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Role of Salicylic Acid in Promoting Salt Stress Tolerance and Enhanced Artemisinin Production in Artemisia annua L.

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Abstract

In the present investigation, the role of salicylic acid (SA) in inducing salinity tolerance was studied in Artemisia annua L., which is a major source of the antimalarial drug artemisinin. SA, when applied at 1.00 mM, provided considerable protection against salt stress imposed by adding 50, 100, or 200 mM NaCl to soil. Salt stress negatively affected plant growth as assessed by length and dry weight of shoots and roots. Salinity also reduced the values of photosynthetic attributes and total chlorophyll content and inhibited the activities of nitrate reductase and carbonic anhydrase. Furthermore, salt stress significantly increased electrolyte leakage and proline content. Salt stress also induced oxidative stress as indicated by the elevated levels of lipid peroxidation compared to the control. A foliar spray of SA at 1.00 mM promoted the growth of plants, independent of salinity level. The activity of antioxidant enzymes, namely, catalase, peroxidase, and superoxide dismutase, was upregulated by salt stress and was further enhanced by SA treatment. Artemisinin content increased at 50 and 100 mM NaCl but decreased at 200 mM NaCl. The application of SA further enhanced artemisinin content when applied with 50 and 100 mM NaCl by 18.3 and 52.4%, respectively. These results indicate that moderate saline conditions can be exploited to obtain higher artemisinin content in A. annua plants, whereas the application of SA can be used to protect plant growth and induce its antioxidant defense system under salt stress.

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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, Moinuddin (2010a) Salicylic acid acts as potent enhancer of growth, photosynthesis and artemisinin production in Artemisia annua L. J Crop Sci Biotech 13:183–188

    Article  Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Singh M, Ram M (2010b) 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 (2010c) Boron induced oxidative stress, antioxidant defense response and changes in artemisinin content in Artemisia annua L. J Agron Crop Sci 196:423–430

    Article  CAS  Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Hashmi N, Moinuddin (2010d) Effect of salt stress on growth, membrane damage, antioxidant metabolism and artemisinin accumulation in Artemisia annua L. Plant Stress 4:36–43

    Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Moinuddin (2010e) Effects of aluminium exposures on growth, photosynthetic efficiency, lipid peroxidation, antioxidant enzymes and artemisinin content of Artemisia annua L. J Phytol 2:23–37

    Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Moinuddin, Hashmi N (2011) Methyl jasmonate counteracts boron toxicity by preventing oxidative stress and regulating antioxidant enzyme activities and artemisinin biosynthesis in Artemisia annua L. Protoplasma. doi:10.1007/s00709-010-0218-5

  • Agarwal S, Sairam RK, Srivastava G, Meena R (2005) Changes in antioxidant enzyme activity and oxidative stress by abscisic acid and salicylic acid in wheat genotypes. Biol Plant 49:541–550

    Article  CAS  Google Scholar 

  • Ashraf M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora 199:361–376

    Article  Google Scholar 

  • Athar HR, Khan A, Ashraf M (2008) Exogenously applied ascorbic acid alleviates salt induced oxidative stress in wheat. Environ Exp Bot 63:224–231

    Article  CAS  Google Scholar 

  • Azooz MM, Shaddad MA, Abdel-Latef AA (2004) The accumulation and compartmentation of proline in relation to salt tolerance of three sorghum cultivars. Indian J Plant Physiol 9:1–8

    CAS  Google Scholar 

  • Barkosky RR, Einhellig FA (1993) Effects of salicylic acid on plant water relationship. J Chem Ecol 1:237–247

    Article  Google Scholar 

  • Bates LS, Walden RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  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 

  • Bethkey PC, Drew MC (1992) Stomatal and non-stomatal components to inhibition of photosynthesis in leaves of Capsium annum during progressive exposure to NaCl salinity. Plant Physiol 99:219–226

    Article  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 

  • Campbell WH (1999) Nitrate reductase structure, function and regulation: bridging the gap between biochemistry and physiology. Annu Rev Plant Physiol Mol Biol 5:277–303

    Article  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 

  • Duke SO, Paul RN (1993) Development and fine structure of the glandular trichomes of Artemisia annua L. Int J Plant Sci 155:107–118

