Abstract
The medicinal plant Artemisia annua L. is presently the sole plant source of artemisinin, the key ingredient of first-line antimalarial drug. As the content of artemisinin in the native plant is very low, the growth and artemisinin biosynthesis of A. annua attract extensive attentions. Endophytic microbes, which spend their entire life spans within plant tissue are widespread in healthy A. annua plants. Although endophytes have emerged in recent years as the novel resources for secondary metabolites of antioxidant, antimicrobial and anticancer activities, the roles of endophytes in plant growth and metabolism have not been fully understood. This review presents the current development of researches into endophytes in model medicinal herb A. annua and focuses on the regulatory roles of endophytes. We introduced the isolation, cultivation and identification method for endophytes in A. annua. Distribution, biodiversity and novel bioactive metabolites of the endophytes were presented. Endophytes promoted the growth of A. annua through the enhanced photosynthesis, nutrient acquisition and phytohormones. The defense resistance against microbial pathogens of A. annua was partially involved with endophyte metabolites. The development of glandular secretory trichomes and the oxidative stress induced by endophytes could be key factors for enhanced artemisinin production. Understanding the endophyte-host partnerships has the potential to improve agricultural practices for A. annua growth and artemisinin production. The aim of this review is to shed light on the importance of endophytes in plant growth and the production of medicinally important secondary metabolites.
Similar content being viewed by others
References
Ahlawat S, Saxena P, Alam P, Wajid S, Abdin MZ (2014) Modulation of artemisinin biosynthesis by elicitors, inhibitor, and precursor in hairy root cultures of Artemisia annua L. J Plant Interact 9(1):811–824. https://doi.org/10.1080/17429145.2014.949885
Alhadrami HA, Sayed AM, El-Gendy AO, Shamikh YI, Gaber Y, Bakeer W, Sheirf NH, Attia EZ, Shaban GM, Khalifa BA, Ngwa CJ, Pradel G, Rateb ME, Hassan HM, Alkhalifah DHM, Abdelmohsen UR, Hozzein WN (2021) A metabolomic approach to target antimalarial metabolites in the Artemisia annua fungal endophytes. Sci Rep 11(1):2770. https://doi.org/10.1038/s41598-021-82201-8
Amna T, Puri SC, Verma V, Sharma JP, Khajuria RK, Musarrat J, Spiteller M, Qazi GN (2006) Bioreactor studies on the endophytic fungus Entrophospora infrequens for the production of an anticancer alkaloid camptothecin. Can J Microbiol 52(3):189–196. https://doi.org/10.1139/W05-122
Arora M, Saxena P, Choudhary DK, Abdin MZ, Varma A (2016) Dual symbiosis between Piriformospora indica and Azotobacter chroococcum enhances the artemisinin content in Artemisia annua L. World J Microbiol Biotechnol 32(2):19. https://doi.org/10.1007/s11274-015-1972-5
Arora M, Saxena P, Abdin MZ, Varma A (2018) Interaction between Piriformospora indica and Azotobacter chroococcum governs better plant physiological and biochemical parameters in Artemisia annua L. plants grown under in vitro conditions. Symbiosis 75(2):103–112. https://doi.org/10.1007/s13199-017-0519-y
Astuti P, Nuryastuti T, Purwantini I (2014) Antimicrobial and cytotoxic activities of endophytic fungi isolated from Artemisia annua L. J Appl Pharm Sci 4(10):47–50. https://doi.org/10.7324/JAPS.2014.401009
