Abstract
Plants are regarded as resources to obtain various industrially important compounds such as pharmaceutical, agrochemical and aromatic products which are produced in their roots, stem, leaves and other aerial parts and mostly extracted from field-grown plants. However, the over-exploitation of plants for secondary metabolites often leads to becoming endangered and in threat of extinction. Owing to these constraints, in vitro culture techniques provide an alternative to overcome problems associated with field production and promotes their conservation. The use of elicitation for the enhancement of secondary metabolite production is gaining importance. Elicitation is defined as an increased production of biomass and secondary metabolites in both in vitro and ex vivo grown plants, subjected to the exposure of different elicitors. The process of elicitation is influenced by culture conditions like elicitor concentration, duration, age and composition of culture. So, this review emphasises the role of these in vitro culture conditions on secondary metabolite production and to pave way for their enhanced in vitro production. Also discussed are various elicitor responses on different biochemical and molecular pathways to elucidate the mechanism of action of jasmonic acid and methyl jasmonate in secondary metabolite production.




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Acosta IF, Gasperini D, Chételat A, Stolz S, Santuari L, Farmer EE (2013) Role of NINJA in root jasmonate signaling. Proc Natl Acad Sci U S A 110:15473–15478
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 9:811–824
Ahlawat S, Saxena P, Ali A, Khan S, Abdin MZ (2017) Comparative study of withanolide production and the related transcriptional responses of biosynthetic genes in fungi elicited cell suspension culture of Withania somnifera in shake flask and bioreactor. Plant Physiol Biochem 114:19–28
Ajungla L, Patil PP, Barmukh RB, Nikam TD (2009) Influence of biotic and abiotic elicitors on accumulation of hyoscyamine and scopolamine in root cultures of Datura metel (L). Indian J Biotechnol 8:317–322
Algar E, Gutierrez-Mañero FJ, Bonilla A, Lucas JA, Radzki W, Ramos-Solano B (2012) Pseudomonas fluorescens N21.4 metabolites enhance secondary metabolism isoflavones in soybean (Glycine max) calli cultures. J Agric Food Chem 60:11080–11087
Ali M, Abbasi BH, Ali GS (2015) Elicitation of antioxidant secondary metabolites with jasmonates and gibberellic acid in cell suspension cultures of Artemisia absinthium L. Plant Cell Tiss Org Cult 120:1099–1106
Ali MB, Yu KW, Hahn EJ, Paek KY (2005) Differential responses of anti-oxidants enzymes, lipoxygenase activity, ascorbate content and the production of saponins in tissue cultured root of mountain Panax ginseng C.A. Mayer and Panax quinquefolium L. in bioreactor subjected to methyl jasmonate stress. Plant Sci 169:83–92
Ali MS, Baek KH (2020) Jasmonic acid signalling pathway in response to abiotic stresses in plants. Int J Mol Sci 21:621. https://doi.org/10.3390/ijms21020621
Amirjani MR (2012) Effects of cadmium on wheat growth and some physiological factors. Int J For Soil Eros 2:50–58
Anderson WC (1978) Tissue-culture propagation of rhododendrons. In vitro-J Tiss Cult Assoc 14:334–334
Anjum S, Abbasi BH, Doussot J, Favre-Réguillon A, Hano C (2017) Effects of photoperiod regimes and ultraviolet-C radiations on biosynthesis of industrially important lignans and neolignans in cell cultures of Linum usitatissimum (L). (flax). J Photochem Photobiol B Biol 167:216–227
Anusha TS, Joseph MV, Elyas KK (2016) Callus induction and elicitation of total phenolics in callus cell suspension culture of Celastrus paniculatus - willd, an endangered medicinal plant in India. Pharmacognosy J 8:471–475. https://doi.org/10.5530/pj.2016.5.10
Baeg IH, So S (2013) The world ginseng market and the ginseng (Korea). J Ginseng Res 37:1–7. https://doi.org/10.5142/jgr.2013.37.1
