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Citral Induces Auxin and Ethylene-Mediated Malformations and Arrests Cell Division in Arabidopsis thaliana Roots

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Abstract

Citral is a linear monoterpene which is present, as a volatile component, in the essential oil of several different aromatic plants. Previous studies have demonstrated the ability of citral to alter the mitotic microtubules of plant cells, especially at low concentrations. The changes to the microtubules may be due to the compound acting directly on the treated root and coleoptile cells or to indirect action through certain phytohormones. This study, performed in Arabidopsis thaliana, analysed the short-term effects of citral on the auxin content and mitotic cells, and the long-term effects of these alterations on root development and ethylene levels. The results of this study show that citral alters auxin content and cell division and has a strong long-term disorganising effect on cell ultra-structure in A. thaliana seedlings. Its effects on cell division, the thickening of the cell wall, the reduction in intercellular communication, and the absence of root hairs confirm that citral is a strong phytotoxic compound, which has persistent effects on root development.

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References

  • Abeles, F. B. 1966. Auxin stimulation of ethylene evolution. Plant Physiol. 41:585–588.

    Article  PubMed  CAS  Google Scholar 

  • Abramson, C. H., Aldana, E., and Sulbaran, E. 2007. Exposure to citral, cinnamon and ruda disrupts the life cycle of a vector of chagas disease. Am. J. Environ. Sci. 3:7–8.

    Article  CAS  Google Scholar 

  • Aouar, L., Chebli, Y., and Geitmann, A. 2010. Morphogenesis of complex plant cell shapes: the mechanical role of crystalline cellulose in growing pollen tubes. Sex. Plant Reprod. 23:15–27.

    Article  PubMed  Google Scholar 

  • Armbruster, B. L., Molin, W. T., and Bugg, M. W. 1991. Effects of the herbicide dithiopyr on cell division in wheat root tips. Pestic. Biochem. Physiol. 39:110–120.

    Article  CAS  Google Scholar 

  • Burton, R. A., Gibeaut, D. M., Bacic, A., Findlay, K., Keith, R., Hamilton, A., Baulcombe, D., and Fincher, G. B. 2000. Virus-induced silencing of a plant cellulose synthase gene. Plant Cell 12:691–706.

    PubMed  CAS  Google Scholar 

  • Chaimovitsh, D., Abu-Abied, M., Belausov, E., Rubin, B., Dudai, N., and Sadot, E. 2010. Microtubules are an intracellular target of the plant terpene citral. Plant J. 61:399–408.

    Article  PubMed  CAS  Google Scholar 

  • Chaimovitsh, D., Rogovoy, O., Altshuler, O., Belausov, E., Abu-Abied, M., Rubin, B., Sadot, E., and Dudai, N. 2012. The relative effect of citral on mitotic microtubules in wheat roots and BY2 cells. Plant Biol. 14:354–364.

    Article  PubMed  CAS  Google Scholar 

  • Cools, T., Iantcheva, A., Maes, S., van den Daele, H., and de Veylder, L. 2010. A replication stress-induced synchronization method for Arabidopsis thaliana root meristems. Plant J. 64:705–714.

    Article  PubMed  CAS  Google Scholar 

  • Dayan, F. E., Romagni, J. G., and Duke, S. O. 2000. Investigating the mode of action of natural phytotoxins. J. Chem. Ecol. 26:2079–2094.

    Article  CAS  Google Scholar 

  • Delfine, S., Csiky, O., Seufert, G., and Loreto, F. 2000. Fumigation with exogenous monoterpenes of a non-isoprenoid-emitting oak (Quercus suber): monoterpene acquisition translocation, and effect of the photosynthetic properties at high temperatures. New Phytol. 146:27–36.

    Article  CAS  Google Scholar 

  • Djiordevic, D., Cercaci, L., Alamed, J., McClements, D. J., and Decker, E. A. 2008. Stability of citral in protein gum Arabic-stabilized oil-in-water emulsions. Food Chem. 106:698–705.

    Article  Google Scholar 

  • Dudai, N., Poljakoff-Mayber, A., Mayer, A. M., Putievsky, E., and Lerner, H. R. 1999. Essential oils as allelochemicals and their potential use as bioherbicides. J. Chem. Ecol. 25:1079–1089.

