[en] Abstract
Allelopathy can provide sustainable alternatives to herbicides because it is based on specific signals rather than generic toxicity. We show that the allelopathic activity of Spearmint and Watermint is linked with their main compounds, (−)-carvone and (+)-menthofuran, both deriving from (−)-limonene. Germination of Poppy and Cress, and root growth of Arabidopsis thaliana are inhibited by very low concentrations of (−)-carvone, acting even through the gas phase. (+)-Menthofuran is active as well, but at lower efficacy. Using fluorescently tagged marker lines in tobacco BY-2 cells and Arabidopsis roots, we demonstrate a rapid degradation of microtubules and a remodeling of actin filaments in response to (−)-carvone and, to a milder extent, to (+)-menthofuran. This cytoskeletal response is followed by cell death. By means of a Root Chip system, we can follow the tissue dependent response of the cytoskeleton and show a cell-type dependent gradient of sensitivity between meristem and distal elongation zone, accompanied by programmed cell death.
Disciplines :
Agriculture & agronomy Chemistry
Author, co-author :
Hering, Nathalie; Joseph Gottlieb Kölreuter Institute for Plant Sciences (JKIP) , Karlsruhe Institute of Technology, 76131 Karlsruhe, Germany
Schmit, Anne-Catherine; Université de Strasbourg Institut de biologie moléculaire des plantes (IBMP), CNRS, , 67084 Strasbourg, France
Herzog, Etienne; Université de Strasbourg Institut de biologie moléculaire des plantes (IBMP), CNRS, , 67084 Strasbourg, France
Corbin, Louis-Thibault; Université de Strasbourg Institut de biologie moléculaire des plantes (IBMP), CNRS, , 67084 Strasbourg, France
Schmidt-Speicher, Leona; Institute of Microstructure Technology (IMT) , Karlsruhe Institute of Technology, 76344 Eggenstein-Leopoldshafen, Germany
Ahrens, Ralf; Institute of Microstructure Technology (IMT) , Karlsruhe Institute of Technology, 76344 Eggenstein-Leopoldshafen, Germany
Fauconnier, Marie-Laure ; Université de Liège - ULiège > TERRA Research Centre > Chemistry for Sustainable Food and Environmental Systems (CSFES)
Nick, Peter; Joseph Gottlieb Kölreuter Institute for Plant Sciences (JKIP) , Karlsruhe Institute of Technology, 76131 Karlsruhe, Germany
Molisch H. Der Einfluß einer Pflanze auf die andere. Allelopathie. Jena: Gustav Fischer; 1937.
Einhellig FA. Allelopathy: current status and future goals. ACS Symp Ser. 1995;582:1–24.
Rizvi SJH, Haque H, Singh VK et al. A discipline called allelopathy. In: Rizvi SJH, Rizvi V, eds. Allelopathy: Basic and applied aspects. Springer: Dordrecht, 1992,1–10.
Von Bertalanffy L. The theory of open Systems in Physics and Biology. Science. 1950;111:23–9.
Karban R, Maron J, Felton GW et al. Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants. Oikos. 2003;100:325–32.
Kopaczyk JM, Warguła J, Jelonek T. The variability of terpenes in conifers under developmental and environmental stimuli. Environ Exp Bot. 2020;180:104197.
Sharkey TD, Singaas EL. Why plants emit isoprene. Nature. 1995;374:769.
Lee GW, Lee S, Chung MS et al. Rice terpene synthase 20 (OsTPS20) plays an important role in producing terpene volatiles in response to abiotic stresses. Protoplasma. 2015;252:997–1007.
Wink M. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry. 2003;64: 3–19.
Gurib-Fakim A. Medicinal plants: traditions of yesterday and drugs of tomorrow. Mol Asp Med. 2006;27:1–93.
Raja RR. Medicinally potential plants of Labiatae (Lamiaceae) family: An overview. Res J Med Plants. 2012;6:203–13.
Drew BT, Sytsma KJ. Phylogenetics, biogeography, and staminal evolution in the tribe Mentheae (Lamiaceae). Am J Bot. 2012;99: 933–53.
Tzima K, Brunton NP, Rai DK. Qualitative and quantitative analysis of polyphenols in Lamiaceae plants - a review. Plan Theory. 2018;7:25.
Gobert V, Moja S, Taberlet P et al. Heterogeneity of three molecular data partition phylogenies of mints related to M. × piperita (mentha; Lamiaceae). Plant Biol. 2006;8:470–85.
