Advertisement

Journal of Chemical Ecology

, Volume 39, Issue 2, pp 271–282 | Cite as

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

  • E. Graña
  • T. Sotelo
  • C. Díaz-Tielas
  • F. Araniti
  • U. Krasuska
  • R. Bogatek
  • M. J. Reigosa
  • A. M. Sánchez-Moreiras
Article

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.

Keywords

Terpenoid Phytotoxicity Mitotic index Pectin content Long-term effects Mode of action 

Notes

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.

References

  1. Abeles, F. B. 1966. Auxin stimulation of ethylene evolution. Plant Physiol. 41:585–588.PubMedCrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.PubMedGoogle Scholar
  6. 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.PubMedCrossRefGoogle Scholar
  7. 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.PubMedCrossRefGoogle Scholar
  8. 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.PubMedCrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. Echeverrigaray, S., Zacaria, J., and Beltrão, R. 2010. Nematicidal activity of monoterpenoids against the root-knot nematode Meloidogyne incognita. Nematology 100:199–203.Google Scholar
  14. Ehlers, K. and Kollmann, R. 2001. Primary and secondary plasmodesmata: structure, origin, and functioning. Plasmodesmata 216:1–30.Google Scholar
  15. 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
  16. 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.PubMedGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. 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.PubMedCrossRefGoogle Scholar
  19. Godard, K.-A., White, R., and Bohlmann, J. 2008. Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69:1838–1849.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. 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.PubMedCrossRefGoogle Scholar
  22. 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.PubMedCrossRefGoogle Scholar
  23. Inderjit, H. K. and Mukerji, G. (eds.) 2006. Allelochemicals: Biological Control of Plant Pathogens and Diseases. Springer, Dordrecht, The Netherlands.Google Scholar
  24. 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.CrossRefGoogle Scholar
  25. Jensen, W. A. 1962. Botanical Histochemistry. W.H. Freeman & Co.: San Francisco & London.Google Scholar
  26. Kho, Y. O. and Baër, J. 1968. Observing pollen tubes by means of fluorescence light. Euphytica. 17:298–302.Google Scholar
  27. 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
  28. 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.PubMedCrossRefGoogle Scholar
  29. 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.Google Scholar
  30. 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.CrossRefGoogle Scholar
  31. Pauly, G., Douce, R., and Carde, J. P. 1981. Effects of β-pinene on spinach chloroplast photosynthesis. Z. Pflanzenphysiol. 104:199–206.Google Scholar
  32. 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
  33. 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.CrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. Reape, T. J. and McCABE, P. F. 2010. Apoptotic-like regulation of programmed cell death in plants. Apoptosis 15:249–256.PubMedCrossRefGoogle Scholar
  36. 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.PubMedCrossRefGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. Roberts, I. N., Lloyd, C. W., and Roberts, K. 1985. Ethylene-induced microtubule reorientations: mediation by helical arrays. Planta 164:439–447.CrossRefGoogle Scholar
  39. Roberts, A. G. and Oparka, K. J. 2003. Plasmodesmata and the control of symplastic transport. Plant Cell Environ. 26:103–124.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. Scheller, H. V., Jensen, J. K., Sørensen, S. O., Harhol, T. J., and Geshi, N. 2007. Biosynthesis of pectin. Physiol. Plant. 129:283–295.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. Schiefelbein, J. W. 2000. Constructing a plant cell. The genetic control of root hair development. Plant Physiol. 124:1525–1531.PubMedCrossRefGoogle Scholar
  45. Somolinos, M., García, D., Condón, S., Mackey, B., and Pagán, R. 2010. Inactivation of Escherichia coli by citral. J. App. Microbiol. 108:1928–1939.Google Scholar
  46. 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.PubMedCrossRefGoogle Scholar
  47. 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.PubMedCrossRefGoogle Scholar
  48. 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.PubMedCrossRefGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.PubMedCrossRefGoogle Scholar
  51. 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.PubMedCrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. Zunino, M. P. and Zygadlo, J. A. 2004. Effect of monoterpenes on lipid peroxidation in maize. Planta 219:303–309.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • E. Graña
    • 1
  • T. Sotelo
    • 2
  • C. Díaz-Tielas
    • 1
  • F. Araniti
    • 3
  • U. Krasuska
    • 4
  • R. Bogatek
    • 4
  • M. J. Reigosa
    • 1
  • A. M. Sánchez-Moreiras
    • 1
  1. 1.Department of Plant Biology and Soil ScienceUniversity of VigoVigoSpain
  2. 2.Misión Biológica de Galicia (CSIC)PontevedraSpain
  3. 3.Dipartimento di Biotecnologie per il Monitoraggio Agro-Alimentare ed Ambientale (BIOMAA)Università Mediterranea di Reggio CalabriaReggio CalabriaItaly
  4. 4.Department of Plant PhysiologyWarsaw University of Life Sciences-SGGWWarsawPoland

Personalised recommendations