Contributions and Limitations of Biophysical Approaches to Study of the Interactions between Amphiphilic Molecules and the Plant Plasma Membrane

Some amphiphilic molecules are able to interact with the lipid matrix of plant plasma membranes and trigger the immune response in plants. This original mode of perception is not yet fully understood and biophysical approaches could help to obtain molecular insights. In this review, we focus on such membrane-interacting molecules, and present biophysically grounded methods that are used and are particularly interesting in the investigation of this mode of perception. Rather than going into overly technical details, the aim of this review was to provide to readers with a plant biochemistry background a good overview of how biophysics can help to study molecular interactions between bioactive amphiphilic molecules and plant lipid membranes. In particular, we present the biomimetic membrane models typically used, solid-state nuclear magnetic resonance, molecular modeling, and fluorescence approaches, because they are especially suitable for this field of research. For each technique, we provide a brief description, a few case studies, and the inherent limitations, so non-specialists can gain a good grasp on how they could extend their toolbox and/or could apply new techniques to study amphiphilic bioactive compound and lipid interactions.

[1]  J. Davis,et al.  Deuterium magnetic resonance study of the gel and liquid crystalline phases of dipalmitoyl phosphatidylcholine. , 1979, Biophysical journal.

[2]  J. Killian,et al.  Conformational analysis of gramicidin-gramicidin interactions at the air/water interface suggests that gramicidin aggregates into tube-like structures similar as found in the gramicidin-induced hexagonal HII phase. , 1987, Biochimica et biophysica acta.

[3]  B. Bechinger,et al.  15N and 31P solid-state NMR investigations on the orientation of zervamicin II and alamethicin in phosphatidylcholine membranes. , 2001, Biochemistry.

[4]  R. Brasseur,et al.  Interaction of Surfactin with Membranes: A Computational Approach , 2003 .

[5]  J. Crowet,et al.  Interactions of sugar-based bolaamphiphiles with biomimetic systems of plasma membranes. , 2016, Biochimie.

[6]  B. Thomma,et al.  Understanding plant immunity as a surveillance system to detect invasion. , 2015, Annual review of phytopathology.

[7]  G. Feigenson,et al.  Asymmetric Bilayers by Hemifusion: Method and Leaflet Behaviors. , 2019, Biophysical journal.

[8]  A. Reddy,et al.  Ligand-dependent reduction in the membrane mobility of FLAGELLIN SENSITIVE2, an arabidopsis receptor-like kinase. , 2007, Plant & cell physiology.

[9]  R. Standaert,et al.  Preparation of asymmetric phospholipid vesicles for use as cell membrane models , 2018, Nature Protocols.

[10]  Chris Oostenbrink,et al.  A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force‐field parameter sets 53A5 and 53A6 , 2004, J. Comput. Chem..

[11]  A. Kyrychenko Using fluorescence for studies of biological membranes: a review , 2015, Methods and applications in fluorescence.

[12]  A. Thomas,et al.  "De novo" design of peptides with specific lipid-binding properties. , 2006, Biophysical journal.

[13]  S. Marčelja,et al.  Physical principles of membrane organization , 1980, Quarterly Reviews of Biophysics.

[14]  C. Zipfel,et al.  Regulation of pattern recognition receptor signalling in plants , 2016, Nature Reviews Immunology.

[15]  R. Brasseur,et al.  The hydrophobic effect in protein folding , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[16]  S. Takeuchi,et al.  Giant liposome formation toward the synthesis of well-defined artificial cells. , 2017, Journal of materials chemistry. B.

[17]  C. Toniolo,et al.  Alamethicin Interaction with Lipid Membranes: A Spectroscopic Study on Synthetic Analogues , 2007, Chemistry & biodiversity.

[18]  Zhaoxin Lu,et al.  Antifungal activity and mechanism of fengycin in the presence and absence of commercial surfactin against Rhizopus stolonifer , 2011, The Journal of Microbiology.