Lange BM, Srividya N. Enzymology of monoterpene functionalization in glandular trichomes. J Exp Bot. 2019;70:1095–108.
Mint Evolutionary Genomics Consortium. Phylogenomic Mining of the Mints Reveals Multiple Mechanisms Contributing to the evolution of chemical diversity in Lamiaceae. Mol Plant. 2018;11: 1084–96.
Tafrihi M, Imran M, Tufail T et al. The wonderful activities of the genus mentha: not only antioxidant properties. Molecules. 2021;26:1118.
Azirak S, Karaman S. Allelopathic effect of some essential oils and components on germination of weed species. Acta Agric Scand Sect B Soil Plant Sci. 2008;58:88–92.
Puig CG, Reigosa MJ, Valentão P et al. Unravelling the bioherbicide potential of Eucalyptus globulus Labill: biochemistry and effects of its aqueous extract. PLoS One. 2018;13:e0192872.
Sarheed M, Schärer HJ, Wang-Müller QY et al. Signal, not poison – horsemint essential oil for weed control. Agriculture. 2023;13:712.
Hamada T. Chapter one - microtubule organization and microtubule-associated proteins in plant cells. Int Rev Cell Mol Biol. 2014;312:1–52.
Graña E, Costas-Gil A, Longueira S et al. Auxin-like effects of the natural coumarin scopoletin on Arabidopsis cell structure and morphology. J Plant Physiol. 2017;218:45–55.
Rudrappa T, Bonsall J, Gallagher JL et al. Root-secreted allelochemical in the noxious weed Phragmites australis deploys a reactive oxygen species response and microtubule assembly disruption to execute rhizotoxicity. J Chem Ecol. 2007;33: 1898–918.
López-González D, Costas-Gil A, Reigosa MJ et al. A natural indole alkaloid, norharmane, affects PIN expression patterns and compromises root growth in Arabidopsis thaliana. Plant Physiol Biochem. 2020;151:378–90.
Araniti F, Graña E, Krasuska U et al. Loss of gravitropism in farnesene-treated arabidopsis is due to microtubule malformations related to hormonal and ROS unbalance. PLoS One. 2016;11:e0160202.
Sarheed MM, Rajabi F, Kunert M et al. Cellular base of mint Allelopathy: menthone affects plant microtubules. Front Plant Sci. 2020;11:546345.
Chaimovitsh D, Abu-Abied M, Belausov E et al. Microtubules are an intracellular target of the plant terpene citral. Plant J. 2010;61: 399–408.
Chaimovitsh D, Rogovoy O, Altshuler O et al. The relative effect of citral on mitotic microtubules in wheat roots and BY2 cells. Plant Biol. 2012;14:354–64.
Elliott A, Shaw SL. Update: plant cortical microtubule arrays. Plant Physiol. 2018;176:94–105.
Hart JW, Sabnis DD. Colchicine and plant microtubules: a critical evaluation. Commentaries in Plant Science. 2013;2:51–60.
Morejohn LC, Fosket DE. The biochemistry of compounds with anti-microtubule activity in plant cells. Pharmacol Ther. 1991;51: 217–30.
Peier AM, Moqrich A, Hergarden AC et al. A TRP channel that senses cold stimuli and menthol. Cell. 2002;108:705–15.
Nagashima A, Higaki T, Koeduka T et al. Transcriptional regulators involved in responses to volatile organic compounds in plants. J Biol Chem. 2019;294:2256–66.
Pauwels L, Barbero GF, Geerinck J et al. NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature. 2010;464: 788–91.
An C, Deng L, Zhai H et al. Regulation of jasmonate signaling by reversible acetylation of TOPLESS in Arabidopsis. Mol Plant. 2022;15:1329–46.
Frank L, Wenig M, Ghirardo A et al. Isoprene and β-caryophyllene confer plant resistance via different plant internal signalling pathways. Plant Cell Environ. 2021;44:1151–64.
Lee JE, Golz JF. Diverse roles of Groucho/Tup1 co-repressors in plant growth and development. Plant Signal Behav. 2012;7:86–92.
Pérez-Porras F, Torres-Sánchez J, López-Granados F et al. Early and on-ground image-based detection of poppy (Papaver rhoeas) in wheat using YOLO architectures. Weed Sci. 2023;71:50–8.
Gaff DF, Okong’o-Ogola O. The use of non-permeating pigments for testing the survival of cells. J Exp Bot. 1971;22:756–8.
Rounds CM, Lubeck E, Hepler PK et al. Propidium iodide competes with Ca2+ to label pectin in pollen tubes and Arabidopsis root hairs. Plant Physiol. 2011;157:175–87.
