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Chemical elicitors versus secondary metabolite production in vitro using plant cell, tissue and organ cultures: recent trends and a sky eye view appraisal

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Abstract

Plant secondary biosynthetic pathways are exceedingly inducible by elicitors and facilitate enhanced metabolite production using plant cell tissue and organ cultures. Elicitors can regulate large number of control points and trigger the expression of key genes with increased cellular activities at biochemical and molecular level involving signal compounds. A large number of chemical elicitors viz: jasmonic acid (JA), methyl jasmonate (MeJA), salicylic acid (SA), acetyl salicylic acid (ASA), ethylene (ET) and ethrel (Ethe), heavy metals (HM), many types of chemical compounds (natural or synthetic) and their combinations are used for elicitation studies. Cell suspensions and hairy roots are commonly used culture systems followed by adventitious roots and multiple shoots for elicitation experiments. Amongst the elicitors and concentrations used 100 µM MeJA was found optimum for secondary metabolite enhancement in majority of experiments compared to SA and JA. Elicitor treatments promoted yield enhancements starting from 1.0 to maximum of 2230-fold across plant species studied. Elicitors singly with media additives, combination of elicitors and elicitors other than signal compounds along with hormones were found beneficial for enhanced secondary metabolite production. Further, a combination of target gene over expression and elicitor treatment also supported higher secondary product yield. The present communication presents information exclusively about the use of chemical elicitors for secondary metabolites production in vitro covering approximately more than a decade of research at one place in one review. Further, this extensive appraisal will be useful for the understanding and manipulation of secondary metabolites for enhanced production in vitro.

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References

  • Abhyankar G, Reddy VD, Giri CC, Rao KV, Lakshmi VV, Prabhakar S, Vairamani M, Thippeswamy BS, Bhattacharya PS (2005) Amplified fragment length polymorphism and metabolomic profiles of hairy roots of Psoralea corylifolia L. Phytochemistry 66:2441–2457

    Article  CAS  PubMed  Google Scholar 

  • 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 metal L. Indian J Biotechnol 8:317–322

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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, Tissue Organ Cult 120:1099–1106

    Article  CAS  Google Scholar 

  • Bae KH, Choi YE, Shin CG, Kim YY, Kim YS (2006) Enhanced ginsenoside productivity by combination of ethephon and methyl jasmoante in ginseng (Panax ginseng C.A. Meyer) adventitious root cultures. Biotechnol Lett 28:1163–1166

    Article  CAS  PubMed  Google Scholar 

  • Baenas N, García-Viguera C, Moreno DA (2014) Elicitation: a tool for enriching the bioactive composition of foods. Molecules 19:13541–13563

    Article  PubMed  CAS  Google Scholar 

  • Ballare CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249–257

    Article  CAS  PubMed  Google Scholar 

  • Banerjee S, Singh S, Rahman LU (2012) Biotransformation studies using hairy root cultures—a review. Biotechnol Adv 30:461–468

    Article  CAS  PubMed  Google Scholar 

  • Baque MA, Moh SH, Lee EJ, Zhong JJ, Paek KY (2012) Production of biomass and useful compounds from adventitious roots of high-value added medicinal plants using bioreactor. Biotechnol Adv 30:1255–1267

    Article  CAS  PubMed  Google Scholar 

  • BBC research report: botanical and plant-derived drugs in global markets. http://www.bccresearch.com/market-research/biotechnology/botanical-plant-derived-drugs-report-bio022g.html

  • Begum F, Nageswara Rao SS, Rao K, Prameela Devi Y, Giri A, Giri CC (2009) Increased vincristine production from Agrobacterium tumefaciens C-58 induced shooty teratomas of Catharanthus roseus. Nat Prod Res 23:973–981

    Article  CAS  PubMed  Google Scholar 

  • Belchi-Navarro S, Almagro L, Lijavetzky D, Bru R, Pedreño MA (2012) Enhanced extracellular production of trans-resveratrol in Vitis vinifera suspension cultured cells by using cyclodextrins and methyljasmonate. Plant Cell Rep 31:81–89

    Article  CAS  PubMed  Google Scholar 

  • Belhadj A, Telef N, Saigne C, Cluzet S, Barrieu F, Hamdi S, Mérillon JM (2008) Effect of methyl jasmonate in combination with carbohydrates on gene expression of PR proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiol Biochem 46:493–499

    Article  CAS  PubMed  Google Scholar 

  • Bhalla R, Narasimhan K, Swarup S (2005) Metabolomics and its role in understanding cellular responses in plants. Plant Cell Rep 24:562–571

    Article  CAS  PubMed  Google Scholar 

  • Bhuvaneswari CH, Rao K, Gandi S, Giri A (2015) Gymnemic acid enhancement in the suspension cultures of Gymnema sylvestre by using the signaling molecules—methyl jasmonate and salicylic acid. In Vitro Cell Dev Biol-Plant 51:88–92