Aswathy AJ, Jasim B, Jyothis M, Radhakrishnan EK (2013) Identification of two strains of Paenibacillus sp. as indole 3 acetic acid-producing rhizome-associated endophytic bacteria from Curcuma longa. 3 Biotech 3(3):219–224. https://doi.org/10.1007/s13205-012-0086-0
Awasthi A, Bharti N, Nair P, Singh R, Shukla AK, Gupta MM, Darokar MP, Kalra A (2011) Synergistic effect of Glomus mosseae and nitrogen fixing Bacillus subtilis strain Daz26 on artemisinin content in Artemisia annua L. Appl Soil Ecol 49:125–130. https://doi.org/10.1016/j.apsoil.2011.06.005
Bertea CM, Freije JR, Van der Woude H, Verstappen FWA, Perk L, Marquez V, De Kraker JW, Posthumus MA, Jansen BJM, de Groot A, Franssen MCR, Bouwmeester HJ (2005) Identification of intermediates and enzymes involved in the early steps of artemisinin biosynthesis in Artemisia annua. Planta Med 71(1):40–47. https://doi.org/10.1055/s-2005-837749
Brown GD, Sy LK (2004) In vivo transformations of dihydroartemisinic acid in Artemisia annua plants. Tetrahedron 60(5):1139–1159. https://doi.org/10.1016/j.tet.2003.11.070
Chaudhary V, Kapoor R, Bhatnagar AK (2008) Effectiveness of two arbuscular mycorrhizal fungi on concentrations of essential oil and artemisinin in three accessions of Artemisia annua L. Appl Soil Ecol 40(1):174–181. https://doi.org/10.1016/j.apsoil.2008.04.003
Chen SA (2011) Effects of mycorrhizal fungus on Artemisia annua of artemisianin content. Dissertation, Northeast Forestry University (in Chinese)
Cosoveanu A, Cabrera R (2018) Endophytic fungi in species of Artemisia. J Fungi 4(2):53. https://doi.org/10.3390/jof4020053
DiTomaso JM, Duke SO (1991) Is polyamine biosynthesis a possible site of action of cinmethylin and artemisinin? Pestic Biochem Phys 39(2):158–167. https://doi.org/10.1016/0048-3575(91)90136-A
Domokos E, Jakab-Farkas L, Darkó B, Bíró-Janka B, Mara G, Albert C, Balog A (2018) Increase in Artemisia annua plant biomass, artemisinin content and guaiacol peroxidase activity using the arbuscular mycorrhizal fungus Rhizophagus irregularis. Front Plant Sci 9:478. https://doi.org/10.3389/fpls.2018.00478
Duke SO, Vaughn KC, Croom EM, Elsohly HN (1987) Artemisinin, constituent of annual wormwood (Artemisia annua), is a selective phytotoxin. Weed Sci 35(4):499–505. https://doi.org/10.2307/2419268
Duke MV, Paul RN, Elsohly HN, Sturtz 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(3):365–372. https://doi.org/10.1086/297173
Durden K, Sellars S, Cowell B, Brown JJ, Pszczolkowski MA (2011) Artemisia annua extracts, artemisinin and 1,8-cineole, prevent fruit infestation by a major, cosmopolitan pest of apples. Pharm Biol 49(6):563–568. https://doi.org/10.3109/13880209.2010.528433
Elferaly FS, Almeshal IA, Alyahya MA, Hifnawy MS (1986) On the possible role of qinghao acid in the biosynthesis of artemisinin. Phytochemistry 25(12):2777–2778. https://doi.org/10.1016/S0031-9422(00)83739-5
Eyberger AL, Dondapati R, Porter JR (2006) Endophyte fungal isolates from Podophyllum peltatum produce podophyllotoxin. J Nat Prod 69(8):1121–1124. https://doi.org/10.1021/np060174f
Gaur R, Tiwari S, Jakhmola A, Thakur JP, Verma RK, Pandey R, Bhakuni RS (2014) Novel biotransformation processes of artemisinic acid to their hydroxylated derivatives 3β-hydroxyartemisinic acid and 3β, 15-dihydroxyartemisinic by fungus Trichothecium roseum, CIMAPN1 and their biological evaluation. J Mol Catal B 106:46–55. https://doi.org/10.1016/j.molcatb.2014.04.008
