Skip to main content
SpringerLink
Log in

Methyl jasmonate counteracts boron toxicity by preventing oxidative stress and regulating antioxidant enzyme activities and artemisinin biosynthesis in Artemisia annua L.

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

An Erratum to this article was published on 16 November 2010

Abstract

Boron is an essential plant micronutrient, but it is phytotoxic if present in excessive amounts in soil for certain plants such as Artemisia annua L. that contains artemisinin (an important antimalarial drug) in its areal parts. Artemisinin is a sesquiterpene lactone with an endoperoxide bridge. It is quite expensive compound because the only commercial source available is A. annua and the compound present in the plant is in very low concentration. Since A. annua is a major source of the antimalarial drug and B stress is a deadly threat to its cultivation, the present research was conducted to determine whether the exogenous application of methyl jasmonate (MeJA) could combat the ill effects of excessive B present in the soil. According to the results obtained, the B toxicity induced oxidative stress and reduced the stem height as well as fresh and dry masses of the plant remarkably. The excessive amounts of soil B also lowered the net photosynthetic rate, stomatal conductance, internal CO2 concentration and total chlorophyll content in the leaves. In contrast, the foliar application of MeJA enhanced the growth and photosynthetic efficiency both in the stressed and non-stressed plants. The excessive B levels also increased the activities of antioxidant enzymes, such as catalase, peroxidase and superoxide dismutase. Endogenous H2O2 and O −2 levels were also high in the stressed plants. However, the MeJA application to the stressed plants reduced the amount of lipid peroxidation and stimulated the synthesis of antioxidant enzymes, enhancing the content and yield of artemisinin as well. Thus, it was concluded that MeJA might be utilized in mitigating the B toxicity and improving the content and yield of artemisinin in A. annua plant.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abdin MZ, Israr M, Rehman RU, Jain SK (2003) Artemisinin, a novel antimalarial drug: biochemical and molecular approaches for enhanced production. Planta Med 69:1–11

    Article  Google Scholar 

  • Able AJ, Guest DI, Sutherland MW (1998) Use of a new tetrazolium based assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoospores of Phytophthora parasitica var nicotianae. Plant Physiol 117:491–499

    Article  PubMed  CAS  Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Singh M, Ram M (2010a) Stimulation of crop productivity, photosynthesis and artemisinin production in Artemisia annua L. by triacontanol and gibberellic acid application. J Plant Interact 5:273–281.

    Article  CAS  Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Ram M (2010b) B induced oxidative stress, antioxidant defense response and changes in artemisinin content in Artemisia annua L. J Agron Crop Sci. doi:10.1111/j.1439-037X.2010.00427.x

    Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Moinuddin (2010c) Salicylic acid act as potent enhancer of growth, photosynthesis and artemisinin production in Artemisia annua L. J Crop Sci Biotech. doi:10.1007/s12829-010-0040-3

    Google Scholar 

  • Alpaslan M, Gunes A (2001) Interactive effects of B and salinity stress on the growth, membrane permeability and mineral composition of tomato and cucumber plants. Plant Soil 236:123–128

    Article  CAS  Google Scholar 

  • Ardic M, Sekmen AH, Tokur S, Ozdemir F, Turkan I (2009) Antioxidant responses of chickpea plants subjected to B toxicity. Plant Biol 11:328–338

    Article  PubMed  CAS  Google Scholar 

  • Asad A, Blamey FPC, Edwards DG (2003) Effects of B foliar applications on vegetative and reproductive growth of sunflower. Ann Bot 92:1–6

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Blevins DG, Lukaszewski KM (1998) B in plant structure and function. Annu Rev Plant Physiol Plant Mol Biol 49:481–500

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I, Horst J (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  CAS  Google Scholar 

  • Cervilla LM, Blasco B, Rios JJ, Romero L, Ruiz JM (2007) Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to B toxicity. Ann Bot 100:747–756

    Article  PubMed  CAS  Google Scholar 

  • Chandlee JM, Scandalios JG (1984) Analysis of variants affecting the catalase development program in maize scutellum. Theor Appl Genet 69:71–77

    Article  CAS  Google Scholar 

  • Cheong JJ, Choi YD (2003) Methyl jasmonate as a vital substance in plants. Trends Genet 19:409–413