    Article  CAS  Google Scholar 

  • Boatwright JL, Pajerowska-Mukhtar K (2013) Salicylic acid: an old hormone up to new tricks. Mol Plant Pathol 14:623–634

    Article  CAS  PubMed  Google Scholar 

  • Caarls L, Pieterse CM, Van Wees SC (2015) How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 6:170 (online first)

    Article  PubMed  PubMed Central  Google Scholar 

  • Caretto S, Quarta A, Durante M, Nisi R, De Paolis A, Blando F, Mita G (2011) Methyl jasmonate and miconazole differently affect arteminisin production and gene expression in Artemisia annua suspension cultures. Plant Biol 13:51–58

    Article  CAS  PubMed  Google Scholar 

  • Coste A, Vlase L, Halmagyi A, Deliu C, Coldea G (2011) Effects of plant growth regulators and elicitors on production of secondary metabolites in shoot cultures of Hypericum hirsutum and Hypericum maculatum. Plant Cell, Tissue Organ Cult 106:279–288

    Article  CAS  Google Scholar 

  • Cui L, Wang Z-Y, Zhou X-H (2012) Optimization of elicitors and precursors to enhance valtrate production in adventitious roots of Valeriana amurensis Smir. ex Kom. Plant Cell, Tissue Organ Cult 108:411–420

    Article  CAS  Google Scholar 

  • Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: a Review. Environ Exp Bot 115:49–57

    Article  CAS  Google Scholar 

  • Dass S, Ramawat KG (2009) Elicitation of guggulsterone production in cell cultures of Commiphora wightii by plant gums. Plant Cell, Tissue Organ Cult 96:349–353

    Article  Google Scholar 

  • Dias DA, Urban S, Roessner U (2012) A historical overview of natural products in drug discovery. Metabolites 2:303–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diwan R, Malpathak N (2011) Bioprocess optimization of furanocoumarin elicitation by medium renewal and re-elicitation: a perfusion-based approach. Appl Biochem Biotechnol 163:756–764

    Article  CAS  PubMed  Google Scholar 

  • Dong J, Wan G, Liang Z (2010) Accumulation of salicylic acid-induced phenolic compounds and raised activities of secondary metabolic and antioxidative enzymes in Salvia miltiorrhiza cell culture. J Biotechnol 148:99–104

    Article  CAS  PubMed  Google Scholar 

  • Durante M, Caretto S, Quarta A, De Paolis A, Nisi R, Mita G (2011) β-Cyclodextrins enhance artemisinin production in Artemisia annua suspension cell cultures. Appl Microbiol Biotechnol 90:1905–1913

    Article  CAS  PubMed  Google Scholar 

  • el Jaber-Vazdekis N, Barres ML, Ravelo AG, Zarate R (2008) Effects of elicitors on tropane alkaloids and gene expression in Atropa baetica transgenic hairy roots. J Nat Prod 71:2026–2031

    Article  PubMed  CAS  Google Scholar 

  • Elkington BG (2014) New finding of an anti-TB compound in the genus Marsypopetalum (Annonaceae) from a traditional herbal remedy of Laos. J Ethnopharmacol 151:903–911

    Article  PubMed  Google Scholar 

  • Gai QY, Jiao J, Luo M, Wang W, Gu CB, Fu YJ, Ma W (2016) Tremendous enhancements of isoflavonoid biosynthesis, associatedgene expression and antioxidant capacity in Astragalus membranaceus hairy root cultures elicited by methyl jasmonate. Process Biochem. doi:10.1016/j.procbio.2016.01.012

    Google Scholar 

  • Ghorpade RP, Chopra A, Nikam TD (2011) Influence of biotic and abiotic elicitors on four major isomers of boswellic acid in callus culture of Boswellia serrata Roxb. Plant Omics J 4:169–176

    CAS  Google Scholar 

  • Giri CC, Vijaya Laxmi G (2000) Production of transgenic rice with agronomically useful genes. Biotechnol Adv 18:653–683

    Article  CAS  PubMed  Google Scholar 

  • Giri A, Dhingra V, Giri CC, Singh A, Ward OP, Narasu ML (2001a) Biotransformation using cell, tissue, organ cultures and enzyme systems: current trend and future prospects. Biotechnol Adv 19:175–199

    Article  CAS  PubMed  Google Scholar 

  • Giri A, Giri CC, Dhingra V, Narasu ML (2001b) Enhanced production of podophyllotoxin from Agrobacterium rhizogenes transformed cultures of Podophyllum hexandrum. Nat Prod Lett 15:229–235

    Article  CAS  PubMed  Google Scholar 

  • Giri A, Giri CC, Narasu ML (2003) Recent advances in applications of transgenic hairy roots. In: Jaiwal PK, Singh RP (eds) Plant genetic engineering: improvement of commercial plants—II. Sci Tech Publisher LLC, Houston, pp 23–81

