[en] Oxylipins are lipid-derived molecules that are ubiquitous in eukaryotes and whose functions in plant physiology have been widely reported. They appear to play a major role in plant immunity by orchestrating reactive oxygen species (ROS) and hormone-dependent signalling pathways. The present work focuses on the specific case of fatty acid hydroperoxides (HPOs). Although some studies report their potential use as exogenous biocontrol agents for plant protection, evaluation of their efficiency in planta is lacking and no information is available about their mechanism of action. In this work, the potential of 13(S)-hydroperoxy-(9Z,11E)-octadecadienoic acid (13-HPOD) and 13(S)-hydroperoxy-(9Z,11E,15Z)-octadecatrienoic acid (13-HPOT), as plant defence elicitors and the underlying mechanism of action are investigated. Arabidopsis thaliana leaf resistance to Botrytis cinerea was observed after root application with HPOs. They also activate early immunity-related defence responses, like ROS. As previous studies have demonstrated their ability to interact with plant plasma membranes (PPM), we have further investigated the effects of HPOs on biomimetic PPM structure using complementary biophysics tools. Results show that HPO insertion into PPM impacts its global structure without solubilizing it. Relationship between biological assays and biophysical analysis suggests that lipid amphiphilic elicitors that directly act on membrane lipids might trigger early plant defence events.
Aranda, F.J., Espuny, M.J., Marqués, A., Teruel, J.A., Manresa, Á. & Ortiz, A. (2007) Thermodynamics of the interaction of a dirhamnolipid biosurfactant secreted by Pseudomonas aeruginosa with phospholipid membranes. Langmuir, 23, 2700–2705.
van Aubel, G., Cambier, P., Dieu, M., Van & Cutsem, P. (2016) Plant immunity induced by COS-OGA elicitor is a cumulative process that involves salicylic acid. Plant Science, 247, 60–70.
Bahar, O., Mordukhovich, G., Luu, D.D., Schwessinger, B., Daudi, A., Jehle, A.K. et al. (2016) Bacterial Outer Membrane Vesicles Induce Plant Immune Responses. Molecular Plant-Microbe Interactions, 29, 374–384.
Baker, C.J. & Mock, N.M. (2004) A method to detect oxidative stress by monitoring changes in the extracellular antioxidant capacity in plant suspension cells. Physiological and Molecular Plant Pathology, 64, 255–261.
Bartlett, G.R. (1958) Calorimetric assay phosphorylated for free glyceric acids. Journal of Biological Chemistry, 234, 469–471.
Blée, E. (2002) Impact of phyto-oxylipins in plant defense. Trends in Plant Science, 7, 315–321.
Boller, T. & Felix, G. (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology, 60, 379–406.
Cabrera, J., Boland, A., Cambier, P., Frettinger, P., Van & Cutsem, P. (2010) Chitosan oligosaccharides modulate the supramolecular conformation and the biological activity of oligogalacturonides in Arabidopsis. Glycobiology, 20, 775–786.
Camejo, D., Guzmán-cedeño, A., Vera-macias, L. & Jiménez, A. (2019) Oxidative post-translational modi fi cations controlling plant-pathogen interaction. Plant Physiology and Biochemistry, 144, 110–117.
Carvalho, F.P. (2017) Pesticides, environment, and food safety. Food and Energy Security, 6, 48–60.
Clinckemaillie, A., Decroës, A., van Aubel, G., Carrola dos Santos, S., Renard, M.E., Van Cutsem, P. et al. (2017) The novel elicitor COS-OGA enhances potato resistance to late blight. Plant Pathology, 66, 818–825.
Come, B., Donato, M., Potenza, L.F., Mariani, P., Itri, R. & Spinozzi, F. (2021) The intriguing role of rhamnolipids on plasma membrane remodelling: from lipid rafts to membrane budding. Journal of Colloid and Interface Science, 582, 669–677.