Ge HM, Song YC, Chen JR, Hu S, Wu JY, Tan RX (2006) Paranolin: a new xanthene-based metabolite from Paraphaeosphaeria nolinae. Helv Chim Acta 89(3):502–506. https://doi.org/10.1002/hlca.200690051
Gouda S, Das G, Sen SK, Shin H-S, Patra JK (2016) Endophytes: a treasure house of bioactive compounds of medicinal importance. Front Microbiol 7:1538. https://doi.org/10.3389/fmicb.2016.01538
Graham IA, Besser K, Blumer S, Branigan CA, Czechowski T, Elias L, Guterman I, Harvey D, Isaac P, Khan AM, Larson TR, Li Y, Pawson T, Penfield T, Rae AM, Rathbone DA, Reid S, Ross J, Smallwood MF, Segura V, Townsend T, Vyas D, Winzer T, Bowles D (2010) The genetic map of Artemisia annua L. identifies loci affecting yield of the antimalarial drug artemisinin. Science 327(5963):328–331. https://doi.org/10.1126/science.1182612
Gu W, Ge HM, Song YC, Ding H, Zhu HL, Zhao XA, Tan RX (2007) Cytotoxic benzo[j]fluoranthene metabolites from Hypoxylon truncatum IFB-18, an endophyte of Artemisia annua. J Nat Prod 70(1):114–117. https://doi.org/10.1021/np0604127
Guo B, Wang Y, Sun X, Tang K (2008) Bioactive natural products from endophytes: a review. Appl Biochem Microbiol 44(2):136–142. https://doi.org/10.1134/s0003683808020026
Gupta S, Chaturvedi P, Kulkarni MG, van Staden J (2020) A critical review on exploiting the pharmaceutical potential of plant endophytic fungi. Biotechno Adv 39:107462. https://doi.org/10.1016/j.biotechadv.2019.107462
Hao XL, Zhong YJ, Fu XQ, Lv ZY, Shen Q, Yan TX, Shi P, Ma YN, Chen MH, Lv XY, Wu ZKY, Zhao JY, Sun XF, Li L, Tang KX (2017) Transcriptome analysis of genes associated with the artemisinin biosynthesis by jasmonic acid treatment under the light in Artemisia annua. Front Plant Sci 8:971. https://doi.org/10.3389/fpls.2017.00971
Huang HY, Li J, Zhao GZ, Zhu WY, Yang LL, Tang HY, Xu LH, Li WJ (2012) Sphingomonas endophytica sp. nov., isolated from Artemisia annua L. Int J Syst Evol Microbiol 62(7):1576–1580. https://doi.org/10.1099/ijs.0.031484-0
Hussain MA, Mahajan V, Rather IA, Awasthi P, Chouhan R, Dutt P, Sharma YP, Bedi YS, Gandhi SG (2017) Isolation and identification of growth promoting endophytic fungi from Artemisia annua L. and its effects on artemisinin content. Trends Phytochem Res 1(4):207–214
Kayani WK, Kiani BH, Dilshad E, Mirza B (2018) Biotechnological approaches for artemisinin production in Artemisia. World J Microb Biot 34(4):54. https://doi.org/10.1007/s11274-018-2432-9
Klayman DL (1985) Qinghaosu (Artemisinin): an antimalarial drug from China. Scinence 228(4703):1049–1055. https://doi.org/10.1126/science.3887571
Kong LY, Tan RX (2015) Artemisinin, a miracle of traditional Chinese medicine. Nat Prod Rep 32(12):1617–1621. https://doi.org/10.1039/c5np00133a
Li J (2010) Resources of endophytic actinobacteria associated with Artemisia annua and their influences on the growth and artemisinin biosynthesis of host plant. Dissertation, Yunnan University (in Chinese)
Li J, Zhao GZ, Huang HY, Zhu WY, Lee JC, Xu LH, Kim CJ, Li WJ (2011a) Nonomuraea endophytica sp. nov., an endophytic actinomycete isolated from Artemisia annua L. Int J Syst Evol Microbiol 61(4):757–761. https://doi.org/10.1099/ijs.0.022558-0
Li J, Zhao GZ, Zhu WY, Huang HY, Xu LH, Zhang S, Li WJ (2011b) Phytomonospora endophytica gen. nov., sp. nov., isolated from the roots of Artemisia annua L. Int J Syst Evol Microbiol 61(12):2967–2973. https://doi.org/10.1099/ijs.0.030205-0
