Biosynthetic Capacity of Artemisia annua L. “Hairy” Roots

Authors

Keywords:

Artemisia annua, , carbohydrates, amino acids

Abstract

Transformation using Agrobacterium rhizogenes is a widely used method for obtaining “hairy” roots of different plant species. Such roots are characterized by rapid growth under simple growing conditions. Incorporation of bacterial rol genes into the plant genome after the transformation can lead to changes in bioactive compounds synthesis in "hairy" roots. Analysis of the content of carbohydrates and amino acids in Artemisia annua L. “hairy” roots was the aim of the work Inulin content in transgenic root lines increased by 1.52 - 1.86 folds compared to the roots of the control plants. The “hairy” roots lines, in contrast, to the control plants, did not contain inositol. There was a decreased glutamine (up to 5.92 folds) and increased arginine hydrochloride (up to 1.72 folds) and proline (up to 2.53 folds) content in transformed root lines. Seven of the total identified amino acids are indispensable amino acids: valine, isoleucine, leucine, lysine, threonine, tryptophan, and phenylalanine. The results of the study demonstrated that the genetic transformation of A. annua plants has led to changes in the accumulation of carbohydrates and amino acids (both quantitatively and qualitatively). “Hairy” root lines with increased content of individual carbohydrates and amino acids were identified.

References

Aires, A., Fernandes, C., Carvalho, R., Bennett, R. N., Saavedra, M. J., & Rosa, E. A. S. (2011). Seasonal Effects on Bioactive Compounds and Antioxidant Capacity of Six Economically Important Brassica Vegetables. Molecules, 16(8), 6816–6832. https://doi.org/10.3390/MOLECULES16086816

Anwar, A., She, M., Wang, K., Riaz, B., & Ye, X. (2018). Biological Roles of Ornithine Aminotransferase (OAT) in Plant Stress Tolerance: Present Progress and Future Perspectives. International Journal of Molecular Sciences 2018, Vol. 19, Page 3681, 19(11), 3681. https://doi.org/10.3390/IJMS19113681

Balasubramanian, M., Anbumegala, M., Surendran, R., Arun, M., & Shanmugam, G. (2018). Elite hairy roots of Raphanus sativus (L.) as a source of antioxidants and flavonoids. 3 Biotech, 8(2), 128. https://doi.org/10.1007/s13205-018-1153-y

Brown, G. D. (2010). The Biosynthesis of Artemisinin (Qinghaosu) and the Phytochemistry of Artemisia annua L. (Qinghao). Molecules 2010, Vol. 15, Pages 7603-7698, 15(11), 7603–7698. https://doi.org/10.3390/MOLECULES15117603

Caleffi, E. R., Krausová, G., Hyršlová, I., Paredes, L. L. R., dos Santos, M. M., Sassaki, G. L., Gonçalves, R. A. C., & de Oliveira, A. J. B. (2015). Isolation and prebiotic activity of inulin-type fructan extracted from Pfaffia glomerata (Spreng) Pedersen roots. International Journal of Biological Macromolecules, 80, 392–399. https://doi.org/10.1016/J.IJBIOMAC.2015.06.053

Cardillo, A. B., Rodriguez Talou, J., & Giulietti, A. M. (2016). Establishment, Culture, and Scale-up of Brugmansia candida Hairy Roots for the Production of Tropane Alkaloids. Methods in Molecular Biology, 1391, 173–186. https://doi.org/10.1007/978-1-4939-3332-7_12

Cérantola, S., Kervarec, N., Pichon, R., Magné, C., Bessieres, M. A., & Deslandes, E. (2004). NMR characterisation of inulin-type fructooligosaccharides as the major water-soluble carbohydrates from Matricaria maritima (L.). Carbohydrate Research, 339(14), 2445–2449. https://doi.org/10.1016/J.CARRES.2004.07.020

Corrêa-Ferreira, M. L., Noleto, G. R., & Oliveira Petkowicz, C. L. (2014). Artemisia absinthium and Artemisia vulgaris: A comparative study of infusion polysaccharides. Carbohydrate Polymers, 102(1), 738–745. https://doi.org/10.1016/J.CARBPOL.2013.10.096

Daddy, N. B., Kalisya, L. M., Bagire, P. G., Watt, R. L., Towler, M. J., & Weathers, P. J. (2017). Artemisia annua dried leaf tablets treated malaria resistant to ACT and i.v. artesunate: Case reports. Phytomedicine, 32, 37–40. https://doi.org/10.1016/J.PHYMED.2017.04.006

de Vries, P. J., & Dien, T. K. (1996). Clinical Pharmacology and Therapeutic Potential of Artemisinin and its Derivatives in the Treatment of Malaria. Drugs 1996 52:6, 52(6), 818–836. https://doi.org/10.2165/00003495-199652060-00004

Drobot, K. O., Matvieieva, N. А., & Shakhovsky, A. M. (2016). Features of Agrobacterium rhizogenes-mediated genetic transformation of Artemisia vulgaris L., Artemisia annua L. and Ruta graveolens L. medicinal plants. Faktori Eksperimental’noi Evolucii Organizmiv, 19, 117–120.