[19]  H. Heerklotz,et al.  Additive and synergistic membrane permeabilization by antimicrobial (lipo)peptides and detergents. , 2014, Biophysical journal.

[20]  C. Toniolo,et al.  The fluorescence and infrared absorption probe para‐cyanophenylalanine: Effect of labeling on the behavior of different membrane‐interacting peptides , 2015, Biopolymers.

[21]  Helgi I Ingólfsson,et al.  Lipid organization of the plasma membrane. , 2014, Journal of the American Chemical Society.

[22]  Julien Gronnier,et al.  Revisiting Plant Plasma Membrane Lipids in Tobacco: A Focus on Sphingolipids1 , 2015, Plant Physiology.

[23]  A. Carvalho,et al.  Diphenylhexatriene membrane probes DPH and TMA-DPH: A comparative molecular dynamics simulation study. , 2016, Biochimica et biophysica acta.

[24]  B. L. de Groot,et al.  CHARMM36m: an improved force field for folded and intrinsically disordered proteins , 2016, Nature Methods.

[25]  Julien Gronnier,et al.  Plant lipids: Key players of plasma membrane organization and function. , 2019, Progress in lipid research.

[26]  N. Matsumori,et al.  Dynamic membrane interactions of antibacterial and antifungal biomolecules, and amyloid peptides, revealed by solid-state NMR spectroscopy. , 2018, Biochimica et biophysica acta. General subjects.

[27]  Chanhui Lee,et al.  Harpins, multifunctional proteins secreted by gram-negative plant-pathogenic bacteria. , 2013, Molecular plant-microbe interactions : MPMI.

[28]  B. Lentz,et al.  Use of fluorescent probes to monitor molecular order and motions within liposome bilayers. , 1993, Chemistry and physics of lipids.

[29]  Petra Schwille,et al.  Probing Lipid Mobility of Raft-exhibiting Model Membranes by Fluorescence Correlation Spectroscopy* , 2003, Journal of Biological Chemistry.

[30]  C. Clément,et al.  Rhamnolipid Biosurfactants as New Players in Animal and Plant Defense against Microbes , 2010, International journal of molecular sciences.

[31]  M. Romantschuk,et al.  Functional mapping of harpin HrpZ of Pseudomonas syringae reveals the sites responsible for protein oligomerization, lipid interactions and plant defence induction. , 2011, Molecular plant pathology.

[32]  F. Baluška,et al.  Di-4-ANEPPDHQ, a fluorescent probe for the visualisation of membrane microdomains in living Arabidopsis thaliana cells. , 2015, Plant physiology and biochemistry : PPB.

[33]  V. Labhasetwar,et al.  Biophysical interactions with model lipid membranes: applications in drug discovery and drug delivery. , 2009, Molecular pharmaceutics.

[34]  George Khelashvili,et al.  Mechanisms of Lipid Scrambling by the G Protein-Coupled Receptor Opsin. , 2017, Structure.

[35]  L. Brown,et al.  Membrane proteins in their native habitat as seen by solid‐state NMR spectroscopy , 2015, Protein science : a publication of the Protein Society.

[36]  W. Wimley,et al.  A high-throughput screen for identifying transmembrane pore-forming peptides. , 2001, Analytical biochemistry.

[37]  C. Toniolo,et al.  Hypersensitive‐Like Response to the Pore‐Former Peptaibol Alamethicin in Arabidopsis Thaliana , 2010, Chembiochem : a European journal of chemical biology.

[38]  A. Ortiz,et al.  Permeabilization of biological and artificial membranes by a bacterial dirhamnolipid produced by Pseudomonas aeruginosa. , 2010, Journal of colloid and interface science.

[39]  Helgi I. Ingólfsson,et al.  Computational Modeling of Realistic Cell Membranes , 2019, Chemical reviews.

[40]  B. Charloteaux,et al.  Tilted properties of the 67–78 fragment of α‐synuclein are responsible for membrane destabilization and neurotoxicity , 2007, Proteins.

[41]  Elliot L Elson,et al.  Fluorescence correlation spectroscopy: past, present, future. , 2011, Biophysical journal.