Li J, Zhao GZ, Huang HY, Qin S, Zhu WY, Zhao LX, Xu LH, Zhang S, Li WJ, Strobel G (2012a) Isolation and characterization of culturable endophytic actinobacteria associated with Artemisia annua L. Antonie Van Leeuwenhoek 101(3):515–527. https://doi.org/10.1007/s10482-011-9661-3
Li J, Zhao GZ, Varma A, Qin S, Xiong Z, Huang HY, Zhu WY, Zhao LX, Xu LH, Zhang S, Li WJ (2012b) An endophytic Pseudonocardia species induces the production of artemisinin in Artemisia annua. PLoS ONE 7(12):e51410. https://doi.org/10.1371/journal.pone.0051410
Li J, Zhao GZ, Zhu WY, Huang HY, Xu LH, Zhang S, Li WJ (2013) Streptomyces endophyticus sp. nov., a novel endophytic actinomycete isolated from Artemisia annua L. Int J Syst Evol Microbiol 63(1):224–229. https://doi.org/10.1099/ijs.0.035725-0
Lin L, Ge HM, Yan T, Qin YH, Tan RX (2012) Thaxtomin A-deficient endophytic Streptomyces sp. enhances plant disease resistance to pathogenic Streptomyces scabies. Planta 236(6):1849–1861. https://doi.org/10.1007/s00425-012-1741-8
Liu CH, Zou WX, Lu H, Tan RX (2001) Antifungal activity of Artemisia annua endophyte cultures against phytopathogenic fungi. J Biotechnol 88(3):277–282. https://doi.org/10.1016/S0168-1656(01)00285-1
Liu JY, Liu CH, Zou WX, Tian X, Tan RX (2002) Leptosphaerone, a metabolite with a novel skeleton from Leptosphaeria sp. IV403, an endophytic fungus in Artemisia annua. Helv Chim Acta 85(9):2664–2667
Liu JY, Liu CH, Zou WX, Tan RX (2003) Leptosphaeric acid, a metabolite with a novel carbon skeleton from Leptosphaeria sp. IV403, an endophytic fungus in Artemisia annua. Helv Chim Acta 86(3):657–660. https://doi.org/10.1002/hlca.200390064
Liu JH, Wu LF, Zhang HW (2011) Isolation and preliminary identification of endophytes from Artemisia annua Linn. Amino Acids Biotic Resour 33(4):27–30. https://doi.org/10.14188/j.ajsh.2011.04.004 (in Chinese)
Liu ZZ, Chen Y, Lian B, Zhang Z, Zhao YY, Ji ZH, Lv YN, Li HG (2019) Comparative study on population ecological distribution and extracellular enzyme activities of endophytic fungi in Artemisia annua. J Biosci Med 7(8):94–105. https://doi.org/10.4236/jbm.2019.78008
Lu H, Zou WX, Meng JC, Hu J, Tan RX (2000) New bioactive metabolites produced by Colletotrichum sp., an endophytic fungus in Artemisia annua. Plant Sci 151(1):67–73. https://doi.org/10.1016/S0168-9452(99)00199-5
Ma CF, Wang HH, Lu X, Wang H, Xu GW, Liu BY (2009) Terpenoid metabolic profiling analysis of transgenic Artemisia annua L. by comprehensive two-dimensional gas chromatography time-of-flight mass spectrometry. Metabolomics 5(4):497–506. https://doi.org/10.1007/s11306-009-0170-6
Mandal S, Upadhyay S, Wajid S, Ram M, Jain DC, Singh VP, Abdin MZ, Kapoor R (2015) Arbuscular mycorrhiza increase artemisinin accumulation in Artemisia annua by higher expression of key biosynthesis genes via enhanced jasmonic acid levels. Mycorrhiza 25(5):345–357. https://doi.org/10.1007/s00572-014-0614-3
Mannan A, Liu CZ, Arsenault PR, Towler MJ, Vail DR, Lorence A, Weathers PJ (2010) DMSO triggers the generation of ROS leading to an increase in artemisinin and dihydroartemisinic acid in Artemisia annua shoot cultures. Plant Cell Rep 29(2):143–152. https://doi.org/10.1007/s00299-009-0807-y
Ngankaranatikarn P, Chuanasa T, Sriubolmas N, Suwanborirux K (2013) Antileukemic activity and secondary metabolites of an endophytics fungus Phomopsis sp. from Artemisia annua. Thai J Pharm Sci 38:195–198
