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Essential oils of two Nepeta species inhibit growth and induce oxidative stress in ragweed (Ambrosia artemisiifolia L.) shoots in vitro

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Abstract

In vitro shoot cultures of ragweed (Ambrosia artemisiifolia L.), an important weed and allergen species, were established and utilized to explore the phytotoxic effect of essential oils of Nepeta rtanjensis Diklić and Milojević, and N. cataria L. Ragweed shoots were exposed to the atmosphere enriched with volatile compounds emitted from essential oils which differ in their qualitative and quantitative nepetalactone content. Essential oil of N. rtanjensis, an endemic and critically endangered perennial in Serbia, was characterized by high amounts of 4aα,7α,7aβ-nepetalactone (trans,cis-nepetalactone), while essential oil of N. cataria, possessed high amounts of 4aα,7α,7aα-nepetalactone (cis,trans-nepetalactone). After 2 weeks of exposure to Nepeta essential oil (2 and 4 %, final nepetalactone concentrations), in vitro morphogenesis of ragweed shoots was significantly altered. Reduction in fresh weight of shoots and roots and rooting inhibition was observed together with prominent discoloration of shoots. Alterations in antioxidative defense system of ragweed shoots as a response to essential oils treatments were characterized by increased peroxidase activity and decreased catalase and superoxide dismutase activity. Generally, essential oil of N. cataria, which possesses cis,trans-stereoisomer of nepetalactone, had stronger inhibitory effect on shoot growth, catalase activity, and was more efficient in stimulating peroxidase activity. N. rtanjensis essential oil, and thus trans,cis-nepetalactone, was more efficient in inhibiting rooting and root growth, and in suppressing superoxide dismutase activity. Therefore, essential oils of N. rtanjensis and N. cataria might find another application as potential bioherbicides against highly invasive species such as ragweed.

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Abbreviations

BM:

Basal medium

BSA:

Bovine serum albumin

CAT:

Catalase

DTT:

Dithiothreitol

EDTA:

Ethylenediaminetetraacetic acid

EO:

Essential oil

GC–FID:

Gas chromatography with flame ionization detector

GC–MS:

Gas chromatography with mass spectrometry

NBT:

Nitro blue tetrazolium chloride

NFDM:

Non-fat dry milk

PAGE:

Polyacrylamide gel electrophoresis

PBS:

Phosphate-buffered saline

PMSF:

Phenylmethanesulfonyl fluoride

POX:

Peroxidase

PVPP:

Polyvinylpolypyrrolidone

ROS:

Reactive oxygen species

SB:

Sample buffer

SDS:

Sodium dodecyl sulfate

SOD:

Superoxide dismutase

TEMED:

Tetramethylethylenediamine

TPBS:

Tween (0.05 %) in PBS buffer

VOC:

Volatile compound

References

  • Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry. Allured Publishing Corporation, Illinois

    Google Scholar 

  • Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Akin-Idowu PE, Ibitoye DO, Ademoyegun OT (2009) Tissue culture as a plant production technique for horticultural crops. Afr J Biotechnol 8(16):3782–3788

    Google Scholar 

  • Araniti F, Graña E, Reigosa MJ, Sánchez-Moreiras AM, Abenavoli MR (2013) Individual and joint activity of terpenoids, isolated from Calamintha nepeta extract, on Arabidopsis thaliana. Nat Prod Res 27(24):2297–2303

    Article  CAS  PubMed  Google Scholar 

  • Bates RB, Sigel CW (1963) Terpenoids, cis-trans and trans-cis nepetalactones. Experientia 19:564–565

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Beyer WF Jr, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161(2):559–566

    Article  CAS  PubMed  Google Scholar 

  • Bhagwath SG, Hjortsø MA (2000) Statistical analysis of elicitation strategies for thiarubrine A production in hairy root cultures of Ambrosia artemisiifolia. J Biotechnol 80:159–167

    Article  CAS  PubMed  Google Scholar 

  • Birkett MA, Pickett JA (2003) Aphid sex pheromones: from discovery to commercial production. Phytochemistry 62(5):651–656

