Skip to main content
Log in

Bio Prospecting of Endophytes and PGPRs in Artemisinin Production for the Socio-economic Advancement

  • Review Article
  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The growing demand for Artemisia annua plants in healthcare, food, and pharmaceutical industries has led to increased cultivation efforts to extract a vital compound, Artemisinin. The efficacy of Artemisinin as a potent drug against malaria disease is well established but its limited natural abundance. However, the common practice of using chemical fertilizers for maximum yield has adverse effects on plant growth, development, and the quality of phytochemicals. To address these issues, the review discusses the alternative approach of harnessing beneficial rhizosphere microbiota, particularly plant growth-promoting rhizobacteria (PGPR). Microbes hold substantial biotechnological potential for augmenting medicinal plant production, offering an environmentally friendly and cost-effective means to enhance medicinal plant production. This review article aims to identify a suitable endophytic population capable of enabling Artemisia sp. to thrive amidst abiotic stress while simultaneously enhancing Artemisinin production, thereby broadening its availability to a larger population. Furthermore, by subjecting endophytes to diverse combinations of harsh conditions, this review sheds light on the modulation of essential artemisinin biosynthesis pathway genes, both up regulated and down regulated. The collective findings suggest that through the in vitro engineering of endophytic communities and their in vivo application to Artemisia plants cultivated in tribal population fields, artemisinin production can be significantly augmented. The overall aim of this review to explore the potential of harnessing microbial communities, their functions, and services to enhance the cultivation of medicinal plants. It outlines a promising path toward bolstering artemisinin production, which holds immense promise in the fight against malaria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63(7):2541–2556. https://doi.org/10.1093/jxb/err431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Compeau PE, Pevzner PA, Tesler G (2011) How to apply de Bruijn graphs to genome assembly. Nat Biotechnol 29(11):987–991. https://doi.org/10.1038/nbt.2023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38(suppl 2):W64–W70. https://doi.org/10.1093/nar/gkq310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29(7):644–652. https://doi.org/10.1038/nbt.1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hsu FC et al (2013) Submergence confers immunity mediated by the WRKY22 transcription factor in Arabidopsis. Plant Cell 25(7):2699–2713. https://doi.org/10.1105/tpc.113.114447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–D462. https://doi.org/10.1093/nar/gkv1070

    Article  CAS  PubMed  Google Scholar 

  7. Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 45:D353–D361. https://doi.org/10.1093/nar/gkw1092

    Article  CAS  PubMed  Google Scholar 

  8. Le DT, Nishiyama RIE, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18(4):263–276. https://doi.org/10.1093/dnares/dsr015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Lévesque F, Seeberger PH (2012) Continuous-flow synthesis of the anti-malaria drug artemisinin. Angew Chem Int Ed 51(7):1706–1709. https://doi.org/10.1002/anie.201107446

    Article  CAS  Google Scholar 

  10. Liu W, Zhao T, Wang H, Zeng J, Xiang L, Zhu S et al (2015) Reference gene selection in Artemisia annua L., a plant species producing anti-malarial artemisinin. Plant Cell Tissue Organ Cult 121:141–152. https://doi.org/10.1007/s11240-014-0690-2

    Article  CAS  Google Scholar 

  11. Lv Y, Fu S, Chen S, Zhang W, Qi C (2016) Ethylene response factor BnERF2-like (ERF2.4) from Brassica napus L. enhances submergence tolerance and alleviates oxidative damage caused by submergence in Arabidopsis thaliana. Crop J 4(3):199–211. https://doi.org/10.1016/j.cj.2016.01.004

    Article  Google Scholar 

  12. Zhang JY, Huang SN, Mo ZH, Xuan JP, Jia XD, Wang G, Guo ZR (2015) De novo transcriptome sequencing and comparative analysis of differentially expressed genes in kiwifruit under waterlogging stress. Mol Breed 35:1–12. https://doi.org/10.1007/s11032-015-0408-0

