Insights into the Relationships Between Herbicide Activities, Molecular Structure and Membrane Interaction of Cinnamon and Citronella Essential Oils Components
Lins, Laurence; Dal Maso, Simon; Foncoux, Béréniceet al.
2019 • In International Journal of Molecular Sciences, 20, p. 4007
[en] Since the 50’s, the massive and “environmental naïve” use of synthetic chemistry has
revolutionized the farming community facing the dramatic growth of demography. However, nowadays,
the controversy grows regarding the long-term harmful effects of these products on human health
and the environment. In this context, the use of essential oils (EOs) could be an alternative to chemical
products and a better understanding of theirmode of biological action for new and optimal applications
is of importance. Indeed, if the biocidal effects of some EOs or their components have been at least
partly elucidated at the molecular level, very little is currently known regarding their mechanism of
action as herbicides at themolecular level. Here, we showed that cinnamon and Java citronella essential
oils and some of their main components, i.e., cinnamaldehyde (CIN), citronellal (CitA), and citronellol
(CitO) could act as efficient herbicides when spread on A. thaliana leaves. The individual EO molecules
are small amphiphiles, allowing for them to cross the mesh of cell wall and directly interact with
the plant plasma membrane (PPM), which is one of the potential cellular targets of EOs. Hence,
we investigated and characterized their interaction with biomimetic PPMwhile using an integrative
biophysical approach. If CitO and CitA, maintaining a similar chemical structure, are able to interact
with the model membranes without permeabilizing effect, CIN belonging to the phenylpropanoid
family, is not. We suggested that different mechanisms of action for the two types of molecules
can occur: while the monoterpenes could disturb the lipid organization and/or domain formation,
the phenylpropanoid CIN could interact with membrane receptors.
Laurin, Yoann ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbial, food and biobased technologies
Genva, Manon ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Chimie des agro-biosystèmes
Jijakli, Haissam ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs
De Clerck, Caroline ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs
Fauconnier, Marie-Laure ✱; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Chimie des agro-biosystèmes
Deleu, Magali ✱; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Chimie des agro-biosystèmes
✱ These authors have contributed equally to this work.
Language :
English
Title :
Insights into the Relationships Between Herbicide Activities, Molecular Structure and Membrane Interaction of Cinnamon and Citronella Essential Oils Components
Publication date :
16 August 2019
Journal title :
International Journal of Molecular Sciences
ISSN :
1661-6596
eISSN :
1422-0067
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI), Switzerland
Dudai, N.; Poljakoff-Mayber, A.; Mayer, A.M.; Putievsky, E.; Lerner, H.R. Essential Oils as Allelochemicals and Their Potential Use as Bioherbicides. J. Chem. Ecol. 1999, 25, 1079–1089. [CrossRef]
Tworkoski, T. Herbicide effects of essential oils. Weed Sci. 2002, 50, 425–431. [CrossRef]
Amri, I.; Hamrouni, L.; Hanana, M.; Jamoussi, B. Reviews on phytotoxic effects of essential oils and their individual components: news approach for weeds management. Int. J. Appl. Biol. Pharm. Technol. 2013, 4, 96–114.
Maffei, M.; Camusso, W.; Sacco, S. Effect of Mentha x piperita essential oil and monoterpenes on cucumber root membrane potential. Phytochemistry 2001, 58, 703–707. [CrossRef]
Zunino, M.P.; Zygadlo, J.A. Effect of monoterpenes on lipid oxidation in maize. Planta 2004, 219, 303–309. [PubMed]
Baser, K.H.C.; Buchbauer, G. Handbook of Essential Oils: Science, Technology, and Applications, 2nd ed.; CRC Press: Boca Raton, FL, USA, 2015.