    Article  CAS  PubMed  Google Scholar 

  • Birkett MA, Hassanali A, Hoglund S, Pettersson J, Pickett JA (2011) Repellent activity of catmint, Nepeta cataria, and iridoid nepetalactone isomers against Afro-tropical mosquitoes, ixodid ticks and red poultry mites. Phytochemistry 72:109–114

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1):248–254

    Article  CAS  PubMed  Google Scholar 

  • Chalchat JC, Gorunović MS, Petrović SD, Maksimović ZA (2000) Composition of the essential oils of Nepeta rtanjensis Diklić and Milojević, Lamiaceae from Serbia. J Essent Oil Res 12:238–240

    CAS  Google Scholar 

  • Chowhan N, Singh HP, Batish DR, Kohli RK (2011) Phytotoxic effects of β-pinene on early growth and associated biochemical changes in rice. Acta Physiol Plant 33:2369–2376

    Article  CAS  Google Scholar 

  • Chowhan N, Singh HP, Batish DR, Kaur S, Ahuja N, Kohli RK (2013) β-Pinene inhibited germination and early growth involves membrane peroxidation. Protoplasma 250:691–700

    Article  CAS  PubMed  Google Scholar 

  • Dayan FE, Cantrell CL, Duke SO (2009) Natural products in crop protection. Bioor Med Chem 17(12):4022–4034

    Article  CAS  Google Scholar 

  • Dhindsa RA, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence correlated with increased permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 126:93–101

    Article  Google Scholar 

  • Ding J, Sun Y, Xiao CL, Shi K, Zhou YH, Yu JQ (2007) Physiological basis of different allelopathic reactions of cucumber and figleaf gourd plants to cinnamic acid. J Exp Bot 58(13):3765–3773

    Article  CAS  PubMed  Google Scholar 

  • Duke SO (2010) Allelopathy: current status of research and the future of the discipline: a commentary. Allelopathy J 25(1):17–30

    Google Scholar 

  • Gkinis G, Tzakou O, Iliopoulou D, Roussis V (2003) Chemical composition and biological activity of Nepeta parnassica oil and isolated Nepeta lactons. Natur forsch 58:681–686

    CAS  Google Scholar 

  • Gomez-Barrious ML, Parodi FJ, Vargas D, Quijano L, Hjortso MA, Flores AE, Fischer NH (1992) Studies on the biosynthesis of thiarubrine A in hairy root cultures of Ambrosiaartemisiifolia using 13C-labelled acetates. Phytochemistry 31:2703–2707

    Article  Google Scholar 

  • Grayson BT, Williams KS, Freehauf PA, Pease RR, Ziesel WT, Sereno RL, Reinsfelder RE (1987) The physical and chemical properties of the herbicide cinmethylin. Pestic Sci 21(2):143–153

    Article  CAS  Google Scholar 

  • Gyoffry B, Hunyadi K, Kadar A, Molnar J, Toth A (1995) Hungarian national weed surveys 1950–1992. EWRS Symposium (9th) Budapest 1–11

  • Hong Y, Hu H-Y, Xiea Li F-M (2008) Responses of enzymatic antioxidants and non-enzymatic antioxidants in the cyanobacterium Microcystis aeruginosa to the allelochemical ethyl 2 methyl acetoacetate (EMA) isolated from reed (Phragmites communis). J Plant Physiol 165:1264–1273

    Article  CAS  PubMed  Google Scholar 

  • Hyun Eom S, Yang HS, Weston LA (2006) An evaluation of the allelopathic potential of selected perennial groundcovers: foliar volatiles of catmint (Nepeta faassenii) inhibit seedling growth. J Chem Ecol 32(8):1835–1848

    Article  Google Scholar 

  • Kalpoutzakis E, Aligiannis N, Mentis A, Mitaku S, Charvala C (2001) Composition of the essential oil of two Nepeta species and in vitro evaluation of their activity against Helicobacter pylori. Planta Med 67:880–883

    Article  CAS  PubMed  Google Scholar 

  • Kobaisy M, Tellez MR, Dayan FE, Mamonov LK, Mukanova GS, Sitpaeva GT, Gemejieva NG (2005) Composition and phytotoxic activity of Nepeta pannonica L. essential oil. J Essent Oil Res 17(6):704–707

