The Arabidopsis SAC9 enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the plasma membrane
Membrane lipids, and especially phosphoinositides, are differentially enriched within the eukaryotic endomembrane system. This generates a landmark code by modulating the properties of each membrane. Phosphatidylinositol 4,5-bisphosphate [PI(4,5)P2] specifically accumulates at the plasma membrane in...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-08-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/73837 |
| _version_ | 1811225687178084352 |
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| author | Alexis Lebecq Mehdi Doumane Aurelie Fangain Vincent Bayle Jia Xuan Leong Frédérique Rozier Maria del Marques-Bueno Laia Armengot Romain Boisseau Mathilde Laetitia Simon Mirita Franz-Wachtel Boris Macek Suayib Üstün Yvon Jaillais Marie-Cécile Caillaud |
| author_facet | Alexis Lebecq Mehdi Doumane Aurelie Fangain Vincent Bayle Jia Xuan Leong Frédérique Rozier Maria del Marques-Bueno Laia Armengot Romain Boisseau Mathilde Laetitia Simon Mirita Franz-Wachtel Boris Macek Suayib Üstün Yvon Jaillais Marie-Cécile Caillaud |
| author_sort | Alexis Lebecq |
| collection | DOAJ |
| description | Membrane lipids, and especially phosphoinositides, are differentially enriched within the eukaryotic endomembrane system. This generates a landmark code by modulating the properties of each membrane. Phosphatidylinositol 4,5-bisphosphate [PI(4,5)P2] specifically accumulates at the plasma membrane in yeast, animal, and plant cells, where it regulates a wide range of cellular processes including endocytic trafficking. However, the functional consequences of mispatterning PI(4,5)P2 in plants are unknown. Here, we functionally characterized the putative phosphoinositide phosphatase SUPPRESSOR OF ACTIN9 (SAC9) in Arabidopsis thaliana (Arabidopsis). We found that SAC9 depletion led to the ectopic localization of PI(4,5)P2 on cortical intracellular compartments, which depends on PI4P and PI(4,5)P2 production at the plasma membrane. SAC9 localizes to a subpopulation of trans-Golgi Network/early endosomes that are enriched in a region close to the cell cortex and that are coated with clathrin. Furthermore, it interacts and colocalizes with Src Homology 3 Domain Protein 2 (SH3P2), a protein involved in endocytic trafficking. In the absence of SAC9, SH3P2 localization is altered and the clathrin-mediated endocytosis rate is reduced. Together, our results highlight the importance of restricting PI(4,5)P2 at the plasma membrane and illustrate that one of the consequences of PI(4,5)P2 misspatterning in plants is to impact the endocytic trafficking. |
| first_indexed | 2024-04-12T09:11:34Z |
| format | Article |
| id | doaj.art-61ef6e6f49164366bd574537a710404c |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T09:11:34Z |
| publishDate | 2022-08-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-61ef6e6f49164366bd574537a710404c2022-12-22T03:38:57ZengeLife Sciences Publications LtdeLife2050-084X2022-08-011110.7554/eLife.73837The Arabidopsis SAC9 enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the plasma membraneAlexis Lebecq0Mehdi Doumane1https://orcid.org/0000-0002-5711-3626Aurelie Fangain2Vincent Bayle3Jia Xuan Leong4Frédérique Rozier5Maria del Marques-Bueno6Laia Armengot7https://orcid.org/0000-0002-3790-9838Romain Boisseau8https://orcid.org/0000-0003-4317-1064Mathilde Laetitia Simon9Mirita Franz-Wachtel10Boris Macek11https://orcid.org/0000-0002-1206-2458Suayib Üstün12Yvon Jaillais13https://orcid.org/0000-0003-4923-883XMarie-Cécile Caillaud14https://orcid.org/0000-0002-0348-7024Laboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, FranceUniversity of Tübingen, Center for Plant Molecular Biology (ZMBP), Tübingen, GermanyLaboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, FranceDivision of Biological Science, University of Montana, Missoula, United StatesLaboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, FranceInterfaculty Institute for Cell Biology, Department of Quantitative Proteomics, University of Tübingen, Tübingen, GermanyInterfaculty Institute for Cell Biology, Department of Quantitative Proteomics, University of Tübingen, Tübingen, GermanyUniversity of Tübingen, Center for Plant Molecular Biology (ZMBP), Tübingen, Germany; Faculty of Biology & Biotechnology, Ruhr-University Bochum, Bochum, GermanyLaboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, FranceMembrane lipids, and especially phosphoinositides, are differentially enriched within the eukaryotic endomembrane system. This generates a landmark code by modulating the properties of each membrane. Phosphatidylinositol 4,5-bisphosphate [PI(4,5)P2] specifically accumulates at the plasma membrane in yeast, animal, and plant cells, where it regulates a wide range of cellular processes including endocytic trafficking. However, the functional consequences of mispatterning PI(4,5)P2 in plants are unknown. Here, we functionally characterized the putative phosphoinositide phosphatase SUPPRESSOR OF ACTIN9 (SAC9) in Arabidopsis thaliana (Arabidopsis). We found that SAC9 depletion led to the ectopic localization of PI(4,5)P2 on cortical intracellular compartments, which depends on PI4P and PI(4,5)P2 production at the plasma membrane. SAC9 localizes to a subpopulation of trans-Golgi Network/early endosomes that are enriched in a region close to the cell cortex and that are coated with clathrin. Furthermore, it interacts and colocalizes with Src Homology 3 Domain Protein 2 (SH3P2), a protein involved in endocytic trafficking. In the absence of SAC9, SH3P2 localization is altered and the clathrin-mediated endocytosis rate is reduced. Together, our results highlight the importance of restricting PI(4,5)P2 at the plasma membrane and illustrate that one of the consequences of PI(4,5)P2 misspatterning in plants is to impact the endocytic trafficking.https://elifesciences.org/articles/73837endocytosisplasma membranephosphoinositides |
| spellingShingle | Alexis Lebecq Mehdi Doumane Aurelie Fangain Vincent Bayle Jia Xuan Leong Frédérique Rozier Maria del Marques-Bueno Laia Armengot Romain Boisseau Mathilde Laetitia Simon Mirita Franz-Wachtel Boris Macek Suayib Üstün Yvon Jaillais Marie-Cécile Caillaud The Arabidopsis SAC9 enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the plasma membrane eLife endocytosis plasma membrane phosphoinositides |
| title | The Arabidopsis SAC9 enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the plasma membrane |
| title_full | The Arabidopsis SAC9 enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the plasma membrane |
| title_fullStr | The Arabidopsis SAC9 enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the plasma membrane |
| title_full_unstemmed | The Arabidopsis SAC9 enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the plasma membrane |
| title_short | The Arabidopsis SAC9 enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the plasma membrane |
| title_sort | arabidopsis sac9 enzyme is enriched in a cortical population of early endosomes and restricts pi 4 5 p2 at the plasma membrane |
| topic | endocytosis plasma membrane phosphoinositides |
| url | https://elifesciences.org/articles/73837 |
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