Drobot, K. O., Matvieieva, N. A., Ostapchuk, A. M., Kharkhota, M. A., & Duplij, V. P. (2017). Study of artemisinin and sugar accumulation in Artemisia vulgaris and Artemisia dracunculus “hairy” root cultures. Preparative Biochemistry & Biotechnology, 47(8), 776–781. https://doi.org/10.1080/10826068.2017.1342262

Gabr, A. M. M., Sytar, O., Ghareeb, H., & Brestic, M. (2019). Accumulation of amino acids and flavonoids in hairy root cultures of common buckwheat (Fagopyrum esculentum). Physiology and Molecular Biology of Plants, 25(3), 787–797. https://doi.org/10.1007/s12298-019-00669-1

Goldraij, A., & Polacco, J. C. (2000). Arginine degradation by arginase in mitochondria of soybean seedling cotyledons. Planta 2000 210:4, 210(4), 652–658. https://doi.org/10.1007/S004250050056

Haynes, R. (2006). From Artemisinin to New Artemisinin Antimalarials: Biosynthesis, Extraction, Old and New Derivatives, Stereochemistry and Medicinal Chemistry Requirements. Current Topics in Medicinal Chemistry, 6(5), 509–537. https://doi.org/10.2174/156802606776743129

Kim, J. K., Shin, E. C., Lim, H. J., Choi, S. J., Kim, C. R., Suh, S. H., Kim, C. J., Park, G. G., Park, C. S., Kim, H. K., Choi, J. H., Song, S. W., & Shin, D. H. (2015). Characterization of Nutritional Composition, Antioxidative Capacity, and Sensory Attributes of Seomae Mugwort, a Native Korean Variety of Artemisia argyi H. Lév. & Vaniot. Journal of Analytical Methods in Chemistry, 2015, 916346. https://doi.org/10.1155/2015/916346

Koo, K. A., Kwak, J. H., Lee, K. R., Zee, O. P., Woo, E. R., Park, H. K., & Youn, H. J. (1994). Antitumor and immunomodulating activities of the polysaccharide fractions from Artemisia selengensis and Artemisia iwayomogi. Archives of Pharmacal Research, 17(5), 371–374. https://doi.org/10.1007/BF02974179

Lee, J. A., Sung, H. N., Jeon, C. H., Gill, B. C., Oh, G. S., Youn, H. J., & Park, J. H. (2008). AIP1, a carbohydrate fraction from Artemisia iwayomogi, modulates the functional differentiation of bone marrow-derived dendritic cells. International Immunopharmacology, 8(4), 534–541. https://doi.org/10.1016/J.INTIMP.2007.12.005

Mashati, P., Esmaeili, S., Dehghan-Nayeri, N., Bashash, D., Darvishi, M., & Gharehbaghian, A. (2019). Methanolic Extract from Aerial Parts of Artemisia Annua L. Induces Cytotoxicity and Enhances Vincristine-Induced Anticancer Effect in Pre-B Acute Lymphoblastic Leukemia Cells. International Journal of Hematology-Oncology and Stem Cell Research, 13(3), 132–139.

Matvieieva, N., Drobot, K., Duplij, V., Ratushniak, Y., Shakhovsky, A., Kyrpa-Nesmiian, T., Mickevičius, S., & Brindza, J. (2019). Flavonoid content and antioxidant activity of Artemisia vulgaris L. “hairy” roots. Preparative Biochemistry and Biotechnology, 49(1), 82–87. https://doi.org/10.1080/10826068.2018.1536994

Mi, Y., Zhu, Z., Qian, G., Li, Y., Meng, X., Xue, J., Chen, Q., Sun, W., & Shi, Y. (2020). Inducing Hairy Roots by Agrobacterium rhizogenes-Mediated Transformation in Tartary Buckwheat (Fagopyrum tataricum). JoVE (Journal of Visualized Experiments), 2020(157), e60828. https://doi.org/10.3791/60828

Mirbehbahani, F. S., Hejazi, F., Najmoddin, N., & Asefnejad, A. (2020). Artemisia annua L. as a promising medicinal plant for powerful wound healing applications. Progress in Biomaterials 2020 9:3, 9(3), 139–151. https://doi.org/10.1007/S40204-020-00138-Z