Harikumar, K.G.; Puri, V.; Singh, R.D.; Hanada, K.; Pagano, R.E.; Miller, L.J. Differential Effects of Modification of Membrane Cholesterol and Sphingolipids on the Conformation, Function, and Trafficking of the G Protein-coupled Cholecystokinin Receptor. J. Biol. Chem. 2005, 280, 2176–2185. [CrossRef]
Maxfield, F.R.; Tabas, I. Role of cholesterol and lipid organization in disease. Nature 2005, 438, 612–621. [CrossRef]
Khandelia, H.; Ipsen, J.H.; Mouritsen, O.G. The impact of peptides on lipid membranes. Biochim. Biophys. Acta Biomembr. 2008, 1778, 1528–1536. [CrossRef]
Lee, A.G. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta. 2004, 1666, 62–87. [CrossRef]
Ruysschaert, J.-M.; Lonez, C. Role of lipid microdomains in TLR-mediated signalling. BBA Biomembr. 2015, 1848, 1860–1867. [CrossRef] [PubMed]
Dhifi, W.; Bellili, S.; Jazi, S.; Bahloul, N.; Mnif, W. Essential Oils’ Chemical Characterization and Investigation of Some Biological Activities: A Critical Review. Medicines 2016, 3, 25. [CrossRef] [PubMed]
Altshuler, O.; Abu-Abied, M.; Chaimovitsh, D.; Shechter, A.; Frucht, H.; Dudai, N.; Sadot, E. Enantioselective Effects of (+)-and (−)-Citronellal on Animal and Plant Microtubules. J. Nat. Prod. 2013, 76, 1598–1604. [CrossRef] [PubMed]
Chaimovitsh, D.; Shachter, A.; Abu-Abied, M.; Rubin, B.; Sadot, E.; Dudai, N. Herbicidal Activity of Monoterpenes Is Associated with Disruption of Microtubule Functionality and Membrane Integrity. Weed Sci. 2017, 65, 19–30. [CrossRef]
Cavalieri, A.; Fischer, R.; Larkov, O.; Dudai, N. Enantioselectivity of the Bioconversion of Chiral Citronellal during the Inhibition of Wheat Seeds Germination. Chem. Biodivers. 2014, 11, 419–426. [CrossRef] [PubMed]
Da Silva, A.C.; Lopes, P.M.; De Azevedo, M.M.; Costa, D.C.; Alviano, C.S.; Alviano, D.S. Biological Activities of a-Pinene and β-Pinene Enantiomers. Molecules 2012, 17, 6305–6316. [CrossRef] [PubMed]
Tao, N.; Jia, L.; Zhou, H. Anti-fungal activity of Citrus reticulata Blanco essential oil against Penicillium italicum and Penicillium digitatum. Food Chem. 2014, 153, 265–271. [CrossRef] [PubMed]
Sharma, Y.; Rastogi, S.K.; Perwez, A.; Rizvi, M.A.; Manzoor, N. β-citronellol alters cell surface properties of Candida albicans to influence pathogenicity related traits. Med. Mycol. 2019, 1–14. [CrossRef] [PubMed]
De Oliveira Pereira, F.; Mendes, J.M.; Lima, I.O.; Mota, K.S.; Oliveira, W.A.; Lima Ede, O. Antifungal activity of geraniol and citronellol, two monoterpenes alcohols, against Trichophyton rubrum involves inhibition of ergosterol biosynthesis. Pharm. Biol. 2005, 53, 228–234. [CrossRef]
Lim, S.; Shin, S. Effects of citronellol and thymol on cell membrane composition of Candida albicans. Korean J. Pharmacogn. 2009, 40, 357–364.