Deboever, E., Deleu, M., Mongrand, S., Lins, L. & Fauconnier, M.-L. (2020) Plant–pathogen interactions: underestimated roles of phyto-oxylipins. Trends in Plant Science, 25, 22–34.
Deleu, M., Deboever, E., Nasir, M.N., Crowet, J.-M., Dauchez, M., Ongena, M. et al. (2019) Linoleic and linolenic acid hydroperoxides interact differentially with biomimetic plant membranes in a lipid specific manner. Colloids and Surfaces B: Biointerfaces, 175, 384–391.
Deleu, M., Lorent, J., Lins, L., Brasseur, R., Braun, N. & El Kirat, K. et al. (2013) Effects of surfactin on membrane models displaying lipid phase separation. Biochimica et Biophysica Acta Biomembranes, 1828, 801–815.
Du, J., Verzaux, E., Chaparro-Garcia, A., Bijsterbosch, G., Keizer, L.C. & Zhou, J. et al. (2015) Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nature Plants, 1, 1–5.
Dufrêne, Y.F. & Lee, G.U. (2000) Advances in the characterization of supported lipid films with the atomic force microscope. Biochimica et Biophysica Acta—Biomembranes, 1509, 14–41.
Fauconnier, M.L. & Marlier, M. (1996) An efficient procedure for the production of fatty acid hydroperoxides from hydrolyzed flax seed oil and soybean lipoxygenase. Biotechnology Techniques, 10, 839–844.
Fu, F.N. & Singh, B.R. (1999) Calcein permeability of liposomes mediated by type a botulinum neurotoxin and its light and heavy chains. Journal of Protein Chemistry, 18, 701–707.
Furlan, L., Laurin, Y., Botcazon, C., Rodr, N. & Buchoux, S. (2020) Contributions and limitations of biophysical approaches to study of the interactions between amphiphilic molecules and the plant. Plants, 9, 1–24.
Gay, H. (2012) Before and after silent spring: from chemical pesticides to biological control and integrated pest management-Britain, 1945-1980. Ambix, 59, 88–108.
Genva, M., Obounou Akong, F., Andersson, M.X., Deleu, M., Lins, L. & Fauconnier, M.L. (2019) New insights into the biosynthesis of esterified oxylipins and their involvement in plant defense and developmental mechanisms. Phytochemistry Reviews, 8, 343–359.
Gerbeau-Pissot, P., Der, C., Thomas, D., Anca, I.A., Grosjean, K., Roche, Y. et al. (2014) Modification of plasma membrane organization in tobacco cells elicited by cryptogein. Plant Physiology, 164, 273–286.
Gómez-Gómez, L. & Boller, T. (2002) Flagellin perception: a paradigm for innate immunity. Trends in Plant Science, 7, 251–256.
Granér, G., Hamberg, M. & Meijer, J. (2003) Screening of oxylipins for control of oilseed rape (Brassica napus) fungal pathogens. Phytochemistry, 63, 89–95.
Gronnier, J., Gerbeau-Pissot, P., Germain, V., Mongrand, S. & Simon-Plas, F. (2018) Divide and rule: plant plasma membrane organization. Trends in Plant Science, 23, 899–917.
Gronnier, J., Germain, V., Gouguet, P., Cacas, J.L. & Mongrand, S. (2016) GIPC: glycosyl inositol phospho ceramides, the major sphingolipids on earth. Plant Signaling and Behavior, 11, 1–7.
Haba, E., Pinazo, A., Pons, R., Pérez, L. & Manresa, A. (2014) Complex rhamnolipid mixture characterization and its influence on DPPC bilayer organization. Biochimica et Biophysica Acta Biomembranes, 1838, 776–783.
Harmel, N., Delaplace, P., Blée, E., du Jardin, P. & Fauconnier, M.L. (2007) Myzus persicae Sulzer aphid contains oxylipins that originate from phloem sap. Journal of Plant Interactions, 2, 31–40.