    Google Scholar 

  • Giri CC, Giri A, Narasu ML (2009) Catharanthus roseus (Periwinckle) a potential drug source for cancer chemotherapy and biotechnological interventions: an overview. In: Trivedi PC (ed) Medicinal plants: utilization and conservation. Aviskar Publishers, Jaipur, pp 475–504

    Google Scholar 

  • Gomez P, Ortuno A, Del Rio JA (2004) Ultrastructural changes and diosgenin content in cell suspensions of Trigonella foenum-graecum L. by ethylene treatment. Plant Growth Regul 44:93–99

    Article  CAS  Google Scholar 

  • Goossens A, Hakkinen ST, Laakso I, Seppänen-Laakso T, Biondi S, De Sutter V, Lammertyn F, Nuutila AM, Söderlund H, Zabeau M, Inzé D, Oksman-Caldentey KM (2003) A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc Natl Acad Sci USA 100:8595–8600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Goyal S, Ramawat KG (2008) Ethrel treatment enhanced isoflavonoids accumulation in cell suspension cultures of Pueraria tuberosa, a woody legume. Acta Physiol Plant 30:849–853

    Article  CAS  Google Scholar 

  • Guillon S, Tremouillaux-Guiller J, Pati PK, Rideau M, Gantet P (2006) Hairy root research: recent scenario and exciting prospects. Curr Opin Plant Biol 11:341–346

    Article  CAS  Google Scholar 

  • Gutierrez-Carbajal MG, Monforte-Gonzalez M, de Miranda-Ham ML, Godoy-Hernandez G, Vazquez-Flota F (2010) Induction of capsaicinoid synthesis in Capsicum chinense cell cultures by salicylic acid or methyl jasmonate. Biol Plant 54:430–434

    Article  CAS  Google Scholar 

  • Hadacek F (2002) Secondary metabolites as plant traits: current assessment and future perspectives. Crit Rev Plant Sci 21:273–322

    Article  CAS  Google Scholar 

  • Hao G, Du X, Zhao F, Shi R, Wang J (2009) Role of nitric oxide in UV-B-induced activation of PAL and stimulation of flavonoid biosynthesis in Ginkgo biloba callus. Plant Cell, Tissue Organ Cult 97:175–185

    Article  CAS  Google Scholar 

  • Hashemi SM, Naghavi MR (2016) Production and gene expression of morphinan alkaloids in hairy root culture of Papaver orientale L. using abiotic elicitors. Plant Cell, Tissue Organ Cult 125:31–41

    Article  CAS  Google Scholar 

  • Hernández-Domínguez E, Campos-Tamayo F, Vázquez-Flota F (2004) Vindoline synthesis in in vitro shoot cultures of Catharanthus roseus. Biotechnol Lett 26:671–674

    Article  PubMed  Google Scholar 

  • Hu FX, Zhong JJ (2008) Jasmonic acid mediates gene transcription of ginsenoside biosynthesis in cell cultures of Panax notoginseng treated with chemically synthesized 2-hydroxyethyl jasmonate. Process Biochem 43:113–118

    Article  CAS  Google Scholar 

  • Hu Y, Yu Y, Piao C, Liu J, Yu H (2011) Methyl jasmonate and salicylic acid induced d-chiro-inositol production in suspension cultures of buckwheat (Fagopyrum esculentum). Plant Cell, Tissue Organ Cult 106:419–424

    Article  CAS  Google Scholar 

  • Huang C, Qian ZG, Zhong JJ (2013) Enhancement of ginsenoside biosynthesis in cell cultures of Panax ginseng by N,N′-dicyclohexylcarbodiimide elicitation. J Biotechnol 165:30–36

    Article  CAS  PubMed  Google Scholar 

  • Hussain MS, Fareed S, Ansari S, Rahman MA, Ahmad IZ, Saeed M (2012) Current approaches towards production of secondary plant metabolites. J Pharm Bioallied Sci 4:10–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong GT, Park DH, Ryu HW, Hwang B, Woo JC, Kim D, Kim SW (2005) Production of antioxidant compounds by culture of Panax ginseng C.A. meyer hairy roots. Appl Biochem Biotechnol 121–124:1147–1158

    Article  PubMed  Google Scholar 

  • Kai G, Liao P, Xu H, Wang J, Zhou C, Zhou W, Qi Y, Xiao J, Wang Y, Zhang L (2012) Molecular mechanism of elicitor-induced tanshinone accumulation in Salvia miltiorrhiza hairy root cultures. Acta Physiol Plant 34:1421–1433

    Article  CAS  Google Scholar 

  • Kang SM, Jung HY, Kang YM, Yun DJ, Bahk JD, Jk Yang, Choi MS (2004) Effects of methyl jasmonate and salicylic acid on the production of tropane alkaloids and the expression of PMT and H6H in adventitious root cultures of Scopolia parviflora. Plant Sci 166:745–751

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Kasparova M, Siatka T, Klimesova V, Dusek J (2012) New Synthetic Pyridine Derivate as potential elicitor in production of isoflavonoids and flavonoids in Trifolium pretense L. suspension culture. Sci World J 2012:1–5