[42]  Jianpeng Ma,et al.  CHARMM: The biomolecular simulation program , 2009, J. Comput. Chem..

[43]  E. Tajkhorshid,et al.  Residue-specific information about the dynamics of antimicrobial peptides from (1)H-(15)N and (2)H solid-state NMR spectroscopy. , 2009, Journal of the American Chemical Society.

[44]  A. Ortiz,et al.  Effect of a dirhamnolipid biosurfactant on the structure and phase behaviour of dimyristoylphosphatidylserine model membranes. , 2019, Colloids and surfaces. B, Biointerfaces.

[45]  S. Reissmann,et al.  Structure and alignment of the membrane-associated peptaibols ampullosporin A and alamethicin by oriented 15N and 31P solid-state NMR spectroscopy. , 2009, Biophysical journal.

[46]  P. Balaram,et al.  Interactions of the channel forming peptide alamethicin with artificial and natural membranes , 1984, Journal of Biosciences.

[47]  Che Ma,et al.  Nuclear magnetic resonance of membrane-associated peptides and proteins. , 2001, Methods in enzymology.

[48]  H. Heerklotz,et al.  Vesicle Leakage Reflects the Target Selectivity of Antimicrobial Lipopeptides from Bacillus subtilis. , 2015, Biophysical journal.

[49]  D. Voelker,et al.  Preparation of Asymmetric Liposomes Using a Phosphatidylserine Decarboxylase. , 2018, Biophysical journal.

[50]  R. Brasseur,et al.  Computer Simulation of Surfactin Conformation at a Hydrophobic/Hydrophilic Interface , 1999 .

[51]  A. Naito,et al.  Structure and orientation of antibiotic peptide alamethicin in phospholipid bilayers as revealed by chemical shift oscillation analysis of solid state nuclear magnetic resonance and molecular dynamics simulation. , 2015, Biochimica et biophysica acta.

[52]  A. Ortiz,et al.  Antimycotic activity of fengycin C biosurfactant and its interaction with phosphatidylcholine model membranes. , 2017, Colloids and surfaces. B, Biointerfaces.

[53]  I. Vattulainen,et al.  Nanoscale Membrane Domain Formation Driven by Cholesterol , 2017, Scientific Reports.

[54]  V. Pashynska Mass spectrometric study of rhamnolipid biosurfactants and their interactions with cell membrane phospholipids , 2009 .

[55]  Yasin F. Dagdas,et al.  Nine things to know about elicitins. , 2016, The New phytologist.

[56]  P. Schwille,et al.  Fluorescence techniques to study lipid dynamics. , 2011, Cold Spring Harbor perspectives in biology.

[57]  E. Hosy,et al.  Structural basis for plant plasma membrane protein dynamics and organization into functional nanodomains , 2017, eLife.

[58]  James H. Davis,et al.  The description of membrane lipid conformation, order and dynamics by 2H-NMR. , 1983, Biochimica et biophysica acta.

[59]  J. Dinić,et al.  Laurdan and di-4-ANEPPDHQ do not respond to membrane-inserted peptides and are good probes for lipid packing. , 2011, Biochimica et biophysica acta.

[60]  Megha,et al.  Preparation and Properties of Asymmetric Vesicles That Mimic Cell Membranes , 2009, Journal of Biological Chemistry.

[61]  R. Brasseur,et al.  Molecular Determinants of the Interaction Between the C‐Terminal Domain of Alzheimer's β‐Amyloid Peptide and Apolipoprotein E α‐Helices , 1999 .

[62]  Wenxu Zhou,et al.  Acclimation-induced changes in cell membrane composition and influence on cryotolerance of in vitro shoots of native plant species , 2013, Plant Cell, Tissue and Organ Culture (PCTOC).

[63]  F. Besson,et al.  Interactions of the natural antimicrobial mycosubtilin with phospholipid membrane models. , 2010, Colloids and surfaces. B, Biointerfaces.

