This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
All documents in ORBi are protected by a user license.
[en] Natural phytotoxic compounds could become an alternative to traditional herbicides in the framework of sustainable agriculture. Nonanoic acid, sarmentine and sorgoleone are such molecules extracted from plants and able to inhibit the growth of various plant species. However, their mode of action is not fully understood and despite clues indicating that they could affect the plant plasma membrane, molecular details of such phenomenon are lacking. In this paper, we investigate the interactions between those natural herbicides and artificial bilayers mimicking the plant plasma membrane. First, their ability to affect lipid order and fluidity is evaluated by means of fluorescence measurements. It appears that sorgoleone has a clear ordering effect on lipid bilayers, while nonanoic acid and sarmentine induce no or little change to these parameters. Then, a thermodynamic characterization of interactions of each compound with lipid vesicles is obtained with isothermal titration calorimetry, and their respective affinity for bilayers is found to be ranked as follows: sorgoleone > sarmentine > nonanoic acid. Finally, molecular dynamics simulations give molecular details about the location of each compound within a lipid bilayer and confirm the rigidifying effect of sorgoleone. Data also suggest that mismatch in alkyl chain length between nonanoic acid or sarmentine and lipid hydrophobic tails could be responsible for bilayer destabilization. Results are discussed regarding their implications for the phytotoxicity of these compounds.
Fonds de la Recherche Scientifique de Belgique (F.R.S.- FNRS) : Consortium des Équipements de Calcul Intensif (CÉCI) University of Liège (gricultureIsLife) : Cellule d’Appui à la Recherche et à l’Enseignement (CARE)
Arouri, A., Lauritsen, K. E., Nielsen, H. L., and Mouritsen, O. G. (2016). Effect of fatty acids on the permeability barrier of model and biological membranes. Chem. Phys. Lipids 200, 139–146. doi: 10.1016/j.chemphyslip.2016. 10.001
Bachar, M., Brunelle, P., Tieleman, D. P., and Rauk, A. (2004). Molecular dynamics simulation of a polyunsaturated lipid bilayer susceptible to lipid peroxidation. J. Phys. Chem. B 108, 7170–7179. doi: 10.1021/jp036981u
Berger, O., Edholm, O., and Jähnig, F. (1997). Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72, 2002–2013. doi: 10.1016/S0006-3495(97)78845-3
Bernik, D. L., Zubiri, D., Tymczyszyn, E., and Disalvo, E. A. (2001). Polarity and packing at the carbonyl and phosphate regions of lipid bilayers. Langmuir 17, 6438–6442. doi: 10.1021/la010570s
Bernsdorff, C., and Winter, R. (2003). Differential properties of the sterols cholesterol, ergosterol, β-sitosterol, trans-7-dehydrocholesterol, stigmasterol and lanosterol on DPPC bilayer order. J. Phys. Chem. B 107, 10658–10664. doi: 10.1021/jp034922a.
Cantor, R. S. (1997). The lateral pressure profile in membranes: a physical mechanism of general anesthesia. Biochemistry 36, 2339–2344. doi: 10.1021/bi9627323
Cantor, R. S. (2003). Receptor desensitization by neurotransmitters in membranes:? are neurotransmitters the endogenous anesthetics? Biochemistry 42, 11891–11897. doi: 10.1021/bi034534z
Cordomí, A., Edholm, O., and Perez, J. J. (2009). Effect of force field parameters on sodium and potassium ion binding to dipalmitoyl phosphatidylcholine bilayers. J. Chem. Theory Comput. 5, 2125–2134. doi: 10.1021/ct9000763
Dayan, F. E., and Duke, S. O. (2014). Natural compounds as next-generation herbicides. Plant Physiol. 166, 1090–1105. doi: 10.1104/pp.114.239061
Dayan, F. E., Howell, J., and Weidenhamer, J. D. (2009). Dynamic root exudation of sorgoleone and its in planta mechanism of action. J. Exp. Bot. 60, 2107–2117. doi: 10.1093/jxb/erp082
Dayan, F. E., Owens, D. K., and Duke, S. O. (2012). Rationale for a natural products approach to herbicide discovery. Pest Manag. Sci. 68, 519–528. doi: 10.1002/ps. 2332
Dayan, F. E., Owens, D. K., Watson, S. B., Asolkar, R. N., and Boddy, L. G. (2015). Sarmentine, a natural herbicide from Piper species with multiple herbicide mechanisms of action. Front. Plant Sci. 6:222. doi: 10.3389/fpls.2015.00222
Dayan, F. E., Rimando, A. M., Pan, Z., Baerson, S. R., Gimsing, A. L., and Duke, S. O. (2010). Sorgoleone. Phytochemistry 71, 1032–1039. doi: 10.1016/j. phytochem.2010.03.011