    Article  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 

  • El-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul 45:215–224

    Article  CAS  Google Scholar 

  • Fariduddin Q, Hayat S, Ahmad A (2003) Salicylic acid influences net photosynthetic rate, carboxylation efficiency, nitrate reductase activity, and seed yield in Brassica juncea. Photosynthetica 41:281–284

    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 

  • Gautam S, Singh PK (2009) Salicylic acid-induced salinity tolerance in corn grown under NaCl stress. Acta Physiol Plant 31:1185–1190

    Article  CAS  Google Scholar 

  • Gunes A, Inal A, Alpaslan M, Cicek N, Guneri E, Eraslan F, Guzelordu T (2005) Effects of exogenously applied salicylic acid on the induction of multiple stress tolerance and mineral nutrition in maize (Zea mays L.). Arch Agron Soil Sci 51:687–695

    Article  CAS  Google Scholar 

  • Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164:728–736

    Article  PubMed  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 

  • Idrees M, Naeem M, Aftab T, Khan MMA, Moinuddin (2011) Salicylic acid mitigates salinity stress by improving antioxidant defence system and enhances vincristine and vinblastine alkaloids production in periwinkle [Catharanthus roseus (L.) G. Don]. Acta Physiol Plant. doi:10.1007/s11738-010-0631-6

  • Jaleel CA, Gopi R, Sankar B, Manivannan P, Kishorekumar A, Sridharan R, Panneerselvam R (2007) Studies on germination, seedling vigour, lipid peroxidation and proline metabolism in Catharanthus roseus seedlings under salt stress. S Afr J Bot 73:190–195

    Article  Google Scholar 

  • Jaleel CA, Riadh K, Gopi R, Manivannan P, Ines J, Al-Juburi HJ, Chang-**ng 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 

  • Jaworski EG (1971) Nitrate reductase assay in intact plant tissue. Biochem Biophys Res Commun 43:1274–1279

    Article  PubMed  CAS  Google Scholar 

  • Khan MH, Panda SK (2008) Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaCl-salinity stress. Acta Physiol Plant 30:89–91

    Google Scholar 

  • Khan W, Prithiviraj B, Smith D (2003) Photosynthetic response of corn and soybean to foliar application of salicylates. J Plant Physiol 160:485–492

    Article  PubMed  CAS  Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Khan MMA, Naeem M (2007) Salinity induced changes in growth, enzyme activities, photosynthesis, proline accumulation and yield in linseed genotypes. World J Agri Sci 3:685–695

    Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M, Khan MMA (2010) Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol Plant 32:121–132

    Article  Google Scholar 

  • Khodary SEA (2004) Effect of salicylic acid on the growth, photosynthesis and carbohydrate metabolism in salt-stressed maize plants. J Agric Biol 6:5–8

    CAS  Google Scholar 

  • Koca H, Bor M, Özdemir F, Türkan I (2007) The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ Exp Bot 60:344–351

    Article  CAS  Google Scholar 

  • Kremsner PG, Krishna S (2004) Antimalarial combinations. Lancet 364:285–294

    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 

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

  • Lutts S, Kinet JM, Bouharmont J (1995) Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. J Exp Bot 46:1843–1852

    Article  CAS  Google Scholar 

  • Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM, Karpinski S (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57:1795–1807

    Article  PubMed  CAS  Google Scholar 

  • Meneguzzo S, Navari-Izzo F, Izzo R (1999) Antioxidative responses of shoots and roots of wheat to increasing NaCl concentrations. J Plant Physiol 155:274–280

    CAS  Google Scholar 

  • Mishra A, Choudhuri MA (1999) Effects of salicylic acid on heavy metal-induced membrane deterioration mediated by lipoxygenase in rice. Biol Plant 42:409–415

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • More SD, Hangarge DS, Raghavaiah CV, Joshi BM (2004) Performance of different safflower, Carthamus tinctorious L. genotypes with varied soil salinity levels. J Oilseeds Res 21:196–197

    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 

  • Nathawat NS, Kuhad MS, Goswami CL, Patel AL, Kumar R (2005) Nitrogen-metabolizing enzymes: effect of nitrogen sources and saline irrigation. J Plant Nutr 28:1089–1101

    Article  CAS  Google Scholar 

  • Noreen Z, Ashraf M, Akram NA (2010) Salt-induced regulation of some key antioxidant enzymes and physio-biochemical phenomena in five diverse cultivars of turnip (Brassica rapa L.). J Agron Crop Sci 196:273–285

