Isolation and identification of growth promoting endophytes from Artemisia annua L. and its effects on artemisinin content

الموضوعات :

Mir Abid Hussain ¹ (Indian Institute of Integrative Medicine (CSIR-IIIM), Council of Scientific and Industrial Research, Canal Road, Jammu-180001, India | Academy of Scientific and Innovative Research, Anusandhan Bhawan, 2 Rafi Marg, New Delhi-110 001, India)
Vidushi Mahajan ² (Indian Institute of Integrative Medicine (CSIR-IIIM), Council of Scientific and Industrial Research, Canal Road, Jammu-180001, India | Academy of Scientific and Innovative Research, Anusandhan Bhawan, 2 Rafi Marg, New Delhi-110 001, India)
Irshad Ahmad Rather ³ (Indian Institute of Integrative Medicine (CSIR-IIIM), Council of Scientific and Industrial Research, Canal Road, Jammu-180001, India)
Praveen Awasthi ⁴ (Indian Institute of Integrative Medicine (CSIR-IIIM), Council of Scientific and Industrial Research, Canal Road, Jammu-180001, India)
Rekha Chouhan ⁵ (Indian Institute of Integrative Medicine (CSIR-IIIM), Council of Scientific and Industrial Research, Canal Road, Jammu-180001, India)
Prabhu Dutt ⁶ (Indian Institute of Integrative Medicine (CSIR-IIIM), Council of Scientific and Industrial Research, Canal Road, Jammu-180001, India)
Yash Pal Sharma ⁷ (Post Graduate Department of Botany, University of Jammu, Jammu and Kashmir, India)
Yashbir S. Bedi ⁸ (Indian Institute of Integrative Medicine (CSIR-IIIM), Council of Scientific and Industrial Research, Canal Road, Jammu-180001, India | Academy of Scientific and Innovative Research, Anusandhan Bhawan, 2 Rafi Marg, New Delhi-110 001, India)
Sumit G. Gandhi ⁹ (Indian Institute of Integrative Medicine (CSIR-IIIM), Council of Scientific and Industrial Research, Canal Road, Jammu-180001, India | Academy of Scientific and Innovative Research, Anusandhan Bhawan, 2 Rafi Marg, New Delhi-110 001, India)

تاريخ الإرسال : 09 الإثنين , شوال, 1438 تاريخ التأكيد : 21 الأربعاء , محرم, 1439 تاريخ الإصدار : 13 الجمعة , ربيع الأول, 1439

الکلمات المفتاحية: <i>Cochliobolus lunatus</i>, elicitor, <i>Colletotrichum gloeosporioides</i>, <i>Curvularia pallescens</i>, <i>Acremonium persicum</i>,

ملخص المقالة :

Artemisinin, a sesquiterpene lactone, is a well-known antimalarial drug isolated from Artemisia annua L. (Asteraceae). Semi-synthetic derivatives of artemisinin like arteether, artemether, artesunate, etc. have also been explored for antimalarial as well as other pharmacological activities. Endophytes are microorganisms which reside inside the living tissues of host plants and can form symbiotic, parasitic or commensalistic relationship depending on the climatic conditions and host genotype. In this study, endophytic fungi were isolated from the leaves of A. annua and were identified using the conventional as well as molecular taxonomic methods. Endophytes were identified as: Colletotrichum gloeosporioides, Cochliobolus lunatus, Curvularia pallescens and Acremonium persicum. Growth promoting activity of endophytes has been reported earlier. After treating potted plants of A. annua with elicitor extracts prepared from these endophytic fungi, we observed an increase in the plant biomass as well as artemisinin content.

المصادر:

Arivudainambi, U.E., Anand, T.D., Shanmugaiah, V., Karunakaran, C., Rajendran, A., 2011. Novel bioactive metabolites producing endophytic fungus Colletotrichum gloeosporioides against multidrug-resistant Staphylococcus aureus. FEMS. Immunol. Med. Microbiol. 61(3), 340-345.

Czechowski, T., Larson, T.R., Catania, T.M., Harvey, D., Brown, G.D., Graham, I.A., 2016. Artemisia annua mutant impaired in artemisinin synthesis demonstrates importance of nonenzymatic conversion in terpenoid metabolism. Proc. Nat. Acad. Sci. 113(52), 15150-15155.