De Vequi-Suplicy, C. C., Benatti, C. R., and Lamy, M. T. (2006). Laurdan in fluid bilayers: position and structural sensitivity. J. Fluoresc. 16, 431–439. doi: 10.1007/s10895-005-0059-3
Deleu, M., Crowet, J.-M., Nasir, M. N., and Lins, L. (2014). Complementary biophysical tools to investigate lipid specificity in the interaction between bioactive molecules and the plasma membrane: a review. Biochim. Biophys. Acta 1838, 3171–3190. doi: 10.1016/j.bbamem.2014.08.023
Einhellig, F. A., and Souza, I. F. (1992). Phytotoxicity of sorgoleone found in grain sorghum root exudates. J. Chem. Ecol. 18, 1–11. doi: 10.1007/BF00997160
Fukuda, M., Tsujino, Y., Fujimori, T., Wakabayashi, K., and Böger, P. (2004). Phytotoxic activity of middle-chain fatty acids I: effects on cell constituents. Pestic. Biochem. Physiol. 80, 143–150. doi: 10.1016/j.pestbp.2004.06.011
Gonzalez, V. M., Kazimir, J., Nimbal, C., Weston, L. A., and Cheniae, G. M. (1997). Inhibition of a photosystem II electron transfer reaction by the natural product sorgoleone. J. Agric. Food Chem. 45, 1415–1421. doi: 10.1021/jf960733w
Gurtovenko, A. A., and Vattulainen, I. (2008). Effect of NaCl and KCl on phosphatidylcholine and phosphatidylethanolamine lipid membranes: insight from atomic-scale simulations for understanding salt-induced effects in the plasma membrane. J. Phys. Chem. B 112, 1953–1962. doi: 10.1021/jp0750708
Harris, F. M., Best, K. B., and Bell, J. D. (2002). Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order. Biochim. Biophys. Acta 1565, 123–128. doi: 10.1016/S0005-2736(02)00514-X
Heerklotz, H., and Seelig, J. (2000). Titration calorimetry of surfactant–membrane partitioning and membrane solubilization. Biochim. Biophys. Acta 1508, 69–85 doi: 10.1016/S0304-4157(00)00009-5
Heimburg, T., and Jackson, A. D. (2007). The thermodynamics of general anesthesia. Biophys. J. 92, 3159–3165. doi: 10.1529/biophysj.106.099754
Hejl, A. M., and Koster, K. L. (2004). The allelochemical sorgoleone inhibits root H+-ATPase and water uptake. J. Chem. Ecol. 30, 2181–2191. doi: 10.1023/B: JOEC.0000048782.87862.7f
Henriksen, J. R., Andresen, T. L., Feldborg, L. N., Duelund, L., and Ipsen, J. H. (2010). Understanding detergent effects on lipid membranes: a model study of lysolipids. Biophys. J. 98, 2199–2205. doi: 10.1016/j.bpj.2010.01.037
Hermans, J., Berendsen, H. J. C., Van Gunsteren, W. F., and Postma, J. P. M. (1984). A consistent empirical potential for water–protein interactions. Biopolymers 23, 1513–1518. doi: 10.1002/bip.360230807
Hess, B., Bekker, H., Berendsen, H. J., and Fraaije, J. G. (1997). LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463–1472. doi: 10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
Hoover, W. G. (1985). Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A 31, 1695–1697. doi: 10.1103/PhysRevA.31.1695
Huang, H., Morgan, C. M., Asolkar, R. N., Koivunen, M. E., and Marrone, P. G. (2010). Phytotoxicity of sarmentine isolated from long pepper (Piper longum) fruit. J. Agric. Food Chem. 58, 9994–10000. doi: 10.1021/jf102087c
Humphrey, W., Dalke, A., and Schulten, K. (1996). VMD: visual molecular dynamics. J. Mol. Graph. 14, 33–38. doi: 10.1016/0263-7855(96)00018-5
Ingólfsson, H. I., Thakur, P., Herold, K. F., Hobart, E. A., Ramsey, N. B., Periole, X., et al. (2014). Phytochemicals perturb membranes and promiscuously alter protein function. ACS Chem. Biol. 9, 1788–1798. doi: 10.1021/cb500086e
Jay, A. G., and Hamilton, J. A. (2017). Disorder amidst membrane order: standardizing laurdan generalized polarization and membrane fluidity terms. J. Fluoresc. 27, 243–249. doi: 10.1007/s10895-016-1951-8
Kaiser, R. D., and London, E. (1998). Location of diphenylhexatriene (DPH) and its derivatives within membranes: comparison of different fluorescence quenching analyses of membrane depth. Biochemistry 37, 8180–8190. doi: 10. 1021/bi980064a
Knight, C. J., and Hub, J. S. (2015). MemGen: a general web server for the setup of lipid membrane simulation systems. Bioinformatics 31, 2897–2899. doi: 10.1093/bioinformatics/btv292
Lakowicz, J. R. (2006). Principles of Fluorescence Spectroscopy. 3rd edn. New York, NY: Springer. doi: 10.1007/978-0-387-46312-4
Lederer, B., Fujimori, T., Tsujino, Y., Wakabayashi, K., and Böger, P. (2004). Phytotoxic activity of middle-chain fatty acids II: peroxidation and membrane effects. Pestic. Biochem. Physiol. 80, 151–156. doi: 10.1016/j.pestbp.2004.06.010.