Harris, F.M., Best, K.B. & Bell, J.D. (2002) Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order. Biochimica et Biophysica Acta Biomembranes, 1565, 123–128.
Henry, G., Deleu, M., Jourdan, E., Thonart, P. & Ongena, M. (2011) The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune-related defence responses. Cellular Microbiology, 13, 1824–1837.
Henry, G., Thonart, P. & Ongena, M. (2012) PAMPs, MAMPs, DAMPs and others: an update on the diversity of plant immunity elicitors. Biotechnology, Agronomy, Society and Environment, 16, 12.
Hernández, A.F., Parrón, T., Tsatsakis, A.M., Requena, M., Alarcón, R. & López-Guarnido, O. (2013) Toxic effects of pesticide mixtures at a molecular level: their relevance to human health. Toxicology, 307, 136–145.
Herzog, M., Tiso, T., Blank, L.M. & Winter, R. (2020) Interaction of rhamnolipids with model biomembranes of varying complexity. Biochimica et Biophysica Acta—Biomembranes, 1862, 183431.
Jogaiah, S., Govind, S.R. & Shetty, H.S. (2019) Role of oomycete elicitors in plant defense signaling. bioactive molecules in plant defense. Springer International Publishing. pp. 59–74.
Jourdan, E., Henry, G., Duby, F., Dommes, J., Barthélemy, J.P., Thonart, P. et al. (2009) Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Molecular Plant-Microbe Interactions, 22, 456–468.
Khonon, M.A.R., Okuma, E., Hossain, M.O., Munemasa, S., Uraji, M., Nakamura, Y. et al. (2011) Involvement of extracellular oxidative burst in salicylic acid-induced stomatal closure in Arabidopsis. Plant Cell and Environment, 34, 434–443.
Koutsioubas, A. (2016) Combined coarse-grained molecular dynamics and neutron ref ectivity characterization of supported lipid membranes. The Journal of Physical Chemistry, 120, 11474–11483.
Koutsioubas, A., Appavou, M.S. & Lairez, D. (2017) Time-resolved neutron reflectivity during supported membrane formation by vesicle fusion. Langmuir, 33, 10598–10605.
Lebecque, S., Lins, L., Dayan, F.E. & Fauconnier, M. (2019) Interactions between natural herbicides and lipid bilayers mimicking the plant plasma membrane. Frontiers in Pharmacology, 10, 1–11.
Ledoux, Q., Van Cutsem, P., Markό, I.E. & Veys, P. (2014) Specific localization and measurement of hydrogen peroxide in Arabidopsis thaliana cell suspensions and protoplasts elicited by COS-OGA. Plant Signaling & Behavior, 9, 1–6.
Luzuriaga-Loaiza, W.P., Schellenberger, R., De Gaetano, Y. et al. (2018) Synthetic Rhamnolipid Bolaforms trigger an innate immune response in Arabidopsis thaliana. Scientific Reports, 8, 1–13.
Ma, Z., Ongena, M. & Höfte, M. (2017) The cyclic lipopeptide orfamide induces systemic resistance in rice to Cochliobolus miyabeanus but not to Magnaporthe oryzae. Plant Cell Reports, 36, 1731–1746.
Malik, A.N.A., Kumar, I.S. & Nadarajah, K. (2020) Elicitor and receptor molecules: orchestrators of plant defense and immunity. International Journal of Molecular Sciences, 21, 963–997.
Mattauch, S., Koutsioubas, A., Ru, U., Korolkov, D., Fracassi, V., Daemen, J. et al. (2018) The high-intensity reflectometer of the Jülich Centre for Neutron Science: MARIA research papers. Journal of Applied Cristallography, 51, 1–9.
Meindl, T., Boller, T. & Felix, G. (2000) The bacterial elicitor flagellin activates its receptor in tomato cells according to the address-message concept. Plant Cell, 12, 1783–1794.
