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A physicochemical cause of betaine lipid evolutionary loss in seed plants?

Bolik Stéphanie, View ORCID ProfileSchlaich Alexander, View ORCID ProfileMukhina Tetiana, View ORCID ProfileAmato Alberto, View ORCID ProfileBastien Olivier, View ORCID ProfileSchneck Emanuel, View ORCID ProfileDemé Bruno, View ORCID ProfileJouhet Juliette
doi: https://doi.org/10.1101/2023.01.24.525350
Bolik Stéphanie
1Laboratoire Physiologie Cellulaire et Végétale, Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG, Grenoble, France
2Large Scale Structures group, Institut Laue-Langevin, 38000, Grenoble, France
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Schlaich Alexander
3Institute for Computational Physics, Universität Stuttgart, Stuttgart, Germany
4Stuttgart Center for Simulation Science (SimTech), Universität Stuttgart, Stuttgart, Germany
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Mukhina Tetiana
5Institute for Condensed Matter Physics, TU Darmstadt, Darmstadt, Germany
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Amato Alberto
1Laboratoire Physiologie Cellulaire et Végétale, Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG, Grenoble, France
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Bastien Olivier
1Laboratoire Physiologie Cellulaire et Végétale, Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG, Grenoble, France
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Schneck Emanuel
5Institute for Condensed Matter Physics, TU Darmstadt, Darmstadt, Germany
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Demé Bruno
2Large Scale Structures group, Institut Laue-Langevin, 38000, Grenoble, France
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Jouhet Juliette
1Laboratoire Physiologie Cellulaire et Végétale, Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG, Grenoble, France
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  • For correspondence: juliette.jouhet@cea.fr
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ABSTRACT

Phosphate is vital for plant and algae growth, yield, and survival, but in most environments, it is poorly available. To cope with phosphate starvation, photosynthetic organisms used their phospholipids as a phosphate reserve. In microalgae, betaine lipids replace phospholipids whereas, in higher plants, betaine lipid synthesis is lost, driving plants to other strategies. The aim of this work was to evaluate to what extent betaine lipids and PC lipids share physicochemical properties and could thus substitute each other. Using neutron diffraction and molecular dynamics simulations of two synthetic lipids, dipalmitoylphosphatidylcholine (DPPC) and dipalmitoyl-diacylglyceryl-N,N,N-trimethylhomoserine (DP-DGTS), we show that DP-DGTS bilayers are thicker, more rigid, and mutually more repulsive than DPPC bilayers. The different properties and hydration response of PC and DGTS provide an explanation for the diversity of betaine lipids observed in marine organisms and for their disappearance in seed plants.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Financial sources: This work was supported by ANR-DFG ANR-18-CE92-0015 and SCHN 1396/2. SB was supported by a joint funding Glyco@Alps / ILL PhD Program, by the French National Research Agency in the framework of the “Investissements d’avenir” program Glyco@Alps (ANR-15-IDEX-02), “Origin Of Life” (ANR-17-EURE-0003), “Oceanomics” (ANR-11-BTBR-0008) and the Labex GRAL, financed within the University Grenoble Alpes graduate school (Ecoles Universitaires de Recherche) CBH-EUR-GS (ANR-17-EURE-0003). AS acknowledges funding from the DFG under Germany’s Excellence Strategy – EXC 2075 – 390740016. Computing time was provided by the state of Baden-Württemberg through bwHPC.

  • Data Availability Statement: The data that support the findings of this study are openly available at https://doi.ill.fr/10.5291/ILL-DATA.8-02-220, https://doi.ill.fr/10.5291/ILL-DATA.TEST-3119 and at https://doi.org/10.18419/darus-2360.

  • Conflict of Interest Statement : The authors declare no conflicts of interest

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted January 24, 2023.
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A physicochemical cause of betaine lipid evolutionary loss in seed plants?
Bolik Stéphanie, Schlaich Alexander, Mukhina Tetiana, Amato Alberto, Bastien Olivier, Schneck Emanuel, Demé Bruno, Jouhet Juliette
bioRxiv 2023.01.24.525350; doi: https://doi.org/10.1101/2023.01.24.525350
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A physicochemical cause of betaine lipid evolutionary loss in seed plants?
Bolik Stéphanie, Schlaich Alexander, Mukhina Tetiana, Amato Alberto, Bastien Olivier, Schneck Emanuel, Demé Bruno, Jouhet Juliette
bioRxiv 2023.01.24.525350; doi: https://doi.org/10.1101/2023.01.24.525350

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