Lipid bilayer properties potentially contributed to the evolutionary disappearance of betaine lipids in seed plants.
Algae
Betaine lipid
Evolution
Molecular dynamics
Neutron membrane diffraction
Phosphate starvation
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
28 Nov 2023
28 Nov 2023
Historique:
received:
18
09
2023
accepted:
21
11
2023
medline:
30
11
2023
pubmed:
29
11
2023
entrez:
29
11
2023
Statut:
epublish
Résumé
Many organisms rely on mineral nutrients taken directly from the soil or aquatic environment, and therefore, developed mechanisms to cope with the limitation of a given essential nutrient. For example, photosynthetic cells have well-defined responses to phosphate limitation, including the replacement of cellular membrane phospholipids with non-phosphorous lipids. Under phosphate starvation, phospholipids in extraplastidial membranes are replaced by betaine lipids in microalgae. In higher plants, the synthesis of betaine lipid is lost, driving plants to other strategies to cope with phosphate starvation where they replace their phospholipids by glycolipids. The aim of this work was to evaluate to what extent betaine lipids and PC lipids share physicochemical properties and could substitute for each other. By neutron diffraction experiments and dynamic molecular simulation of two synthetic lipids, the dipalmitoylphosphatidylcholine (DPPC) and the dipalmitoyl-diacylglyceryl-N,N,N-trimethylhomoserine (DP-DGTS), we found that DP-DGTS bilayers are thicker than DPPC bilayers and therefore are more rigid. Furthermore, DP-DGTS bilayers are more repulsive, especially at long range, maybe due to unexpected unscreened electrostatic contribution. Finally, DP-DGTS bilayers could coexist in the gel and fluid phases. The different properties and hydration responses of PC and DGTS provide an explanation for the diversity of betaine lipids observed in marine organisms and for their disappearance in seed plants.
Sections du résumé
BACKGROUND
BACKGROUND
Many organisms rely on mineral nutrients taken directly from the soil or aquatic environment, and therefore, developed mechanisms to cope with the limitation of a given essential nutrient. For example, photosynthetic cells have well-defined responses to phosphate limitation, including the replacement of cellular membrane phospholipids with non-phosphorous lipids. Under phosphate starvation, phospholipids in extraplastidial membranes are replaced by betaine lipids in microalgae. In higher plants, the synthesis of betaine lipid is lost, driving plants to other strategies to cope with phosphate starvation where they replace their phospholipids by glycolipids.
RESULTS
RESULTS
The aim of this work was to evaluate to what extent betaine lipids and PC lipids share physicochemical properties and could substitute for each other. By neutron diffraction experiments and dynamic molecular simulation of two synthetic lipids, the dipalmitoylphosphatidylcholine (DPPC) and the dipalmitoyl-diacylglyceryl-N,N,N-trimethylhomoserine (DP-DGTS), we found that DP-DGTS bilayers are thicker than DPPC bilayers and therefore are more rigid. Furthermore, DP-DGTS bilayers are more repulsive, especially at long range, maybe due to unexpected unscreened electrostatic contribution. Finally, DP-DGTS bilayers could coexist in the gel and fluid phases.
CONCLUSION
CONCLUSIONS
The different properties and hydration responses of PC and DGTS provide an explanation for the diversity of betaine lipids observed in marine organisms and for their disappearance in seed plants.
Identifiants
pubmed: 38017456
doi: 10.1186/s12915-023-01775-z
pii: 10.1186/s12915-023-01775-z
pmc: PMC10685587
doi:
Substances chimiques
Lipid Bilayers
0
Betaine
3SCV180C9W
Triglycerides
0
Phospholipids
0
Phosphates
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
275Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-18-CE92-0015
Organisme : Agence Nationale de la Recherche
ID : ANR-15-IDEX-02
Organisme : Agence Nationale de la Recherche
ID : ANR-17-EURE-000
Organisme : Agence Nationale de la Recherche
ID : ANR-11-BTBR-0008
Organisme : Deutsche Forschungsgemeinschaft
ID : SCHN 1396/2
Organisme : Deutsche Forschungsgemeinschaft
ID : EXC 2075 - 390740016
Informations de copyright
© 2023. The Author(s).