    Article  CAS  Google Scholar 

  • Echeverrigaray, S., Zacaria, J., and Beltrão, R. 2010. Nematicidal activity of monoterpenoids against the root-knot nematode Meloidogyne incognita. Nematology 100:199–203.

    CAS  Google Scholar 

  • Ehlers, K. and Kollmann, R. 2001. Primary and secondary plasmodesmata: structure, origin, and functioning. Plasmodesmata 216:1–30.

    CAS  Google Scholar 

  • Elsorra, E., Idris, E. E., Bochow, H., Ross, H., and Borriss, R. 2004. Use of Bacillus subtilis as biocontrol agent. VI. Phytohormone like action of culture filtrates prepared from plant growth promoting Bacillus amyloliquefaciens FZB24, FZB42, FZB45 and Bacillus subtilis FZB37. J. Plant Dis. Protect. 111:583–597.

    Google Scholar 

  • Farah, I. O., Trimble, Q., Ndebele, K., and Mawson, A. 2010. Retinoids and citral modulated cell viability, metabolic stability, cell cycle progression and distribution in the a549 lung carcinoma cell line. Biomed. Sci. Instrum. 46:410–421.

    PubMed  Google Scholar 

  • Fusconi, A., Gallo, C., and Camusso, W. 2007. Effects of cadmium on root apical meristems of Pisum sativum L.: Cell viability, cell proliferation and microtubule pattern as suitable markers for assessment of stress pollution. Mutat. Res. 632:9–19.

    Article  PubMed  CAS  Google Scholar 

  • García-Angulo, P., Alonso-Simón, A., Mélida, H., Encina, A., Acebes, J. L., and Álvarez, J. M. 2009. High peroxidase activity and stable changes in the cell wall are related to dichlobenil tolerance. J. Plant Physiol. 166:1229–1240.

    Article  PubMed  Google Scholar 

  • Godard, K.-A., White, R., and Bohlmann, J. 2008. Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69:1838–1849.

    Article  PubMed  CAS  Google Scholar 

  • His, I., Driouich, A., Nicol, F., Jauneau, A., and Höfte, H. 2001. Altered pectin composition in primary cell walls of korrigan, a dwarf mutant of Arabidopsis deficient in a membrane-bound endo-1,4-β-glucanase. Planta 212:348–358.

    Article  PubMed  CAS  Google Scholar 

  • Hogg, B. V., Kacprzyk, J., Molony, E. M., O’Reilly, C., Gallagher, T. F., Gallois, P., and McCabe, P. F. 2011. An in vivo root hair assay for determining rates of apoptotic-like programmed cell death in plants. Plant Methods 7:45–53.

    Article  PubMed  CAS  Google Scholar 

  • Inderjit, H. K. and Kaushik, S. 2005. Cellular evidence of allelopathic interference of benzoic acid to mustard (Brassica juncea L.) seedling growth. Plant Physiol. Biochem. 43:77–81.

    Article  PubMed  Google Scholar 

  • Inderjit, H. K. and Mukerji, G. (eds.) 2006. Allelochemicals: Biological Control of Plant Pathogens and Diseases. Springer, Dordrecht, The Netherlands.

  • Ishii-Iwamoto, E. L., Pergo Coelho, E. M., Reis, B., Moscheta, I. S., and Moacir Bonato, C. 2012. Effects of monoterpenes on physiological processes during seed germination and seedling growth. Curr. Bioact. Compd. 8:50–64.

    Article  CAS  Google Scholar 

  • Jensen, W. A. 1962. Botanical Histochemistry. W.H. Freeman & Co.: San Francisco & London.

  • Kho, Y. O. and Baër, J. 1968. Observing pollen tubes by means of fluorescence light. Euphytica. 17:298–302.

    Google Scholar 

  • Maffei, M., Camusso, W., and Sacco, S. 2001. Effect of Mentha × piperita essential oil and monoterpenes on cucumber root membrane potential. Phytochem 58:703–707.

