Skip to main content
Log in

Investigation of synergistic action between coronatine and nitric oxide in alleviating arsenic-induced toxicity in sweet basil seedlings

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The phytotoxin coronatine (COR) is a jasmonic acid mimic produced by several pathovars of plant pathogen. In this study, we evaluated the protective effect of COR and nitric oxide (NO) against the toxicity of sodium arsenate in sweet basil (Ocimum basilicum L.). According to the statistical analysis, arsenic had a significant adverse effect on length and biomass of plants. Seedlings that pretreated with COR and sodium nitroprusside (SNP), significantly reversed fresh and dry lose and relative water content decay induced by the metalloid. The protective effects of COR and SNP were indicated by extent of lipid peroxidation, increase glutathione (GSH), ascorbate and thiol (–SH) content, promote antioxidant enzymes and reduce H2O2 content in basil seedlings. The present observation suggested that reduction of excess arsenic As-induced toxicity in O. basilicum by COR and NO is through the activation of enzymes involved in ROS detoxification (CAT, SOD, POD, APX, GR) and maintenance contents of molecular antioxidant (GSH, ascorbate, non-protein thiol and protein-thiol). Moreover, the results revealed a mutually amplifying reaction between COR and NO in reducing As-induced damages.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

As:

Arsenic

APX:

Ascorbate peroxidase

COR:

Coronatine

CAT:

Catalase

DW:

Dry weight

DTNB:

5,5-dithiobis-2-nitrobenzoic acid

FW:

Fresh weight

EDTA:

Ethylendiamine tetraacetic acid

GR:

Glutathione reductase

GSH:

Glutathione

JA:

Jasmonic acid

JA-Ile:

Jasmonyl isoleucine

MDA:

Malondialdehyde

NO:

Nitric oxide

H2O2 :

Hydrogen peroxide

RWC:

Relative water content

PMSF:

Phenyl methane sulfonyl fluoride

PVP:

Poly vinyl pyrrolidone

SOD:

Superoxide dismutase

SNP:

Sodium nitroprusside

TW:

Turgid weight

References

  • Beligni MV, Fath A, Bethake PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–1650

    Article  PubMed  CAS  PubMed Central  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 Chem 72:248–254

    CAS  Google Scholar 

  • Cao X, Ma L, Tu C (2004) Antioxidative responses to arsenic in the arsenic-hyperaccumulator Chinese brake fern (Pteris vittata L.). Environ Pollut 128:317–325

    Article  PubMed  CAS  Google Scholar 

  • Chun-xi L, Shu-li F, Yan SH, Li-na J, Xu-yang L, Xiao-li H (2007) Effects of arsenic on seed germination and physiological activities of wheat seedlings. J Environ Sci 19:725–732

    Article  Google Scholar 

  • De Pinto MC, Tommasi F, De Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells. Plant Physiol 130:698–708

    Article  PubMed  PubMed Central  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a secondary signal in plant disease resistance. Nature 394:585–588

    Article  PubMed  CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thrope TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid per oxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:43–101

    Article  Google Scholar 

  • Diaz J, Bernal A, Pomar F, Merino F (2001) Induction of shikimate dehydrogenase and peroxidase in pepper (Capsicum annuum L.) seedlings in response to copper stress and its relation to lignification. Plant Sci 161:179

    Article  CAS  Google Scholar 

  • Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic CMP and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ellman Gl (1959) Tissue sulfydryl groups. Arch Biochem Biophys 82:70–77

    Article  PubMed  CAS  Google Scholar 

  • Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Finnegan PM, Chen W (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol 3(182):1–18

    Google Scholar 

  • Flora SJS (2011) Arsenic-induced oxidative stress and its reversibility. Free Rad Biol Med 51(2):257–281

    Article  PubMed  CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownelee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplast: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  PubMed  CAS  Google Scholar 

  • Garg N, Singla P (2011) Arsenic toxicity in crop plants: physiological effects and tolerance mechanisms. Environ Chem Lett 9:303–321

    Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutase I: occurrence in higher plants. Plant Physiol 59:309–314

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gomes MP, Duarte DM, Miranda PLS, Barreto LC, Matheus MT, Garcia QS (2012) The effects of arsenic on the growth and nutritional status of Anadenanthera peregrina, a Brazilian savanna tree. J Plant Nutr Soil Sci 175(3):466–473

    Article  CAS  Google Scholar 

  • Gupta M, Sharma P, Sarin NB, Sinha AK (2009) Differential response of arsenic stress in two varieties of Brassica juncea L. Chemosensory 74:1201–1208

    CAS  Google Scholar 

  • Gupta DK, Inouheb M, Rodríguez-Serrano M, Romero-Puertas MC, Sandalio LM (2013) Oxidative stress and arsenic toxicity: role of NADPH oxidases. Chemosphere 90(6):1987–1996

    Article  PubMed  CAS  Google Scholar 

  • Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22(3):584–596

    Article  PubMed  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast: I. Kinetic and stochiometry of fatty acid peroxidation. Biochem Biophys 125:189–190

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:1–3

    Google Scholar 

  • Innocenti G, Pucciariello Ch, Gleuher ML, Hopkins J, Stefano MD, Delledonne M, Puppo A, Baudouin E, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597–1602. doi:10.1007/s00425-006-0461-3

    Article  PubMed  CAS  Google Scholar 

  • Jin JW, Xu YF, Huang YF (2010) Protective effect of nitric oxide against arsenic-induced oxidative damage in tall fescue leaves. Afr J Biotechnol 9(11):1619–1627

    CAS  Google Scholar 

  • Kampfenkel K, Van Montagu M, Inzb D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225:165–167

    Article  PubMed  CAS  Google Scholar 

  • Koda Y, Takahashi K, Kikuta Y, Greulich F, Toshima H, Ichihara A (1996) Similarities of the biological activities of coronatine and coronafacic acid to those of jasmonic acid. Phytochemistry 41:93–96

    Article  CAS  Google Scholar 

  • Koricheva J, Roy S, Vranjic JA, Haukioja E, Hughes PR, Han-ninen O (1997) Antioxidant responses to simulated acid rain and heavy metal deposition in birch seedlings. Environ Pollut 95:249–258

    Article  PubMed  CAS  Google Scholar 

  • Kovacik J, Klejdus B, Backor M (2009) Nitric oxide signals ROS scavenger-mediated enhancement of PAL activity in nitrogen-deficient Matricaria chamomilla roots: side effects of scavengers. Free Radic Biol Med 46:1686–1693

    Article  PubMed  CAS  Google Scholar 

  • Lamattina L, Garca-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Ann Rev Plant Biol 54:109–136

    Article  CAS  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    Article  CAS  Google Scholar 

  • Mascher R, Lippmann B, Holzinger S, Bergmann H (2002) Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. Plant Sci 163:961–969

    Article  CAS  Google Scholar 

  • Meirs S, Philosophhadas S, Aharoni N (1992) Ethylene increased accumulation of fluorescent lipid peroxidation products detected during senescence of parsley by a newly developed method. J Am Soc Hortic Sci 117:128–132

    Google Scholar 

  • Melotto M, Mecey Ch, Niu Y, Chung HS, Katsir L, Yao J, Zeng W, Thines B, Staswick P, Browse J, Howe GA, He ShY (2008) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J 55:979–988

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish J Environ Stu 15(4):523–530

    Google Scholar 

  • Michele RD, Vurro E, Rigo Ch, Costa A, Elviri L, Valentin MD, Careri M, Zottini M, Toppi LS, Schiavo FL (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228

    Article  PubMed  PubMed Central  Google Scholar 

  • Mino Y, Sakai R, Uchino K, Sasabuchi T (1980) Effects of coronatine on the metabolism of phenolics in the discs of potato tuber. Ann Phytopathol Soc 46:510–516