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4 680. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Li ZH, Wang Q, Ruan X, Pan CD, Jiang DA (2010) Phenolics and plant allelopathy. Molecules 15:8933–8952

    Article  CAS  PubMed  Google Scholar 

  • Lindinger W, Hansel A, Jordan A (1998) On-line monitoring of volatile organic compounds at pptv levels by means of proton-transfer-reaction mass spectrometry (PTR-MS) medical applications, food control and environmental research. Int J Mass Spectrom 173(3):191–241

    Article  CAS  Google Scholar 

  • Ljaljević Grbić M, Stupar M, Vukojević J, Soković M, Mišić D, Grubišić D, Ristić M (2008) Antifungal activity of Nepeta rtanjensis essential oil. J Serb Chem Soc 3(10):961–965

    Article  Google Scholar 

  • Mancini E, Apostolides AN, Feo V, Formisano C, Rigano D, Piozzi F, Senatore F (2009) Phytotoxic effects of essential oils of Nepeta curviflora Boiss. and Nepeta nuda L. subsp. albiflora growing wild in Lebanon. J Plant Inter 4(4):253–259

    CAS  Google Scholar 

  • Michalski WP (1996) Chromatographic and electrophoretic methods for analysis of superoxide dismutases. J Chromatogr B 684:59–75

    Article  CAS  Google Scholar 

  • Mišić D, Šiler B, Gašić U, Avramov S, Živković S, Nestorović Živković J, Milutinović M, Tešić Ž (2014) Simultaneous UHPLC/DAD/(+/)HESI–MS/MS analysis of phenolic acids and nepetalactones in methanol extracts of Nepeta species: a possible application in chemotaxonomic studies. Phytochem Anal. doi:10.1002/pca.2538

    PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497

    Article  CAS  Google Scholar 

  • Mutlu S, Atici O, Esim N, Mete E (2011) Essential oils of catmint (Nepeta meyeri Benth.) induce oxidative stress in early seedlings of various weed species. Acta Physiol Plant 33:943–951

    Article  CAS  Google Scholar 

  • Nestorović Živković J (2013) Antioxidative, antimicrobial and allelopathic effects of three endemic Nepeta species (Lamiaceae). Dissertation, University of Belgrade

  • Nestorović J, Mišić D, Šiler B, Soković M, Glamočlija J, Ćirić A, Maksimović V, Grubišić D (2010) Nepetalactone content in shoot cultures of three endemic Nepeta species and the evaluation of their antimicrobial activity. Fitoterapia 81(6):621–626

    Article  PubMed  Google Scholar 

  • Nishida N, Tamotsu S, Nagata N, Saito C, Sakai A (2005) Allelopathic effects of volatile monoterpenoids produced by Salvia leucophylla inhibition of cell proliferation and DNA synthesis in the root apical meristem of Brassica campestris seedlings. J Chem Ecol 31(5):1187–1203

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Oleszek W, Stochmal A (2002) Triterpene saponins and flavonoids in the seeds of Trifolium species. Phytochemistry 61(2):165–170

    Article  CAS  PubMed  Google Scholar 

  • Peterson C, Coats J (2001) Insect repellents—past, present and future. Pestic Outlook 12:154–158

    Article  Google Scholar 

  • Peterson CJ, Nemetz LT, Jones LM, Coats JR (2002) Behavioral activity of catnip (Lamiaceae) essential oil components to the German cockroach (Blattodea:Blattellidae). J Econ Entomol 95:377–380

    Article  CAS  PubMed  Google Scholar 

  • Romagni JG, Allen SN, Dayan FE (2000) Allelopathic effects of volatile cineoles on two weedy plant species. J Chem Ecol 26(1):303–313

    Article  CAS  Google Scholar 

  • Romero-Calvo I, Ocón B, Martínez-Moya P, Suárez MD, Zarzuelo A, Martínez-Augustin O, de Medina FS (2010) Reversible Ponceau staining as a loading control alternative to actin in Western blots. Anal Biochem 401(2):318–320

