RESEARCH ARTICLE

Optimizing nitrogen levels combined with gibberellic acid for enhanced yield, photosynthetic attributes, enzyme activities, and artemisinin content of Artemisia annua

  • Tariq AFTAB ,
  • M. Masroor A. KHAN ,
  • Mohd. IDREES ,
  • M. NAEEM ,
  • MOINUDDIN
Expand
  • Plant Physiology Section, Department of Botany, Aligarh Muslim University, Aligarh- 202 002, India

Received date: 25 Sep 2010

Accepted date: 13 Oct 2010

Published date: 05 Mar 2011

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

Abstract

BoldItalic L. is an aromatic-antibacterial herb that destroys malarial parasites, lowers fever, and checks bleeding, and from which the secondary compound of interest is artemisinin. It has become increasingly popular as an effective and safe alternative therapy against malaria, and its derivatives are effective against multidrug resistant BoldItalic strains. Nitrogen is required by the plants in the largest quantity and is most limiting where biomass production is desired. On the other hand, gibberellic acid plays an important role in flowering, growth, and development and also in other physiological and biochemical processes. The feasibility of foliar GA3 (75 mg·L-1) alone or with varying levels of soil applied nitrogen (40, 80, and 120 mg·kg-1 soil) was tested on BoldItalic in the present study. The application of GA3 proved effective in alleviating the growth, photosynthesis, and enzyme activities of BoldItalic. However, N levels combined with GA3 showed better responses, and further improvement in these parameters was observed. Furthermore, the most important task we were interested in was to increase the artemisinin content and its yield on a per plant basis. The N combination (80 mg·kg-1 soil) together with GA3 augmented the content (21.8% more) and yield (55.8% more); this is true for both the treated plants, which were more than the control.

Cite this article

Tariq AFTAB , M. Masroor A. KHAN , Mohd. IDREES , M. NAEEM , MOINUDDIN . Optimizing nitrogen levels combined with gibberellic acid for enhanced yield, photosynthetic attributes, enzyme activities, and artemisinin content of Artemisia annua[J]. Frontiers of Agriculture in China, 0 , 5(1) : 51 -59 . DOI: 10.1007/s11703-011-1065-7

Acknowledgements

The authors would like to thank Mr. M. Ram (SRF-CSIR) for his kind help in HPLC analysis of artemisinin. The financial assistance to the first author in the form of RA fellowship by Council of Science and Technology, UP, Lucknow (CST/D-3539) is gratefully acknowledged.
1
Abdin M Z, Israr M, Rehman R U, Jain S K (2003). Artemisinin, a novel antimalarial drug: biochemical and molecular approaches for enhanced production. Planta Med, 69(4): 289-299

DOI PMID

2
Aftab T, Khan M M A, Idrees M, Naeem M, Ram M (2010b). Boron induced oxidative stress, antioxidant defense response and changes in artemisinin content in Artemisia annua L. J Agron Crop Sci, 196(6): 423-430

DOI

3
Aftab T, Khan M M A, 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(4): 273-281

DOI

4
Akhila A (2007). Metabolic engineering of biosynthetic pathways leading to isoprenoids: Mono- and sesquiterpenes in plastids and cytosol. J Plant Interact, 2(4): 195-204

DOI

5
Ashraf M, Ali Q, Iqbal Z (2006). Effect of nitrogen application rate on the content and composition of oil, essential oil and minerals in black cumin (Nigella sativa L.) seeds. J Sci Food Agric, 86(6): 871-876

DOI

6
Buchanan B B, Gruissem W, Jones R L (2000). Biochemistry and Molecular Biology of Plants, American Society of Plant Physiologists. Rockville, Maryland

7
Davies M J, Atkinson C J, Burns C, Woolley J G, Hipps N A, Arroo R R J, Dungey N, Robinson T, Brown P, Flockart I, Hill C, Smith L, Bentley S (2009). Enhancement of artemisinin concentration and yield in response to optimization of nitrogen and potassium supply to Artemisia annua. Ann Bot (Lond), 104(2): 315-323

DOI PMID

8
Duke S O, Paul R N (1993). Development and fine structure of the glandular trichomes of Artemisia annua L. Int J Plant Sci, 154(1): 107-118

DOI

9
Dwivedi R S, Randhawa N S (1974). Evaluation of rapid test for hidden hunger of zinc in plants. Plant Soil, 40(2): 445-451

