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Marked enhancement in the artemisinin content and biomass productivity in Artemisia annua L. shoots co-cultivated with Piriformospora indica

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Abstract

A significant enhancement in artemisinin content, an important anti-malarial compound, has been achieved in Artemisia annua L. shoots by co-cultivating with Piriformospora indica, a mycorrhiza-like fungus. The in vitro shoots derived from nodal cultures of A. annua were implanted on four different culture media namely, (i) Murashige & Skoog (MS) basal, (ii) MS + 5 μM indole-3-butyric acid (IBA), (iii) MS + P. indica and, (iv) MS + 5 μM IBA + P. indica. After 2 months, it was observed that the cultures reared on MS + 5 μM IBA + P. indica showed optimum growth in terms of shoot and root proliferation over those cultured without P. indica. The average shoot number on MS + 5 μM IBA + P. indica was 17.83 ± 1.01 and on MS + P. indica alone was 12.75 ± 1.10. A drastic decline in shoot number was observed without P. indica which was 2.0 ± 0.12 on basal and 4.9 ± 1.52 on 5 μM IBA. Similarly, a maximum average of 16.83 ± 0.82 roots were achieved on MS + 5 μM IBA + P. indica which declined to 10.75 ± 1.02 on MS + P. indica. A further decrease in root number occurred in shoots without P. indica, their average being 2.5 ± 0.12 on basal and 8.91 ± 1.57 on 5 μM IBA. HPLC analysis of the aforesaid cultures revealed that the quantity of artemisinin was significantly higher (1.30 ± 0.03 %) in shoots cultured on 5 μM IBA + P. indica compared to those of control (0.80 ± 0.01 %).

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References

  • Achatz B, von Ruden S, Andrade D, Neumann E, Pons-Kuhnemann J, Kogel KH, Franken P, Waller F (2010) Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development. Plant Soil 333:59–70

    Article  CAS  Google Scholar 

  • Baldi A, Farkya S, Jain A, Gupta N, Mehra R, Datta V, Srivastava AK, Bisaria VS (2010) Enhanced production of podophyllotoxins by co-culture of transformed Linum album cells with plant growth-promoting fungi. Pure Appl Chem 82:227–241

    Article  CAS  Google Scholar 

  • Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C, Munnik T, Hirt H, Oelmuller R (2011) The OXI1 kinase pathway mediates Piriformospora indica- induced growth promotion in Arabidopsis. PLoS Pathog 7:e1002051

    Article  CAS  Google Scholar 

  • Ceccarelli N, Curadi M, Martelloni L, Sbrana C, Picciarelli P, Giovannetti M (2010) Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant Soil 335:311–323

    Article  CAS  Google Scholar 

  • Das A, Kamal S, Shakil NA, Sherameti I, Oelmuller R, Dua M, Tuteja N, Johri AK, Varma A (2012) The root endophyte fungus Piriformospora indica leads to early flowering, higher biomass and altered secondary metabolites of the medicinal plant, Coleus forskohlii. Plant Signal Behav 7:103–112

    Article  CAS  Google Scholar 

  • Davis TME, Karunajeewa HA, Illett KF (2005) Artemisinin-based combination therapies for uncomplicated malaria. Med J Aust 182:181–185

    Google Scholar 

  • Delabays N, Simonnet X, Gaudin M (2001) The genetics of artemisinin content in Artemisia annua L. and the breeding of high yielding cultivars. Curr Med Chem 8:1795–1801

    Article  CAS  Google Scholar 

  • Dolatabadi HK, Goltapeh EM, Jaimand K, Rohani N, Varma A (2011) Effects of Piriformospora indica and Sebacina vermifera on growth and yield of essential oil in fennel (Foeniculum vulgare) under greenhouse conditions. J Basic Microbiol 51:33–39

    Article  CAS  Google Scholar 

  • Franken P (2012) The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Appl Microbiol Biotechnol 96:1455–1464

    Article  CAS  Google Scholar 

  • George EF, Hall MA, De Klerk GJ (2008) Plant propagation by tissue culture, 3rd edn. Springer, Dordrecht

    Google Scholar 

  • Giri A, Narasu ML (2000) Transgenic hairy roots: recent trends and applications. Biotechnol Adv 18:1–22