[64]  L. Lins,et al.  Interaction of hexadecylbetainate chloride with biological relevant lipids. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[65]  J. Svobodová,et al.  Bacillus subtilis alters the proportion of major membrane phospholipids in response to surfactin exposure. , 2016, Biochimica et biophysica acta.

[66]  J. Crowet,et al.  Differential Interaction of Synthetic Glycolipids with Biomimetic Plasma Membrane Lipids Correlates with the Plant Biological Response. , 2017, Langmuir : the ACS journal of surfaces and colloids.

[67]  F. Marassi,et al.  Hydration-optimized oriented phospholipid bilayer samples for solid-state NMR structural studies of membrane proteins. , 2003, Journal of magnetic resonance.

[68]  S. Mongrand,et al.  Plant-Pathogen Interactions: Underestimated Roles of Phyto-oxylipins. , 2020, Trends in plant science.

[69]  Siewert J. Marrink,et al.  The molecular face of lipid rafts in model membranes , 2008, Proceedings of the National Academy of Sciences.

[70]  C. Zipfel,et al.  Function, Discovery, and Exploitation of Plant Pattern Recognition Receptors for Broad-Spectrum Disease Resistance. , 2017, Annual review of phytopathology.

[71]  Vahid Sandoghdar,et al.  Production of Isolated Giant Unilamellar Vesicles under High Salt Concentrations , 2017, Front. Physiol..

[72]  M. Dauchez,et al.  Exploring the Dual Interaction of Natural Rhamnolipids with Plant and Fungal Biomimetic Plasma Membranes through Biophysical Studies , 2019, International journal of molecular sciences.

[73]  Sanguk Kim,et al.  2D solid state NMR spectral simulation of 310, α, and π-helices , 2004 .

[74]  S. Singer,et al.  The fluid mosaic model of the structure of cell membranes. , 1972, Science.

[75]  F. Marassi A simple approach to membrane protein secondary structure and topology based on NMR spectroscopy. , 2001, Biophysical journal.

[76]  W. Webb,et al.  Fluorescence probe partitioning between Lo/Ld phases in lipid membranes. , 2007, Biochimica et biophysica acta.

[77]  T. Yamashita,et al.  Alterations in detergent-resistant plasma membrane microdomains in Arabidopsis thaliana during cold acclimation. , 2009, Plant & cell physiology.

[78]  T. Ott,et al.  The Nanoscale Organization of the Plasma Membrane and Its Importance in Signaling: A Proteolipid Perspective1[OPEN] , 2019, Plant Physiology.

[79]  D. Tieleman,et al.  The MARTINI force field: coarse grained model for biomolecular simulations. , 2007, The journal of physical chemistry. B.

[80]  T. Kikukawa,et al.  Changes in lipid mobility associated with alamethicin incorporation into membranes. , 2002, Archives of biochemistry and biophysics.

[81]  Holger Gohlke,et al.  The Amber biomolecular simulation programs , 2005, J. Comput. Chem..

[82]  P. Yeagle Laboratory Membrane Systems , 2016 .

[83]  Gerrit Groenhof,et al.  GROMACS: Fast, flexible, and free , 2005, J. Comput. Chem..

[84]  S. Dufour,et al.  Surfactins modulate the lateral organization of fluorescent membrane polar lipids: a new tool to study drug:membrane interaction and assessment of the role of cholesterol and drug acyl chain length. , 2013, Biochimica et biophysica acta.

[85]  C. Eggeling,et al.  Laurdan and Di-4-ANEPPDHQ probe different properties of the membrane , 2016, bioRxiv.

[86]  P. Moreau,et al.  A Combinatorial Lipid Code Shapes the Electrostatic Landscape of Plant Endomembranes. , 2018, Developmental cell.

[87]  Leslie M Loew,et al.  Cholesterol-enriched lipid domains can be visualized by di-4-ANEPPDHQ with linear and nonlinear optics. , 2005, Biophysical journal.

[88]  J. Crowet,et al.  Complementary biophysical tools to investigate lipid specificity in the interaction between bioactive molecules and the plasma membrane: A review. , 2014, Biochimica et biophysica acta.