    CAS  Google Scholar 

  • Prasad A, Kumar D, Anwar M, Singh DV, Jain DC (1998) Response of Artemisia annua L. to soil salinity. J Herbs Spices Med Plants 5:49–55

    Article  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 

  • Qian Z, Gong K, Zhang L, Lv J, **g F, Wang Y, Guan S, Wang G, Tang K (2007) A simple and efficient procedure to enhance artemisinin content in Artemisia annua L. by seeding to salinity stress. African J Biotech 6:1410–1413

    CAS  Google Scholar 

  • Qureshi MI, Israr M, Abdin MZ, Iqbal M (2005) Responses of Artemisia annua L. to lead and salt-induced oxidative stress. Environ Exp Bot 53:185–193

    Article  CAS  Google Scholar 

  • Seeman JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomatal behaviour and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L. Planta 164:151–162

    Article  Google Scholar 

  • Shi Q, Bao Z, Zhu Z, Ying Q, Qian Q (2006) Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativa L. Plant Growth Regul 48:127–135

    Article  CAS  Google Scholar 

  • Siddiqui MH, Khan MN, Mohammad F, Khan MMA (2008) Role of nitrogen and gibberellin (GA3) in the regulation of enzyme activities and in osmoprotectant accumulation in Brassica juncea L. under salt stress. J Agron Crop Sci 194:214–224

    Article  CAS  Google Scholar 

  • Silveira JAG, Melo ARB, Viegas RA, Oliveira JTA (2001) Salinity induced effects on nitrogen assimilation related to growth in cowpea plants. Environ Exp Bot 46:171–179

    Article  CAS  Google Scholar 

  • Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39:137–141

    Article  CAS  Google Scholar 

  • Stepien P, Klobus G (2006) Water relations and photosynthesis in Cucumis sativus L. leaves under salt stress. Biol Plant 50:610–616

    Article  CAS  Google Scholar 

  • Stevens J, Senaratna T, Sivasithamparam K (2006) Salicylic acid induces salinity tolerance in tomato (Lycopersicon esculentum cv. Roma): associated changes in gas exchange, water relations and membrane stabilization. Plant Growth Regul 49:77–83

    CAS  Google Scholar 

  • Sudhir P, Murthy SDS (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:481–486

    Article  CAS  Google Scholar 

  • Syeed S, Khan NA (2010) Physiological aspects of salicylic acid-mediated salinity tolerance in plants. In: Anjum NA (ed) Plant nutrition and abiotic stress tolerance I. Plant stress 4(special issue 1), pp 39–46

  • Van Agtmael MA, Eggelte TA, van Boxtel CJ (1999) Artemisinin drugs in the treatment of malaria: from medicinal herb to registered medication. Trends Pharmacol Sci 20:199–204

    Article  PubMed  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 LJ, Li SH (2006) Thermotolerance and related antioxidant enzyme activities induced by heat acclimation and salicylic acid in grape (Vitis vinifera L.) leaves. Plant Growth Regul 48:137–144

    Article  CAS  Google Scholar 

  • Yang Y, Qi M, Mei C (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919

    Article  PubMed  CAS  Google Scholar 

  • Yildirim E, Turan M, Guvenc I (2008) Effect of foliar salicylic acid applications on growth chlorophyll and mineral content of cucumber (Cucumis sativus L.) grown under salt stress. J Plant Nutr 31:593–612

    Article  CAS  Google Scholar 

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

    Google Scholar 

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Acknowledgments

The authors thank Prof. J. F. S. Ferreira of the U.S. Department of Agriculture—Agriculture Research Service, West Virginia, for his valuable suggestions on cultivation of A. annua plants in India. Financial support to the first author in the form of a Research Assistantship by the Council of Science and Technology, UP, Lucknow (CST/D-3539) is also gratefully acknowledged.

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Aftab, T., Khan, M.M.A., da Silva, J.A.T. et al. Role of Salicylic Acid in Promoting Salt Stress Tolerance and Enhanced Artemisinin Production in Artemisia annua L.. J Plant Growth Regul 30, 425–435 (2011). https://doi.org/10.1007/s00344-011-9205-0

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