Péterfi O, Domokosi E (2018) Mutualistic and endophytic microorganisms of Artemisia annua: description, role and use. Acta Biol Marisiensis 1(2):5–21. https://doi.org/10.2478/abmj-2018-0009
Priti V, Ramesha BT, Singh S, Ravikanth G, Ganeshaiah KN, Suryanarayanan TS, Shaanker RU (2009) How promising are endophytic fungi as alternative sources of plant secondary metabolites? Curr Sci 97(4):477–478. https://doi.org/10.1371/journal.pone.0006787
Purwantini I, Wahyono M, Asmah R (2015) Isolation of endophytic fungi from Artemisia annua, L. and identification of their antimicrobial compound using bioautography method. Int J Pharm Sci 7(12):95–99
Putri AEP (2014) Penelusuran senyawa sitotoksik ekstrak etil asetat kultur fungi endofit kode AA1 dari tanaman Artemisia annua Linn. terhadap sel T47D. Dissertation, Universitas Gadjah Mada (in Indonesian)
Qian YX, Kang JC, Wang L, Lei BX, Hyde KD (2014) In vitro antioxidant and antitumor activities of an endophytic fungus Phomopsis liquidambari QH4 from Artemisia annua. Chiang Mai J Sci 41(5.1):992–1006
Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278(1):1–9. https://doi.org/10.1111/j.1574-6968.2007.00918.x
Sharma G, Agrawal V (2013) Marked enhancement in the artemisinin content and biomass productivity in Artemisia annua L. shoots co-cultivated with Piriformospora indica. World J Microbiol Biotechnol 29(6):1133–1138. https://doi.org/10.1007/s11274-013-1263-y
Shen L, Jiao RH, Ye YH, Wang XT, Xu C, Song YC, Zhu HL, Tan RX (2006) Absolute configuration of new cytotoxic and other bioactive trichothecene macrolides. Chem Eur J 12(21):5596–5602. https://doi.org/10.1002/chem.200600084
Shen L, Shi DH, Song YC, Tan RX (2009) Chemical constituents of liquid culture of endophyte IFB-E012 in Artemisia annua. Chin J Nat Med 7(5):354–356. https://doi.org/10.3724/SP.J.1009.2009.00354
Shen L, Wang JS, Shen HJ, Song YC, Tan RX (2010) A new cytotoxic trichothecene macrolide from the endophyte Myrothecium roridum. Planta Med 76(10):1004–1006. https://doi.org/10.1055/s-0029-1240897
Shen Q, Zhang LD, Liao ZH, Wang SY, Yan TX, Shi P, Liu M, Fu XQ, Pan QF, Wang YL, Lv ZY, Lu X, Zhang FY, Jiang WM, Ma YN, Chen MH, Hao XL, Li L, Tang YL, Lv G, Zhou Y, Sun XF, Brodelius PE, Rose JKC, Tang KX (2018) The genome of Artemisia annua provides insight into the evolution of asteraceae family and artemisinin biosynthesis. Mol Plant 11(6):776–788. https://doi.org/10.1016/j.molp.2018.03.015
Simanjuntak P, Otovina DM, Rahayuningsih M, dan Said EG (2004) Isolation and identification artemisinine from product of endophyte microbe cultivation from Artemisia annua. Indonesian J Pharm 15(2):68–74. https://doi.org/10.1055/s-0028-1110944 (in Indonesian)
Singh A, Vishwakarma RA, Husian A (1988) Evaluation of Artemisia annua strain for higher artemisinin production. Planta Med 54(5):275–277. https://doi.org/10.1055/s-2006-962515
Soetaert SSA, Van Neste CMF, Vandewoestyne ML, Head SR, Goossens A, Van Nieuwerburgh FCW, Deforce DLD (2013) Differential transcriptome analysis of glandular and filamentous trichomes in Artemisia annua. BMC Plant Biol 13:220. https://doi.org/10.1186/1471-2229-13-220
Stierle A, Strobel GA, Stierle D (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science 260(5105):214–216. https://doi.org/10.1126/science.8097061