    Article  CAS  Google Scholar 

  • Kazan K (2015) Diverse role of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229

    Article  CAS  PubMed  Google Scholar 

  • Kehie M, Kumaria S, Tandon P (2016) Biotechnological enhancement of capsaicin biosynthesis in cell suspension cultures of Naga King Chili (Capsicum chinense Jacq.). Bioprocess Biosyst Eng 39:205–210

    Article  CAS  PubMed  Google Scholar 

  • Kikowska M, Budzianowski J, Krawczyk A, Thiem B (2012) Accumulation of rosmarinic, chlorogenic and caffeic acids in in vitro cultures of Eryngium planum L. Acta Physiol Plant 34:2425–2433

    Article  CAS  Google Scholar 

  • Kikowska M, Kędziora I, Krawczyk A, Thiem B (2015) Methyl jasmonate, yeast extract and sucrose stimulate phenolic acids accumulation in Eryngium planum L. shoot cultures. Acta Biochim Pol 62:197–200

    Article  CAS  PubMed  Google Scholar 

  • Kim OT, Kim MY, Hong MH, Ahn JC, Hwang B (2004) Stimulation of asiaticoside accumulation in the whole plant cultures of Centella asiatica (L.) urban by elicitors. Plant Cell Rep 23:339–344

    Article  CAS  PubMed  Google Scholar 

  • Kim YS, Cho JH, Park S, Han JY, Back K, Choi YE (2011) Gene regulation patterns in triterpene biosynthetic pathway driven by overexpression of squalene synthase and methyl jasmonate elicitation in Bupleurum falcatum. Planta 233:343–355

    Article  CAS  PubMed  Google Scholar 

  • Kim OT, Yoo NH, Kim GS, Kim YC, Bang KH, Hyun DY, Kim SH, Kim MY (2013) Stimulation of Rg3 ginsenoside biosynthesis in ginseng hairy roots elicited by methyl jasmonate. Plant Cell, Tissue Organ Cult 112:87–93

    Article  CAS  Google Scholar 

  • Kopyra M, Gwozdz EA (2004) The role of nitric oxide in plant growth regulation and responses to abiotic stress. Acta Physiol Plant 26:459–472

    Article  CAS  Google Scholar 

  • Lakhotia P, Pal SK, Singh SK, Singh MC, Prasad KV, Kishan S (2014) Influence of biotic and abiotic elicitors on production of betalain pigments in bougainvillea callus cultures. Indian J Hortic 71:373–378

    Google Scholar 

  • Lee KH (2010) Discovery and development of natural product-derived chemotherapeutic agents based on a medicinal chemistry approach. J Nat Prod 73:500–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, Tissue Organ Cult 120:1–10

    Article  CAS  Google Scholar 

  • Li W, Koike K, Asada Y, Yoshikawa T, Nikaido T (2005) Rosmarinic acid production by Coleus forskohlii hairy root cultures. Plant Cell, Tissue Organ Cult 80:151–155

    Article  CAS  Google Scholar 

  • Li M, Peebles CA, Shanks JV, San KY (2011) Effect of sodium nitroprusside on growth and terpenoid indole alkaloid production in Catharanthus roseus hairy root cultures. Biotechnol Prog 27:625–630

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Liang ZS, Yang DF, Liang X, Zhang YJ, Liu Y, Liu FH (2012) Roles of reactive oxygen species in methyl jasmonate and nitric oxide-induced tanshinone production in Salvia miltiorrhiza hairy roots. Plant Cell Rep 31:873–883

    Article  CAS  PubMed  Google Scholar 

  • Liu XN, Zhang XQ, Sun JS (2007) Effects of cytokinins and elicitors on the production of hypericins and hyperforin metabolites in Hypericum sampsonii and Hypericum perforatum. Plant Growth Regul 53:207–214

    Article  CAS  Google Scholar 

  • Liu J, Zhu J, Tang L, Wen W, Lv S, Yu R (2014) Enhancement of vindoline and vinblastine production in suspension-cultured cells of Catharanthus roseus by artemisinic acid elicitation. World J Microbiol Biotechnol 30:175–180

    Article  CAS  PubMed  Google Scholar 

  • Luczkiewicz M, Kokotkiewicz A (2012) Elicitation and permeabilisation affect the accumulation and storage profile of phytoestrogens in high productive suspension cultures of Genista tinctoria. Acta Physiol Plant 31:1–16

    Article  CAS  Google Scholar 

  • Mangas S, Bonfill M, Osuna L, Moyano E, Tortoriello J, Cusido RM, Piñol MT, Palazón J (2006) The effect of methyl jasmonate on triterpene and sterol metabolisms of Centella asiatica, Ruscus aculeatus and Galphimia glauca. Phytochemistry 67:2041–2049

    Article  CAS  PubMed  Google Scholar 

  • Mannan A, Liu C, 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 29:143–152