DOI

10
Fernandes M S, Rossiello R O P (1995). Mineral nitrogen in plant physiology and plant nutrition. Crit Rev Plant Sci, 14: 111-148

11
Ferreira J F S (2007). Nutrient deficiency in the production of artemisinin, dihydroartemisinic acid, and artemisinic acid in Artemisia annua L. J Agric Food Chem, 55(5): 1686-1694

DOI PMID

12
Ferreira J F S, Laughlin J C, Delabays N, Magalhães P M, de Magalhães P M (2005). Cultivation and genetics of Artemisia annua L. for increased production of the antimalarial artemisinin. Plant Genetic Res, 3: 206-229

DOI

13
Ferreira J F S, Simon J E, Janick J (1997). Artemisia annua: botany, horticulture and pharmacology. Hort Rev (Am Soc Hortic Sci), 19: 319-371

14
Gautam A K, Kumar D, Shivay Y S, Mishra B N (2008). Influence of nitrogen levels and plant spacing on growth, productivity and quality of two inbred varieties and a hybrid of aromatic rice. Arch Agron Soil Sci, 54(5): 515-532

DOI

15
Georgios A, Dimou M, Flemetakis E, Plati F, Katinakis P, Drossopoulos J B (2004). Immunolocalization of carbonic anhydrase and phosphoenolpyruvate carboxylase in developing seeds of Medicago sativa. Plant Physiol Biochem42: 181-186

16
Jaworski E G (1971). Nitrate reductase assay in intact plant tissues. Biochem Biophys Res Commun, 43(6): 1274-1279

DOI PMID

17
Khan N A, Ansari H R, Samiullah (1998). Effect of gibberellic acid spray during ontogeny of mustard on growth, nutrient uptake and yield characteristics. J Agron Crop Sci, 181(1): 61-73

DOI

18
Khan N A, Mir R, Khan M, Javid S, Samiullah (2002). Effects of gibberellic acid spray on nitrogen yield efficiency of mustard growth with different nitrogen levels. Plant Growth Regul, 38(3): 243-247

DOI

19
Khan R, Khan M M A, Singh M, Nasir S, Naeem M, Siddiqui M H, Mohammad F (2007). Gibberellic acid and triacontanol can ameliorate the opium yield and morphine production in opium poppy (Papaver somniferum L.). Acta Agric Scand B Soil Plant Sci, 57: 307-312

20
Klayman D L (1985). Qinghaosu (artemisinin): an antimalarial drug from China. Science, 228(4703): 1049-1055

DOI PMID

21
Kremsner P G, Krishna S (2004). Antimalarial combinations. Lancet, 364(9430): 285-294

DOI PMID

22
Lichtenthaler H K, Buschmann C (2001). Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protoc Food Analyt Chem. John Wiley and Sons (New York),F4.3.1-F4.3.8

23
Lindner R C (1944). Rapid analytical methods for some of the common inorganic constitutes of plant tissues. Plant Physiol, 19(1): 76-89

DOI PMID

24
Malaria R B (2004). Malaria in Africa. http://www.rbm.who.int/cmc_upload/0/000/015/ 370/ RBMInfosheet _3.htm

25
Marschner H (2002). Mineral Nutrition of Higher Plants, 2nd ed. London: Academic Press

26
Meshnick S R, Jefford C W, Posner G H, Avery M A, Peters W (1996). Second-generation antimalarial endoperoxides. Parasitol Today, 12(2): 79-82

DOI PMID

27
Mohammad F, Khan T, Afridi R M, Fatma A (1997). Effect of nitrogen on carbonic anhydrase activity, stomatal conductance, net photosynthetic rate and yield of mustard. Photosynthetica, 34(4): 595-598

DOI

28
Nathawat N S, Kuhad M S, Goswami C L, Patel A L, Kumar R (2005). Nitrogen-metabolizing enzymes: effect of nitrogen sources and saline irrigation. J Plant Nutr, 28(6): 1089-1101

DOI

29
Novozamsky I, Houba V J G, Eck R V, Vark V W (1983). A noval digestion technique for multi-element plant analysis. Commun Soil Sci Plant Anal, 14(3): 239-248

DOI

30
Ohlsson A B, Bjork L (1988). Effects of gibberellic acid on cardenolide accumulation by Digitalis lanata tissue cultures grown in light and darkness. J Plant Physiol, 133: 535-538