Lange, Y.; Ye, J.; Duban, M.-E.; Steck, T.L. Activation of Membrane Cholesterol by 63 Amphipaths. Biochemistry 2009, 48, 8505–8515. [CrossRef] [PubMed]
Kaur, S.; Rana, S.; Pal Singh, H.; Batish, D.; Kohli, R. Citronellol Disrupts Membrane Integrity by Inducing Free Radical Generation. Z. Naturforsch. C. 2011, 66, 260–266. [CrossRef] [PubMed]
Nazzaro, F.; Fratianni, F.; Coppola, R.; De Feo, V. Essential oils and antifungal activity. Pharmaceuticals 2017, 10, 86. [CrossRef] [PubMed]
Zore, G.B.; Thakre, A.D.; Jadhav, S.; Karuppayil, S.M.; Candida, A. Terpenoids inhibit Candida albicans growth by affecting membrane integrity and arrest of cell cycle. Eur. J. Integr. Med. 2011, 18, 1181–1190. [CrossRef] [PubMed]
Singh, S.; Fatima, Z.; Hameed, S. Citronellal-induced disruption of membrane homeostasis in Candida albicans and attenuation of its virulence attributes. Rev. Soc. Bras. Med. Trop. 2016, 49, 465–472. [CrossRef] [PubMed]
Dudai, N.; Larkov, O.; Putievsky, E.; Lerner, H.R.; Ravid, U.; Lewinsohn, E.; Mayer, A.M. Biotransformation of constituents of essential oils by germinating wheat seed. Phytochemistry 2000, 55, 375–382. [CrossRef]
Singh, H.P.; Batish, D.R.; Kaur, S.; Kohli, R.K.; Arora, K. Phytotoxicity of the volatile monoterpene citronellal against some weeds. Zeitschrift fur Naturforsch. Sect. C J. Biosci. 2006, 61, 334–340. [CrossRef]
Ootani, M.A.; Dos Reis, M.R.; Cangussu, A.S.R.; Capone, A.; Fidelis, R.R.; Oliverira, W.; Barros, H.B.; Portella, A.C.F.; De Souza Aguiar, R.W.; Dos Santos, W.F. Phytotoxic effects of essential oils in controlling weed species Digitaria horizontalis and Cenchrus echinatus. Biocatal. Agric. Biotechnol. 2017, 12, 59–65. [CrossRef]
Gill, A.O.; Holley, R.A. Disruption of Escherichia coli, Listeria monocytogenes and Lactobacillus sakei cellular membranes by plant oil aromatics. Int. J. Food Microbiol. 2006, 108, 1–9. [CrossRef]
Shen, S.; Zhang, T.H.; Yuan, Y.; Lin, S.Y.; Xu, J.Y.; Ye, H.Y. Effects of cinnamaldehyde on Escherichia coli and Staphylococcus aureus membrane. Food Control 2015, 47, 196–202. [CrossRef]
He, T.-F.; Zhang, Z.-H.; Zeng, X.-A.; Wang, L.-H.; Brennan, C.S. Determination of membrane disruption and genomic DNA binding of cinnamaldehyde to Escherichia coli by use of microbiological and spectroscopic techniques. J. Photochem. Photobiol. B Biol. 2018, 178, 623–630. [CrossRef] [PubMed]
Di Pasqua, R.; Hoskins, N.; Betts, G.; Mauriello, G. Changes in membrane fatty acids composition of microbial cells induced by addiction of thymol, carvacrol, limonene, cinnamaldehyde, and eugenol in the growing media. J. Agric. Food Chem. 2006, 54, 2745–2749. [CrossRef] [PubMed]
Nowotarska, S.; Nowotarski, K.; Friedman, M.; Situ, C. Effect of Structure on the Interactions between Five Natural Antimicrobial Compounds and Phospholipids of Bacterial Cell Membrane on Model Monolayers. Molecules 2014, 19, 7497–7515. [CrossRef] [PubMed]
Shreaz, S.; Sheikh, R.A.; Rimple, B.; Hashmi, A.A.; Nikhat, M.; Khan, L.A. Anticandidal activity of cinnamaldehyde, its ligand and Ni(II) complex: Effect of increase in ring and side chain. Microb. Pathog. 2010, 49, 75–82. [CrossRef] [PubMed]
Huang, F.; Kong, J.; Ju, J.; Zhang, Y.; Guo, Y.; Cheng, Y.; Qian, H.; Xie, Y.; Yao, W. Membrane damage mechanism contributes to inhibition of trans-cinnamaldehyde on Penicillium italicum using Surface-Enhanced Raman Spectroscopy (SERS). Sci. Rep. 2019, 9, 1–10. [CrossRef] [PubMed]
Chotsaeng, N.; Laosinwattana, C.; Charoenying, P. Inhibitory Effects of a Variety of Aldehydes on Amaranthus tricolor L. and Echinochloa crus-galli (L.) Beauv. Molecules 2018, 23, 471. [CrossRef] [PubMed]
Genva, M.; Lins, L.; Fauconnier, M.L. Penetration of the cinnamon and citronella essential oils components into A. thaliana leaves. 2019; unpublished work.