    Article  CAS  Google Scholar 

  13. Zhang X, Cheng Z, Lin Q, Wang J, Wan J (2011) Cloning of cold-inducible gene SLCMYB1 and its heterologous expression in rice. Acta Agron Sin 37(4):587–594. https://doi.org/10.3724/SP.J.1006.2011.00587

    Article  CAS  Google Scholar 

  14. Tripathi A, Awasthi A, Singh S, Sah K, Maji D, Patel VK et al (2020) Enhancing artemisinin yields through an ecologically functional community of endophytes in Artemisia annua. Ind Crops Prod 150:112375. https://doi.org/10.1016/j.indcrop.2020.112375

    Article  CAS  Google Scholar 

  15. Naika M, Shameer K, Mathew OK, Gowda R, Sowdhamini R (2013) STIFDB2: an updated version of plant stress-responsive transcription factor database with additional stress signals, stress-responsive transcription factor binding sites and stress-responsive genes in Arabidopsis and rice. Plant Cell Physiol 54(2):e8. https://doi.org/10.1093/pcp/pcs185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Priest HD, Fox SE, Rowley ER, Murray JR, Michael TP, Mockler TC (2014) Analysis of global gene expression in Brachypodium distachyon reveals extensive network plasticity in response to abiotic stress. PLoS One 9(1):e87499. https://doi.org/10.1371/journal.pone.0087499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Tripathi A, Pandey P, Tripathi SN, Kalra A (2022) Perspectives and potential applications of endophytic microorganisms in cultivation of medicinal and aromatic plants. Front Plant Sci. https://doi.org/10.3389/fpls.2022.985429

    Article  PubMed  PubMed Central  Google Scholar 

  18. Elfawal MA, Towler MJ, Reich NG, Golenbock D, Weathers PJ, Rich SM (2012) Dried whole plant Artemisia annua as an antimalarial therapy. PLoS One 7(12):e52746. https://doi.org/10.1371/journal.pone.0052746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Rastogi S et al (2014) De novo sequencing and comparative analysis of holy and sweet basil transcriptomes. BMC Genom 15:588. https://doi.org/10.1186/1471-2164-15-588

    Article  Google Scholar 

  20. Qureshi MI, Israr M, Abdin MZ, Iqbal M (2005) Responses of Artemisia annua L. to lead and salt induced oxidative stress. Environ Exp Bot 53(2):185–193. https://doi.org/10.1016/j.envexpbot.2004.03.014

    Article  CAS  Google Scholar 

  21. Marchese JA, Ferreira JF, Rehder VL, Rodrigues O (2010) Water deficit effect on the accumulation of biomass and artemisinin in annual wormwood (Artemisia annua L., Asteraceae). Braz J Plant Physiol 22:1–9. https://doi.org/10.1590/S1677-04202010000100001

    Article  Google Scholar 

  22. Misra A, Chanotiya CS, Gupta MM, Dwivedi UN, Shasany AK (2012) Characterization of cytochrome P450 monooxygenases isolated from trichome enriched fraction of Artemisia annua L. leaf. Gene 510(2):193–201. https://doi.org/10.1016/j.gene.2012.09.015

    Article  CAS  PubMed  Google Scholar 

  23. Bulgarelli D, Schlaeppi K, Spaepen S, Van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. https://doi.org/10.1146/annurev-arplant-050312-120106

    Article  CAS  PubMed  Google Scholar 

  24. Rani N et al (2023) Plant growth-promoting attributes of zinc solubilizing Dietzia maris isolated from polyhouse rhizospheric soil of Punjab. Curr Microbiol 80(1):1–10. https://doi.org/10.1007/s00284-022-03147-2

    Article  CAS  Google Scholar 

  25. Köberl M, Schmidt R, Ramadan EM, Bauer R, Berg G (2013) The microbiome of medicinal plants: diversity and importance for plant growth, quality and health. Front Microbiol 4:400. https://doi.org/10.3389/fmicb.2013.00400

