Abstract
Elicitation, the process of stimulating plants to enhance the production of valuable secondary metabolites, has emerged as a significant avenue in the field of plant biotechnology. This review paper provides a comprehensive examination of elicitation, encompassing its mechanisms, the imperative for its utilization, and the diverse array of elicitors employed, including abiotic, biotic, and nanoparticle-based agents. By exploring the intricate signaling pathways and molecular responses triggered by external stimuli in this review, we gain insights into how plants tailor their metabolite production in reaction to their environment. Intricately intertwined with the mechanisms, the types of elicitors utilized are extensively discussed. Abiotic elicitors, encompassing physical factors and chemicals, biotic elicitors involving microbe-derived molecules, plant hormones and symbiotic microorganisms, and the emerging application of nanoparticles as elicitation agents are explored. The review further examines the application of these elicitors in both in-vitro and in-vivo cultures, showcasing their practical utility in controlled laboratory settings and real-world environments. By assessing the efficacy of diverse elicitors, this paper provides valuable insights into tailoring elicitation strategies to enhance secondary metabolite yields for various applications. Addressing the limitations and leveraging emerging technologies will undoubtedly steer elicitation research towards innovative breakthroughs, further enhancing our capacity to harness plants for sustainable and efficient secondary metabolite production.
Similar content being viewed by others
References
Abbasi BH, Stiles AR, Saxena PK, Liu CZ (2012) Gibberellic acid increases secondary metabolite production in Echinacea purpurea hairy roots. Appl Biochem Biotechnol 168:2057–2066
Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant growth-promoting rhizobacterium allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929
Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacterium: Current perspective. J King Saud Univ Sci 26:1–20
Ahmad I, Younas Z, Mashwani ZUR, Raja NI, Akram A (2023) Phytomediated selenium nanoparticles improved physio-morphological, antioxidant, and oil bioactive compounds of sesame under induced biotic stress. ACS Omega 8(3):3354–3366
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 2009:317–322
Akhgari A, Laakso I, Maaheimo H, Choi YH, Seppänen-Laakso T, Oksman-Caldentey KM, Rischer H (2019) Methyljasmonate elicitation increases terpenoid indole alkaloid accumulation in Rhazya stricta hairy root cultures. Plants 8(12):534
Akhzari D, Attaeian B, Arami A, Mahmoodi F, Aslani F (2015) Effects of vermicompost and arbuscular mycorrhizal fungi on soil properties and growth of Medicago polymorpha L. Compost Sci Utilization 23:142–153
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(44):11080–11087
Ali A, Mohammad S, Khan MA, Raja NI, Arif M, Kamil A, Mashwani ZUR (2019) Silver nanoparticles elicited in vitro callus cultures for accumulation of biomass and secondary metabolites in Caralluma tuberculata. Artif Cells Nanomed Biotechnol 47(1):715–724
Aliniaeifard S, Shomali A, Seifikalhor M, Lastochkina O (2020) Calcium signaling in plants under drought. In: Hasanuzzaman M, Tanveer M (eds) Salt and drought stress tolerance in plants: signaling networks and adaptive mechanisms. Springer, Cham, pp 259–298
Al-Oubaidi HKM, Kasid NM (2015) Increasing phenolic and flavonoids compounds of Cicer arietinum L. from embryo explant using titanium dioxide nanoparticle in vitro. World J Pharm Res 4(11):1791–1799
Amer A (2019) Biotechnology approaches for in vitro production of flavonoids. J Microbiol Biotechnol Food Sci 2019:457–468
Anand U, Jacobo-Herrera N, Altemimi A, Lakhssassi N (2019) A comprehensive review on medicinal plants as antimicrobial therapeutics: potential avenues of biocompatible drug discovery. Metabolites 9(11):258
Angelova Z, Georgiev S, Roos W (2006) Elicitation of plants. Biotechnol Biotechnol Equip 20(2):72–83