Ballare CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249–257
Barrientos Carvacho H, Pérez C, Zúñiga G, Mahn A (2014) Effect of methyl jasmonate, sodium selenate and chitosan as exogenous elicitors on the phenolic compounds profile of broccoli sprouts. J Sci Food Agr 94:2555–2561
Bensaddek L, Gillet F, Saucedo JEN, Fliniaux MA (2001) The effect of nitrate and ammonium concentrations on growth and alkaloid accumulation of Atropa belladonna hairy roots. J Biotechnol 85:35–40
Biswas T, Pandey SS, Maji D, Gupta V, Kalra A, Singh M, Mathur A, Mathur AK (2018) Enhanced expression of ginsenoside biosynthetic genes and in vitro ginsenoside production in elicited Panax sikkimensis (Ban) cell suspensions. Protoplasma 255:1147–1160
Causier B, Ashworth M, Guo W, Davies B (2012) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158:423–438
Chandran H, Meena M, Barupal T, Sharma K (2020) Plant tissue culture as a perpetual source for production of industrially important bioactive compounds. Biotechnol Rep 26:e00450. https://doi.org/10.1016/j.btre.2020.e00450
Chang JH, Shin JH, Chung IS, Lee HJ (1998) Improved menthol production from chitosan-elicited suspension culture of Mentha piperita. Biotechnol Lett 20:1097–1099
Chen G, Wang S, Huang X, Hong J, Du L, Zhang L, Ye L (2015) Environmental factors affecting growth and development of Banlangen (Radix isatidis) in China. African J Plant Sci 9:421–426
Chen R, Jiang H, Li L, Zhai Q, Qi L, Zhou W, Liu X, Li H, Zheng W, Sun J, Li C (2012) The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant Cell 24:2898–2916
Cheng Q, He Y, Li G, Liu Y, Gao W, Huang L (2013) Effects of combined elicitors on tanshinone metabolic profiling and SmCPS expression in Salvia miltiorrhiza hairy root cultures. Molecules 18:7473–7485
Chini A, Gimenez-Ibanez S, Goossens A, Solano R (2016) Redundancy and specificity in jasmonate signalling. Curr Opin Plant Biol 33:147–156
Cho HY, Son SY, Rhee HS, Yoon SYH, Lee-Parsons CW, Park JM (2008) Synergistic effects of sequential treatment with methyl jasmonate, salicylic acid and yeast extract on benzophenanthridine alkaloid accumulation and protein expression in Eschscholtzia californica suspension cultures. J Biotechnol 135:117–122
De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17:349–359
Docimo T, Davis AJ, Luck K, Fellenberg C, Reichelt M, Phillips M, Gershenzon J, D’Auria JC (2015) Influence of medium and elicitors on the production of cocaine, amino acids and phytohormones by Erythroxylum coca calli. Plant Cell Tiss Org Cult 120:1061–1075
Efferth T (2019) Biotechnology applications of plant callus cultures. Engineering 5:50–59
Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297
Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350
Fritz C, Palacios Rojas N, Feil R, Stitt M (2006) Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J 46:533–548
Fu CX, Xu YJ, Zhao DX, Ma FS (2006) A comparison between hairy root cultures and wild plants of Saussurea involucrata in phenylpropanoids production. Plant Cell Rep 24:750–754
Gadzovska S, Maury S, Delaunay A, Spasenoski M, Joseph C, Hagege D (2007) Jasmonic acid elicitation of Hypericum perforatum L. cell suspensions and effects on the production of phenylpropanoids and naphtodianthrones. Plant Cell Tiss Org Cult 89:1–13
Gamborg OL, Murashige T, Thorpe TA, Vasil IK (1976) Plant-tissue culture media. In vitro-J Tiss Cult Assoc 12:473–478
Ganapathi G, Kargi F (1990) Recent advances in indole alkaloid production by Catharanthus roseus (Periwinkle). J Exp Bot 41:259–267
Gautam S, Mishra A, Tiwari A (2011) Catharanthus alkaloids and their enhanced production using elicitors: a review. Intl J Pharm Technol 3:713–724
Georgiev MI, Pavlov AI, Bley T (2007) Hairy root type plant in vitro systems as sources of bioactive substances. Appl Microbiol Biotechnol 74:1175–1185
Georgiev MI, Weber J, Maciuk A (2009) Bioprocessing of plant cell cultures for mass production of targeted compounds. Appl Microbiol Biotechnol 83:809–823