Chithra, S., Jasim, B., Sachidanandan, P., Jyothis, M., Radhakrishnan, E.K., 2013. Piperine production by endophytic fungus Colletotrichum gloeosporioides isolated from Piper nigrum. Phytomedicine 21(4), 534-540.

Dama, S., Abdoulaye A. D., Ogobara K. D., 2017. Methods for monitoring artemisinin-based combination therapies efficacy. Clin. Rev. Opinions 8(1), 1-13.

Dondorp, A.M., Nosten, F., Yi, P., Das, D., Phyo, A.P., Tarning, J., Lwin, K.M., Ariey, F., Hanpithakpong, W., Lee, S.J., Ringwald, P., 2009. Artemisinin resistance in Plasmodium falciparum malaria. N. Engl. J. Med.361(5), 455-467.

Doyle, J.J., Doyle, J.L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull 19, 11-15.

Duke, M.V., Paul, R.N., Elsohly, H.N., Sturtz, G., Duke, S.O., 1994. Localization of artemisinin and artemisitene in foliar tissues of glanded and glandless biotypes of Artemisia annua L. Int. J. Plant Sci. 155(3), 365-372.

El-Deeb, H.M., Arab, Y.A., 2013. Acremonium as an endophytic bioagent against date palm Fusarium wilt. Arch. Phytopathol. Plant Prot. 46(10), 1214-1221.

Elmorshedy, H., Tanner, M., Bergquist, R.N., Sharaf, S., Barakat, R., 2016. Prophylactic effect of artemether on human Schistosomiasis mansoni among Egyptian children: a randomized controlled trial. Acta Tropica 158, 52-58.

Farhi, M., Kozin, M., Duchin, S., Vainstein, A., 2013. Metabolic engineering of plants for artemisinin synthesis. Biotechnol. Genet. Eng. Rev. 29(2), 135-148.

Ferreira, J.F.S., Luthria, D.L., 2010. Drying affects artemisinin, dihydroartemisinic acid, artemisinic acid, and the antioxidant capacity of Artemisia annua L. leaves. J. Agric. Food Chem. 58(3), 1691-1698.

Gandhi, S.G., Mahajan, V., Bedi, Y.S., 2015. Changing trends in biotechnology of secondary metabolism in medicinal and aromatic plants. Planta 241(2), 303-317.

Gupta, S.K., Singh, P., Bajpai, P., Ram, G., Singh, D., Gupta, M.M., Jain, D.C., Khanuja, S.P., Kumar, S., 2002. Morphogenetic variation for artemisinin and volatile oil in Artemisia annua. Ind. Crops Prod. 16(3), 217-224.

Gold, D., Alian, M., Domb, A., Karawani, Y., Jbarien, M., Chollet, J., Haynes, R.K., Wong, H.N., Buchholz, V., Greiner, A., Golenser, J., 2017. Elimination of Schistosoma mansoni in infected mice by slow release of artemisone. Int. J. Parasitol. Drugs Drug Resist. 7(2), 241-247.

Huang, W.Y., Cai, Y., Surveswaran, S., Hyde, K.D., Corke, H., Sun, M., 2009. Molecular phylogenetic identification of endophytic fungi isolated from three Artemisia species. Fungal Divers. 36, 69-88.

Khanuja, S.P.S., Srivastava, S., Kumar, T.R.S., Shasany, A.K., Jain, D.C., Darokar, M.P., Saikia, D., Kumar, S., 2002. Anti-microbial composition and method for producing the same. US6423741.

Kumar, S., Gupta, S.K., Singh, P., Bajpai, P., Gupta, M.M., Singh, D., Gupta, A.K., Ram, G., Shasany, A.K., Sharma, S., 2004. High yields of artemisinin by multi-harvest of Artemisia annua crops. Ind. Crops Prod. 19(1), 77-90.

Lei, C., Ma, D., Pu, G., Qiu, X., Du, Z., Wang, H., Li, G., Ye, H., Liu, B., 2011. Foliar application of chitosan activates artemisinin biosynthesis in Artemisia annua L. Ind. Crops Prod. 33(1), 176-182.

Li, J., Zhao, G.Z., Varma, A., Qin, S., Xiong, Z., Huang, H.Y., Zhu, W.Y., Zhao, L.X., Xu, L.H., Zhang, S., Li, W.J., 2012. An endophytic Pseudonocardia species induces the production of artemisinin in Artemisia annua. PLoS One 7(12), e51410.