    Article  CAS  PubMed  Google Scholar 

  • Rothe GM (2002) Enzyme assays after gel electrophoresis. In: Eisenthal R, Danson MJ (eds) Enzyme assays, a practical approach, 2nd edn. Oxford University Press, Oxford, p 198

    Google Scholar 

  • Schulz M, Kussmann F, Knop M, Kriegs B, Gresens F, Eichert T, Ulbrich A, Marx F, Fabricius H, Goldbach H, Noga G (2007) Allelopathic monoterpenes interfere with Arabidopsis thaliana cuticular waxes and enhance transpiration. Plant Signal Behav 2(4):231–239

    Article  PubMed Central  PubMed  Google Scholar 

  • Singh HP, Batish DR, Kaur S, Ramezani H, Kohli RK (2002) Comparative phytotoxicity of four monoterpenes against Cassia occidentalis. Ann Appl Biol 141:111–116

    Article  CAS  Google Scholar 

  • Singh HP, Batish DR, Kohli RK (2004) Allelopathic effect of two volatile monoterpenes against bill goat weed (Ageratum conyzoides L.). Crop protection 21:347–350

    Article  Google Scholar 

  • Singh HP, Batish DR, Kaur S, Kohli RK, Arora K (2006a) Phytotoxicity of the volatile monoterpene citronellal against some weeds. Zeitschrift für Naturforschung C 61:334–340

    Article  CAS  Google Scholar 

  • Singh HP, Batish DR, Kaur S, Arora K, Kohli RK (2006b) α-pinene inhibits growth and induces oxidative stress in roots. Ann Bot 98:1261–1269

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Singh HP, Kaur S, Mittal S, Batish DR, Kohli RK (2009) Essential oil of Artemisia scoparia inhibits plant growth by generating reactive oxygen species and causing oxidative damage. J Chem Ecol 35:154–162

    Article  CAS  PubMed  Google Scholar 

  • Soltys D, Krasuska U, Bogatek R, Gniazdowska A (2013) Allelochemicals as Bioherbicides—Present and perspectives, In: Price A (ed) Herbicides—Current research and case studies in use, InTech, doi: 10.5772/56185. Available from: http://www.intechopen.com/books/herbicides-current-research-and-case-studies-in-use/allelochemicals-as-bioherbicides-present-and-perspectives

  • Stojanović G, Radulović N, Lazarević J, Miladinović D, Đoković D (2005) Antimicrobial activity of Nepeta rtanjensis essential oil. J Essent Oil Res 17:587–589

    Article  Google Scholar 

  • Taipale R, Ruuskanen TM, Rinne J, Kajos MK, Hakola H, Pohja T, Kulmala M (2008) Technical Note: quantitative long-term measurements of VOC concentrations by PTR-MS–measurement, calibration, and volume mixing ratio calculation methods. Atmos Chem Phys 8(22):6681–6698

    Article  CAS  Google Scholar 

  • Taramarcaz P, Lambelet C, Clot B, Keimer C, Hauser C (2005) Ragweed (Ambrosia) progression and its health risks: will Switzerland resist the invasion? Swiss Med Wkly 135:538–548

    CAS  PubMed  Google Scholar 

  • Thorpe T (2007) History of plant tissue culture. J Mol Microbiol Biotechnol 37:169–180

    CAS  Google Scholar 

  • Woodbury W, Spencer AK, Stahmann MA (1971) An improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem 44:301–305

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the Serbian Ministry of Education, Science and Technological development (grants No. OI173024 and III 41011). The authors would like to thank Dr. Michael Birkett (Biological Chemistry and Crop Protection Department, Rothamsted Research, Harpenden, Herts., Great Britain) for providing N. cataria EO.

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Correspondence to Slavica Dmitrović.

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Communicated by M. J. Reigosa.

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Dmitrović, S., Perišić, M., Stojić, A. et al. Essential oils of two Nepeta species inhibit growth and induce oxidative stress in ragweed (Ambrosia artemisiifolia L.) shoots in vitro. Acta Physiol Plant 37, 64 (2015). https://doi.org/10.1007/s11738-015-1810-2

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  • DOI: https://doi.org/10.1007/s11738-015-1810-2

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