    Article  PubMed  CAS  Google Scholar 

  • Christov C, Pounieva M, Bozhkova M, Toncheva S, Fournadzieva S, Zafirova T (2001) Influence of temperature and methyl jasmonate on Scenedesmus incrassulatus. Biol Plant 44:367–371

    Article  CAS  Google Scholar 

  • Dwivedi RS, Randhawa NS (1974) Evaluation of rapid test for hidden hunger of zinc in plants. Plant Soil 40:445–451

    Article  CAS  Google Scholar 

  • Eraslan F, Inal A, Gunes A, Apaslan M (2007) B toxicity alters nitrate reductase activity, proline accumulation, membrane permeability, and mineral constituents of tomato and pepper plants. J Plant Nutr 30:981–994

    Article  CAS  Google Scholar 

  • Fedina IS, Benderliev KM (2000) Response of Scenedesmus incrassatulus to salt stress as affected by methyl jasmonate. Biol Plant 43:625–627

    Article  CAS  Google Scholar 

  • Ferreira JFS (2007) Nutrient deficiency in the production of artemisinin, dihydroartemisinic acid, and artemisinic acid in Artemisia annua L. J Agric Food Chem 55:1686–1694

    Article  PubMed  CAS  Google Scholar 

  • Golovatskaya IF, Karnachuk RA (2008) Effect of jasmonic acid on morphogenesis and photosynthetic pigment level in Arabidopsis seedlings grown under green light. Russ J Plant Physiol 55:240–244

    Google Scholar 

  • Gong H, Zhu X, Chen K, Wang S, Zhang C (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321

    Google Scholar 

  • Gunes A, Soylemezoglu G, Inal A, Bagci EG, Coban S, Sahin O (2006) Antioxidant and stomatal responses of grapevine (Vitis vinifera L) to B toxicity. Sci Hort 110:279–284

    Article  CAS  Google Scholar 

  • Gunes A, Inal A, Bagci EG, Coban S, Sahin O (2007) Silicon increases B tolerance and reduces oxidative damage of wheat grown in soil with excess B. Biol Plant 51:571–574

    Article  CAS  Google Scholar 

  • Guo XX, Yang XQ, Yang RY, Zeng QP (2010) Salicylic acid and methyl jasmonate but not Rose Bengal enhance artemisinin production through invoking burst of endogenous singlet oxygen. Plant Sci 178:390–397

    Article  CAS  Google Scholar 

  • Hampel D, Mosandl A, Wust M (2005) Induction of de novo volatile terpene biosynthesis via cytosolic and plastidial pathways by methyl jasmonate in foliage of Vitis vinifera L. J Agric Food Chem 53:2652–2657

    Article  PubMed  CAS  Google Scholar 

  • Han S, Tang N, Jiang HX, Yang LT, Li Y, Chen LS (2009) CO2 assimilation, photosystem II photochemistry, carbohydrate metabolism and antioxidant system of citrus leaves in response to B stress. Plant Sci 176:143–153

    Article  CAS  Google Scholar 

  • Hu H, Brown PH (1997) Absorption of B by plant roots. Plant Soil 193:49–58

    Article  CAS  Google Scholar 

  • Inal A, Pilbeam DJ, Gunes A (2009) Silicon increases tolerance to B toxicity and reduces oxidative damage in barley. J Plant Nutr 32:112–128

    Article  CAS  Google Scholar 

  • Jaleel CA, Riadh K, Gopi R, Manivannan P, Inès J, Al-Juburi HJ, Chang-Xing Z, Hong-Bo S, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436

    Article  Google Scholar 

  • Jung C, Yeu SY, Koo YJ, Kim M, Choi YD, Cheong JJ (2007) Transcript profile of transgenic Arabidopsis constitutively producing methyl jasmonate. J Plant Biol 50:12–17

    Article  CAS  Google Scholar 

  • Karabal E, Yücel M, Ökte HA (2003) Antioxidants responses of tolerant and sensitive barley cultivars to B toxicity. Plant Sci 164:925–933

    Article  CAS  Google Scholar 

  • Kaya C, Tuna AL, Dikilitas M, Ashraf M, Koskeroglu S, Guneri M (2009) Supplementary phosphorus can alleviate B toxicity in tomato. Sci Hort 121:284–288

    Article  CAS  Google Scholar 

  • Kim YS, Yeung EC, Hahn EJ, Paek KY (2007) Combined effects of phytohormone, indole-3-butyric acid, and methyl jasmonate on root growth and ginsenoside production in adventitious root cultures of Panax ginseng C.A. Meyer. Biotechnol Lett 29:1789–1792

    Article  PubMed  CAS  Google Scholar 

  • Klayman DL (1985) Qinghaosu (artemisinin): an antimalarial drug from China. Science 228:1049–1055

    Article  PubMed  CAS  Google Scholar 

  • Kumar KB, Khan PA (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine coracana cv. PR 202) leaves during senescence. Indian J Exp Bot 20:412–416

    CAS  Google Scholar 

  • Lee SKD (2006) Hot pepper response to interactive effects of salinity and B. Plant Soil Environ 52:227–233

    Google Scholar 

  • Li Y, Huang H, Wu YL (2006) Qinghaosu (artemisinin)—a fantastic antimalarial drug from a traditional Chinese medicine. In: Tian X, Liang WSF (eds) Medicinal chemistry of bioactive natural products. Wiley, Hoboken, pp 183–256

    Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV–VIS spectroscopy. In: Wrolstad RE (ed) Current protocols in food analytical chemistry. Wiley, New York, pp F4.3.1–F4.3.8

    Google Scholar 

  • Maksymiec W, Krupa Z (2006) The effects of short term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57:187–194

    Article  CAS  Google Scholar 

  • Mannan A, Liu C, Arsenault PR, Towler MJ, Vail DR, Lorence A, Weathers PJ (2010) DMSO triggers the generation of ROS leading to an increase in artemisinin and dihydroartemisinic acid in Artemisia annua shoot cultures. Plant Cell Rep 29:143–152

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Molassiotis A, Sotiropoulos T, Tanou G, Diamantidis G, Therios I (2006) B induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM9 (Malus domestica Borkh). Environ Exp Bot 56:54–62

    Article  CAS  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  CAS  Google Scholar 

  • Nable RO, Banuelos GS, Paull JG (1997) B toxicity. Plant Soil 193:181–198

    Article  CAS  Google Scholar 

  • Norastehnia A, Nojavan-Asghari M (2006) Effect of methyl jasmonate on the enzymatic antioxidant defense system in Maize seedling subjected to paraquat. Asian J Plant Sci 5:17–23

    Article  CAS  Google Scholar 

  • Papadakis IE, Dimassi KN, Bosabalidis AM, Therios IN, Patakas A, Giannakoula A (2004) Effects of B excess on some physiological and anatomical parameters of ‘Navelina’ orange plants grafted on two rootstocks. Environ Exp Bot 51:247–257

    Article  CAS  Google Scholar 

  • Parks JL, Edwards M (2005) B in the environment. Crit Rev Env Sci Biotechnol 35:81–114

    Article  CAS  Google Scholar 

  • Parra-Lobato MC, Fernandez-Garcia N, Olmos E, Alvarez-Tinaut MC, Gómez-Jiménez MC (2009) Methyl jasmonate-induced antioxidant defence in root apoplast from sunflower seedlings. Environ Exp Bot 66:9–17

    Article  CAS  Google Scholar 

  • Paull JG, Nable RO, Rathjen AJ (1992) Physiological and genetic control of the tolerance of wheat to high concentrations of B and implications for plant breeding. Plant Soil 146:251–260

    Article  CAS  Google Scholar 

  • Pedranzani H, Racagni G, Alemano S, Miersch O, Ramirez I, Pena-Cortes H, Machado-Domenech E, Abdala G (2003) Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul 41:149–158

    Article  CAS  Google Scholar 

  • Pu GB, Ma DM, Chen JL, Ma LQ, Wang H, Li GF, Ye HC, Liu BY (2009) Salicylic acid activates artemisinin biosynthesis in Artemisia annua L. Plant Cell Rep 28:1127–1135

    Article  PubMed  CAS  Google Scholar 

  • Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI (2005) The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214–217

    Article  PubMed  CAS  Google Scholar 

  • Srivastava NK, Sharma S (1990) Influence of micronutrient imbalance on growth and artemisinin content in Artemisia annua. Indian J Pharm Sci 82:225–227

    Google Scholar 

  • Sudhakar C, Lakshmi S, Giridarakumar S (2001) Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci 161:613–619

    Article  CAS  Google Scholar 

  • Wallaart TE, van Uden W, Lubberink HG, Woerdenbag HJ, Pras N, Quax WJ (1999) Isolation and identification of dihydroartemisinic acid from Artemisia annua and its possible role in the biosynthesis of artemisinin. J Nat Prod 62:430–433

    Article  PubMed  CAS  Google Scholar 

  • Wallaart TE, Pras N, Beekman AC, Quax WJ (2000) Seasonal variation of artemisinin and its biosynthetic precursors in plants of Artemisia annua of different geographical origin: proof for the existence of chemotypes. Planta Med 66:57–62

    Article  PubMed  CAS  Google Scholar 

  • Wang SY (1999) Methyl jasmonate reduces water stress in strawberry. J Plant Growth Regul 18:127–134

    Article  PubMed  Google Scholar 

  • Wang H, Ma C, Li Z, Ma L, Wang H, Ye H, Xu G, Liu B (2009) Effects of exogenous methyl jasmonate on artemisinin biosynthesis and secondary metabolites in Artemisia annua L. Ind Crops Prod 31:214–218

    Article  Google Scholar 

  • Wasternack C, Hause B (2002) Jasmonates and octadecanoids—signals in plant stress responses and development. In: Moldave K (ed) Progress in nucleic acid research and molecular biology. Academic, New York, pp 165–221

    Google Scholar 

  • WHO (2006) WHO guidelines for the treatment of malaria. World Health Organization, Geneva

    Google Scholar 

  • Wolf B (1971) The determination of B in soil extracts, plant materials, composts, manures, water and nutrient solutions. Comm Soil Sci Plant Anal 2:363–374

    Article  CAS  Google Scholar 

  • Wolucka BA, Goossens A, Inze D (2005) Methyl jasmonate stimulates the de novo biosynthesis of vitamin C in plant cell suspensions. J Exp Bot 56:2527–2538

    Article  PubMed  CAS  Google Scholar 

  • Yau SK, Ryan J (2008) B toxicity tolerance in crops: a viable alternative to soil amelioration. Crop Sci 48:854–865

    Article  CAS  Google Scholar 

  • Yoon JY, Hamayun M, Lee SK, Lee IJ (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotech 12:63–68

    Article  Google Scholar 

  • Zhao SS, Zeng MY (1986) Determination of Qinghaosu in Artemisia annua L. by high performance liquid chromatography. Chin J Pharma Anal 6:3–5

    Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Authors wish to thank Mr. M. Ram (SRF-CSIR) of Jamia Hamdard (Hamdard University) for his kind help in HPLC analysis regarding artemisinin. The financial support to the first author in the form of Research Assistantship by Council of Science and Technology, UP, Lucknow (CST/D-3539) is also gratefully acknowledged.

Conflict of interest

Authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Plant Physiology Section, Department of Botany, Aligarh Muslim University, Aligarh, 202 002, Uttar Pradesh, India

    Tariq Aftab, M. Masroor A. Khan, Mohd. Idrees, M. Naeem,  Moinuddin & Nadeem Hashmi

Authors
  1. Tariq Aftab
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Masroor A. Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohd. Idrees
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Naeem
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Moinuddin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nadeem Hashmi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tariq Aftab.

Additional information

Handling Editor: Peter Nick

An erratum to this article can be found at http://dx.doi.org/10.1007/s00709-010-0238-1

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aftab, T., Khan, M.M.A., Idrees, M. et al. Methyl jasmonate counteracts boron toxicity by preventing oxidative stress and regulating antioxidant enzyme activities and artemisinin biosynthesis in Artemisia annua L.. Protoplasma 248, 601–612 (2011). https://doi.org/10.1007/s00709-010-0218-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-010-0218-5

Keyword

Search

Navigation