Ghanati F, Bakhtiarian S (2014) Effect of methyl jasmonate and silver nanoparticles on production of secondary metabolites by Calendula officinalis L. (Asteraceae). Trop J Pharm Res 13:1783–1789
Ghosh S, Ghosh B, Jha S (2006) Aluminium chloride enhances colchicine production in root cultures of Gloriosa superba. Biotechnol Lett 28:497–503
Giri CC, Zaheer M (2016) Chemical elicitors versus secondary metabolite production in vitro using plant cell, tissue and organ cultures: recent trends and a sky eye view appraisal. Plant Cell Tiss Org Cult 126:1–18. https://doi.org/10.1007/s11240-016-0985-6
Gorelick J, Bernstein N (2014) Elicitation: an underutilized tool in the development of medicinal plants as a source of therapeutic secondary metabolites. In: Sparks DL (ed) Advances in Agronomy, Book Series, vol 124. Elsevier, UK, pp 201–230
Gundlach H, Muller MJ, Kutchan TM, Zenk MH (1992) Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci U S A 89:2389–2393
Halder M, Roychowdhury D, Jha S (2018) A critical review on biotechnological interventions for production and yield enhancement of secondary metabolites in hairy root cultures. In: Srivastava V, Mehrotra S, Mishra S (eds) Hairy roots. Springer Nature, Singapore, pp 21–44
Halder M, Sarkar S, Jha S (2019) Elicitation: a biotechnological tool for enhanced production of secondary metabolites in hairy root cultures. Eng Life Sci 19:880–895
Han GZ (2017) Evolution of jasmonate biosynthesis and signalling mechanisms. J Exp Bot 68:1323–1331
Hasanloo T, Sepehrifar R, Rahnama H, Shams MR (2009) Evaluation of the yeast-extract signaling pathway leading to silymarin biosynthesis in milk thistle hairy root culture. World J Microbiol Biotechnol 25:1901–1909
Hayashi H, Huang P, Inoue K (2003) Up-regulation of soyasaponin biosynthesis by methyl jasmonate in cultured cell of Glycyrrhiza glabra. Plant Cell Physiol 44:404–411
Ho TT, Murthy HN, Park SY (2020) Methyl Jasmonate induced oxidative stress and accumulation of secondary metabolites in plant cell and organ cultures. Intl J Mol Sci 21:716
Isah T, Umar S, Mujib A, Sharma MP, Rajasekharan PE, Zafar N, Frukh A (2018) Secondary metabolism of pharmaceuticals in the plant in vitro cultures: strategies, approaches, and limitations to achieving higher yield. Plant Cell Tiss Org Cult 132:239–265
Jafari HR, Payamnoor V, Ghasemi BK, Ahmadian CN (2016) Optimization of callus induction and cell suspension culture of Betula pendula Roth for improved production of betulin, betulinic acid, and antioxidant activity. In Vitro Cell Dev Biol - Plant 52:400–407. https://doi.org/10.1007/s11627-016-9773-6
Jaleel CA, Gopi R, Manivannan P, Panneerselvam R (2007) Antioxidative potentials as a protective mechanism in Catharanthus roseus (L.) G. Don. plants under salinity stress. Turk J Bot 31:245–251
Jeong GA, Park DH (2007) Enhanced secondary metabolite biosynthesis by elicitation in transformed plant root system. Appl Biochem Biotechnol 130:436–446
Jeong GT, Park DH, Ryu HW, Hwang B, Woo JC, Kim D, Kim SW (2005) Production of antioxidant compounds by culture of Panax ginseng CA Meyer hairy roots. In: Twenty-sixth symposium on biotechnology for fuels and chemicals. Humana Press, pp 1147–1157
Jesionek A, Kokotkiewicz A, Krolicka A, Zabiegala B, Luczkiewicz M (2018) Elicitation strategies for the improvement of essential oil content in Rhododendron tomentosum (Ledum palustre) bioreactor-grown microshoots. Ind Crops Prod 123:461–469
John R, Ahmad P, Gadgil K, Sharma S (2008) Effect of cadmium and lead on growth, biochemical parameters and uptake in Lemna polyrrhiza L. Plant Soil Environ 54:262–270
Jones AMP, Saxena PK, Murch SJ (2009) Elicitation of secondary metabolism in Echinacea purpurea L. by gibberellic acid and triazoles. Eng Life Sci 9:205–210
Jwa CS, Yang YT, Koh JS (2000) Changes in free sugars, organic acids, free amino acids and minerals by harvest time and parts of Acanthopanax koreanum. J Kor Soc Agric Chem Biotechnol 43:106–109
