo GRAS-1 is a novel regulator of early meiotic chromosome dynamics in C. elegans. PLoS Genetics |
| title | GRAS-1 is a novel regulator of early meiotic chromosome dynamics in C. elegans. |
| title_full | GRAS-1 is a novel regulator of early meiotic chromosome dynamics in C. elegans. |
| title_fullStr | GRAS-1 is a novel regulator of early meiotic chromosome dynamics in C. elegans. |
| title_full_unstemmed | GRAS-1 is a novel regulator of early meiotic chromosome dynamics in C. elegans. |
| title_short | GRAS-1 is a novel regulator of early meiotic chromosome dynamics in C. elegans. |
| title_sort | gras 1 is a novel regulator of early meiotic chromosome dynamics in c elegans |
| url | https://doi.org/10.1371/journal.pgen.1010666 |
| work_keys_str_mv | AT marinamartinezgarcia gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT pedroroblesnaharro gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT marniewskinner gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT kerstinabaran gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT laurailascarezlagunas gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT saravanapriahnadarajan gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT narashin gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT carlosgsilvagarcia gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT takamunetsaito gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT sarabeesesims gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT briannandiazpacheco gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT elizavetaberson gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT anabcastaner gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT saraipacheco gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT enriquemartinezperez gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT philipwjordan gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans AT monicapcolaiacovo gras1isanovelregulatorofearlymeioticchromosomedynamicsincelegans |