    Article  CAS  PubMed  Google Scholar 

  • Matkowski A (2008) Plant in vitro culture for the production of antioxidants—a review. Biotechnol Adv 6:548–560

    Article  CAS  Google Scholar 

  • Matsuura HN, Rau MR, Fett-Neto AG (2014) Oxidative stress and production of bioactive monoterpene indole alkaloids: biotechnological implications. Biotechnol Lett 36:191–200

    Article  CAS  PubMed  Google Scholar 

  • Miao GP, Zhu CS, Yang YQ, Feng MX, Ma ZQ, Feng JT, Zhang X (2014) Elicitation and in situ adsorption enhanced secondary metabolites production of Tripterygium wilfordii Hook. f. adventitious root fragment liquid cultures in shake flask and a modified bubble column bioreactor. Bioprocess Biosyst Eng 37:641–650

    Article  CAS  PubMed  Google Scholar 

  • Mobin M, Wu CH, Tewari RK, Paek KY (2015) Studies on the glyphosate-induced amino acid starvation and addition of precursors on caffeic acid accumulation and profiles in adventitious roots of Echinacea purpurea (L.) Moench. Plant Cell, Tissue Organ Cult 120:291–301

    Article  CAS  Google Scholar 

  • Moore BD, Andrew RL, Kulheim C, Foley WJ (2014) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol 201:733–750

    Article  PubMed  Google Scholar 

  • 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, Tissue Organ Cult 118:1–16

    Article  CAS  Google Scholar 

  • Namdeo AG (2007) Plant cell elicitation for production of secondary metabolites: a review. Pharmacogn Rev 1:69–79

    CAS  Google Scholar 

  • Nasim SA, Dhir B, Kapoor R, Fatima S, Mahmooduzzafar Mujib A (2010) Alliin production in various tissues and organs of Allium sativum grown under normal and sulphur-supplemented in vitro conditions. Plant Cell, Tissue Organ Cult 101:59–63

    Article  CAS  Google Scholar 

  • Oksman-Caldentey KM, Inzé D (2004) Plant cell factories in the postgenome era: new ways to produce designer secondary metabolites. Trends Plant Sci 9:433–440

    Article  CAS  PubMed  Google Scholar 

  • Onrubia M, Cusido RM, Ramirez K, Hernandez-Vazquez L, Moyano E, Bonfill M, Palazon J (2013) Bioprocessing of plant in vitro systems for the mass production of pharmaceutically important metabolites: paclitaxel and its derivatives. Curr Med Chem 20:880–891

    CAS  PubMed  Google Scholar 

  • Pan W (2014) Bioactive compounds from Vitex leptobotrys. J Nat Prod 77:663–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandey H, Pandey P, Singh S, Gupta R, Banerjee S (2015) Production of anti-cancer triterpene (betulinic acid) from callus cultures of different Ocimum species and its elicitation. Protoplasma 252:647–655

    Article  CAS  PubMed  Google Scholar 

  • Patil JG, Ahire ML, Nitnaware KM, Panda S, Bhatt VP, Kishor PB, Nikam TD (2013) In vitro propagation and production of cardiotonic glycosides in shoot cultures of Digitalis purpurea L. by elicitation and precursor feeding. Appl Microbiol Biotechnol 97:2379–2393

    Article  CAS  PubMed  Google Scholar 

  • Pawar KD, Thengane SR (2011) Influence of abiotic elicitation on production of dipyranocoumarins in suspension cultures of Calophyllum inophyllum L. Acta Physiol Plant 33:2149–2158

    Article  CAS  Google Scholar 

  • Peebles CA, Hughes EH, Shanks JV, San KY (2009) Transcriptional response of the terpenoid indole alkaloid pathway to the overexpression of ORCA3 along with jasmonic acid elicitation of Catharanthus roseus hairy roots over time. Metab Eng 11:76–86

    Article  CAS  PubMed  Google Scholar 

  • Pi Y, Jiang K, Hou R, Gong Y, Lin J, Sun X, Tang K (2010) Examination of camptothecin and 10-hydroxycamptothecin in Camptotheca acuminata plant and cell culture, and the affected yields under several cell culture treatments. Biocell 34:139–143

    PubMed  Google Scholar 

  • Pichersky E, Gang DR (2000) Genetics and biochemistry of secondary metabolites: an evolutionary perspective. Trends Plant Sci 5:439–445

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ptak A, Tahchy AEI, Wyzgolik G, Henry M, Laurain-Mattar D (2010) Effects of ethylene on somatic embryogenesis and galanthamine content in Leucojum aestivum L. cultures. Plant Cell, Tissue Organ Cult 102:61–67

    Article  CAS  Google Scholar 

  • Putalun W, Udomsin O, Yusakul G, Juengwatanatrakul T, Sakamoto S, Tanaka H (2010) Enhanced plumbagin production from in vitro cultures of Drosera burmanii using elicitation. Biotechnol Lett 32:721–724

