Biophysical analysis of the plant-specific GIPC sphingolipids reveals multiple modes of membrane regulation

Adiilah Mamode Cassim, Yotam Navon, Yu Gao, Marion Decossas, Laetitia Fouillen, Axelle Grélard, Minoru Nagano, Olivier Lambert, Delphine Bahammou, Pierre van Delft, Lilly Maneta-Peyret, Françoise Simon-Plas, Laurent Heux, Bruno Jean, Giovanna Fragneto, Jenny C. Mortimer, Magali Deleu, Laurence Lins, Sébastien Mongrand

Research output: Contribution to journalArticlepeer-review

23 Scopus citations

Abstract

The plant plasma membrane (PM) is an essential barrier between the cell and the external environment, controlling signal perception and transmission. It consists of an asymmetrical lipid bilayer made up of three different lipid classes: sphingolipids, sterols, and phospholipids. The glycosyl inositol phosphoryl ceramides (GIPCs), representing up to 40% of total sphingolipids, are assumed to be almost exclusively in the outer leaflet of the PM. However, their biological role and properties are poorly defined. In this study, we investigated the role of GIPCs in membrane organization. Because GIPCs are not commercially available, we developed a protocol to extract and isolate GIPC-enriched fractions from eudicots (cauliflower and tobacco) and monocots (leek and rice). Lipidomic analysis confirmed the presence of trihydroxylated long chain bases and 2-hydroxylated very long-chain fatty acids up to 26 carbon atoms. The glycan head groups of the GIPCs from monocots and dicots were analyzed by gas chromatograph-mass spectrometry, revealing different sugar moieties. Multiple biophysics tools, namely Langmuir monolayer, ζ-Potential, light scattering, neutron reflectivity, solid state 2H-NMR, and molecular modeling, were used to investigate the physical properties of the GIPCs, as well as their interaction with free and conjugated phytosterols. We showed that GIPCs increase the thickness and electronegativity of model membranes, interact differentially with the different phytosterols species, and regulate the gel-to-fluid phase transition during temperature variations. These results unveil the multiple roles played by GIPCs in the plant PM.

Original languageEnglish
Article number100602
JournalJournal of Biological Chemistry
Volume296
DOIs
StatePublished - 1 Jan 2021
Externally publishedYes

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

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