Karuppusamy S (2009) A review on trends in production of secondary metabolites from higher plants by in vitro tissue, organ and cell cultures. J Med Plants Res 3:1222–1239
Khan A, Khan MA, Alam M, Akbar R, Ali A, Mohammad S et al (2019) Analysis of the differential effects of methyl jasmonate on induction of adventitious roots and antioxidant potential in Artemisia scoparia. Int J Biosci 15:547–558. https://doi.org/10.12692/ijb/15.2.547-558
Khojasteh D, Kazerooni M, Salarian S, Kamali R (2016) Droplet impact on superhydrophobic surfaces: a review of recent developments. J Ind Eng Chem 42:1–14
Kim HJ, Chen F, Wang X, Rajapakse NC (2005) Effect of chitosan on the biological properties of sweet basil (Ocimum basilicum L.). J Agric Food Chem 53:3696–3701
Kim JH, Shin JH, Lee HJ, Chung IS, Lee HJ (1997) Effect of chitosan on indirubin production from suspension culture of Polygonum tinctorium. J Ferment Bioeng 83:206–208
Komaraiah P, Reddy GV, Reddy PS, Raghavendra AS, Ramakrishna SV, Reddanna P (2003) Enhanced production of antimicrobial sesquiterpenes and lipoxygenase metabolites in elicitor-treated hairy root cultures of Solanum tuberosum. Biotechnol Lett 25:593–597
Kováčik J, Klejdus B, Babula P, Jarošová M (2014) Variation of antioxidants and secon dary metabolites in nitrogen–deficient barley plants. J Plant Physiol 171:260–268
Królicka A, Maliński E, Łojkowska E, Szafranek J (2003) Elicitation of secondary metabolites in in vitro cultures of Ammi majus (L). Enzym Microb Technol 33:565–568
Kundu S, Chakraborty D, Kundu A, Pal A (2013) Proteomics approach combined with biochemical attributes to elucidate compatible and incompatible plant-virus interactions between Vigna mungo and mungbean yellow mosaic India virus. Proteome Sci 11:1–14
Lambert E, Faizal A, Geelen D (2011) Modulation of triterpene saponin production: in vitro cultures, elicitation, and metabolic engineering. Appl Biochem Biotechnol 164:220–237
Largia MJV, Pothiraj G, Shilpha J, Ramesh M (2015) Methyl jasmonate and salicylic acid synergism enhances bacoside A content in shoot cultures of Bacopa monnieri (L.). Plant Cell Tiss Org Cult 122:9–20
Lee EJ, Park SY, Paek KY (2015) Enhancement strategies of bioactive compound production in adventitious root cultures of Eleutherococcus koreanum Nakai subjected to methyl jasmonate and salicylic acid elicitation through airlift bioreactors. Plant Cell Tiss Org Cult 120:1–10
Li B, Wang B, Li H, Peng L, Ru M, Liang Z, Yan X, Zhu Y (2016) Establishment of Salvia castanea Diels f. tomentosa Stib. hairy root cultures and the promotion of tanshinone accumulation and gene expression with Ag+, methyl jasmonate, and yeast extract elicitation. Protoplasma 253:87–100
Li Y, Qin L, Zhao J, Muhammad T, Cao H, Li H, Zhang Y, Liang Y (2017) SlMAPK3 enhances tolerance to tomato yellow leaf curl virus (TYLCV) by regulating salicylic acid and jasmonic acid signaling in tomato (Solanum lycopersicum). PLoS One 12:e0172466
Lu MB, Wong HL, Teng WL (2001) Effects of elicitation on the production of saponin in cell culture of Panax ginseng. Plant Cell Rep 20:674–677
Marsik P, Langhansova L, Dvorakova M, Cigler P, Hruby M, Vanek T (2014) Increased ginsenosides production by elicitation of in vitro cultivated Panax ginseng adventitious roots. Med Aromat Plant 3:1–5
Mathew R, Sankar PD (2012) Effect of methyl jasmonate and chitosan on growth characteristics of Ocimum basilicum L., Ocimum sanctum L. and Ocimum gratissimum L. cell suspension cultures. African J Biotechnol 11:4759–4766. https://doi.org/10.5897/AJB11.3183
Mendoza D, Cuaspud O, Arias JP, Ruiz O, Arias M (2018) Effect of salicylic acid and methyl jasmonate in the production of phenolic compounds in plant cell suspension cultures of Thevetia peruviana. Biotechnol Rep 19:e00273
Mir MY, Kamili AN, Hassan QP, Tyub S (2017) Effect of light and dark conditions on biomass accumulation and secondary metabolite production in suspension cultures of Artemisia amygdalina Decne. J Himal Ecol Sustain Dev 12:1–6