    Article  CAS  PubMed  Google Scholar 

  • Qian ZG, Zhao ZJ, Xu Y, Qian X, Zhong JJ (2005) A novel synthetic fluoro-containing jasmonate derivative acts as a chemical inducing signal for plant secondary metabolism. Appl Microbiol Biotechnol 68:98–103

    Article  CAS  PubMed  Google Scholar 

  • Qiao W, Fan LM (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50:1238–1246

    Article  CAS  PubMed  Google Scholar 

  • Qin B, Ma L, Wang Y, Chen M, Lan X, Wu N, Liao Z (2014) Effects of acetylsalicylic acid and UV-B on gene expression and tropane alkaloid biosynthesis in hairy root cultures of Anisodus luridus. Plant Cell, Tissue Organ Cult 117:483–490

    Article  CAS  Google Scholar 

  • Qu J, Zhang W, Yu X (2011) A combination of elicitation and precursor feeding leads to increased anthocyanin synthesis in cell suspension cultures of Vitis vinifera. Plant Cell, Tissue Organ Cult 107:261–269

    Article  CAS  Google Scholar 

  • Ram M, Prasad KV, Singh SK, Hada BS, Kumar S (2013) Influence of salicylic acid and methyl jasmonate elicitation on anthocyanin production in callus cultures of Rosa hybrida L. Plant Cell, Tissue Organ Cult 113:459–467

    Article  CAS  Google Scholar 

  • Ramakrishna A, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6:1720–1731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Roat C, Ramawat KG (2009) Elicitor-induced accumulation of stilbenes in cell suspension cultures of Cayratia trifolia (L.) Domin. Plant Biotechnol Rep 3:135–138

    Article  Google Scholar 

  • San Miguel-Chavez R, Soto-Hernandez M, Ramos-Valdivia AC, Kite G (2007) Alkaloid production in elicited cell suspension cultures of Erythrina americana Miller. Phytochem Rev 6:167–173

    Article  CAS  Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signaling. Nature 459:1071–1078

    Article  CAS  PubMed  Google Scholar 

  • Saw NMMT, Riedel H, Cai Z, Kutuk O, Smetanska I (2012) Stimulation of anthocyanin synthesis in grape (Vitis vinifera) cell cultures by pulsed electric fields and ethephon. Plant Cell, Tissue Organ Cult 108:47–54

    Article  CAS  Google Scholar 

  • Senger RS, Phisalaphong M, Karim MN, Linden JC (2006) Development of a culture sub-population induction model: signaling pathways synergy and taxanes production by Taxus canadensis. Biotechnol Prog 22:1671–1682

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Shimizu Y, Maeda K, Kato M, Shimomura K (2010) Methyl jasmonate induces anthocyanin accumulation in Gynura bicolor cultured roots. In Vitro Cell Dev Biol-Plant 46:460–465

    Article  CAS  Google Scholar 

  • Shinde AN, Malpathak N, Fulzele DP (2009) Enhanced production of phytoestrogenic isoflavones from hairy root cultures of Psoralea corylifolia L. using elicitation and precursor feeding. Biotechnol Bioprocess Eng 14:288–294

    Article  CAS  Google Scholar 

  • Shyamkumar B, Anjaneyulu C, Giri CC (2007) Genetic transformation of Terminalia chebula Ritz. and detection of tannin in transformed tissue. Current Sci 92:361–367

    CAS  Google Scholar 

  • Silja PK, Gisha GP, Satheeshkumar K (2014) Enhanced plumbagin accumulation in embryogenic cell suspension cultures of Plumbago rosea L. following elicitation. Plant Cell, Tissue Organ Cult 119:469–477

    Article  CAS  Google Scholar 

  • Sivanandhan G, Rajesh M, Arun M, Jeyaraj M, Kapil Dev G, Arjunan A, Manickavasagam M, Muthuselvam M, Selvaraj N, Ganapathi A (2013) Effect of culture conditions, cytokinins, methyl jasmonate and salicylic acid on the biomass accumulation and production of withanolides in multiple shoot culture of Withania somnifera (L.) Dunal using liquid culture. Acta Physiol Plant 35:715–728

    Article  CAS  Google Scholar 

  • Soejarto DD, Gyllenhaal C, Kadushin MR, Southavong B, Sydara K, Bouamanivong S, Xaiveu M, Zhang HJ, Franzblau SG, Tan GT, Pezzuto JM, Riley MC, Elkington BG, Waller DP (2012) An ethnobotanical survey of medicinal plants of Laos toward the discovery of bioactive compounds as potential candidates for pharmaceutical development. Pharm Biol 50:42–60

    Article  CAS  PubMed  Google Scholar 

  • Song MC, Kim EJ, Kim E, Rathwell K, Nama SJ, Yoon YJ (2014) Microbial biosynthesis of medicinally important plant secondary metabolites. Nat Prod Rep 31:1497–1509