Mukatay, U., Kemelbek, M., Seilkhan, A., Ross, S. A., & Zhubanova, A. A. (2021). Study of amino acids in Artemisia heptapotamica Poljak and Artemisia albida Willd. E3S Web of Conferences, 254, 03006. https://doi.org/10.1051/e3sconf/202125403006

Murashige, T., & Skoog, F. (1962). A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiologia Plantarum, 15(3), 473–497. https://doi.org/10.1111/J.1399-3054.1962.TB08052.X

Nair, M. S., Huang, Y., Fidock, D. A., Polyak, S. J., Wagoner, J., Towler, M. J., & Weathers, P. J. (2021). Artemisia annua L. extracts inhibit the in vitro replication of SARS-CoV-2 and two of its variants. Journal of Ethnopharmacology, 274, 114016. https://doi.org/10.1016/J.JEP.2021.114016

Ochkur, A. V., Kovaleva, A. M., & Kolesnik, Y. S. (2013). Amino-Acid Composition of Subgenus Artemisia Herbs. Chemistry of Natural Compounds 2013 49:3, 49(3), 589–591. https://doi.org/10.1007/S10600-013-0684-Z

Pék, Z., Daood, H., Nagyné, M. G., Neményi, A., & Helyes, L. (2013). Effect of environmental conditions and water status on the bioactive compounds of broccoli. Central European Journal of Biology, 8(8), 777–787. https://doi.org/10.2478/s11535-013-0172-7

Rassias, D. J., & Weathers, P. J. (2019). Dried leaf Artemisia annua efficacy against non-small cell lung cancer. Phytomedicine, 52, 247–253. https://doi.org/10.1016/J.PHYMED.2018.09.167

Shysh, S. N., Shutava, H. G., Skakovski, E. D., & Tychinskaya, L. Y. (2017). NMR Investigation of the Composition of Aqueous Extracts from Pot Marigold Inflorescence. Proceedings of the National Academy of Sciences of Belarus, Chemical Series, 3, 45–52.

Skakovski, E. D., Tychinskaya, L. Y., Molchanova, O. A., Kolechkina, A. I., Kukharchik, N. V., & Kapichnikova, N. G. (2013). A preliminary estimation of an apple juice composition using the method of a nuclear magnetic resonance. In V. A. Samus et al. (Eds.), Fruit-growing: proceedings (Vol. 25, pp. 469 – 480). Samochvalovitchi, Belarus: Institute for Fruit Growing.

Skakovskii, E. D., Tychinskaya, L. Y., Matveichuk, S. V., Karankevich, E. G., Agabalaeva, E. D., & Reshetnikov, V. N. (2014). NMR Spectroscopy of Aqueous Extracts of Fenugreek (Trigonella foenum-graecum L.). Journal of Applied Spectroscopy 2014 81:4, 81(4), 597–601. https://doi.org/10.1007/S10812-014-9975-9

Srivastava, S., & Srivastava, A. K. (2007). Hairy Root Culture for Mass-Production of High-Value Secondary Metabolites. Critical Reviews in Biotechnology, 27(1), 29–43. https://doi.org/10.1080/07388550601173918

Uozumi, N. (2004). Large-Scale Production of Hairy Root. Advances in Biochemical Engineering/Biotechnology, 91, 75–103. https://doi.org/10.1007/B94206

Xie, G., Schepetkin, I. A., Siemsen, D. W., Kirpotina, L. N., Wiley, J. A., & Quinn, M. T. (2008). Fractionation and characterization of biologically-active polysaccharides from Artemisia tripartita. Phytochemistry, 69(6), 1359–1371. https://doi.org/10.1016/J.PHYTOCHEM.2008.01.009

Yang, H., Sun, M., Lin, S., Guo, Y., Yang, Y., Zhang, T., & Zhang, J. (2017). Transcriptome analysis of Crossostephium chinensis provides insight into the molecular basis of salinity stress responses. PLOS ONE, 12(11), e0187124. https://doi.org/10.1371/JOURNAL.PONE.0187124

Zhang, G. H., Liang, Y. R., Jin, J., Lu, J. L., Borthakur, D., Dong, J. J., & Zheng, X. Q. (2015). Induction of hairy roots by Agrobacterium rhizogenes in relation to L-theanine production in Camellia sinensis. The Journal of Horticultural Science and Biotechnology, 82(4), 636–640. https://doi.org/10.1080/14620316.2007.11512284

Downloads

Published

2021-12-15

How to Cite

Shutava, H., Tychinskaya, L., Skakovskii, E., Duplij, V., Ratushniak, Y., & Matvieieva, N. (2021). Biosynthetic Capacity of Artemisia annua L. “Hairy” Roots. Natural Products and Biotechnology, 1(2), 85–95. Retrieved from https://natprobiotech.com/index.php/natprobiotech/article/view/18

Issue

Section

Research Article