Lentz, B. R. (1989). Membrane “fluidity” as detected by diphenylhexatriene probes. Chem. Phys. Lipids 50, 171–190. doi: 10.1016/0009-3084(89)90049-2
Lentz, B. R. (1993). Use of fluorescent probes to monitor molecular order and motions within liposome bilayers. Chem. Phys. Lipids 64, 99–116. doi: 10.1016/0009-3084(93)90060-G
Lewis, R., and McElhaney, R. N. (1992). The Mesomorphic Phase Behavior of Lipid Bilayers. CRC Press: Boca Raton, FL.
Malde, A. K., Zuo, L., Breeze, M., Stroet, M., Poger, D., Nair, P. C., et al. (2011). An automated force field topology builder (ATB) and repository: version 1.0. J. Chem. Theory Comput. 7, 4026–4037. doi: 10.1021/ct200196m
Morales-Cedillo, F., González-Solís, A., Gutiérrez-Angoa, L., Cano-Ramírez, D. L., and Gavilanes-Ruiz, M. (2015). Plant lipid environment and membrane enzymes: the case of the plasma membrane H+-ATPase. Plant Cell Rep. 34, 617–629. doi: 10.1007/s00299-014-1735-z
Morrow, M. R., Davis, P. J., Jackman, C. S., and Keough, K. M. (1996). Thermal history alters cholesterol effect on transition of 1-palmitoyl-2-linoleoyl phosphatidylcholine. Biophys. J. 71, 3207–3214. doi: 10.1016/S0006-3495(96) 79514-0
Murphy, A. S., Schulz, B., and Peer, W. (2011). The Plant Plasma Membrane. Berlin: Springer-Verlag doi: 10.1007/978-3-642-13431-9
Nimbal, C. I., Yerkes, C. N., Weston, L. A., and Weller, S. C. (1996). Herbicidal activity and site of action of the natural product sorgoleone. Pestic. Biochem. Physiol. 54, 73–83. doi: 10.1006/pest.1996.0011
Nosé, S. (1984). A molecular dynamics method for simulations in the canonical ensemble. Mol. Phys. 52, 255–268. doi: 10.1080/00268978400101201
Oostenbrink, C., Villa, A., Mark, A. E., and Van Gunsteren, W. F. (2004). A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6. J. Comput. Chem. 25, 1656–1676. doi: 10.1002/jcc.20090
Parasassi, T., De Stasio, G., Ravagnan, G., Rusch, R. M., and Gratton, E. (1991). Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of laurdan fluorescence. Biophys. J. 60, 179–189. doi: 10.1016/S0006-3495(91)82041-0
Parrinello, M., and Rahman, A. (1981). Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52, 7182–7190. doi: 10.1063/1.328693
Pernille H., Davidsen, J., and Jørgensen, K. (2001). Lipid membrane partitioning of lysolipids and fatty acids: effects of membrane phase structure and detergent chain length§. J. Phys. Chem. B 105, 2649–2657. doi: 10.1021/jp003631o
Roach, C., Feller, S. E., Ward, J. A., Shaikh, S. R., Zerouga, M., and Stillwell, W. (2004). Comparison of cis and trans fatty acid containing phosphatidylcholines on membrane properties. Biochemistry 43, 6344–6351. doi: 10.1021/bi049917r
Schuler, I., Milon, A., Nakatani, Y., Ourisson, G., Albrecht, A. M., Benveniste, P., et al. (1991). Differential effects of plant sterols on water permeability and on acyl chain ordering of soybean phosphatidylcholine bilayers. Proc. Natl. Acad. Sci. U.S.A. 88, 6926–6930. doi: 10.1073/pnas.88.16.6926
Shinitsky, M., and Barenholz, Y. (1978). Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim. Biophys. Acta 515, 367–394. doi: 10.1016/0304-4157(78)90010-2
Stott, B. M., Vu, M. P., McLemore, C. O., Lund, M. S., Gibbons, E., Brueseke, T. J., et al. (2008). Use of fluorescence to determine the effects of cholesterol on lipid behavior in sphingomyelin liposomes and erythrocyte membranes. J. Lipid Res. 49, 1202–1215. doi: 10.1194/jlr.M700479-JLR200
Tieleman, D. P. (2018). Biocomputing Group University of Calgary. Available at: http://wcm.ucalgary.ca/tieleman/downloads [accessed May 3].
Zakanda, F. N., Lins, L., Nott, K., Paquot, M., Lelo, G. M., and Deleu, M. (2012). Interaction of hexadecylbetainate chloride with biological relevant lipids. Langmuir 28, 3524–3533. doi: 10.1021/la2040328
Zawilska, P., and Cieślik-Boczula, K. (2017). Laurdan emission study of the cholesterol-like effect of long-chain alkylresorcinols on the structure of dipalmitoylphosphocholine and sphingomyelin membranes. Biophys. Chem. 221, 1–9. doi: 10.1016/j.bpc.2016.11.004