    Article  CAS  PubMed  Google Scholar 

  • Srivastava S, Srivastava AK (2007) Hairy root culture for mass-production of high-value secondary metabolites. Crit Rev Biotechnol 27:29–43

    Article  CAS  PubMed  Google Scholar 

  • Sykłowska-Baranek K, Pilarek M, Bonfill M, Kafel K, Pietrosiuk A (2015) Perfluorodecalin-supported system enhances taxane production in hairy root cultures of Taxus x media var. Hicksii carrying a taxadiene synthase transgene. Plant Cell, Tissue Organ Cult 120:1051–1059

    Article  CAS  Google Scholar 

  • Tewari RK, Lee SY, Hahn EJ, Paek KY (2007) Temporal changes in the growth, saponin content and antioxidant defense in the adventitious roots of Panax ginseng subjected to nitric oxide elicitation. Plant Biotechnol Rep 1:227–235

    Article  Google Scholar 

  • Thethewey RN (2004) Metabolite profiling as an aid to metabolic engineering in plants. Curr Opin Plant Biol 7:196–201

    Article  CAS  Google Scholar 

  • Touno K, Tamaoka J, Ohashi Y, Shimomura K (2005) Ethylene induced shikonin biosynthesis in shoot culture of Lithospermum erythrorhizon. Plant Physiol Biochem 43:101–105

    Article  CAS  PubMed  Google Scholar 

  • Trujillo-Villanueva K, Rubio-Pina J, Monforte-Gonzalez M, Ramírez-Benítez E, Vázquez-Flota F (2012) The sequential exposure to jasmonate, salicylic acid and yeast extract promotes sanguinarine accumulation in Argemone mexicana cell cultures. Biotechnol Lett 34:379–385

    Article  CAS  PubMed  Google Scholar 

  • Tůmová L, Tůma J, Megusar K, Dolezal M (2010) Substituted pyrazinecarboxamides as abiotic elicitors of flavolignan production in Silybum marianum (L.) gaertn cultures in vitro. Molecules 15:331–340

    Article  PubMed  CAS  Google Scholar 

  • Udomsuk L, Jarukamjorn K, Tanaka H, Putalun W (2011) Improved isoflavonoid production in Pueraria candollei hairy root cultures using elicitation. Biotechnol Lett 33:369–374

    Article  CAS  PubMed  Google Scholar 

  • Vanisree M, Tsay HS (2004) Plant cell cultures—an alternative and efficient source for the production of biologically important secondary metabolites. Int J App Sci Eng 1:29–48

    Google Scholar 

  • Vazquez-Flota F, Hernandez-Domınguez E, de Lourdes Miranda-Ham M, Monforte-González M (2009) A differential response to chemical elicitors in Catharanthus roseus in vitro cultures. Biotechnol Lett 31:591–595

    Article  CAS  PubMed  Google Scholar 

  • Verma P, Khan SA, Mathur AK, Ghosh S, Shanker K, Kalra A (2014) Improved sanguinarine production via biotic and abiotic elicitations and precursor feeding in cell suspensions of latex-less variety of Papaver somniferum with their gene expression studies and upscaling in bioreactor. Protoplasma 251:1359–1371

    Article  CAS  PubMed  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Ann Rev Phytopathol 47:177–206

    Article  CAS  Google Scholar 

  • Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JW, Zheng LP, Wu JY, Tan RX (2006) Involvement of nitric oxide in oxidative burst, phenylalanine ammonia-lyase activation and taxol production induced by low-energy ultrasound in Taxus yunnanensis cell suspension cultures. Nitric Oxide 15:351–358

    Article  CAS  PubMed  Google Scholar 

  • Wang JW, Zheng LP, Zhang B, Zou T (2009) Stimulation of artemisinin synthesis by combined cerebroside and nitric oxide elicitation in Artemisia annua hairy roots. Appl Microbiol Biotechnol 85:285–292

    Article  CAS  PubMed  Google Scholar 

  • Wang QJ, Zheng LP, Sima YH, Yuan HY, Wang JW (2013) Methyl jasmonate stimulates 20-hydroxyecdysone production in cell suspension cultures of Achyranthes bidentata. Plant Omics J 6:116–120

    Google Scholar 

  • Wang S, Guo LP, Xie T, Yang J, Tang JF, Li X, Wang X, Huang LQ (2014) Different secondary metabolic responses to MeJA treatment in shikonin proficient and shikonin-deficient cell lines from Arnebia euchroma (Royle) Johnst. Plant Cell, Tissue Organ Cult 119:587–598

    Article  CAS  Google Scholar 

  • Wasternack C (2014) Action of jasmonates in plant stress responses and development–applied aspects. Biotechnol Adv 32:31–39

    Article  CAS  PubMed  Google Scholar 

  • Wielanek M, Urbanek H (2006) Enhanced glucotropaeolin production in hairy root cultures of Tropaeolum majus L. by combining elicitation and precursor feeding. Plant Cell, Tissue Organ Cult 86:177–186