Tian XM, Wu YF, Zhang Y (2008) Isolation and screening of endophytes from Artemisia annua and their antagonistic activity to plant pathogens. Acta Agr Boreali-Occidentalis Sinica 17(4):186–190. https://doi.org/10.2967/jnmt.107.044081 (in Chinese)
Tian H, Ma YJ, Li WY, Wang JW (2018) Efficient degradation of triclosan by an endophytic fungus Penicillium oxalicum B4. Environ Sci Pollut Res 25(9):8963–8975. https://doi.org/10.1007/s11356-017-1186-5
Tian H, Li XP, Zhao JP, Gao HW, Xu QM, Wang JW (2021) Biotransformation of artemisinic acid to bioactive derivatives by endophytic Penicillium oxalicum B4 from Artemisia annua L. Phytochemistry 185:112682. https://doi.org/10.1016/j.phytochem.2021.112682
Tripathi A, Awasthi A, Singh S, Sah K, Maji D, Patel VK, Verma RK, Kalra A (2020) Enhancing artemisinin yields through an ecologically functional community of endophytes in Artemisia annua. Ind Crop Prod 150:112375. https://doi.org/10.1016/j.indcrop.2020.112375
Tu YY, Ni MY, Zhong YR, Li LN, Cui SL, Zhang MQ, Wang XZ, Ji Z, Liang XT (1982) Studies on the constituents of Artemisia annua, Part II. Planta Med 44(3):143–145. https://doi.org/10.1055/s-2007-971424
Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206(4):1196–1206. https://doi.org/10.1111/nph.13312
Wahyono P, Widyati P (2010) Testing of antiplasmodium activity substance from endophytic fungus of Artemisia annua L. Indonesian J Pharm 21(4):230–235. https://doi.org/10.14499/indonesianjpharm0iss0pp230-235 (in Indonesian)
Wani KI, Choudhary S, Zehra A, Naeem M, Weathers P, Aftab T (2021) Enhancing artemisinin content in and delivery from Artemisia annua: a review of alternative, classical, and transgenic approaches. Planta 254:29. https://doi.org/10.1007/s00425-021-03676-3
Wang JW, Zhang Z, Tan RX (2001) Stimulation of artemisinin production in Artemisia annua hairy roots by the elicitor from the endophytic Colletotrichum sp. Biotechnol Lett 23(11):857–860. https://doi.org/10.1023/A:1010535001943
Wang JW, Xia ZH, Tan RX (2002) Elicitation on artemisinin biosynthesis in Artemisia annua hairy roots by the oligosaccharide extract from the endophytic Colletotrichum sp. B501. Acta Bot Sin 44(10):1233–1238. https://doi.org/10.1016/S0014-5793(02)03191-5
Wang JW, Zheng LP, Tan RX (2006) The preparation of an elicitor from a fungal endophyte to enhance artemisinin production in hairy root cultures of Artemisia annua L. Chin J Biotechnol 22(5):829–834. https://doi.org/10.1016/S1872-2075(06)60057-5 (in Chinese)
Wang HH, Ma CF, Ma LQ, Du ZG, Wang H, Ye HC, Li GF, Liu BY, Xu GW (2009a) Secondary metabolic profiling and artemisinin biosynthesis of two genotypes of Artemisia annua. Planta Med 75(15):1625–1633. https://doi.org/10.1055/s-0029-1185814
Wang JW, Zheng LP, Zhang B, Zou T (2009b) Stimulation of artemisinin synthesis by combined cerebroside and nitric oxide elicitation in Artemisia annua hairy roots. Appl Microbiol Biotechnol 85(2):285–292. https://doi.org/10.1007/s00253-009-2090-9
Wang JW, Zheng LP, Zhang B, Zou T, Tan RX (2009c) Interactions between fungal endophytes and their host Artemisa annua: growth, antifungal activity and artemisinin biosynthesis. In: Liu J, Vittori S, Yang C (eds) Proceedings of 2009 International Conference of Natural Product and Traditional Medicine. Scientific & Technical Development Inc., Flushing, pp 143–145. ISBN: 978-0-982-24412-8
Wang ZL, Yang LY, Yang XW, Zhang XH (2014) Advances in the chemical synthesis of artemisinin. Synth Commun 44(14):1987–2003. https://doi.org/10.1080/00397911.2014.884225
