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The Arabidopsis SAC9 enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the plasma membrane

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Lebecq, Alexis, Doumane, Mehdi, Fangain, Aurelie, Bayle, Vincent, Leong, Jia Xuan, Rozier, Frédérique, Marques-Bueno, Maria del, Armengot, Laia, Boisseau, Romain, Simon, Mathilde Laetitia, Franz-Wachtel, Mirita, Macek, Boris, Üstün, Suayib, Jaillais, Yvon, Caillaud, Marie-Cécile·2022·eLife
DOI 10.7554/elife.73837PMC PMC9436410

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Abstract

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)P 2 ] 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)P 2 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)P 2 on cortical intracellular compartments, which depends on PI4P and PI(4,5)P 2 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)P 2 at the plasma membrane and illustrate that one of the consequences of PI(4,5)P 2 misspatterning in plants is to impact the endocytic trafficking.

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Metadata

Authors
Lebecq, A., Doumane, M., Fangain, A., Bayle, V., Leong, J. X., Rozier, F., Marques-Bueno, M. D., Armengot, L., Boisseau, R., Simon, M. L., Franz-Wachtel, M., Macek, B., Üstün, S., Jaillais, Y., & Caillaud, M.-C.
Affiliations
  • École Normale Supérieure de Lyon (FR)
  • Laboratoire Reproduction et Développement des Plantes, Université de Lyon
  • University of Tübingen (DE)
  • University of Montana (US)
  • Interfaculty Institute for Cell Biology, Department of Quantitative Proteomics, University of Tübingen
  • University of Tübingen, Center for Plant Molecular Biology (ZMBP)
Corresponding author
  • Jaillais, Yvon
  • Caillaud, Marie-Cécile
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2022-08-31
Volume
11
Pages
e73837
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.73837
PMC
PMC9436410
OpenAlex
W4293763014
Cited by
31
References
1
Citations by year
2026: 6 · 2025: 8 · 2024: 8 · 2023: 8
FWCI
3.21
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • HAL (submittedVersion, cc-by)
  • Dipòsit Digital de Documents de la UAB (Universitat Autònoma de Barcelona) (submittedVersion, cc-by)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Agence Nationale de la Recherche (ANR-16-CE13-0021)
  • European Research Council (3363360-APPL)
  • Deutsche Forschungsgemeinschaft (UE188/2-1)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Keywords
phosphoinositide phosphatase, phosphatidylinositol 4,5-bisphosphate, early endosomes, trans-Golgi network, clathrin-mediated endocytosis, endosomal trafficking, Arabidopsis thaliana, cell cortex
MeSH terms
Animals, Cell Membrane, Clathrin, Endocytosis, Phosphatidylinositols, Endosomes, Arabidopsis, Phosphatidylinositol 4,5-Diphosphate, Transport Vesicles

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