Furt, F.; Simon-Plas, F.; Mongrand, S. Lipids of the Plant Plasma Membrane; Springer International Publishing: Berlin/Heidelberg, Germany, 2011; pp. 3–30. [CrossRef]
Ducarme, P.; Rahman, M.; Brasseur, R. IMPALA: a simple restraint field to simulate the biological membrane in molecular structure studies. Proteins 1998, 30, 357–371. [CrossRef]
Marsh, D. Lateral pressure in membranes. Biochim. Biophys. Acta Biomembr. 1996, 1286, 183–223. [CrossRef]
Cristani, M.; D’Arrigo, M.; Mandalari, G.; Castelli, F.; Sarpietro, M.G.; Micieli, D.; Venuti, V.; Bisignano, G.; Saija, A.; Trombetta, D. Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J. Agric. Food Chem. 2007, 55, 6300–6308. [CrossRef]
Henry, G.; Deleu, M.; Jourdan, E.; Thonart, P.; Ongena, M. The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune-related defence responses. Cell. Microbiol. 2011, 13, 1824–1837. [CrossRef] [PubMed]
Tsagareli, M.G.; Tsiklauri, N.; Zanotto, K.L.; Carstens, M.I.; Klein, A.H.; Sawyer, C.M.; Gurtskaia, G.; Abzianidze, E.; Carstens, E. Behavioral evidence of thermal hyperalgesia and mechanical allodynia induced by intradermal cinnamaldehyde in rats. Neurosci. Lett. 2010, 473, 233–236. [CrossRef] [PubMed]
Chung, G.; Im, S.T.; Kim, Y.H.; Jung, S.J.; Rhyu, M.R.; Oh, S.B. Activation of transient receptor potential ankyrin 1 by eugenol. Neuroscience 2014, 261, 53–60. [CrossRef] [PubMed]
Namer, B.; Seifert, F.; Handwerker, H.O.; Maihofner, C. TRPA1 and TRPM8 activation in humans: effects of cinnamaldehyde and menthol. Neuroreport 2005, 16, 955–959. [CrossRef] [PubMed]
Tanoh, E.A.; Nea, F.; Kemene, T.K.; Genva, M.; Saive, M.; Tonzibo, F.Z.; Fauconnier, M.L. Antioxidant and Lipoxygenase Inhibitory Activities of Essential Oils from Endemic Plants of Côte d’Ivoire: Zanthoxylum mezoneurispinosum Ake Assi and Zanthoxylum psammophilum Ake Assi. Molecules 2019, 24, 2445. [CrossRef] [PubMed]
Benini, C.; Ringuet, M.; Wathelet, J.P.; Lognay, G.; Du Jardin, P.; Fauconnier, M.L. Variations in the essential oils from ylang-ylang (Cananga odorata [Lam.] Hook f. & Thomson forma genuina) in the Western Indian Ocean islands. Flavour Fragr. J. 2012, 27, 356–366.