Murashige T, Tucker DPH (1969) Growth factor requirements of citrus tissue culture. In: Chapman HD (ed) Proceedings of the 1st international Citrus symposium. University of California–Riverside Publication, Riverside, pp 1155–1161
Murthy HN, Lee EJ, Paek KY (2014) Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell Tiss Org Cult 118:1–16
Namdeo A, Patil S, Fulzele DP (2002) Influence of fungal elicitors on production of ajmalicine by cell cultures of Catharanthus roseus. Biotechnol Prog 18:159–162
Namdeo AG (2007) Plant cell elicitation for production of secondary metabolites: a review. Pharmacogn Rev 1:69–79
Ncube B, Finnie JF, Van Staden J (2012) Quality from the field: the impact of environmental factors as quality determinants in medicinal plants. S Afr J Bot 82:11–20
Núñez M, Mazzafera P, Mazorra LM, Siqueira WJ, Zullo MAT (2003) Influence of a brassinosteroid analogue on antioxidant enzymes in rice grown in culture media with NaCl. Biol Plant 47:67–70
Nurchgani N, Solichatun S, Anggarwulan E (2008) The reserpine production and callus growth of Indian snake root (Rauvolfia serpentina (L.) Benth. Ex Kurz.) cultured by addition of Cu2+. Biodiversitas 9:177–179
Okršlar V, Plaper I, Kovač M, Erjavec A, Obermajer T, Rebec A, Ravnikar M, Žel J (2007) Saponins in tissue culture of Primula veris L. In Vitro Cell Dev Biol - Plant 43:644–651
Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA (2001) Hydrogen peroxide acts as a secondary messenger for the induction of defence genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191
Owolabi IO, Yupanqui CT, Siripongvutikorn S (2018) Enhancing secondary metabolites (emphasis on phenolics and antioxidants) in plants through elicitation and metabolomics. Pak J Nut 17:411–420
Pan W (2014) Bioactive compounds from Vitex leptobotrys. J Nat Prod 77:663–667
Pandey N, Pandey-Rai S (2014) Short term UV-B radiation-mediated transcriptional responses and altered secondary metabolism of in vitro propagated plantlets of Artemisia annua (L). Plant Cell Tiss Org Cult 116:371–385
Parast BM, Chetri SK, Sharma K, Agrawal V (2011) In vitro isolation, elicitation of psoralen in callus cultures of Psoralea corylifolia and cloning of psoralen synthase gene. Plant Physiol Biochem 49:1138–1146
Park JM, Yoon SY, Giles KL, Songstad DD, Eppstein D, Novakovski D, Friesen L, Roewer I (1992) Production of sanguinarine by suspension culture of Papaver somniferum in bioreactors. J Ferment Bioeng 74:292–296
Patel H, Krishnamurthy R (2013) Elicitors in plant tissue culture. J Pharmacog Phytochem 2:60–65
Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez AC, Chico JM, Vanden R, Sewell J, Gil E et al (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791
Perassolo M, Quevedo CV, Giulietti AM, Talou JR (2011) Stimulation of the proline cycle and anthraquinone accumulation in Rubia tinctorum cell suspension cultures in the presence of glutamate and two proline analogs. Plant Cell Tiss Org Cult 106:153–159
Pirbalouti AG, Sajjadi SE, Parang K (2014) A review (research and patents) on jasmonic acid and its derivatives. Arch Pharm Chem Life Sci 347:229–239
Pirian K, Piri K (2012) Effect of methyl jasmonate and salicylic acid on noradrenalin accumulation in hairy roots of Portulaca oleracea (L). Int Res J Appl Basic Sci 3:213–218
Pitta-Alvarez SI, Spollansky TC, Giulietti AM (2000) The influence of different biotic and abiotic elicitors on the production and profile of tropane alkaloids in hairy root cultures of Brugmansia candida. Enzym Microb Technol 26:252–258
Portu J, López R, Santamaría P, Garde-Cerdán T (2017) Elicitation with methyl jasmonate supported by precursor feeding with phenylalanine: effect on Garnacha grape phenolic content. Food Chem 237:416–422
Qi T, Song S, Ren Q, Wu D, Huang H, Chen Y, Fan M, Peng W, Ren C, Xiea D (2011) The jasmonate-ZIM-domain proteins interact with the WD-repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell 23:1795–1814