Wang JW, Tian H, Ma YJ, Zheng LP (2018) An application of endophytic Bacillus cereus SZ1. CN Patent No. ZL 201511025514.3 (in Chinese)
Weathers PJ, Elkholy S, Wobbe KK (2006) Artemisinin: the biosynthetic pathway and its regulation in Artemisia annua, a terpenoid-rich species. In Vitro Cell Dev 42(4):309–317. https://doi.org/10.1079/IVP2006782
Wei BY, Huang HY, Li SX, Rao LQ, Gao GG (2008) The antimicrobial activity screening of endophytic fungi of Artemisia annua. Hunan Agric Sci 4:100–101. https://doi.org/10.3969/j.issn.1006-060X.2008.04.038 (in Chinese)
Woerdenbag HJ, Pras N, Chan NG, Bang BT, Bos R, van Uden W, Van YP, van Boi N, Batterman S, Lugt CB (1994) Artemisinin, related sesquiterpenes, and essential oil in Artemisia annua during a vegetation period in Vietnam. Planta Med 60(3):272–275. https://doi.org/10.1055/s-2006-959474
Wu XL, Cui GL, Liu F, Li LY (2018) Isolation and molecular identification of endophytic fungi from Artemisia annua and promoting effect of Trichoderma atroviride on its growth. J Trop Subtrop Bot 26(1):56–64. https://doi.org/10.11926/jtsb.3768 (in Chinese)
Xiao L, Tan HX, Zhang L (2016) Artemisia annua glandular secretory trichomes: the biofactory of antimalarial agent artemisinin. Sci Bull 61(1):26–36. https://doi.org/10.1007/s11434-015-0980-z
Yu Z, He YY, Gao XN, Wang H, Huang LL (2014) Isolation and identification of the metabolites produced by actinomycetes A5 from annua. Nat Prod Res 26:848–850. https://doi.org/10.16333/j.1001-6880.2014.06.009 (in Chinese)
Yuan YF, Dong T, Wang JW (2011a) Effect of endophytic Penicillium sp. Y2 on growth and artemisinin biosynthesis of plantlets in tissue cultures of Artemisia annua L. Amino Acids Biotic Resour 33(4):1–4. https://doi.org/10.14188/j.ajsh.2011.04.005 (in Chinese)
Yuan ZL, Chen YC, Ma XJ (2011b) Symbiotic fungi in roots of Artemisia annua with special reference to endophytic colonizers. Plant Biosyst 145(2):495–502. https://doi.org/10.1080/11263504.2010.544863
Zeng Q, Chen X, Tian WY, Wang P, Lei BX (2015) Biodiversity of endophytic fungi from Artemisia annua and their antagonistic activity to plant pathogens. Guizhou Agric Sci 43(9):164–169 (in Chinese)
Zhang YS, Ye HC, Liu BY, Wang H, Li GF (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. https://doi.org/10.1007/s11183-005-0009-6
Zhang J, Ge HM, Jiao RH, Li J, Peng H, Wang YR, Wu JH, Song YC, Tan RX (2010) Cytotoxic chaetoglobosins from the endophyte Chaetomium globosum. Planta Med 76(16):1910–1914. https://doi.org/10.1055/s-0030-1249936v
Zhang HW, Bai XL, Wu BX (2012) Evaluation of antimicrobial activities of extracts of endophytic fungi from Artemisia annua. Bangl J Pharmacol 7(2):120–123. https://doi.org/10.3329/bjp.v7i2.10951
Zhang HW, Ying C, Tang YF (2014) Four ardeemin analogs from endophytic Aspergillus fumigatus SPS-02 and their reversal effects on multidrug-resistant tumor cells. Chem Biodivers 11(1):85–91. https://doi.org/10.1002/cbdv.201300220
Zhang X, Wei W, Tan RX (2015) Symbionts, a promising source of bioactive natural products. Sci China Chem 58(7):1097–1109. https://doi.org/10.1007/s11426-015-5398-6
Zhao GZ, Li J, Qin S, Huang HY, Zhu WY, Xu LH, Li WJ (2010) Streptomyces artemisiae sp. nov., isolated from surface-sterilized tissue of Artemisia annua L. Int J Syst Evol Microbiol 60(1):27–32. https://doi.org/10.1099/ijs.0.011965-0
