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Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L.

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Abstract

Annual wormwood (Artemisia annua L.) produces an array of complex terpenoids including artemisinin, a compound of current interest in the treatment of drug-resistant malaria. However, this promising antimalarial compound remains expensive and is hardly available on the global scale. Synthesis of artemisinin has not been proved to be feasible commercially. Therefore, increase in yield of naturally occurring artemisinin is an important area of investigation. The effects of inoculation by two arbuscular mycorrhizal (AM) fungi, Glomus macrocarpum and Glomus fasciculatum, either alone or supplemented with P-fertilizer, on artemisinin concentration in A. annua were studied. The concentration of artemisinin was determined by reverse-phase high-performance liquid chromatography with UV detection. The two fungi significantly increased concentration of artemisinin in the herb. Although there was significant increase in concentration of artemisinin in nonmycorrhizal P-fertilized plants as compared to control, the extent of the increase was less compared to mycorrhizal plants grown with or without P-fertilization. This suggests that the increase in artemisinin concentration may not be entirely attributed to enhanced P-nutrition and improved growth. A strong positive linear correlation was observed between glandular trichome density on leaves and artemisinin concentration. Mycorrhizal plants possessed higher foliar glandular trichome (site for artemisinin biosynthesis and sequestration) density compared to nonmycorrhizal plants. Glandular trichome density was not influenced by P-fertilizer application. The study suggests a potential role of AM fungi in improving the concentration of artemisinin in A. annua.

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References

  • Allen SE (1989) Chemical analysis of ecological materials, 2nd edn. Blackwell Scientific Publishers, Oxford, London

    Google Scholar 

  • Arnon DJ (1949) Copper enzyme in isolated chloroplasts polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avery MA, Chang WKM, White CJ (1992) Stereoselective total synthesis of (+)-artemisinin, the antimalarial constituent of Artemisia annua L. J Am Chem Soc 114:974–979

    Article  CAS  Google Scholar 

  • Biermann BJ, Linderman RG (1981) Quantifying vesicular arbuscular mycorrhizae: a proposed method towards standardization. New Phytol 89:57–63

    Google Scholar 

  • Blanke V, Renker C, Wagner M, Füllner K, Held M, Kuhn AJ, Buscot F (2005) Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytol 166:981–992

    Article  CAS  PubMed  Google Scholar 

  • Bryla DR, Duniway JM (1997) Effects of mycorrhizal infection on drought tolerance and recovery in safflower and wheat. Plant Soil 197:95–103

    Article  CAS  Google Scholar 

  • Burleigh SH, Cavagnaro T, Jakobsen I (2002) Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J Exp Bot 53:1593–1601

    Article  CAS  PubMed  Google Scholar 

  • Charles DJ, Simon JE, Wood KV, Heinstein P (1990) Germplasm variation in artemisinin content of Artemisia annua L. using an alternative method of artemisinin analysis from crude plant extracts. J Nat Prod 53:157–160

    Article  CAS  Google Scholar 

  • Copetta C, Lingua G, Berta G (2006) Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. Var. Genovese. Mycorrhiza 16:485–494 DOI 10.1007/s00572-006-0065-6

    Article  CAS  PubMed  Google Scholar 

  • Dixon RK, Garret HE, Cox GS (1988) Cytokinins in the root pressure exudate of Citrus Jambhiri Lush. colonized by vesicular arbuscular mycorrhiza. Tree Physiol 4:9–18

    Article  CAS  PubMed  Google Scholar 

  • Duke MV, Paul RN, El-Sohly HN, Strutz G, Duke SO (1994) Localization of artemisinin and artemisitene in foliar tissues of glanded and glandless biotypes of Artemisia annua L. Int J Plant Sci 155:365–372

    Article  Google Scholar 

  • Enserink M (2005) Source of new hope against malaria is in short supply. Science 307:33

    Article  CAS  PubMed  Google Scholar 

  • Ferreira JFS, Janick J (1995) Floral morphology of Artemisia annua with special reference to trichomes. Int J Plant Sci 156:807–815

    Article  Google Scholar 

  • Fitter AH (1988) Water relations of red clover Trifolium pretense L. as affected by VA mycorrhizal infection and phosphorus supply before and during drought. J Exp Bot 202:595–603

    Article  Google Scholar 

  • Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175

    Article  Google Scholar 

  • Hiscox JD, Israelstam CP (1979) A method for extraction of chlorophyll from leaf tissues without maceration. Can J Bot 57:1331–1334

    Article  Google Scholar 

  • Kapoor R, Bhatnagar AK (2007) IAttenuation of cadmium toxicity in mycorrhizal Celery (Apium graveolens L.). World J Microbiol Biotechnol (in press) DOI 10.1007/s11274-006-9337-8