Mingeot-Leclercq, M.P., Deleu, M., Brasseur, R. & Dufrêne, Y.F. (2008) Atomic force microscopy of supported lipid bilayers. Nature Protocols, 3, 1654–1659.
Mittler, R. (2017) ROS are good. Trends in Plant Science, 22, 11–19.
Monnier, N., Furlan, A., Botcazon, C., Dahi, A., Mongelard, G., Cordelier, S. et al. (2018) Rhamnolipids from Pseudomonas aeruginosa are elicitors triggering Brassica napus protection against Botrytis cinerea without physiological disorders. Frontiers in Plant Science, 9, 1–14.
Nelson, A. (2006) Co-refinement of multiple-contrast neutron/X-ray reflectivity data using MOTOFIT. Journal of Applied Cristallography, 39, 273–276.
Névot, L. & Croce, P. (1980) Caractérisation des surfaces par réflexion rasante de rayons X. Application à l'étude du polissage de quelques verres silicates. Revue de Physique Appliquée, 15, 761–779.
Ngou, B.P.M., Ahn, H.K., Ding, P. & Jones, J.D.G. (2021a) Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature, 592, 110–115.
Ngou, B.P.M., Jones, J.D.G. & Ding, P. (2021b) Plant immune networks. Trends in Plant Science, 444, 1–19.
Nimchuk, Z., Eulgem, T., Holt, B.F. & Dangl, J.L. (2003) Recognition and response in the plant immune system. Annual Review of Genetics, 37, 579–609.
Nishad, R., Ahmed, T., Rahman, V.J. & Kareem, A. (2020) Modulation of plant defense system in response to microbial interactions. Frontiers in Microbiology, 11, 1–13.
Ongena, M., Daayf, F., Jacques, P., Thonart, P., Benhamou, N., Paulitz, T.C. et al. (2000) Systemic induction of phytoalexins in cucumber in response to treatments with fluorescent pseudomonads. Plant Pathology, 49, 523–530.
Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B. et al. (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environmental Microbiology, 9, 1084–1090.
Parasassi, T. & Gratton, E. (1995) Membrane lipid domains and dynamics as detected by Laurdan fluorescence. Journal of Fluorescence, 5, 59–69.
Parasassi, T., De Stasio, G., Ravagnan, G., Rusch, R.M. & Gratton, E. (1991) Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of Laurdan fluorescence. Biophysical Journal, 60, 179–189.
Parasassi, T., Di Stefano, M., Ravagnan, G., Sapora, O. & Gratton, E. (1992) Membrane aging during cell growth ascertained by laurdan generalized polarization. Experimental Cell Research, 202, 432–439.
Prost, I., Dhondt, S., Rothe, G., Vicente, J., Rodriguez, M. J. & Kift, N. et al. (2005) Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiology, 139, 1902–1913.
Pršić, J. & Ongena, M. (2020) Elicitors of plant immunity triggered by beneficial bacteria. Frontiers in Plant Science, 11, 1–12.
Rondelli, V., Brocca, P., Motta, S., Messa, M., Colombo, L., Salmona, M. et al. (2016) Amyloidβ Peptides in interaction with raft-mime model membranes: a neutron reflectivity insight. Scientific Reports, 6, 1–11.
Rondelli, V., Cola, E.D.i, Koutsioubas, A., Alongi, J., Ferruti, P., Ranucci, E. et al. (2019) Mucin thin layers: a model for mucus-covered tissues. International Journal of Molecular Sciences, 20, 1–15.
Rondelli, V., Del Favero, E., Brocca, P., Fragneto, G., Trapp, M. & Mauri, L. et al. (2018) Directional K + channel insertion in a single phospholipid bilayer: neutron reflectometry and electrophysiology in the joint exploration of a model membrane functional platform. Biochimica et Biophysica Acta—General Subjects, 1862, 1742–1750.