Zhao GZ, Li J, Huang HY, Zhu WY, Park DJ, Kim CJ, Xu LH, Li WJ (2011a) Pseudonocardia kunmingensis sp. nov., an actinobacterium isolated from surface-sterilized roots of Artemisia annua L. Int J Syst Evol Microbiol 61(9):2292–2297. https://doi.org/10.1099/ijs.0.027607-0
Zhao GZ, Li J, Huang HY, Zhu WY, Zhao LX, Tang SK, Xu LH, Li WJ (2011b) Pseudonocardia artemisiae sp. nov., isolated from surface-sterilized Artemisia annua L. Int J Syst Evol Microbiol 61(5):1061–1065. https://doi.org/10.1099/ijs.0.021931-0
Zhao GZ, Li J, Zhu WY, Klenk HP, Xu LH, Li WJ (2011c) Nocardia artemisiae sp. nov., an endophytic actinobacterium isolated from a surface-sterilized stem of Artemisia annua L. Int J Syst Evol Microbiol 61(12):2933–2937. https://doi.org/10.1099/ijs.0.029306-0
Zhao GZ, Li J, Zhu WY, Li XP, Tian SZ, Zhao LX, Xu LH, Li WJ (2011d) Pseudonocardia bannaensis sp. nov., a novel actinomycete isolated from the surface-sterilized roots of Artemisia annua L. Antonie Van Leeuwenhoek 100(1):35–42. https://doi.org/10.1007/s10482-011-9562-5
Zhao GZ, Zhu WY, Li J, Xie Q, Xu LH, Li WJ (2011e) Pseudonocardia serianimatus sp. nov., a novel actinomycete isolated from the surface-sterilized leaves of Artemisia annua L. Antonie Van Leeuwenhoek 100(4):521–528. https://doi.org/10.1007/s10482-011-9607-9
Zhao GZ, Li J, Zhu WY, Tian SZ, Zhao LX, Yang LL, Xu LH, Li WJ (2012a) Rhodococcus artemisiae sp. nov., an endophytic actinobacterium isolated from the pharmaceutical plant Artemisia annua L. Int J Syst Evol Micr 62(4):900–905. https://doi.org/10.1099/ijs.0.031930-0
Zhao GZ, Li J, Zhu WY, Wei DQ, Zhang JL, Xu LH, Li WJ (2012b) Pseudonocardia xishanensis sp. nov., an endophytic actinomycete isolated from the roots of Artemisia annua L. Int J Syst Evol Microbiol 62(10):2395–2399. https://doi.org/10.1099/ijs.0.037028-0
Zhao JC, Cheng J, Zhang Q, Gao ZW, Zhang MY, Zhang YX (2018) Flavobacterium artemisiae sp. nov. isolated from the rhizosphere of Artemisia annua L. and emended descriptions of Flavobacterium compostarboris and Flavobacterium procerum. Int J Syst Evol Micr 68(5):1509–1513. https://doi.org/10.1099/ijsem.0.002701
Zheng LP, Zhang B, Zou T, Chen ZH, Wang JW (2010) Nitric oxide interacts with reactive oxygen species to regulate oligosaccharide-induced artemisinin biosynthesis in Artemisia annua hairy roots. J Med Plants Res 4(9):758–765. https://doi.org/10.1016/j.jep.2010.02.010
Zheng LP, Tian H, Yuan YF, Wang JW (2016a) The influence of endophytic Penicillium oxalicum B4 on growth and artemisinin biosynthesis of in vitro propagated plantlets of Artemisia annua L. Plant Growth Regul 80(1):93–102. https://doi.org/10.1007/s10725-016-0162-2
Zheng LP, Zou T, Ma YJ, Wang JW, Zhang YQ (2016b) Antioxidant and DNA damage protecting activity of exopolysaccharides from the endophytic bacterium Bacillus cereus SZ1. Molecules 21(2):174. https://doi.org/10.3390/molecules21020174
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Nos. 82073955 and 81273487) and the Priority Academic Program Development of the Jiangsu Higher Education Institutes (PAPD).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Daolong Dou.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zheng, L.P., Li, X.P., Zhou, L.L. et al. Endophytes in Artemisia annua L.: new potential regulators for plant growth and artemisinin biosynthesis. Plant Growth Regul 95, 293–313 (2021). https://doi.org/10.1007/s10725-021-00751-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-021-00751-3