    Article  CAS  Google Scholar 

  • Gosal SK, Karlupia A, Gosal SS, Chibba IM, Varma A (2010) Biotization with Piriformospora indica and Pseudomonas fluorescens improves survival rate, nutrient acquisition, field performance and saponin content of micropropagated Chlorophytum sp. Indian J Biotechnol 9:289–297

    CAS  Google Scholar 

  • Kafer E (1977) Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv Genet 19:33–131

    Article  CAS  Google Scholar 

  • Lee YC, Johnson JM, Chien CT, Sun C, Cai D, Lou B (2011) Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Plant Microb Interact 24:421–431

    Article  CAS  Google Scholar 

  • Malla R, Singh A, Zeyaullah MD, Yadav V, Verma A, Varma A, Rai M (2002) Piriformospora indica and plant growth promoting rhizobacteria: an appraisal. In: Rao GP, Manoharchari C, Bhat DJ, Rajak RC, Lakhanpal TN (eds) Frontiers of fungal diversity in India. International Book Distributing Co, Lucknow, pp 401–419

    Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Rai M, Acharya D, Singh A, Varma A (2001) Positive growth responses of the medicinal plants Spilanthes calva and Withania sominifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11:123–128

    Article  Google Scholar 

  • Rai MK, Varma A, Pandey AK (2004) Enhancement of antimycotic potential in Spilanthes calva after inoculation of Piriformospora indica, a new growth promoter. Mycoses 47:479–481

    Article  CAS  Google Scholar 

  • Satheesan J, Narayanan AK, Sakunthala M (2012) Induction of root colonization by Piriformospora indica leads to enhanced asiaticoside production in Centella asiatica. Mycorrhiza 22:195–202

    Article  CAS  Google Scholar 

  • Schafer P, Pfiffi S, Voll LM, Zajic D, Chandler PM, Waller F, Scholz U, Pons-Kuhnemann J, Sonnewald S, Sonnewald U, Kogel KH (2009) Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J 59:461–474

    Article  Google Scholar 

  • Shahollari B, Varma A, Oelmüller R (2005) Expression of a receptor kinase in roots is stimulated by the basidiomycete Piriformospora indica and the protein accumulates in Triton-X-100 insoluble plasma membrane micro domains. J Plant Physiol 162:945–958

    Article  CAS  Google Scholar 

  • Sun C, Johnson JM, Cai D, Sherameti I, Oelmuller R, Lou B (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid localized CAS protein. J Plant Physiol 167:1009–1017

    Article  CAS  Google Scholar 

  • Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant Microb Interact 21:1371–1383

    Article  CAS  Google Scholar 

  • Vadassery J, Ranf S, Drzewiecki C, Mithofer A, Mazars C, Scheel D, Lee J, Oelmuller R (2009) A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 59:193–206

    Article  CAS  Google Scholar 

  • Varma A, Sudha S, Franken P (1999) Piriformospora indica-a cultivable plant growth promoting root endophyte with similarities to arbuscular mycorrhizal fungi. Appl Environ Microbiol 65:2741–2744

    CAS  Google Scholar 

  • Varma A, Bakshi M, Lou B, Hartmann A, Oelmueller R (2012) Piriformospora indica: a novel plant growth promoting mycorrhizal fungus. Agric Res 1:117–131

    Article  Google Scholar 

  • Verma S, Varma A, Rexer KH, Kost G, Sarbhoy A, Bisen P, Butehorn B, Franken P (1998) Piriformospora indica, gen. nov. sp. nov., a new root-colonizing fungus. Mycologia 95:896–903

    Article  Google Scholar 

  • Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Veena Agrawal and Gaurav Sharma are grateful to the Indian Council of Medical Research (ICMR), New Delhi for providing financial assistance in the form of Major research Project to former and SRF to latter. The authors are also thankful to Professor Ajit Varma, Director, Institute of Microbial Technology, Amity University, NOIDA for providing inoculums of Piriformospora indica.

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  1. Department of Botany, University of Delhi, Delhi, 110007, India

    Gaurav Sharma & Veena Agrawal

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  1. Gaurav Sharma
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  2. Veena Agrawal
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Correspondence to Veena Agrawal.

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Sharma, G., Agrawal, V. Marked enhancement in the artemisinin content and biomass productivity in Artemisia annua L. shoots co-cultivated with Piriformospora indica . World J Microbiol Biotechnol 29, 1133–1138 (2013). https://doi.org/10.1007/s11274-013-1263-y

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