Sanchez, S.A., Tricerri, M.A., Gunther, G. & Gratton, E. (2007) Laurdan generalized polarization: from cuvette to microscope. Modern Research and Educational Topics in Microscopy, 1007–1014.
Sandor, R., Der, C., Grosjean, K., Anca, I., Noirot, E., Leborgne-Castel, N. et al. (2016) Plasma membrane order and fluidity are diversely triggered by elicitors of plant defence. Journal of Experimental Botany, 67, 5173–5185.
Sautrey, G., Zimmermann, L., Deleu, M., Delbar, A., Machado, L.S., Jeannot, K. et al. (2014) New amphiphilic neamine derivatives active against resistant Pseudomonas aeruginosa and their interactions with lipopolysaccharides. Antimicrobial Agents and Chemotherapy, 58, 4420–4430.
Schellenberger, R., Crouzet, J., Nickzad, A., Kutschera, A., Gerster, T. & Borie, N. et al. (2021) The bacterial virulence factors rhamnolipids and their (R)-3-hydroxyalkanoate precursors activate Arabidopsis innate immunity through two independent mechanisms. bioRxiv.
Schellenberger, R., Touchard, M., Clément, C., Baillieul, F., Cordelier, S., Crouzet, J. et al. (2019) Apoplastic invasion patterns triggering plant immunity: plasma membrane sensing at the frontline. Molecular Plant Pathology, 20, 1602–1616.
Shang-Guan, K., Wang, M., Htwe, N.M.P.S., Li, Y., Qi, F., Zhang, D. et al. (2018) Lipopolysaccharides trigger two successive bursts of reactive oxygen species at distinct cellular locations. Plant Physiology, 176, 2543–2556.
Shimanouchi, T., Ishii, H., Yoshimoto, N., Umakoshi, H. & Kuboi, R. (2009) Calcein permeation across phosphatidylcholine bilayer membrane: Effects of membrane fluidity, liposome size, and immobilization. Colloids and Surfaces B: Biointerfaces, 73, 156–160.
Smith, J.M. & Heese, A. (2014) Rapid bioassay to measure early reactive oxygen species production in Arabidopsis leave tissue in response to living Pseudomonas syringae. Plant Methods, 10, 1–9.
Song, W., Forderer, A., Yu, D. & Chai, J. (2021) Structural biology of plant defence. New Phytologist, 229, 692–711.
Thakur, M. & Sohal, B.S. (2013) Role of elicitors in inducing resistance in plants against pathogen infection: a review. ISRN. Biochemistry, 2013, 1–10.
Wang, K.-D., Borrego, E.J., Kenerley, C.M. & Kolomiets, M.V. (2020) Oxylipins other than jasmonic acid are xylem-resident signals regulating systemic resistance induced by Trichoderma virens in maize. The Plant cell, 32, 166–185.
Wang, S., Wang, Z., Zhang, Y., Wang, J. & Guo, R. (2013) Pesticide residues in market foods in Shaanxi Province of China in 2010. Food Chemistry, 138, 2016–2025.
Wasternack, C. & Feussner, I. (2018) The oxylipin pathways: biochemistry and function. Annual Review of Plant Biology, 69, 363–386.
Wasternack, C. & Strnad, M. (2018) Jasmonates: news on occurrence, biosynthesis, metabolism and action of an ancient group of signaling compounds. International Journal of Molecular Sciences, 19, 2539.
Yu, X., Feng, B., He, P. & Shan, L. (2017) From chaos to harmony: responses and signaling upon microbial pattern recognition. Annual Review of Phytopathology, 55, 109–137.
Zaid, A. & Wani, S.H. (2019) Reactive oxygen species generation, scavenging and signaling in plant defense responses. Bioactive Molecules in Plant Defense. Springer International Publishing. pp. 111–132.
Zhao, J.L., Zhou, L.G. & Wu, J.Y. (2010) Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Applied Microbiology and Biotechnology, 87, 137–144.