    Article  PubMed  PubMed Central  Google Scholar 

  26. Shi H, Chan Z (2014) Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J Integr Plant Biol 56(2):114–121. https://doi.org/10.1111/jipb.12128

    Article  CAS  PubMed  Google Scholar 

  27. Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 6:902. https://doi.org/10.3389/fpls.2015.00902

    Article  PubMed  PubMed Central  Google Scholar 

  28. Skopelitis DS et al (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18(10):2767–2781. https://doi.org/10.1105/tpc.105.038323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316(5832):1746–1748. https://doi.org/10.1126/science.1143082

    Article  CAS  PubMed  Google Scholar 

  30. Singh R, Parameswaran TN, Rao EVSP, Puttanna K, Kalra A, Srinivas KVNS, Bagyaraj DJ, Divya S (2009) Effect of arbuscular mycorrhizal fungi and Pseudomonas fluorescens on root-rot and wilt, growth and yield of Coleus forskohlii. Biocontrol Sci Technol 19:835–841. https://doi.org/10.1080/09583150903137601

    Article  Google Scholar 

  31. Tian ZD, Zhang Y, Liu J, Xie CH (2010) Novel potato C2H2 type zinc finger protein gene, StZFP1, which responds to biotic and abiotic stress, plays a role in salt tolerance. Plant Biol 12(5):689–697. https://doi.org/10.1111/j.1438-8677.2009.00276.x

    Article  CAS  PubMed  Google Scholar 

  32. Tuteja N et al (2014) Pea p68, a DEAD-box helicase, provides salinity stress tolerance in transgenic tobacco by reducing oxidative stress and improving photosynthesis machinery. PLoS One 9(5):e98287. https://doi.org/10.1371/journal.pone.0098287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Sun Y, Yu D (2015) Activated expression of AtWRKY53 negatively regulates drought tolerance by mediating stomatal movement. Plant Cell Rep 34(8):1295–1306. https://doi.org/10.1007/s00299-015-1787-8

    Article  CAS  PubMed  Google Scholar 

  34. World Health Organization (2012) Effectiveness of non-pharmaceutical forms of Artemisia annua L. against malaria: WHO position statement (No. WHO/HTM/GMP/2012.07). World Health Organization. https://apps.who.int/iris/bitstream/handle/10665/337992/WHO-HTM-GMP-2012.07-eng.pdf

  35. Bechtold U et al (2013) Arabidopsis HEAT SHOCK TRANSCRIPTION FACTORA1b overexpression enhances water productivity, resistance to drought, and infection. J Exp Bot 64(11):3467–3481. https://doi.org/10.1093/jxb/ert185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Xiong H et al (2014) Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS One 9(3):e92913. https://doi.org/10.1371/journal.pone.0092913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Yadav RK, Sangwan RS, Sabir F, Srivastava AK, Sangwan NS (2014) Effect of prolonged water stress on specialized secondary metabolites, peltate glandular trichomes, and pathway gene expression in Artemisia annua L. Plant Physiol Biochem 74:70–83. https://doi.org/10.1016/j.plaphy.2013.10.023

    Article  CAS  PubMed  Google Scholar 

  38. Yadav RK, Sangwan RS, Srivastava AK, Sangwan NS (2017) Prolonged exposure to salt stress affects specialized metabolites Artemisinin and essential oil accumulation in Artemisia annua L.: metabolic acclimation in preferential favour of enhanced terpenoid accumulation accompanying vegetative to reproductive phase transition. Protoplasma 254(1):505–522. https://doi.org/10.1007/s00709-016-0971-1

    Article  CAS  PubMed  Google Scholar 

  39. Zheng LP, Li XP, Zhou LL, Wang JW (2021) Endophytes in Artemisia annua L.: new potential regulators for plant growth and artemisinin biosynthesis. Plant Growth Regul. https://doi.org/10.1007/s10725-021-00751-3