Ludwig-Müller, J., 2015. Plants and endophytes: equal partners in secondary metabolite production? Biotechnol. Lett. 37(7), 1325-1334

Lyons, P.C., Evans, J.J., Bacon, C.W., 1990. Effects of the fungal endophyte Acremonium coenophialum on nitrogen accumulation and metabolism in tall fescue. Plant Physiol. 92(3), 726-732.

Ming, Q., Su, C., Zheng, C., Jia, M., Zhang, Q., Zhang, H., Rahman, K., Han, T., Qin, L., 2013. Elicitors from the endophytic fungus Trichoderma atroviride promote Salvia miltiorrhiza hairy root growth and tanshinone biosynthesis. J. Exp. Bot. 64(18), 5687-5694.

Mohammadhosseini, M., 2017. Essential oils extracted using microwave-assisted hydrodistillation from aerial parts of eleven Artemisia species: Chemical compositions and diversities in different geographical regions of Iran. Rec. Nat. Prod. 11(2), 114-129.

Mohammadhosseini, M., Akbarzadeh, A., Hashemi-Moghaddam, H., Mohammadi Nafchi, A., Mashayekhi, H.A., Aryanpour, A., 2016. Chemical composition of the essential oils from the aerial parts of Artemisia sieberi by using conventional hydrodistillation and microwave assisted hydrodistillation: A comparative study. J. Essent. Oil-Bear. Plants 19(1), 32-45.

Mondal, M.M.A., Malek, M.A., Puteh, A.B., Ismail, M.R., Ashrafuzzaman, M., Naher, L., 2012. Effect of foliar application of chitosan on growth and yield in okra. Aust. J. Crop Sci. 6(5), 918.

Mucciarelli, M., Scannerini, S., Bertea, C.M., Maffei, M., 2002. An ascomycetous endophyte isolated from Mentha piperita L.: biological features and molecular studies. Mycologia 94(1), 28-39.

Nageeb, A., Al-Tawashi, A., Emwas, A-H.M., Al-Talla, Z.A-H., Al-Rifai, N., 2013. Comparison of Artemisia annua bioactivities between traditional medicine and chemical extracts. Curr. Bioact. Compd. 9, 324-332.

Nekoei, M., Mohammadhosseini, M., Akhlaghi, H., 2012. Chemical composition of the volatile oils from the aerial parts of Artemisia annua L. (Asteraceae) by using head space solid phase microextraction and hydrodistillation methods prior to gas chromatographic-mass spectrometric determination: A comparative investigation. J. Essent. Oil-Bear. Plants 15(6), 926-933.

Obeid, S., Alen, J., Pham, V.C., Meuleman, P., Pannecouque, C., Le, T.N., Neyts, J., Dehaen, W., Paeshuyse, J., 2013. Artemisinin analogues as potent inhibitors of in vitro hepatitis C virus replication. PLoS One 8(12), e81783.

Olsson, M.E., Olofsson, L.M., Lindahl, A.L., Lundgren, A., Brodelius, M., Brodelius, P.E., 2009. Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L. Phytochemistry 70(9), 1123-1128.

Paddon, C.J., Westfall, P.J., Pitera, D.J., Benjamin, K., Fisher, K., McPhee, D., Leavell, M.D., Tai, A., Main, A., Eng, D., Polichuk, D.R., 2013. High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 496(7446), 528-532.

Pandey, N., Pandey-Rai, S., 2016. Updates on artemisinin: an insight to mode of actions and strategies for enhanced global production. Protoplasma 253(1), 15-30.

Pasha Zanousi, M.B., Nekoei, M., Mohammadhosseini, M., 2016. Composition of the essential oils and volatile fractions of Artemisia absinthium by three different extraction methods: Hydrodistillation, solvent-free microwave extraction and headspace solid-phase microextraction combined with a novel QSRR evaluation. J. Essent. Oil-Bear. Plants 19(7), 1561-1581.

Pasha Zanousi, M.B., Nekoei, M., Mohammadhosseini, M., 2017. Chemical compositions of the essential oils from stems, leaves and fruits of Artemisia tschernieviana and exploring quantitative structure-retention relationships (QSRRs) for prediction of corresponding retention indices. J. Essent. Oil-Bear. Plants 20(3), 672-687.