Anjum S, Anjum I, Hano C, Kousar S (2019) Advances in nanomaterials as novel elicitors of pharmacologically active plant specialized metabolites: current status and future outlooks. RSC Adv 9(69):40404–40423
Asadollahei MV, Tabatabaeian J, Yousefifard M, Mahdavi SME, Nekonam MS (2023) Impact of elicitors on essential oil compositions and phytochemical constituents in Lavandula stoechas L. Plant Physiol Biochem 194:722–730
Aslam S, Gul N, Mir MA, Asgher M, Al-Sulami N, Abulfaraj AA, Qari S (2021) Role of jasmonates, calcium, and glutathione in plants to combat abiotic stresses through precise signaling cascade. Front Plant Sci 12:668029
Back K, Tan DX, Reiter RJ (2016) Melatonin biosynthesis in plants: multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J Pineal Res 61(4):426–437
Baenas N, García-Viguera C, Moreno DA (2014) Biotic elicitors effectively increase the glucosinolates content in Brassicaceae sprouts. J Agric Food Chem 62(8):1881–1918
Bajwa MN, Bibi A, Idrees MZ, Zaman G, Farooq U, Bhatti TT (2021) Elicitation, a mechanistic approach to change the metabolic pathway of plants to produce pharmacological important compounds in in-vitro cell cultures. Glob J Eng 8:10
Baskar V, Nayeem S, Kuppuraj SP, Muthu T, Ramalingam S (2018) Assessment of the effects of metal oxide nanoparticles on the growth, physiology and metabolic responses in in vitro grown eggplant (Solanum melongena). 3 Biotech 8:1–12
Begum P, Fugetsu B (2012) Phytotoxicity of multi-walled carbon nanotubes on red spinach (Amaranthus tricolor L) and the role of ascorbic acid as an antioxidant. J Hazard Mater 243:212–222
Bhaskar R, Xavier LSE, Udayakumaran G, Kumar DS, Venkatesh R, Nagella P (2022) Biotic elicitors: a boon for the in-vitro production of plant secondary metabolites. Plant Cell Tiss Organ Cult 149(1–2):7–24
Bhat AH, Sharma H (2020) Medicinal plants: a potent source of diuretics. In: Singh A, Singh P, Bithel N (eds) Advanced pharmacological uses of medicinal plants and natural products. IGI Global, Hershey, p 67
Boots AW, Haenen GR, Bast A (2008) Health effects of quercetin: from antioxidant to nutraceutical. Eur J Pharmacol 585(2–3):325–337
Bosmaia TC, Agarwal P, Dangariya M, Khedia J, Gangapur DR, Agarwal PK (2023) Transcriptomic analysis towards identification of defence-responsive genes and pathways upon application of Sargassum seaweed extract on tomato plants infected with Macrophomina phaseolina. 3 Biotech 13(6):179
Campobenedetto C, Agliassa C, Mannino G, Vigliante I, Contartese V, Secchi F, Bertea CM (2021) A biostimulant based on seaweed (Ascophyllum nodosum and Laminaria digitata) and yeast extracts mitigates water stress effects on tomato (Solanum lycopersicum L.). Agriculture 11(6):557
Chambard M, Ben Mlouka MA, Jing L, Plasson C, Cosette P, Leprince J, Boulogne I (2022) Elicitation of roots and AC-DC with PEP-13 peptide shows differential defense responses in multi-omics. Cells 11(16):2605
Chamkhi I, Benali T, Aanniz T, El Menyiy N, Guaouguaou FE, El Omari N, Bouyahya A (2021) Plant-microbial interaction: the mechanism and the application of microbial elicitor induced secondary metabolites biosynthesis in medicinal plants. Plant Physiol Biochem 167:269–295
Chan LK, Koay SS, Boey PL, Bhatt A (2010) Effects of abiotic stress on biomass and anthocyanin production in cell cultures of Melastoma malabathricum. Biol Res 43(1):127–135
Chen X, Ding Y, Yang Y, Song C, Wang B, Yang S, Gong Z (2021) Protein kinases in plant responses to drought, salt, and cold stress. J Integr Plant Biol 63(1):53–78
Chen H, Chen J, Qi Y, Chu S, Ma Y, Xu L, Liang Z (2022) Endophytic fungus Cladosporium tenuissimum DF11, an efficient inducer of tanshinone biosynthesis in Salvia miltiorrhiza roots. Phytochemistry 194:113021
Chomel M, Guittonny-Larchevêque M, Fernandez C, Gallet C, DesRochers A, Paré D, Baldy V (2016) Plant secondary metabolites: a key driver of litter decomposition and soil nutrient cycling. J Ecol 104(6):1527–1541
Chung IM, Rajakumar G, Subramanian U, Venkidasamy B, Thiruvengadam M (2019) Impact of copper oxide nanoparticles on enhancement of bioactive compounds using cell suspension cultures of Gymnema sylvestre (Retz) R Br. Appl Sci 9(10):2165
Coleman AD, Maroschek J, Raasch L, Takken FL, