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Protoplasma

, Volume 248, Issue 3, pp 601–612 | Cite as

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

  • Tariq AftabEmail author
  • M. Masroor A. Khan
  • Mohd. Idrees
  • M. Naeem
  • Moinuddin
  • Nadeem Hashmi
Original Article

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.

Keyword

Artemisia annua L. Artemisinin Boron Methyl jasmonate (MeJA) Reactive oxygen species (ROS) 

Notes

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.

References

  1. Abdin MZ, Israr M, Rehman RU, Jain SK (2003) Artemisinin, a novel antimalarial drug: biochemical and molecular approaches for enhanced production. Planta Med 69:1–11CrossRefGoogle Scholar
  2. 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 117:491–499PubMedCrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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
  5. 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
  6. 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 236:123–128CrossRefGoogle Scholar
  7. Ardic M, Sekmen AH, Tokur S, Ozdemir F, Turkan I (2009) Antioxidant responses of chickpea plants subjected to B toxicity. Plant Biol 11:328–338PubMedCrossRefGoogle Scholar
  8. Asad A, Blamey FPC, Edwards DG (2003) Effects of B foliar applications on vegetative and reproductive growth of sunflower. Ann Bot 92:1–6CrossRefGoogle Scholar
  9. Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287PubMedCrossRefGoogle Scholar
  10. Blevins DG, Lukaszewski KM (1998) B in plant structure and function. Annu Rev Plant Physiol Plant Mol Biol 49:481–500PubMedCrossRefGoogle Scholar
  11. 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 83:463–468CrossRefGoogle Scholar
  12. 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 100:747–756PubMedCrossRefGoogle Scholar
  13. Chandlee JM, Scandalios JG (1984) Analysis of variants affecting the catalase development program in maize scutellum. Theor Appl Genet 69:71–77CrossRefGoogle Scholar
  14. Cheong JJ, Choi YD (2003) Methyl jasmonate as a vital substance in plants. Trends Genet 19:409–413PubMedCrossRefGoogle Scholar
  15. Christov C, Pounieva M, Bozhkova M, Toncheva S, Fournadzieva S, Zafirova T (2001) Influence of temperature and methyl jasmonate on Scenedesmus incrassulatus. Biol Plant 44:367–371CrossRefGoogle Scholar
  16. Dwivedi RS, Randhawa NS (1974) Evaluation of rapid test for hidden hunger of zinc in plants. Plant Soil 40:445–451CrossRefGoogle Scholar
  17. 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 30:981–994CrossRefGoogle Scholar
  18. Fedina IS, Benderliev KM (2000) Response of Scenedesmus incrassatulus to salt stress as affected by methyl jasmonate. Biol Plant 43:625–627CrossRefGoogle Scholar
  19. Ferreira JFS (2007) Nutrient deficiency in the production of artemisinin, dihydroartemisinic acid, and artemisinic acid in Artemisia annua L. J Agric Food Chem 55:1686–1694PubMedCrossRefGoogle Scholar
  20. 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 55:240–244Google Scholar
  21. Gong H, Zhu X, Chen K, Wang S, Zhang C (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321Google Scholar
  22. 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 110:279–284CrossRefGoogle Scholar
  23. 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 51:571–574CrossRefGoogle Scholar
  24. 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 178:390–397CrossRefGoogle Scholar
  25. 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 53:2652–2657PubMedCrossRefGoogle Scholar
  26. 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 176:143–153CrossRefGoogle Scholar
  27. Hu H, Brown PH (1997) Absorption of B by plant roots. Plant Soil 193:49–58CrossRefGoogle Scholar
  28. Inal A, Pilbeam DJ, Gunes A (2009) Silicon increases tolerance to B toxicity and reduces oxidative damage in barley. J Plant Nutr 32:112–128CrossRefGoogle Scholar
  29. 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 31:427–436CrossRefGoogle Scholar
  30. 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 50:12–17CrossRefGoogle Scholar
  31. Karabal E, Yücel M, Ökte HA (2003) Antioxidants responses of tolerant and sensitive barley cultivars to B toxicity. Plant Sci 164:925–933CrossRefGoogle Scholar
  32. Kaya C, Tuna AL, Dikilitas M, Ashraf M, Koskeroglu S, Guneri M (2009) Supplementary phosphorus can alleviate B toxicity in tomato. Sci Hort 121:284–288CrossRefGoogle Scholar
  33. 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 29:1789–1792PubMedCrossRefGoogle Scholar
  34. Klayman DL (1985) Qinghaosu (artemisinin): an antimalarial drug from China. Science 228:1049–1055PubMedCrossRefGoogle Scholar
  35. Kumar KB, Khan PA (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine coracana cv. PR 202) leaves during senescence. Indian J Exp Bot 20:412–416Google Scholar
  36. Lee SKD (2006) Hot pepper response to interactive effects of salinity and B. Plant Soil Environ 52:227–233Google Scholar
  37. 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 183–256Google Scholar
  38. 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–F4.3.8Google Scholar
  39. 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 57:187–194CrossRefGoogle Scholar
  40. 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 29:143–152PubMedCrossRefGoogle Scholar
  41. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedCrossRefGoogle Scholar
  42. 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 56:54–62CrossRefGoogle Scholar
  43. 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 58:166–170CrossRefGoogle Scholar
  44. Nable RO, Banuelos GS, Paull JG (1997) B toxicity. Plant Soil 193:181–198CrossRefGoogle Scholar
  45. 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 5:17–23CrossRefGoogle Scholar
  46. 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 51:247–257CrossRefGoogle Scholar
  47. Parks JL, Edwards M (2005) B in the environment. Crit Rev Env Sci Biotechnol 35:81–114CrossRefGoogle Scholar
  48. 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 66:9–17CrossRefGoogle Scholar
  49. 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 146:251–260CrossRefGoogle Scholar
  50. 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 41:149–158CrossRefGoogle Scholar
  51. 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 28:1127–1135PubMedCrossRefGoogle Scholar
  52. Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI (2005) The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214–217PubMedCrossRefGoogle Scholar
  53. Srivastava NK, Sharma S (1990) Influence of micronutrient imbalance on growth and artemisinin content in Artemisia annua. Indian J Pharm Sci 82:225–227Google Scholar
  54. 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 161:613–619CrossRefGoogle Scholar
  55. 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 62:430–433PubMedCrossRefGoogle Scholar
  56. 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 66:57–62PubMedCrossRefGoogle Scholar
  57. Wang SY (1999) Methyl jasmonate reduces water stress in strawberry. J Plant Growth Regul 18:127–134PubMedCrossRefGoogle Scholar
  58. 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 31:214–218CrossRefGoogle Scholar
  59. 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 165–221Google Scholar
  60. WHO (2006) WHO guidelines for the treatment of malaria. World Health Organization, GenevaGoogle Scholar
  61. Wolf B (1971) The determination of B in soil extracts, plant materials, composts, manures, water and nutrient solutions. Comm Soil Sci Plant Anal 2:363–374CrossRefGoogle Scholar
  62. Wolucka BA, Goossens A, Inze D (2005) Methyl jasmonate stimulates the de novo biosynthesis of vitamin C in plant cell suspensions. J Exp Bot 56:2527–2538PubMedCrossRefGoogle Scholar
  63. Yau SK, Ryan J (2008) B toxicity tolerance in crops: a viable alternative to soil amelioration. Crop Sci 48:854–865CrossRefGoogle Scholar
  64. Yoon JY, Hamayun M, Lee SK, Lee IJ (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotech 12:63–68CrossRefGoogle Scholar
  65. Zhao SS, Zeng MY (1986) Determination of Qinghaosu in Artemisia annua L. by high performance liquid chromatography. Chin J Pharma Anal 6:3–5Google Scholar
  66. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Tariq Aftab
    • 1
    Email author
  • M. Masroor A. Khan
    • 1
  • Mohd. Idrees
    • 1
  • M. Naeem
    • 1
  • Moinuddin
    • 1
  • Nadeem Hashmi
    • 1
  1. 1.Plant Physiology Section, Department of BotanyAligarh Muslim UniversityAligarhIndia

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