Références
Biochim Biophys Acta. 2015 Feb;1848(2):532-43
pubmed: 25445167
J Chem Theory Comput. 2013 Aug 13;9(8):3527-37
pubmed: 26584109
Phys Rev E Stat Nonlin Soft Matter Phys. 2008 Dec;78(6 Pt 1):061924
pubmed: 19256885
J Phys Chem B. 2015 Nov 5;119(44):14157-67
pubmed: 26439409
Biophys J. 2011 May 4;100(9):2151-9
pubmed: 21539782
Phytochemistry. 1997 Nov;46(5):883-92
pubmed: 9375419
J Chem Phys. 2011 Aug 7;135(5):055105
pubmed: 21823736
Biochim Biophys Acta. 1991 Feb 26;1082(1):108-11
pubmed: 2009297
Biochim Biophys Acta. 2000 Nov 10;1469(3):159-95
pubmed: 11063882
Eukaryot Cell. 2005 Feb;4(2):242-52
pubmed: 15701786
Biophys J. 1996 Jan;70(1):349-57
pubmed: 8770211
Langmuir. 2019 Feb 12;35(6):2399-2411
pubmed: 30632763
J Cell Biol. 2004 Dec 6;167(5):863-74
pubmed: 15569715
Mol Biol Evol. 2018 Jun 1;35(6):1547-1549
pubmed: 29722887
Nat Commun. 2014 Sep 15;5:4937
pubmed: 25222494
Chem Phys Lipids. 2017 Jun;205:18-24
pubmed: 28412174
FEBS J. 2005 Oct;272(20):5101-9
pubmed: 16218944
New Phytol. 2002 Nov;156(2):255-264
pubmed: 33873275
Biochemistry. 1986 May 6;25(9):2591-6
pubmed: 3718966
Plant Physiol. 2015 Jan;167(1):118-36
pubmed: 25489020
J Phys Chem Lett. 2017 Jul 6;8(13):2869-2874
pubmed: 28590133
Nature. 2009 Mar 5;458(7234):69-72
pubmed: 19182781
Biophys J. 1982 Mar;37(3):667-72
pubmed: 7074192
Curr Opin Plant Biol. 2002 Jun;5(3):250-7
pubmed: 11960744
Commun Biol. 2022 Jan 11;5(1):19
pubmed: 35017659
BMC Evol Biol. 2010 Jul 13;10:210
pubmed: 20626897
Plant Physiol. 2017 Dec;175(4):1543-1559
pubmed: 29051196
Cell Rep. 2014 Jan 16;6(1):70-80
pubmed: 24388754
J Mol Biol. 1976 Jan 25;100(3):359-78
pubmed: 943549
Biophys J. 2006 Jun 1;90(11):L83-5
pubmed: 16617085
Mol Biol Evol. 2008 Jul;25(7):1307-20
pubmed: 18367465
J Biol Chem. 2005 Jul 29;280(30):27578-86
pubmed: 15927962
Protist. 2016 Jun;167(3):254-67
pubmed: 27179349
J Am Chem Soc. 1988 Mar 1;110(6):1657-66
pubmed: 27557051
Biophys J. 1997 May;72(5):2002-13
pubmed: 9129804
Proc Natl Acad Sci U S A. 2012 Sep 4;109(36):14405-9
pubmed: 22908241
Biochemistry. 2008 Jul 8;47(27):7090-6
pubmed: 18543943
Int J Mol Sci. 2013 Jan 24;14(2):2282-302
pubmed: 23348926
Phytochemistry. 2016 Apr;124:68-78
pubmed: 26895707
Prog Lipid Res. 1996 Mar;35(1):1-51
pubmed: 9039425
Phytochemistry. 2015 Sep;117:34-42
pubmed: 26057227
Nat Commun. 2014 Dec 10;5:5764
pubmed: 25493338
Prog Lipid Res. 2004 Sep;43(5):383-402
pubmed: 15458813
J Theor Biol. 1987 Dec 21;129(4):411-25
pubmed: 3455469
J Biomater Sci Polym Ed. 1991;3(2):127-47
pubmed: 1768635
Biochim Biophys Acta. 2002 Sep 20;1565(1):29-35
pubmed: 12225849
Biophys J. 2000 Dec;79(6):3172-92
pubmed: 11106622
Z Naturforsch C J Biosci. 1997 Jul-Aug;52(7-8):487-95
pubmed: 9309879
Syst Biol. 2012 May;61(3):539-42
pubmed: 22357727
BMC Evol Biol. 2010 Dec 02;10:377
pubmed: 21126361
Plant Physiol. 2001 Jan;125(1):423-9
pubmed: 11154349
J Phys Chem B. 2014 May 1;118(17):4571-81
pubmed: 24745688
Bioinformatics. 2003 Aug 12;19(12):1572-4
pubmed: 12912839
Biochim Biophys Acta Biomembr. 2022 Dec 1;1864(12):184037
pubmed: 36041508
J Cheminform. 2012 Aug 13;4(1):17
pubmed: 22889332
Phys Rev B Condens Matter. 1988 Aug 1;38(4):2297-2311
pubmed: 9946532
Plant Physiol. 2021 Apr 2;185(3):815-835
pubmed: 33793914
Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
pubmed: 9254694
Prog Lipid Res. 2017 Jan;65:12-23
pubmed: 27871883
Plant Physiol. 2018 May;177(1):181-193
pubmed: 29555786
Phys Chem Chem Phys. 2019 Aug 21;21(31):16989-17000
pubmed: 31343009
Biophys J. 2020 Apr 7;118(7):1602-1611
pubmed: 32097623
Nat Commun. 2017 Apr 03;8:14899
pubmed: 28367975
Nat Rev Microbiol. 2011 Jun;9(6):403-13
pubmed: 21572457
J Chem Phys. 2008 Sep 28;129(12):124105
pubmed: 19045004
Biophys J. 1991 Jan;59(1):162-73
pubmed: 2015381
Biophys J. 1982 Mar;37(3):657-65
pubmed: 7074191
J Chem Phys. 2007 Jan 7;126(1):014101
pubmed: 17212484
Plant Cell. 2019 Nov;31(11):2768-2788
pubmed: 31511316
Eur Phys J E Soft Matter. 2006 Jun;20(2):221-30
pubmed: 16802069
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Arch Biochem Biophys. 2005 Sep 1;441(1):96-105
pubmed: 16095555
Syst Biol. 2012 Dec 1;61(6):973-99
pubmed: 22723471
Biochem J. 2020 Jul 17;477(13):2543-2559
pubmed: 32556082
Prog Lipid Res. 2019 Apr;74:31-68
pubmed: 30703388
New Phytol. 2017 Jan;213(2):700-713
pubmed: 27605045