    Article  Google Scholar 

  40. Yang RY et al (2010) Senescent leaves of Artemisia annua are one of the most active organs for overexpression of Artemisinin biosynthesis responsible genes upon burst of singlet oxygen. Planta Med 76(7):734–742. https://doi.org/10.1055/s-0029-1240620

    Article  CAS  PubMed  Google Scholar 

  41. Trivedi G, Patel P, Saraf M (2020) Synergistic effect of endophytic selenobacteria on biofortification and growth of Glycine max under drought stress. S Afr J Bot 134:27–35. https://doi.org/10.1016/j.sajb.2019.10.001

    Article  CAS  Google Scholar 

  42. Das G, Varshney U (2006) Peptidyl-tRNA hydrolase and its critical role in protein biosynthesis. Microbiology 152(8):2191–2195. https://doi.org/10.1099/mic.0.29024-0

    Article  CAS  PubMed  Google Scholar 

  43. Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta (BBA) Gene Regul Mech 1819(2):137–148. https://doi.org/10.1016/j.bbagrm.2011.05.001

    Article  CAS  Google Scholar 

  44. Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19(6):479–509. https://doi.org/10.1080/07352680091139277

    Article  CAS  Google Scholar 

  45. Mao X, Zhang H, Tian S, Chang X, Jing R (2010) TaSnRK2.4, an SNF1-type serine/threonine protein kinase of wheat (Triticum aestivum L.), confers enhanced multistress tolerance in Arabidopsis. J Exp Bot 61(3):683–696. https://doi.org/10.1093/jxb/erp331

    Article  CAS  PubMed  Google Scholar 

  46. Zsigmond L et al (2008) Arabidopsis PPR40 connects abiotic stress responses to mitochondrial electron transport. Plant Physiol 146(4):1721–1737. https://doi.org/10.1104/pp.107.111260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Awasthi A, Bharti N, Nair P, Singh R, Shukla AK, Gupta MM et al (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

    Article  Google Scholar 

  48. Nath A, Dixit K, Sundaram S (2019) Developing designer microalgae consortia: a suitable approach to sustainable wastewater treatment. Application of microalgae in wastewater treatment, vol 1, domestic and industrial wastewater treatment, pp 57–80. https://doi.org/10.1007/978-3-030-13913-1_4

  49. Procter M, Kundu B, Sudalaimuthuasari N, AlMaskari RS, Saeed EE, Hazzouri KM, Amiri KM (2022) Microbiome of Citrullus colocynthis (L.) Schrad. reveals a potential association with non-photosynthetic cyanobacteria. Microorganisms 10(10):2083. https://doi.org/10.3390/microorganisms10102083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Álvarez C, Navarro JA, Molina-Heredia FP, Mariscal V (2020) Endophytic colonization of rice (Oryza sativa L.) by the symbiotic strain Nostoc punctiforme PCC 73102. Mol Plant Microbe Interact 33(8):1040–1045. https://doi.org/10.1094/MPMI-01-20-0015-SC

    Article  PubMed  Google Scholar 

  51. Feng W, Zhang Y, Wu B, Qin S, Lai Z (2014) Influence of environmental factors on carbon dioxide exchange in biological soil crusts in desert areas. Arid Land Res Manag 28(2):186–196. https://doi.org/10.1080/15324982.2013.835006

    Article  CAS  Google Scholar 

  52. Marler TE, Snyder LR, Shaw CA (2010) Cycas micronesica (Cycadales) plants devoid of endophytic cyanobacteria increase in β-methylamino-l-alanine. Toxicon 56(4):563–568. https://doi.org/10.1016/j.toxicon.2010.05.015

    Article  CAS  PubMed  Google Scholar 

  53. Bidyarani N, Prasanna R, Chawla G, Babu S, Singh R (2015) Deciphering the factors associated with the colonization of rice plants by cyanobacteria. J Basic Microbiol 55(4):407–419. https://doi.org/10.1002/jobm.201400591