Harhour, A.; Brada, M.; Fauconnier, M.-L.; Lognay, G. Chemical Composition and Antioxidant Activity of Algerian Juniperus Phoenicea Essential Oil. Nat. Prod. Sci. 2018, 24, 125. [CrossRef]
Lichiheb, N.; Bedos, C.; Personne, E.; Benoit, P.; Bergheaud, V.; Fanucci, O.; Bouhlel, J.; Barriuso, E. Measuring Leaf Penetration and Volatilization of Chlorothalonil and Epoxiconazole Applied on Wheat Leaves in a Laboratory-Scale Experiment. J. Environ. Qual. 2015, 44, 1782–1790. [CrossRef]
Lins, L.; Brasseur, R.; Malaisse, W.J.; Biesemans, M.; Verheyden, P.; Willem, R. Importance of the hydrophobic energy: Structural determination of a hypoglycemic drug of the meglitinide family by nuclear magnetic resonance and molecular modeling. Biochem. Pharmacol. 1996, 52, 1155–1168. [CrossRef]
Hess, B.; Bekker, H.; Berendsen, M.H.J.C.; Fraaije, J.G.E. LINCS: A Linear Constraint Solver for molecular simulations. J. Comput. Chem. 1997, 18, 1463–1472. [CrossRef]
Malde, A.K.; Zuo, L.; Breeze, M.; Stroet, M.; Poger, D.; Nair, P.C.; Oostenbrink, C.; Mark, A.E. An Automated force field Topology Builder (ATB) and repository: Version 1.0. J. Chem. Theory Comput. 2011, 7, 4026–4037. [CrossRef] [PubMed]
Parrinello, M.; Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method. J. Appl. Phys. 1981, 7182. [CrossRef]
Berger, O.; Edholm, O.; Jähnig, F. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 1997, 72, 2002–2013. [CrossRef]
Bachar, M.; Brunelle, P.; Tieleman, D.P.; Rauk, A. Molecular dynamics simulation of a polyunsaturated lipid bilayer susceptible to lipid peroxidation. J. Phys. Chem. B 2004, 108, 7170–7179. [CrossRef]
Knight, C.J.; Hub, J.S. MemGen: A general web server for the setup of lipid membrane simulation systems. Bioinformatics 2015, 31, 2897–2899. [CrossRef] [PubMed]
Hermans, J.; Berendsen, M.H.J.C.; Van Gunsteren, W.F.; Postma, J.P.M. A consistent empirical potential for water–protein interactions. Biopolymers 1984, 23, 1513–1518. [CrossRef]
Nosé, S. A unified formulation of the constant temperature molecular dynamics methods. J. Chem. Phys. 1984, 81, 511. [CrossRef]
Essmann, U.; Perera, L.; Berkowitz, M.L. A smooth particle mesh Ewald method. J. Chem. Phys. 1995, 103, 8577. [CrossRef]
Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graph. 1996, 14, 33–38. [CrossRef]
Razafindralambo, H.; Dufour, S.; Paquot, M.; Deleu, M. Thermodynamic studies of the binding interactions of surfactin analogues to lipid vesicles. J. Therm. Anal. Calorim. 2009, 95, 817–821. [CrossRef]
Calvez, P.; Bussieres, S.; Eric, D.; Salesse, C. Parameters modulating the maximum insertion pressure of proteins and peptides in lipid monolayers. Biochimie 2009, 91, 718–733. [CrossRef] [PubMed]
Van Bambeke, F.; Kerkhofs, A.; Schanck, A.; Remacle, C.; Sonveaux, E.; Tulkens, P.M.; Mingeot-Leclercq, M.P. Biophysical studies and intracellular destabilization of pH-sensitive liposomes. Lipids 2000, 35, 213–223. [CrossRef] [PubMed]
Cacas, J.-L.; Buré, C.; Grosjean, K.; Gerbeau-Pissot, P.; Lherminier, J.; Rombouts, Y.; Maes, E.; Bossard, C.; Gronnier, J.; Furt, F.; et al. Revisiting plant plasma membrane lipids in tobacco: A focus on sphingolipids. Plant Physiol. 2016, 170, 367–384. [CrossRef] [PubMed]
Maes, C.; Bouquillon, S.; Fauconnier, M.L. Encapsulation of Essential Oils for the Development of Biosourced Pesticides with Controlled Release: A Review. Molecules 2019, 24, 2539. [CrossRef] [PubMed]