Combellack JH. Herbicide application: a review of ground application techniques. Crop Prot. 1984;3:9–34.
Chaimovitsh D, Shachter A, Abu-Abied M et al. Herbicidal activity of monoterpenes is associated with disruption of microtubule functionality and membrane integrity. Weed Sci. 2017;65: 19–30.
Mahmoud SS, Croteau RB. Menthofuran regulates essential oil biosynthesis in peppermint by controlling a downstream monoterpene reductase. Proc Natl Acad Sci. 2003;100:14481–6.
Gong P, Khattab I, Kaźmierczak A et al. Two ways to die: species dependent PCD modes in grapevine cells. Plant Sci. 2023;332:111695.
Zhang KX, Shi WJ, Zheng X et al. A rice tubulin tyrosine ligase like 12 regulates phospholipase D activity and tubulin synthesis. Plant Sci. 2022;316:111155.
Kumar N. Taxol-induced polymerization of purified tubulin. Mechanism of action. J Biol Chem. 1981;256:10435–41.
Koselski M, Tre̢bacz K, Dziubinska H. Vacuolar ion channels in the liverwort Marchantia polymorpha: influence of ion channel inhibitors. Planta. 2017;245:1049–60.
Ebihara L, Hall JE, Macdonald RC et al. Effect of benzyl alcohol on lipid bilayers-comparison of bilayer systems. Biophys J. 1979;28: 185–96.
Lyman GH, Preisler HD, Papahadjopoulos D. Membrane action of DMSO and other chemical inducers of friend leukaemic cell differentiation. Nature. 1976;262:360–3.
Krtková J, Benáková M, Schwarzerová K. Multifunctional microtubule-associated proteins in plants. Front Plant Sci. 2016;7:474.
Ge X, Huang Z, Tian J et al. S-(+)-carvone/HPβCD inclusion complex: preparation, characterization and its application as a new sprout suppressant during potato storage. Food Chemistry Advances. 2022;1:100100.
Eggenberger K, Sanyal P, Hundt S et al. Challenge integrity: the cell-permeating peptide BP100 interferes with the actin-auxin oscillator. Plant Cell Physiol. 2017;58:71–85.
Coll NS, Vercammen D, Smidler A et al. Arabidopsis type I Meta-caspases control cell death. Science. 2010;330:1393–7.
Fasulo L, Ugolini G, Visintin M et al. The neuronal microtubule-associated protein tau is a substrate for caspase-3 and an effector of apoptosis. J Neurochem. 2000;75:624–33.
Kaźmierczak A, Siatkowska E, Li R et al. Kinetin induces microtubular breakdown, cell cycle arrest and programmed cell death in tobacco BY-2 cells. Protoplasma. 2023;260:349–69.
Ketelaar T, Voss C, Dimmock SA et al. Arabidopsis homologues of the autophagy protein Atg8 are a novel family of microtubule binding proteins. FEBS Lett. 2004;567:302–6.
Zientara-Rytter K, Sirko A. Selective autophagy receptor Joka2 co-localizes with cytoskeleton in plant cells. Plant Signal Behav. 2014;9:e28523.
Nakamura M, Naoi K, Shoji T et al. Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol. 2004;45:1330–4.
Nagata T, Nemoto Y, Hasezawa S. Tobacco BY-2 cell line as the “HeLa”cell in the cell biology of higher plants. Int Rev Cytol. 1992;132:1–30.
Kumagai F, Yoneda A, Tomida T et al. Fate of nascent microtubules organized at the M/G1 interface, as visualized by synchronized tobacco BY-2 cells stably expressing GFP-tubulin: time-sequence observations of the reorganization of cortical microtubules in living plant cells. Plant Cell Physiol. 2001;42: 723–32.
Sano T, Higaki T, Oda Y et al. Appearance of actin microfilament ‘twin peaks’in mitosis and their function in cell plate formation, as visualized in tobacco BY-2 cells expressing GFP–fimbrin. Plant J. 2005;44:595–605.
Maisch J, Nick P. Actin is involved in auxin-dependent patterning. Plant Physiol. 2007;143:1695–704.
Finkbeiner T, Manz C, Raorane ML et al. A modular microf luidic bioreactor to investigate plant cell-cell interactions. Protoplasma. 2022;259:173–86.
Kühn S, Liu Q, Eing C et al. Nanosecond electric pulses target to a plant-specific kinesin at the plasma membrane. J Membr Biol. 2013;246:927–38.