    Google Scholar 

  • Marcussen, J., Ulvskov, P., Olsen, C. E., and Rajagopal, R. 1989. Preparation and properties of antibodies against indoloacetic acid (IAA)-C5-BSA, a novel ring-coupled IAA antigen, as compared to two other types of IAA-specific antibodies. Plant Physiol. 89:1071–1078.

    Article  PubMed  CAS  Google Scholar 

  • Morrissey, J. P. 2009. Biological Activity of Defence-Related Plant Secondary Metabolites (cap.13), in Plant-derived Natural Products. Anne E. Osbourn, Virginia Lanzotti (Eds.), Springer.

  • Muller, W. H., Lorber, P., Haley, B., and Johnson, K. 1969. Volatile growth inhibitors produced by Salvia leucophylla: effect on oxygen uptake by mitochondrial suspensions. Bull. Torrey Bot. Club 96:89–96.

    Article  CAS  Google Scholar 

  • Pauly, G., Douce, R., and Carde, J. P. 1981. Effects of β-pinene on spinach chloroplast photosynthesis. Z. Pflanzenphysiol. 104:199–206.

    CAS  Google Scholar 

  • Pierik, R., Djakovic-Petrovic, T., Keuskamp, D. H., de Wit, M., and Voesenek, L. A. C. J. 2009. Auxin and ethylene regulate elongation responses to neighbor proximity signals independent of gibberellin and della proteins in Arabidopsis. Plant Physiol. 149:1701–1712.

    Google Scholar 

  • Prasad, M. N. V. and Subhashini, P. 1994. Mimosine-inhibited seed germination, seedling growth, and enzymes of Oryza sativa L. J. Chem. Ecol. 20:1689–1696.

    Article  CAS  Google Scholar 

  • Rahman, A., Ahamed, A., Amakawa, T., Goto, N., and Tsurumi, S. 2001. Chromosaponin I specifically interacts with AUX1 protein in regulating the gravitropic response of Arabidopsis roots. Plant Physiol. 125:990–1000.

    Article  PubMed  CAS  Google Scholar 

  • Reape, T. J. and McCABE, P. F. 2010. Apoptotic-like regulation of programmed cell death in plants. Apoptosis 15:249–256.

    Article  PubMed  CAS  Google Scholar 

  • Rentzsch, S., Podzimska, D., Voegele, A., Imbeck, M., Müller, K., Linkies, A., and Leubner-Metzger, G. 2012. Dose- and tissue-specific interaction of monoterpenes with the gibberellin-mediated release of potato tuber bud dormancy, sprout growth and induction of α-amylases and β-amylases. Planta 235:137–151.

    Article  PubMed  CAS  Google Scholar 

  • Reynolds, E. S. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17:208–212.

    Article  PubMed  CAS  Google Scholar 

  • Roberts, I. N., Lloyd, C. W., and Roberts, K. 1985. Ethylene-induced microtubule reorientations: mediation by helical arrays. Planta 164:439–447.

    Article  Google Scholar 

  • Roberts, A. G. and Oparka, K. J. 2003. Plasmodesmata and the control of symplastic transport. Plant Cell Environ. 26:103–124.

    Article  Google Scholar 

  • Rodov, V., Ben-Yehoshua, S., Fand, D. Q., Kim, J. J., and Ashkenaza, R. 1995. Performed antifungal compounds of lemon fruit: citral and its relation to disease resistance. J. Agric. Food Chem. 43:1057–1061.

    Article  CAS  Google Scholar 

  • Romagni, J. G., Allen, S. N., and Dayan, F. E. 2000. Allelopathic effects of volatile cineoles on two weedy plant species. J. Chem. Ecol. 26:303–313.

    Article  CAS  Google Scholar 

  • Scheller, H. V., Jensen, J. K., Sørensen, S. O., Harhol, T. J., and Geshi, N. 2007. Biosynthesis of pectin. Physiol. Plant. 129:283–295.

    Article  CAS  Google Scholar 

  • Shibaoka, H. 1994. Plant hormone-induced changes in the orientation of cortical microtubules: Alterations in the cross-linking between microtubules and the plasma membrane. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45:527–544.