    Article  CAS  PubMed  Google Scholar 

  54. Liu Y, Wei X (2021) Dark septate endophyte improves the drought-stress resistance of Ormosia hosiei seedlings by altering leaf morphology and photosynthetic characteristics. Plant Ecol 222:761–771. https://doi.org/10.1007/s11258-021-01135-3

    Article  Google Scholar 

  55. Niu Y, She Z, Su C, Zhao Q, Wang S, Xiao B (2022) The effects and the mechanisms of naringenin from Artemisia ordosica Krasch on allergic rhinitis based on mast cell degranulation model and network pharmacology. J Pharm Pharmacol 74(3):397–408. https://doi.org/10.1093/jpp/rgab166

    Article  PubMed  Google Scholar 

  56. Kanjanamaneesathian P, Shah A, Ridgway H, Jones EE (2022) Diversity and bioactivity of endophytic actinobacteria associated with grapevines. Curr Microbiol 79(12):390. https://doi.org/10.1007/s00284-022-03068-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Chen X et al (2014) ZmCIPK21, a maize CBL-interacting kinase, enhances salt stress tolerance in Arabidopsis thaliana. Int J Mol Sci 15(8):14819–14834. https://doi.org/10.3390/ijms150814819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Jaizme-Vega MC, Rodríguez-Romero AS, Guerra MP (2005) Effect of arbuscular mycorrhizal fungi (AMF) and other rhizosphere microorganisms on development of the banana root system. In: Banana root system: towards a better understanding for its productive management: proceedings of an international symposium/Sistema Radical del Banano: hacia un mejor conocimiento para su manejo productivo: Memorias de un simposio internacional, p 178. http://www.inibap.org/pdf/IN050550_en

  59. Gahlan P et al (2012) De novo sequencing and characterization of Picrorhiza kurrooa transcriptome at two temperatures showed major transcriptome adjustments. BMC Genom 13:126. https://doi.org/10.1186/1471-2164-13-126

    Article  CAS  Google Scholar 

  60. Kalra A, Chandra M, Awasthi A, Singh AK, Khanuja SPS (2010) Natural compounds enhancing growth and survival of rhizobial inoculants in vermicompost-based formulations. Biol Fertil Soils 46:521–524. https://doi.org/10.1007/s00374-010-0443-2

    Article  Google Scholar 

  61. Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18. https://doi.org/10.1007/s00253-009-2092-7

    Article  CAS  PubMed  Google Scholar 

  62. Wani KI, Zehra A, Choudhary S, Naeem M, Khan MMA, Khan R, Aftab T (2023) Exogenous strigolactone (GR24) positively regulates growth, photosynthesis, and improves glandular trichome attributes for enhanced artemisinin production in Artemisia annua. J Plant Growth Regul 42(8):4606–4615. https://doi.org/10.1007/s00344-022-10654-w

    Article  CAS  Google Scholar 

  63. Coutinho BG, Licastro D, Mendonça-Previato L, Cámara M, Venturi V (2015) Plant-influenced gene expression in the rice endophyte Burkholderia kururiensis M130. Mol Plant Microbe Interact 28(1):10–21. https://doi.org/10.1094/MPMI-07-14-0225-R

    Article  CAS  PubMed  Google Scholar 

  64. Nath A, Sundaram S (2020) Microbiome community interactions with social forestry and agroforestry. In: Microbial services in restoration ecology. Elsevier, pp 71–82. https://doi.org/10.1016/B978-0-12-819978-7.00005-1

  65. Barder HE, Sundet K, Rund BR, Evensen J, Haahr U, Ten Velden Hegelstad W et al (2013) Ten year neurocognitive trajectories in first-episode psychosis. Front Hum Neurosci 7:643. https://doi.org/10.3389/fnhum.2013.00643