[89]  E. London,et al.  Preparation of Artificial Plasma Membrane Mimicking Vesicles with Lipid Asymmetry , 2014, PloS one.

[90]  S. Mongrand,et al.  Modification of Plasma Membrane Organization in Tobacco Cells Elicited by Cryptogein1[W] , 2013, Plant Physiology.

[91]  K. Edwards,et al.  All-or-none membrane permeabilization by fengycin-type lipopeptides from Bacillus subtilis QST713. , 2011, Biochimica et biophysica acta.

[92]  H. Heerklotz,et al.  Engineering Asymmetric Lipid Vesicles: Accurate and Convenient Control of the Outer Leaflet Lipid Composition. , 2018, Langmuir : the ACS journal of surfaces and colloids.

[93]  E. Dufourc,et al.  Dynamics of phosphate head groups in biomembranes. Comprehensive analysis using phosphorus-31 nuclear magnetic resonance lineshape and relaxation time measurements. , 1992, Biophysical journal.

[94]  W. Webb,et al.  GUV preparation and imaging: minimizing artifacts. , 2010, Biochimica et biophysica acta.

[95]  L. Lins,et al.  Analysis of calcium-induced effects on the conformation of fengycin. , 2013, Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy.

[96]  J. Crowet,et al.  Linoleic and linolenic acid hydroperoxides interact differentially with biomimetic plant membranes in a lipid specific manner. , 2019, Colloids and surfaces. B, Biointerfaces.

[97]  Jinxing Lin,et al.  Quantification of Membrane Protein Dynamics and Interactions in Plant Cells by Fluorescence Correlation Spectroscopy. , 2016, Molecular plant.

[98]  R. Pons,et al.  Complex rhamnolipid mixture characterization and its influence on DPPC bilayer organization. , 2014, Biochimica et biophysica acta.

[99]  J. Cartaud,et al.  Formation of unilamellar vesicles by repetitive freeze-thaw cycles: characterization by electron microscopy and 31P-nuclear magnetic resonance , 2000, European Biophysics Journal.

[100]  D. MacLean,et al.  Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains , 2017, eLife.

[101]  T. Boubekeur,et al.  Remorin, a Solanaceae Protein Resident in Membrane Rafts and Plasmodesmata, Impairs Potato virus X Movement[W] , 2009, The Plant Cell Online.

[102]  M. Uemura,et al.  Cold Acclimation of Arabidopsis thaliana (Effect on Plasma Membrane Lipid Composition and Freeze-Induced Lesions) , 1995, Plant physiology.

[103]  R. Brasseur,et al.  Effects of surfactin on membrane models displaying lipid phase separation. , 2013, Biochimica et biophysica acta.

[104]  A. Ortiz,et al.  Effects of dirhamnolipid on the structural properties of phosphatidylcholine membranes. , 2006, International journal of pharmaceutics.

[105]  E. Dufourc,et al.  Surfactin-triggered small vesicle formation of negatively charged membranes: a novel membrane-lysis mechanism. , 2008, Biophysical journal.

[106]  L. Hellgren,et al.  Lipid asymmetry in plant plasma membranes: phosphate deficiency‐induced phospholipid replacement is restricted to the cytosolic leaflet , 2010, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[107]  London,et al.  Location of diphenylhexatriene (DPH) and its derivatives within membranes: comparison of different fluorescence quenching analyses of membrane depth , 1998, Biochemistry.

[108]  L. Bagatolli,et al.  To see or not to see: lateral organization of biological membranes and fluorescence microscopy. , 2006, Biochimica et biophysica acta.

[109]  Laxmikant V. Kalé,et al.  Scalable molecular dynamics with NAMD , 2005, J. Comput. Chem..

[110]  S. Mongrand,et al.  Eudicot plant-specific sphingolipids determine host selectivity of microbial NLP cytolysins , 2017, Science.

[111]  Julien Gronnier,et al.  Divide and Rule: Plant Plasma Membrane Organization. , 2018, Trends in plant science.