Ramani S, Chelliah J (2007) UV-B-induced signaling events leading to enhanced-production of catharanthine in Catharanthus roseus cell suspension cultures. BMC Plant Biol 7:61
Ramirez-Estrada K, Vidal-Limon H, Hidalgo D, Moyano E, Golenioswki M, Cusidó RM, Palazon J (2016) Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21:182. https://doi.org/10.3390/molecules21020182
Rao SR, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153
Raomai S, Kumaria S, Kehie M, Tandon P (2015) Plantlet regeneration of Paris polyphylla Sm. via thin cell layer culture and enhancement of steroidal saponins in mini-rhizome cultures using elicitors. Plant Growth Regul 75:341–353
Rhee HS, Cho HY, Son SY, Yoon SYH, Park JM (2010) Enhanced accumulation of decursin and decursinol angelate in root cultures and intact roots of Angelica gigas Nakai following elicitation. Plant Cell Tiss Org Cult 101:295–302
Rijhwani SK, Shanks JV (1998) Effect of elicitor dosage and exposure time on biosynthesis of indole alkaloids by Catharanthus roseus hairy root cultures. Biotechnol Prog 14:442–449
Ruan J, Zhou Y, Zhou M, Yan J, Khurshid M, Weng W, Cheng J, Zhang K (2019) Jasmonic acid signaling pathway in plants. Int J Mol Sci 20:2479
Ruiz-May E, Galaz-Avalos RM, Loyola-Vargas VM (2009) Differential secretion and accumulation of terpene indole alkaloids in hairy roots of Catharanthus roseus treated with methyl jasmonate. Mol Biotechnol 41:278–285
Saeed S, Ali H, Khan T, Kayani W, Khan MA (2017) Impacts of methyl jasmonate and phenyl acetic acid on biomass accumulation and antioxidant potential in adventitious roots of Ajuga bracteosa (Wall ex Benth) a high valued endangered medicinal plant. Physiol Mol Biol Plant 23:229–237
Sajc L, Grubisic D, Vunjak-Novakovic G (2000) Bioreactors for plant engineering: an outlook for further research. Biochem Engineer J 4:89–99
Saranya Krishnan SR, Siril EA (2018) Elicitor mediated adventitious root culture for the large-scale production of anthraquinones from Oldenlandia umbellata L. Ind Crop Prod 114:173–179
Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499
Schenke D, Utami HP, Zhou Z, Gallegos M-T, Cai D (2019) Suppression of UV-B stress induced flavonoids by biotic stress: is there reciprocal crosstalk? Plant Physiol Biochem 134:53–63
Sellapan P, Rohani ER, Noor NM (2018) Sesquiterpene production in methyl Jasmonate-induced Persicaria minor cell suspension culture. Sains Malaysiana 47:3051–3059
Sevón N, Hiltunen R, Oksman-Caldentey KM (1992) Chitosan increases hyoscyamine content in hairy root cultures of Hyoscyamus muticus. Pharm Pharmacol Lett 2:96–99
Shabani L, Ehsanpour AA, Asghari G, Emami J (2009) Glycyrrhizin production by in vitro cultured Glycyrrhiza glabra elicited by methyl jasmonate and salicylic acid. Russ J Plant Physiol 56:621–626
Shakeran Z, Keyhanfar M, Asghari G, Ghanadian M (2015) Improvement of atropine production by different biotic and abiotic elicitors in hairy root cultures of Datura metel. Turk J Biol 39:111–118
Sharafi E, Nekoei SMK, Fotokian MH, Davoodi D, Mirzaei HH, Hasanloo T (2013) Improvement of hypericin and hyperforin production using zinc and iron nano-oxides as elicitors in cell suspension culture of St John’s wort (Hypericum perforatum L.). J Med Plant By-Products 2:177–184
Sharma M, Ahuja A, Gupta R, Mallubhotla S (2015) Enhanced bacoside production in shoot cultures of Bacopa monnieri under the influence of abiotic elicitors. Nat Prod Res 29:745–749
Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu FF, Sharon M, Browse J, He SY (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405
Shinde AN, Malpathak N, Fulzele DP (2009) Studied enhancement strategies for phytoestrogens production in shake flasks by suspension culture of Psoralea corylifolia. Bioresour Technol 100:1833–1839
Shukla N, Kiridena S (2016) A fuzzy rough sets-based multi-agent analytics framework for dynamic supply chain configuration. Intl J Prod Res 54:6984–6996