    Article  PubMed  PubMed Central  Google Scholar 

  66. Pinski A, Betekhtin A, Hupert-Kocurek K, Mur LA, Hasterok R (2019) Defining the genetic basis osf plant–endophytic bacteria interactions. Int J Mol Sci 20(8):1947. https://doi.org/10.3390/ijms20081947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Harika K, Mondi SD, Laxmibai DJ, Chidravar VR, Rao VUM (2014) A comprehensive review on cardioprotective medicinal plants. Int J Invent Pharm Sci 2(4):793–799

    Google Scholar 

  68. Alhadrami HA, Sayed AM, El-Gendy AO et al (2021) A metabolomic approach to target antimalarial metabolites in the Artemisia annua fungal endophytes. Sci Rep 11:2770. https://doi.org/10.1038/s41598-021-82201-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Ikram NK, Simonsen HT (2017) A review of biotechnological artemisinin production in plants. Front Plant Sci 8:1966. https://doi.org/10.3389/fpls.2017.01966

    Article  PubMed  PubMed Central  Google Scholar 

  70. Knudsmark Jessing K, Duke SO, Cedergreeen N (2014) Potential ecological roles of artemisinin produced by Artemisia annua L. J Chem Ecol 40:100–117. https://doi.org/10.1007/s10886-014-0384-6

    Article  CAS  PubMed  Google Scholar 

  71. Bergna A, Cernava T, Zachow C, Berg G (2019) Analysing seed endophytes for biotechnology. In: Endophyte biotechnology: potential for agriculture and pharmacology. CABI, Wallingford, pp 42–58. https://doi.org/10.1079/9781786399427.0042

  72. Aghdam SA, Brown AMV (2021) Deep learning approaches for natural product discovery from plant endophytic microbiomes. Enviro Microbiome 16(1):1–20. https://doi.org/10.1186/s40793-021-00375-0

    Article  Google Scholar 

  73. Pandey SS, Jain R, Bhardwaj P, Thakur A, Kumari M, Bhushan S, Kumar S (2022) Plant probiotics-endophytes pivotal to plant health. Microbiol Res 263:127148. https://doi.org/10.1016/j.micres.2022.127148

    Article  CAS  PubMed  Google Scholar 

  74. Wang J (2001) Glucose biosensors: 40 years of advances and challenges. Electroanalysis 13(12):983–988. https://doi.org/10.1002/1521-4109(200108)13:12%3C983::AIDELAN983%3E3.0.CO;2-%23

  75. Liu CH, Mishra AK, Tan RX, Tang C, Yang H, Shen YF (2006) Repellent and insecticidal activities of essential oils from Artemisia princeps and Cinnamomum camphora and their effect on seed germination of wheat and broad bean. Biores Technol 97(15):1969–1973. https://doi.org/10.1016/j.biortech.2005.09.002

    Article  CAS  Google Scholar 

  76. Olofsson L, Engström A, Lundgren A, Brodelius PE (2011) Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biol 11:1–12. http://www.biomedcentral.com/1471-2229/11/45

  77. Zhang X, Wang H, He L, Lu K, Sarmah A, Li J, Huang H (2013) Using biochar for remediation of soils contaminated with heavy metals and organic pollutants. Environ Sci Pollut Res 20(12):8472–8483. https://doi.org/10.1007/s11356-013-1659-0

    Article  CAS  Google Scholar 

  78. Lu ZL, Dosher BA (2000) Spatial attention: different mechanisms for central and peripheral temporal precues? J Exp Psychol Hum Percept Perform 26(5):1534. https://doi.org/10.1037/0096-1523.26.5.1534

    Article  CAS  PubMed  Google Scholar 

  79. Shen A, Kamp HD, Gründling A, Higgins DE (2006) A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression. Genes Dev 20(23):3283–3295. https://doi.org/10.1101/gad.1492606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Xie D, Zou Z, Ye H, Li G, Guo Z (2001) Selection of hairy root clones of Artemisia annua L. for artemisinin production. Isr J Plant Sci 49(2):129–134. https://doi.org/10.1560/N11N-6BLG-ER7C-XKCT

    Article  CAS  Google Scholar 

  81. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439(7076):589–593. https://doi.org/10.1038/nature04404