[112]  C. Clément,et al.  Apoplastic invasion patterns triggering plant immunity: plasma membrane sensing at the frontline , 2019, Molecular plant pathology.

[113]  C. Zipfel Early molecular events in PAMP-triggered immunity. , 2009, Current opinion in plant biology.

[114]  Nohad Gresh,et al.  Tinker-HP: a massively parallel molecular dynamics package for multiscale simulations of large complex systems with advanced point dipole polarizable force fields† †Electronic supplementary information (ESI) available. See DOI: 10.1039/c7sc04531j , 2017, Chemical science.

[115]  N. Leborgne-Castel,et al.  Plasma membrane order and fluidity are diversely triggered by elicitors of plant defence , 2016, Journal of experimental botany.

[116]  F. Ausubel Are innate immune signaling pathways in plants and animals conserved? , 2005, Nature Immunology.

[117]  Huey W. Huang,et al.  Action of Antimicrobial Peptides on Bacterial and Lipid Membranes: A Direct Comparison. , 2017, Biophysical journal.

[118]  K. A. Noghabi,et al.  Interaction of a bacterial monorhamnolipid secreted by Pseudomonas aeruginosa MA01 with phosphatidylcholine model membranes. , 2012, Chemistry and physics of lipids.

[119]  E. Gratton,et al.  Direct Observation of Lipid Domains in Free-Standing Bilayers Using Two-Photon Excitation Fluorescence Microscopy , 2001, Journal of Fluorescence.

[120]  Enrico Gratton,et al.  Laurdan and Prodan as Polarity-Sensitive Fluorescent Membrane Probes , 1998, Journal of Fluorescence.

[121]  J. Seelig,et al.  Leakage and lysis of lipid membranes induced by the lipopeptide surfactin , 2007, European Biophysics Journal.

[122]  D. Nikolelis,et al.  Artificial Lipid Membranes: Past, Present, and Future , 2017, Membranes.

[123]  Bozhong Mu,et al.  Surfactin effect on the physicochemical property of PC liposome , 2010 .

[124]  Alexander P Lyubartsev,et al.  Extension of the Slipids Force Field to Polyunsaturated Lipids. , 2016, The journal of physical chemistry. B.

[125]  R. Brasseur,et al.  Impacts of the carbonyl group location of ester bond on interfacial properties of sugar-based surfactants: experimental and computational evidences. , 2009, The journal of physical chemistry. B.

[126]  C. Toniolo,et al.  Alamethicin Supramolecular Organization in Lipid Membranes from 19F Solid-State NMR. , 2016, Biophysical journal.

[127]  A. Ortiz,et al.  Interaction of a bacterial dirhamnolipid with phosphatidylcholine membranes: a biophysical study. , 2009, Chemistry and physics of lipids.

[128]  N. Nielsen,et al.  Mechanisms of Peptide-Induced Pore Formation in Lipid Bilayers Investigated by Oriented 31P Solid-State NMR Spectroscopy , 2012, PloS one.

[129]  T. Nylander,et al.  Effect of fengycin, a lipopeptide produced by Bacillus subtilis, on model biomembranes. , 2008, Biophysical journal.

[130]  P. Thonart,et al.  The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune‐related defence responses , 2011, Cellular microbiology.

[131]  D. Choi,et al.  Current Understandings of Plant Nonhost Resistance. , 2017, Molecular plant-microbe interactions : MPMI.

[132]  R. Pastor,et al.  Molecular modeling of lipid membrane curvature induction by a peptide: more than simply shape. , 2014, Biophysical journal.

[133]  G. van Meer,et al.  Cellular lipidomics , 2005, The EMBO journal.

[134]  S. Mongrand,et al.  Differential Effect of Plant Lipids on Membrane Organization , 2015, The Journal of Biological Chemistry.

[135]  P. Schwille,et al.  Dual-color fluorescence cross-correlation spectroscopy for multicomponent diffusional analysis in solution. , 1997, Biophysical journal.