CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing
Abstract Eukaryotes must balance the need for gene transcription by RNA polymerase II (Pol II) against the danger of mutations caused by transposable element (TE) proliferation. In plants, these gene expression and TE silencing activities are divided between different RNA polymerases. Specifically,...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2024-11-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-54268-0 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850107638687203328 |
|---|---|
| author | Luisa Felgines Bart Rymen Laura M. Martins Guanghui Xu Calvin Matteoli Christophe Himber Ming Zhou Josh Eis Ceyda Coruh Marcel Böhrer Lauriane Kuhn Johana Chicher Vijaya Pandey Philippe Hammann James Wohlschlegel Florent Waltz Julie A. Law Todd Blevins |
| author_facet | Luisa Felgines Bart Rymen Laura M. Martins Guanghui Xu Calvin Matteoli Christophe Himber Ming Zhou Josh Eis Ceyda Coruh Marcel Böhrer Lauriane Kuhn Johana Chicher Vijaya Pandey Philippe Hammann James Wohlschlegel Florent Waltz Julie A. Law Todd Blevins |
| author_sort | Luisa Felgines |
| collection | DOAJ |
| description | Abstract Eukaryotes must balance the need for gene transcription by RNA polymerase II (Pol II) against the danger of mutations caused by transposable element (TE) proliferation. In plants, these gene expression and TE silencing activities are divided between different RNA polymerases. Specifically, RNA polymerase IV (Pol IV), which evolved from Pol II, transcribes TEs to generate small interfering RNAs (siRNAs) that guide DNA methylation and block TE transcription by Pol II. While the Pol IV complex is recruited to TEs via SNF2-like CLASSY (CLSY) proteins, how Pol IV partners with the CLSYs remains unknown. Here, we identified a conserved CYC-YPMF motif that is specific to Pol IV and is positioned on the complex exterior. Furthermore, we found that this motif is essential for the co-purification of all four CLSYs with Pol IV, but that only one CLSY is present in any given Pol IV complex. These findings support a “one CLSY per Pol IV” model where the CYC-YPMF motif acts as a CLSY-docking site. Indeed, mutations in and around this motif phenocopy pol iv null and clsy quadruple mutants. Together, these findings provide structural and functional insights into a critical protein feature that distinguishes Pol IV from other RNA polymerases, allowing it to promote genome stability by targeting TEs for silencing. |
| format | Article |
| id | doaj-art-e8bc24794bde4fd99cb9297cd2c4e890 |
| institution | OA Journals |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-e8bc24794bde4fd99cb9297cd2c4e8902025-08-20T02:38:32ZengNature PortfolioNature Communications2041-17232024-11-0115111610.1038/s41467-024-54268-0CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencingLuisa Felgines0Bart Rymen1Laura M. Martins2Guanghui Xu3Calvin Matteoli4Christophe Himber5Ming Zhou6Josh Eis7Ceyda Coruh8Marcel Böhrer9Lauriane Kuhn10Johana Chicher11Vijaya Pandey12Philippe Hammann13James Wohlschlegel14Florent Waltz15Julie A. Law16Todd Blevins17Institut de Biologie Moléculaire des Plantes, CNRS, Université de StrasbourgInstitut de Biologie Moléculaire des Plantes, CNRS, Université de StrasbourgPlant Molecular and Cellular Biology Laboratory, Salk Institute for Biological StudiesPlant Molecular and Cellular Biology Laboratory, Salk Institute for Biological StudiesInstitut de Biologie Moléculaire des Plantes, CNRS, Université de StrasbourgInstitut de Biologie Moléculaire des Plantes, CNRS, Université de StrasbourgPlant Molecular and Cellular Biology Laboratory, Salk Institute for Biological StudiesPlant Molecular and Cellular Biology Laboratory, Salk Institute for Biological StudiesPlant Molecular and Cellular Biology Laboratory, Salk Institute for Biological StudiesInstitut de Biologie Moléculaire des Plantes, CNRS, Université de StrasbourgInstitut de Biologie Moléculaire et Cellulaire, CNRS, Plateforme Protéomique Strasbourg-EsplanadeInstitut de Biologie Moléculaire et Cellulaire, CNRS, Plateforme Protéomique Strasbourg-EsplanadeDepartment of Biological Chemistry, University of CaliforniaInstitut de Biologie Moléculaire et Cellulaire, CNRS, Plateforme Protéomique Strasbourg-EsplanadeDepartment of Biological Chemistry, University of CaliforniaBiozentrum, University of BaselPlant Molecular and Cellular Biology Laboratory, Salk Institute for Biological StudiesInstitut de Biologie Moléculaire des Plantes, CNRS, Université de StrasbourgAbstract Eukaryotes must balance the need for gene transcription by RNA polymerase II (Pol II) against the danger of mutations caused by transposable element (TE) proliferation. In plants, these gene expression and TE silencing activities are divided between different RNA polymerases. Specifically, RNA polymerase IV (Pol IV), which evolved from Pol II, transcribes TEs to generate small interfering RNAs (siRNAs) that guide DNA methylation and block TE transcription by Pol II. While the Pol IV complex is recruited to TEs via SNF2-like CLASSY (CLSY) proteins, how Pol IV partners with the CLSYs remains unknown. Here, we identified a conserved CYC-YPMF motif that is specific to Pol IV and is positioned on the complex exterior. Furthermore, we found that this motif is essential for the co-purification of all four CLSYs with Pol IV, but that only one CLSY is present in any given Pol IV complex. These findings support a “one CLSY per Pol IV” model where the CYC-YPMF motif acts as a CLSY-docking site. Indeed, mutations in and around this motif phenocopy pol iv null and clsy quadruple mutants. Together, these findings provide structural and functional insights into a critical protein feature that distinguishes Pol IV from other RNA polymerases, allowing it to promote genome stability by targeting TEs for silencing.https://doi.org/10.1038/s41467-024-54268-0 |
| spellingShingle | Luisa Felgines Bart Rymen Laura M. Martins Guanghui Xu Calvin Matteoli Christophe Himber Ming Zhou Josh Eis Ceyda Coruh Marcel Böhrer Lauriane Kuhn Johana Chicher Vijaya Pandey Philippe Hammann James Wohlschlegel Florent Waltz Julie A. Law Todd Blevins CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing Nature Communications |
| title | CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing |
| title_full | CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing |
| title_fullStr | CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing |
| title_full_unstemmed | CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing |
| title_short | CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing |
| title_sort | clsy docking to pol iv requires a conserved domain critical for small rna biogenesis and transposon silencing |
| url | https://doi.org/10.1038/s41467-024-54268-0 |
| work_keys_str_mv | AT luisafelgines clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT bartrymen clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT laurammartins clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT guanghuixu clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT calvinmatteoli clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT christophehimber clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT mingzhou clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT josheis clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT ceydacoruh clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT marcelbohrer clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT laurianekuhn clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT johanachicher clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT vijayapandey clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT philippehammann clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT jameswohlschlegel clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT florentwaltz clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT juliealaw clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing AT toddblevins clsydockingtopolivrequiresaconserveddomaincriticalforsmallrnabiogenesisandtransposonsilencing |