    Article  CAS  PubMed  Google Scholar 

  82. Aftab T, Masroor M, Khan A, Idrees M, Naeem M (2010) Salicylic acid acts as potent enhancer of growth, photosynthesis and artemisinin production in Artemisia annua L. J Crop Sci Biotechnol 13(3):183–188. https://doi.org/10.1007/s12892-010-0040-3

    Article  Google Scholar 

  83. Zheng V, Cao B, Zheng Y, Xie X, Yang Q (2010) Collaborative filtering meets mobile recommendation: A user-centered approach. In: Proceedings of the AAAI conference on artificial intelligence, vol 24, no 1, pp 236–241. https://doi.org/10.1609/aaai.v24i1.7577

  84. Aftab T, Khan MMA, Idrees M, Naeem M, Hashmi N, Varshney L (2011) Enhancing the growth, photosynthetic capacity and artemisinin content in Artemisia annua L. by irradiated sodium alginate. Radiat Phys Chem 80(7):833–836. https://doi.org/10.1016/j.radphyschem.2011.03.004

    Article  CAS  Google Scholar 

  85. Wu Y et al (2014) Comparative transcriptome profiling of a desert evergreen shrub, Ammopiptanthus mongolicus, in response to drought and cold stresses. BMC Genom 15(1):671. https://doi.org/10.1186/1471-2164-15-671

    Article  CAS  Google Scholar 

  86. Zheng Y, Jiao C, Sun H, Rosli HG, Pombo MA, Zhang P et al (2016) iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol Plant 9(12):1667–1670. https://doi.org/10.1016/j.molp.2016.09.014

    Article  CAS  PubMed  Google Scholar 

  87. Hussain Y, Ullah SF, Akhter G, Aslam AQ (2017) Groundwater quality evaluation by electrical resistivity method for optimized tubewell site selection in an ago-stressed Thal Doab Aquifer in Pakistan. Model Earth Syst Environ 3(1):1–9. https://doi.org/10.1007/s40808-017-0282-3

    Article  Google Scholar 

  88. Mandal S, Van Treuren W, White RA, Eggesbø M, Knight R, Peddada SD (2015) Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb Ecol Health Dis 26(1):27663. https://doi.org/10.3402/mehd.v26.27663

    Article  PubMed  Google Scholar 

  89. 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

    Article  PubMed  PubMed Central  Google Scholar 

  90. Arora S, Cohen N, Hazan E (2018). On the optimization of deep networks: implicit acceleration by overparameterization. In: Proceedings of the 35th international conference on machine learning. Proceedings of machine learning research, vol 80, pp 244–253. https://proceedings.mlr.press/v80/arora18a.html

  91. Gupta DK, Palma JM, Corpas FJ (eds) (2016) Redox state as a central regulator of plant-cell stress responses. Springer, Berlin, p 386. https://doi.org/10.1007/978-3-319-44081-1

  92. Paul F, Arkin YA, Giladi A, Jaitin DA, Kenigsberg E, Keren-Shaul H et al (2015) Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 163(7):1663–1677. https://doi.org/10.1016/j.cell.2015.11.013

    Article  CAS  PubMed  Google Scholar 

  93. Bhagavathy GV, Nieves GMV, Webb MZ, Chauhan KR (2015) Arthropod deterrents from Artemisia pallens (davana oil) components. Nat Prod Commun 10(8):1934578X1501000802. https://doi.org/10.1177/1934578X1501000802

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adi Nath.

Ethics declarations

Conflict of interest

There is no conflict of interest for this manuscript. The authors declare that they have no known competing financial interest.

Ethical approval

Not applicable.

Consent of participate

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nath, A., Sharma, A., Singh, S.K. et al. Bio Prospecting of Endophytes and PGPRs in Artemisinin Production for the Socio-economic Advancement. Curr Microbiol 81, 4 (2024). https://doi.org/10.1007/s00284-023-03516-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03516-5

Navigation