Siddiqui ZH, Mujib A (2012) Accumulation of vincristine in calcium chloride elicitated Catharanthus roseus cultures. Nat Prod J 2:307–315
Singh A, Dwivedi P (2018) Methyl-jasmonate and salicylic acid as potent elicitors for secondary metabolite production in medicinal plants. A review. J Pharmacogn Phytochem 7:750–757
Siva G, Sivakumar S, Premkumar G, Senthil KT, Jayabalan N (2015) Enhanced production of psoralen through elicitors treatment in adventitious root culture of Psoralea corylifolia (L). Int J Pharm Pharm Sci 7:146–149
Sivanandhan G, Dev GK, Jeyaraj M, Rajesh M, Arjunan A, Muthuselvam M, Manickavasagam M, Selvaraj N, Ganapathi A (2013) Increased production of withanolide A, withanone, and withaferin a in hairy root cultures of Withania somnifera (L.) Dunal. elicited with methyl jasmonate and salicylic acid. Plant Cell Tiss Org Cult 114:121–129
Skrzypczak-Pietraszek E, Urbańska A, Żmudzki P, Pietraszek J (2019) Elicitation with methyl jasmonate combined with cultivation in the Plantform™ temporary immersion bioreactor highly increases the accumulation of selected centellosides and phenolics in Centella asiatica (L.) urban shoot culture. Eng Life Sci 19:931–943
Song MC, Kim EJ, Kim E, Rathwell K, Nama SJ, Yoon YJ (2014) Microbial biosynthesis of medicinally important plant secondary metabolites. Nat Prod Res 31:1497–1509
Songstad DD, Giles KL, Park J, Novakovski D, Epp D, Friesen L, Roewer I (1989) Effect of ethylene on sanguinarine production from Papaver somniferum cell cultures. Plant Cell Rep 8:463–466
Suan See K, Bhatt A, Lai Keng C (2011) Effect of sucrose and methyl jasmonate on biomass and anthocyanin production in cell suspension culture of Melastoma malabathricum (Melastomaceae). Revista Biol Tropic 59:597–606
Taguchi G, Yazawa T, Hayashida N, Okazaki M (2001) Molecular cloning and heterologous expression of novel glucosyltransferases from tobacco cultured cells that have broad substrate specificity and are induced by salicylic acid and auxin. Eur J Biochem 268:4086–4094
Taj F, Khan MA, Ali H, Khan RS (2019) Improved production of industrially important essential oils through elicitation in the adventitious roots of Artemisia amygdalina. Plants 8:430
Talanova VV, Titov AF, Repkina NS, Ignatenko AA (2018) Effect of methyl jasmonate on the expression of Wcs genes and the activity of antioxidant enzymes at wheat cold adaptation. In: Doklady biochemistry and biophysics, vol 482. Pleiades Publishing, pp 238–241
Thakur M, Bhattacharya S, Khosla PK, Puri S (2019) Improving production of plant secondary metabolites through biotic and abiotic elicitation. J Appl Res Med Aromat Plants 12:1–12
Thaweesak J, Seiichi S, Hiroyuki T, Waraporn P (2011) Elicitation effect on production of plumbagin in in vitro culture of Drosera indica (L). J Med Plant Res 5:4949–4953
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–666
Urdová J, Rexová M, Mučaji P, Balažová A (2015) Elicitation–a tool to improve secondary metabolites production in Melissa Officinalis (L). Suspension cultures/Elicitácia ako nástroj na zlepšenie produkcie sekundárnych metabolitov v suspenzných kultúrach Melissa Officinalis (L). Europe Pharm J 62:46–50
Veersham C (2004) In elicitation: medicinal plant biotechnology. CBS Publisher, Delhi, pp 70–293
Wang F, Yu G, Liu P (2019) Transporter-mediated subcellular distribution in the metabolism and signaling of jasmonates. Front Plant Sci 10:390
Wang J, Man S, Gao W, Zhang L, Huang L (2013) Cluster analysis of ginseng tissue cultures, dynamic change of growth, total saponins, and specific oxygen uptake rate in bioreactor and immuno-regulative effect of ginseng adventitious root. Ind Crop Prod 41:57–63
Wang J, Qian J, Yao L, Lu Y (2015) Enhanced production of flavonoids by methyl jasmonate elicitation in cell suspension culture of Hypericum perforatum. Bioresource Bioprocess 2:5