31
Ozguven M, Sener B, Orhan I, Sekerglu N, Kirpik M, Kartal M, Pesin I, Kaya Z (2008). Effects of varying nitrogen doses on yield, yield components and artemisinin content of Artemisia annua L. Ind Crops Prod, 27(1): 60-64

DOI

32
Ries S K, Wert V (1977). Growth responses of rice seedlings to triacontanol in light and dark. Planta, 135(1): 77-82

DOI

33
Ritchey K D, Ferreira J F S (2006). Short term response of Artemisia annua to Lime, P, K and N in a dystrophic soil. J Herbs Spices Med Plants, 12(1): 49-59

DOI

34
Roth-Bejerano N, Lips S H (1970). Hormonal regulation of nitrate reductase activity in leaves. New Phytol, 69(1): 165-169

DOI

35
Sadowska A, Racka M, Staszkiewicz J, Sadowska M (1984). Effect of some growth substances upon rooting of cuttings, yield and alkaloid content of Catharanthus roseus. Acta Hortic, 144: 99-102

36
Salisbury F B, Ross C W (1992). Plant Physiology, 2nd ed. Wadsworth Publishing Company, Inc., Belmont

37
Santos B M, Morales-Payan J P, Stall W M, Dusky J A (1998). Effects of gibberrellic acid combinations on basil growth. Proc Soil Crop Sci Soc Fla, 57: 99-101

38
Sekeroglu N, Ozguven M (2006). Effects of different nitrogen doses and plant densities on yield and quality of Oenothera biennis L. grown in irrigated lowland and un-irrigated dryland conditions. Turk J Agric For, 30: 125-135

39
Shah S H, Ahmad I, Samiullah (2007). Responses of Nigella sativa to foliar application of gibberellic acid and kinetin. Biol Plant, 51(3): 563-566

DOI

40
Shukla A, Farooqi A H A, Shukla Y N, Sharma S (1992). Effect of triacontanol and chlormequat on growth, plant hormones and artemisinin yield in Artemisia annua L. Plant Growth Regul, 11(2): 165-171

DOI

41
Siddiqui M H, Khan M N, Mohammad F, Khan M M A (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(3): 214-224

DOI

42
Singh M (2001). Effects of nitrogen, phosphorus and potassium nutrition on herb, oil and artemisinin yield of Artemisia annua under semi-arid tropical condition. J Med Arom Plant Sci, 20: 368-369

43
Singh N, Luthra R, Sangwan R S (1990). Oxidative pathway of essential oil biosynthesis in the developing Cymbopogon flexuosus leaf. Plant Physiol Biochem, 28: 703-710

44
Singh P, Srivastava N K, Mishra A, Sharma S (1999). Influence of ethereal and gibberellic acid on carbon metabolism, growth and essential oil accumulation in spearmint (Mentha spicata). Photosynthetica, 36(4): 509-517

DOI

45
Taiz L, Zeiger E (2006). Plant Physiology,4th ed. Sinauer Associates Inc., Publishers, Sunderland, Massachusetts, USA

46
van Agtmael M A, Eggelte T A, van Boxtel C J (1999). Artemisinin drugs in the treatment of malaria: from medicinal herb to registered medication. Trends Pharmacol Sci, 20(5): 199-205

DOI PMID

47
von Wiren N, Gazzarrini S, Gojon A, Frommer W B (2000). The molecular physiology of ammonium uptake and retrieval. Curr Opin Plant Biol, 3(3): 254-261

DOI PMID

48
Weathers P J, Bunk G, Mccoy M C (2005). The effect of phytohormones on growth and artemisinin production in Artemisia annua hairy roots. In Vitro Cell Dev Biol Plant, 41(1): 47-53

DOI

49
WHO (2006). WHO Guidelines for the Treatment of Malaria. World Health Organization

50
Yuan L, Xu D Q (2001). Stimulation effect of gibberellic acid short-term treatment on leaf photosynthesis related to the increase in Rubisco content in broad bean and soybean. Photosynth Res, 68(1): 39-47

DOI PMID

51
Zhang Y S, Ye H C, Liu B Y, Wang H, Li G F (2005). Exogenous GA3 and flowering induce the conversion of artemisinic acid to artemisinin in Artemisia annua plants. Russ J Plant Physiol, 52(1): 58-62

DOI

52
Zhao S S, Zeng M Y (1986). Determination of qinghaosuin in Artemisia annua L. by high performance liquid chromatography. Chinese J Pharma Anal, 6: 3-5

Outlines

/