    Article  CAS  Google Scholar 

  • Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signaling in plants. Plant, Cell Environ 31:622–631

    Article  CAS  Google Scholar 

  • Wu CH, Murthy HN, Hahn EJ, Paek KY (2008) Establishment of adventitious root co-culture of Ginseng and Echinacea for the production of secondary metabolites. Acta Physiol Plant 30:891–896

    Article  CAS  Google Scholar 

  • Wungsintaweekul J, Choo-malee J, Charoonratana T, Keawpradub N (2012) Methyl jasmonate and yeast extract stimulate mitragynine production in Mitragyna speciosa (Roxb.) Korth. shoot culture. Biotechnol Lett 34:1945–1950

    Article  PubMed  Google Scholar 

  • Xiao WH, Cheng JS, Yuan YJ (2009) Spatial–temporal distribution of nitric oxide involved in regulation of phenylalanine ammonialyase activation and taxol production in immobilized Taxus cuspidata cells. J Biotechnol 139:222–228

    Article  CAS  PubMed  Google Scholar 

  • Xu MJ, Dong JF, Zhang G (2005) Enhancement of hypericin production and cell growth of Hypericum perforatum L. suspension cells by nitric oxide. Chin J Biotechnol 21:66–70

    Google Scholar 

  • Yoo SD, Cho Y, Sheen J (2009) Emerging connections in the ethylene signaling network. Trends Plant Sci 14:270–279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoo NH, Kim OT, Kim JB, Kim SH, Kim YC, Bang KH, Hyun DY, Cha SW, Kim MY, Hwang B (2011) Enhancement of centelloside production from cultured plants of Centella asiatica by combination of thidiazuron and methyl jasmonate. Plant Biotechnol Rep 5:283–287

    Article  Google Scholar 

  • Yousefzadi M, Sharifi M, Behmanesh M, Ghasempour A, Moyano E, Palazon J (2010) Salicylic acid improves podophyllotoxin production in cell cultures of Linum album by increasing the expression of genes related with its biosynthesis. Biotechnol Lett 32:1739–1743

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zaheer M, Giri CC (2015) Multiple shoot induction and jasmonic versus salicylic acid driven elicitation for enhanced andrographolide production in Andrographis paniculata. Plant Cell, Tissue Organ Cult 122:553–563

    Article  CAS  Google Scholar 

  • Zaheer M, Reddy VD, Giri CC (2016) Enhanced daidzin production from jasmonic and acetyl salicylic acid elicited hairy root cultures of Psoralea corylifolia L. (Fabaceae). Nat Prod Res. doi:10.1080/14786419.2015.1054823

    PubMed  Google Scholar 

  • Zaker A, Sykora C, Gossnitzer F, Abrishamchi P, Asili J, Mousavic SH, Wawrosch C (2015) Effects of some elicitors on tanshinone production in adventitious root cultures of Perovskia abrotanoides Karel. Ind Crops Prod 67:97–102

    Article  CAS  Google Scholar 

  • Zare N, Farjaminezhad R, Asghari-Zakaria R, Farjaminezhad M (2014) Enhanced thebaine production in Papaver bracteatum cell suspension culture by combination of elicitation and precursor feeding. Nat Prod Res 28:711–717

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Zheng SH, Fujita K, Sakai K (2004) Jasmonate and ethylene signalling and their interaction are integral parts of the elicitor-signalling pathway leading to β-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J Exp Bot 55:1003–1012

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 3:283–333

    Article  CAS  Google Scholar 

  • Zheng LP, Guo YT, Wang JW, Tan RX (2008) Nitric oxide potentiates oligosaccharide-induced artemisinin production in Artemisia annua hairy roots. J Integr Plant Biol 50:49–55

    Article  CAS  PubMed  Google Scholar 

  • Zhou LG, Wu JY (2006) Development and application of medicinal plant tissue cultures for production of drugs and herbal medicinals in China. Nat Prod Rep 23:789–810

    Article  CAS  PubMed  Google Scholar 

  • Zhou ML, Zhu XM, Shao JR, Wu YM, Tang YX (2010) Transcriptional response of the catharanthine biosynthesis pathway to methyl jasmonate/nitric oxide elicitation in Catharanthus roseus hairy root culture. Appl Biochem Biotechnol 88:737–750

    CAS  Google Scholar 

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Acknowledgments

Authors would like to thank sponsors University Grants Commission (UGC), Department of Science and Technology (DST), New Delhi OU-DST-PURSE Project and thank OU-UGC-CPEPA Programme UGC, New Delhi for financial support. Mr. Mohd Zaheer thanks UGC and DST, New Delhi for the Research Fellowships.

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  1. Centre for Plant Molecular Biology (CPMB), Osmania University, Hyderabad, Telangana, 500007, India

    Charu Chandra Giri & Mohd Zaheer

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Giri, C.C., Zaheer, M. 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 Organ Cult 126, 1–18 (2016). https://doi.org/10.1007/s11240-016-0985-6

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