    Article  CAS  Google Scholar 

  • Schiefelbein, J. W. 2000. Constructing a plant cell. The genetic control of root hair development. Plant Physiol. 124:1525–1531.

    Article  PubMed  CAS  Google Scholar 

  • Somolinos, M., García, D., Condón, S., Mackey, B., and Pagán, R. 2010. Inactivation of Escherichia coli by citral. J. App. Microbiol. 108:1928–1939.

    CAS  Google Scholar 

  • Stepanova, A. N., Yun, J., Likhacheva, A. V., and Alonso, J. M. 2007. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185.

    Article  PubMed  CAS  Google Scholar 

  • Swarup, R., Perry, P., Hagenbeek, D., van der Straeten, D., Beemster, G. T. S. C., Sandberg, G., Bhalerao, R., Ljung, K., and Bennett, M. J. 2007. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196.

    Article  PubMed  CAS  Google Scholar 

  • Vandenbussche, F., Vriezen, W. H., Smalle, J., Laarhoven, L. J. J., Harren, F. J. M., and Van Der Straeten, D. 2003. Ethylene and auxin control the Arabidopsis response to decreased light intensity. Plant Physiol. 133:517–527.

    Article  PubMed  CAS  Google Scholar 

  • Vaughn, K. C., Hoffman, J. C., Hahn, M. G., and Staehelin, L. A. 1996. The herbicide dichlobenil disrupts cell plate formation: inmunogold characterization. Protoplasma 194:117–132.

    Article  CAS  Google Scholar 

  • Yao, N., Eisfelder, B. J., Marvin, J., and Greenberg, J. T. 2004. The mitochondrion—and organelle commonly involved in probrammed cell death in Arabidopsis thaliana. Plant J. 40:596–610.

    Article  PubMed  CAS  Google Scholar 

  • Young, R. E., McFarlane, H. E., Hahn, M. G., Western, T. L., Haughn, G. W., and Samuels, A. L. 2008. Analysis of the Golgi apparatus in Arabidopsis seed coat cells during polarized secretion of pectin-rich mucilage. Plant Cell 20:1623–1638.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, T. and Rost, T. L. 2000. Directional cell-to-cell communication in the Arabidopsis root apical meristem. III. Plasmodesmata turnover and apoptosis in meristem and root cap cells during four weeks after germination. Protoplasma 213:99–107.

    Article  Google Scholar 

  • Zunino, M. P. and Zygadlo, J. A. 2004. Effect of monoterpenes on lipid peroxidation in maize. Planta 219:303–309.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors especially thank Jesús Méndez and Inés Pazos from the Central Research Services of the University of Vigo (CACTI) for technical assistance on all the microscopic analyses. This research was supported by the Regional Government of Galicia through Project No. 10PXIB310261PR and a grant to Elisa Graña, and by the Spanish Ministry of Science and Technology AGL2010-17885 through a grant to Carla Díaz.

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Authors and Affiliations

  1. Department of Plant Biology and Soil Science, University of Vigo, Campus Lagoas-Marcosende s/n, 36310, Vigo, Spain

    E. Graña, C. Díaz-Tielas, M. J. Reigosa & A. M. Sánchez-Moreiras

  2. Misión Biológica de Galicia (CSIC), PO Box 28, 36080, Pontevedra, Spain

    T. Sotelo

  3. Dipartimento di Biotecnologie per il Monitoraggio Agro-Alimentare ed Ambientale (BIOMAA), Università Mediterranea di Reggio Calabria, Salita Melissari, Reggio Calabria, RC, Italy

    F. Araniti

  4. Department of Plant Physiology, Warsaw University of Life Sciences-SGGW, Nowoursynowska 159, 02-776, Warsaw, Poland

    U. Krasuska & R. Bogatek

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  1. E. Graña
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Correspondence to A. M. Sánchez-Moreiras.

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Graña, E., Sotelo, T., Díaz-Tielas, C. et al. Citral Induces Auxin and Ethylene-Mediated Malformations and Arrests Cell Division in Arabidopsis thaliana Roots. J Chem Ecol 39, 271–282 (2013). https://doi.org/10.1007/s10886-013-0250-y

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