    Article  Google Scholar 

  • Nakano V, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate–specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Panda P, Nath Sh, Chanu ThTh, Sharma GD, Panda SK (2011) Cadmium stress-induced oxidative stress and role of nitric oxide in rice (Oryza sativa L.). Acta Physiol. doi:10.1007/s11738-011-0710-3

    Google Scholar 

  • Pigna M, Cozzolino V, Violante A, Meharg AA (2009) Influence of phosphate on the arsenic uptake by wheat (Triticum durum L.) irrigated with arsenic solutions at three different concentrations. Water Air Soil Pollut 197:371–380

    Article  CAS  Google Scholar 

  • Piotrowska A, Bajguza A, Godlewska-Zylkiewicz B, Czerpak R (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ Exp Bot 66:507–513

    Google Scholar 

  • Putter J (1974) Peroxidases. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 2. Academic Press, New York, pp 685–690

    Chapter  Google Scholar 

  • Romero-Puertas MC, Corpas FJ, Rodríguez-Serrano M, Gomez M, Rio LAD, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. Plant Physiol 164:1346–1357

    Article  CAS  Google Scholar 

  • Sanchez-Viveros G (2010) Short term effects of As-induced toxicity on growth, chlorophyll and carotenoid contents and total content of phenolic compounds of Azolla filiculoides. Water Air Soil Pollut. doi:10.1007/s11270-010-0600-0

    Google Scholar 

  • Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668

    Article  PubMed  CAS  Google Scholar 

  • Sedlak J, Lindsay RH (1968) Estimation of total, protein- bound, and non-protein sulfhydryl groups in tissue by Ellman’s reagent. Anal Biochem 25:192–208

    Article  PubMed  CAS  Google Scholar 

  • Shan Ch, Liang Z (2010) Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Sci 178:130–139

  • Sharma SS, Dietz KJ (2006) The significance of amino acid and amino acid-derived molecules in plant responses and adaption to heavy metal stress. J Exp Bot 57(4):711–726

    Article  PubMed  CAS  Google Scholar 

  • Shri M, Kumar S, Chakrabarty D, Kumar-Trivedi P, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72:1102–1110

    Article  PubMed  CAS  Google Scholar 

  • Singh N, Ma LQ, Srivastava M, Rathinasabapathi B (2006) Metabolic adaptations to arsenic-induced oxidative stress in Pteris vittata L. and Pteris ensiformis L. Plant Sci 170:274–282

    Article  CAS  Google Scholar 

  • Singh HP, Kaur Sh, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297

    Article  PubMed  CAS  Google Scholar 

  • Singleton VL, Rossi IA (1965) Colorimetry of total phenolics with phosphomolybdic–phosphotungstic acid reagents. Am J Enol Vitic 16:144–158

    CAS  Google Scholar 

  • Stamler JS, Toone EJ, Stuart AL, Sucher NJ (1997) NO signals: translocation, regulation, and a consensus motif. Neuron 18:691–696

    Article  PubMed  CAS  Google Scholar 

  • Tamogami S, Kodama O (2000) Coronatine elicits phytoalexin production in rice leaves (Oryza sativa L.) in the same manner as jasmonic acid. Phytochemistry 54:689–694

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Kojima M, Uritani I (1974) Properties, development and cellular-localization of cinnamic acid 4-hydroxylase in cut injured sweet potato. Plant Cell Physiol 15:843–854

    CAS  Google Scholar 

  • Tarchoune I, Sgherri C, Izzo R, Lachaal M, Ouerghi Z, Navari-Izzo F (2010) Antioxidative responses of Ocimum basilicum to sodium chloride or sodium sulphate salinization. Plant Physiol Biochem 48:772–777

    Article  PubMed  CAS  Google Scholar 

  • Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJM (2007) Arsenic hazards; strategies for tolerance and remediation by plants. Trends Biotechnol 25:158–165

    Article  PubMed  CAS  Google Scholar 

  • Turner NC (1981) Techniques and experimental approaches for the measurement of plant water status. Plant Soil 58:339–366