  • Kapoor R, Giri B, Mukerji KG (2002a) Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in dill (Anethum graveolens L.) and carum (Trachyspermum ammi (Linn.) Sprague). World J Microbiol Biotechnol 18:459–463

    Article  CAS  Google Scholar 

  • Kapoor R, Giri B, Mukerji KG (2002b) Mycorrhization of coriander (Coriandrum sativum L.) to enhance the concentration and quality of essential oil. J Sci Food Agric 88:1–4

    Google Scholar 

  • Kapoor R, Giri B, Mukerji KG (2004) Improved growth and essential oil yield and quality in Foeniculum vulgare Mill. on mycorrhizal inoculation supplemented with P-fertilizer. Bioresour Technol 93:307–311

    Article  CAS  PubMed  Google Scholar 

  • Khaosaad T, Vierheilig H, Nell M, Zitterl-Eglseer K, Noval J (2006) IArbuscular mycorrhiza alter the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 16:443–446

    Article  CAS  PubMed  Google Scholar 

  • Munkrold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364

    Article  Google Scholar 

  • Nair MSR, Acton N, Klayman DL, Kendrick K, Basile DV, Mante S (1986) Production of artemisinin in tissue cultures of Artemisia annua. J Nat Prod 49:504–507

    Article  CAS  PubMed  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–160

    Article  Google Scholar 

  • Qian G-P, Yang Y-W, Ren Q-L (2005) Determination of artemisinin in Artemisia annua L. by reversed phase HPLC. J Liq Chromatogr Relat Technol 22:705–712

    Article  Google Scholar 

  • Ram M, Jain DC, Kumar S (1997) Cultivation of Quinghaosu Artemisia annua In: Farm bulletin no. 003. Central Institute of Medicinal and Aromatic Plants, Lucknow

    Google Scholar 

  • Ravnskov S, Jakobsen I (1995) Functional compatibility in arbuscular mycorrhizas measured as hyphae P transport to the plant. New Phytol 129:611–618

    Article  Google Scholar 

  • Ro DK et al (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440:940–943

    Article  CAS  PubMed  Google Scholar 

  • Sailo GL, Bagyaraj DJ (2005) Influence of different AM-fungi on the growth, nutrition and forskolin content of Coleus forskohlii. Mycol Res 109:795–798

    Article  CAS  PubMed  Google Scholar 

  • Sharma MP, Gaur A, Bhatia NP, Adholeya A (1996) Growth responses and dependence of Acacia nilotica var. cupressiformis on the indigenous arbuscular mycorrhizal consortium of a marginal wasteland soil. Mycorrhiza 6:441–446

    Article  Google Scholar 

  • Shukla A, Abad Farooqi AH, Shukla YN, Sharma S (1992) Effect of triacontanol and chlormequat on growth, plant hormones and artemisinin yield in Artemisia annua L. Plant Growth Regul 11:165–171

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Smith FA, Jakobsen I, Smith SE (2000) Spatial differences in acquisition of soil phosphate between two arbuscular mycorrhizal fungi in symbiosis with Medicago truncatula. New Phytol 147:357–366

    Article  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Taiz L, Zeiger E (1998) Plant physiology, 2nd edn. Sinauer, Sunderland

    Google Scholar 

  • Ultra V, Tanaka S, Sakurai K, Iwasaki K (2007) Effects of arbuscular mycorrhizal and phosphorus application on arsenic toxicity in sunflower (Helianthus annuus l.) and on the transformation of arsenic in the rhizosphere. Plant Soil 290:29–41

    Article  CAS  Google Scholar 

  • van Gelgre E, Vergauwe A, van den Eeckhout E (1997) State of the art of the production of the antimalarial compound artemisinin in plants. Plant Mol Biol 33:199–209

    Article  Google Scholar 

  • Wagner GF (1991) Secreting glandular trichomes. Plant Physiol 96:675–679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warcup JH, Mc Gee PA (1983) The mycorrhizal associations in some Australian Asteraceae. New Phytol 95:667–672

    Article  Google Scholar 

  • Wu S, Schalk M, Clark A, Miles RB, Coates R, Chappel J (2006) Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat Biotechnol 24:1441–1447

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was funded by the Department of Science and Technology, New Delhi, India. We are thankful to the Director of the National Bureau of Plant Genetic Resources, Regional Station Bhowali (Uttaranchal), for providing seeds of A. annua.

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Correspondence to Rupam Kapoor.

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Kapoor, R., Chaudhary, V. & Bhatnagar, A.K. Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L.. Mycorrhiza 17, 581–587 (2007). https://doi.org/10.1007/s00572-007-0135-4

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