Wang ZY, Zhong JJ (2002) Repeated elicitation enhances taxane production in suspension cultures of Taxus chinensis in bioreactors. Biotechnol Lett 24:445–448
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058
Wasternack C, Song S (2017) Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J Exp Bot 68:1303–1321
Wasternack C, Strnad M (2016) Jasmonate signaling in plant stress responses and development-active and inactive compounds. New Biotechnol 33:604–613. https://doi.org/10.1016/j.nbt.2015.11.001
Weathers PJ, Bunk G, McCoy MC (2005) The effect of phytohormones on growth and artemisinin production in Artemisia annua hairy roots. In Vitro Cell Dev Biol - Plant 41:47–53
Wink M, Alfermann AW, Franke R, Wetterauer B, Distl M, Windhövel J, Wildi E (2005) Sustainable bioproduction of phytochemicals by plant in vitro cultures: anticancer agents. Plant Genetic Res 3:90–100
Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223
Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66:2839–2856
Yoon JH, Kim KH, Ma JC, Huh H (2000) Induced accumulation of triterpenoids in Scutellaria baicalensis suspension cultures using a yeast elicitor. Biotechnol Lett 22:1071–1075
Yosefi A, Mozafari AA, Javaidi T (2020) Jasmonic acid improves in vitro strawberry (Fragaria x ananassa Duch.) resistance to PEG-induced water stress. Plant Cell Tiss Org Cult 14:549–558
Yukimune Y, Tabata H, Higashi Y, Hara Y (1996) Methyl jasmonate induced overproduction of paclitaxel and baccatin III in Taxus cell suspension culture. Nature Biotecnol 14:1129–1132
Zabala MA, Angarita M, Restrepo JM, Caicedo LA, Perea M (2010) Elicitation with methyl-jasmonate stimulates peruvoside production in cell suspension cultures of Thevetia peruviana. In Vitro Cell Dev Biol - Plant 46:233–238
Zafar N, Mujib A, Ali M, Tonk D, Gulzar B (2017) Aluminum chloride elicitation (amendment) improves callus biomass growth and reserpine yield in Rauvolfia serpentina leaf callus. Plant Cell Tiss Org Cult 130:357–368
Zaragoza-Martínez F, Lucho-Constantino GG, Ponce-Noyola T, Esparza-García F, Poggi-Varaldo H, Cerda-García-Rojas CM, Trejo-Tapia G, Ramos-Valdivia AC (2016) Jasmonic acid stimulates the oxidative responses and triterpene production in Jatropha curcas cell suspension cultures through mevalonate as biosynthetic precursor. Plant Cell Tiss Org Cult 127:47–56
Zhang C, Yan Q, Cheuk W, Wu J (2004) Enhancement of tanshinone production in Salvia miltiorrhiza hairy root cultures by Ag+ elicitation and nutrition feeding. Planta Med 70:147–151
Zhang X, Liu CJ (2015) Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Mol Plant 8:17–27
Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333
Zhao J, Zhu WH, Hu Q, He XW (2000) Improved alkaloid production in Catharanthus roseus suspension cell cultures by various chemicals. Biotechnol Lett 22:1221–1226
Zhao JL, Zhou LG, Wu JY (2010a) Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 87:137–144
Zhao JL, Zhou LG, Wu JY (2010b) Promotion of Salvia miltiorrhiza hairy root growth and tanshinone production by polysaccharide–protein fractions of plant growth-promoting rhizobacterium Bacillus cereus. Process Biochem 45:1517–1522
Zhou M, Memelink J (2016) Jasmonate-responsive transcription factors regulating plant secondary metabolism. Biotechnol Adv 34:441–449
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NN is very thankful to University Grants Commission, India for research grant no. 191000913.
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NN and PS collected and reviewed the literature. NN and PS designed the idea. NN, SS and PS edited and approved the final version.
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Nabi, N., Singh, S. & Saffeullah, P. Responses of in vitro cell cultures to elicitation: regulatory role of jasmonic acid and methyl jasmonate: a review. In Vitro Cell.Dev.Biol.-Plant 57, 341–355 (2021). https://doi.org/10.1007/s11627-020-10140-6
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DOI: https://doi.org/10.1007/s11627-020-10140-6