    Article  Google Scholar 

  • Uppalapati SR, Ayoubi P, Weng H, Palmer DA, Mitchell RE, Jones W, Bender CL (2005) The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J 42:201–217

    Article  PubMed  CAS  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Protective role of exogenous polyamines. Plant Sci 151:59–66

    Google Scholar 

  • Wagner GJ (1979) Content and vacuole/extravacuole distribution of neutral sugars, free amino acids, and anthocyanin in protoplasts. Plant Physiol 64:88–93

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang BQ, Li AH, Eneji AE, Tian XL, Zhai ZX, Li JM, Duan LS (2008) Effects of coronatine on growth, gas exchange traits, chlorophyll content, antioxidant enzymes and lipid peroxidation in maize (Zea mays L.) seedlings under simulated drought stress. Plant Prod Sci 11:283–290

    Article  Google Scholar 

  • Wang JW, Wu JY (2005) Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of taxus cells. Plant Cell Physiol 46(6):923–930

    Google Scholar 

  • Wang L, Chen WJ, Wang Q, Eneji AE, Li ZH, Duan LS (2009) Coronatine enhances chilling tolerance in cucumber (Cucumis sativus L.) seedlings by improving the antioxidative defence system. Agron Crop Sci 195:377–383

    Article  CAS  Google Scholar 

  • Weiler EW, Kutchan TM, Gorba T, Brodschelm W, Niesel U, Bublitz F (1994) The Pseudomonas phytotoxin coronatine mimics octadecanoid signalling molecules of higher plants. FEBS Lett 345:9–13

    Article  PubMed  CAS  Google Scholar 

  • Wendehenne D, Durner J, Klessig DF (2004) Nitric oxide: a new player in plant signaling and defence responses. Plant Biol 7:449–455

    CAS  Google Scholar 

  • Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Plant Biol 5:218

    CAS  Google Scholar 

  • Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Xie ZX, Duan LS, Tian XL, Wang BQ, Eneji AE, Li ZH (2008) Coronatine alleviates salinity stress in cotton by improving the antioxidative defense system and radical-scavenging activity. J Plant Physiol 165:375–384

    Article  PubMed  CAS  Google Scholar 

  • Xiong J, Fu G, Tao L, Zhu Ch (2010) Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch Biochem Biophys 497:13–20

    Article  PubMed  CAS  Google Scholar 

  • Xu MJ, Dong JF (2008) Synergistic action between jasmonic acid and nitric oxide in inducing matrine accumulation of Sophora flavescens suspension cells. J Integr Plant Biol 50(1):92–101

    Article  PubMed  CAS  Google Scholar 

  • Xu MJ, Dong JF, Zhu MY (2006) Nitric oxide mediates the fungal elicitor-induced puerarin production in Pueraria thomsonii suspension cells through a salicylic acid (SA)-dependent or a jasmonic acid (JA)-dependent signal pathway. Sci China Ser 49:379–389

    Article  CAS  Google Scholar 

  • Yu C, Hung KT, Kao C (2005) Nitric oxide reduces Cu toxicity and Cu-induced NH4 + accumulation in rice leaves. Plant Physiol 162:1319–1330

    Article  CAS  Google Scholar 

  • Yukimune Y, Tabata H, Higashi Y (1996) Methyl jasmonate-induced of overproduction of paclitaxel and baccatio in Taxus cell suspension cultures. Nat Biotechnol 14:1129–1132

    Article  PubMed  CAS  Google Scholar 

  • Zhao FJ, Ma JF, Meharg AA, McGrath MP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zare Dehabadi Saeid.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saeid, Z.D., Zahra, A. & Abdolhamid, N.S. Investigation of synergistic action between coronatine and nitric oxide in alleviating arsenic-induced toxicity in sweet basil seedlings. Plant Growth Regul 74, 119–130 (2014). https://doi.org/10.1007/s10725-014-9903-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-014-9903-2

Keywords

Navigation