Peter, M.G. 2005. Chitin and Chitosan in Fungi, in: Steinbüchel, A. (Ed), Biopolym. Online. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany, p 6.

Prasad, A., Mathur, A., Kalra, A., Gupta, M.M., Lal, R.K., Mathur, A.K., 2013. Fungal elicitor-mediated enhancement in growth and asiaticoside content of Centella asiatica L. shoot cultures. Plant Growth Regul. 69(3), 265-273.

Poulson, M.E., Thai, T., 2015. Effect of high light intensity on photoinhibition, oxyradicals and artemisinin content in Artemisia annua L. Photosynthetica. 53(3), 403-409.

Pusztahelyi, T., Holb, I.J., Pócsi, I., 2015. Secondary metabolites in fungus-plant interactions. Front. Plant Sci. 6, 573

Raviraja, N.S., 2005. Fungal endophytes in five medicinal plant species from Kudremukh Range, Western Ghats of India. J. Basic Microbiol. 45(3), 230-235.

Ro, D.K., Paradise, E.M., Ouellet, M., Fisher, K.J., Newman, K.L., Ndungu, J.M., Ho, K.A., Eachus, R.A., Ham, T.S., Kirby, J., Chang, M.C., 2006. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440(7086), 940-943.

Rodriguez, R., Freeman, D.C., McArthur, E.D., Kim, Y.O., Redman, R.S., 2009. Symbiotic regulation of plant growth, development and reproduction. Commun. Integr. Biol. 2(2), 141-143.

Shuhua, X., Tanner, M., N'Goran, E.K., Utzinger, J., Chollet, J., Bergquist, R., Minggang, C., Jiang, Z., 2002. Recent investigations of artemether, a novel agent for the prevention of Schistosomiasis japonica, mansoni and haematobia. Acta Trop. 82(2), 175-181.

Steketee, R. W., Thomas, P. E., 2017. Watching the availability and use of rapid diagnostic tests (RDTs) and artemisinin-based combination therapy (ACT). Malaria journal. 16(1), 165.

Strobel, G., Daisy, B., 2003. Bioprospecting for microbial endophytes and their natural products. Microbiol. Mol. Biol. Rev. 67(4), 491-502.

Tan, R.X., Zou, W.X., 2001. Endophytes: a rich source of functional metabolites. Nat. Prod. Rep. 18(4), 448-459.

Thu, B.T.T., Minh, T.V., Lim, B.P., Keng, C.L. 2011. Effects of environmental factors on growth and artemisinin content of Artemisia annua L. Trop. Life Sci. Res. 22(2), 37-43.

Vadassery, J., Ranf, S., Drzewiecki, C., Mithöfer, A., Mazars, C., Scheel, D., Lee, J., Oelmüller, 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(2), 193-206.

Wang, J.W., Zheng, L.P., Tan, R.X., 2006. The preparation of an elicitor from a fungal endophyte to enhance artemisinin production in hairy root cultures of Artemisia annua L. Sheng Wu Gong Cheng Xue Bao. 22(5), 829-834.

Wang, J.W., Zhang, Z., Tan, R.X., 2001. Stimulation of artemisinin production in Artemisia annua hairy roots by the elicitor from the endophytic Colletotrichum sp. Biotechnol. Lett. 23(11), 857-860.

Wang, S., Towler, M.J., Weathers, P.J., 2016. Root regulation of artemisinin production in Artemisia annua: trichome and metabolite evidence. Planta 244(5), 999-1010.

Wei, T., Liu, J., 2017. Anti-angiogenic properties of artemisinin derivatives. Int. J. Mol. Med. 40(4), 972-978.

White, T.J., Bruns, T., Lee, S.J.W.T., Taylor, J.W., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J. (Eds.), PCR protocols: A Guide to Methods and Applications. Academic Press, New York, pp. 315-322.

Wilson, D., 1995. Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73, 274-276.

Zhang, Q., Wei, X., Wang, J., 2012. Phillyrin produced by Colletotrichum gloeosporioides, an endophytic fungus isolated from Forsythia suspensa. Fitoterapia 83(8), 1500-1505.

Zou, W.X., Meng, J.C., Lu, H., Chen, G.X., Shi, G.X., Zhang, T.Y., Tan, R.X., 2000. Metabolites of Colletotrichum gloeosporioides, an endophytic fungus in Artemisia mongolica. J. Nat. Prod. 63(11), 1529-1530.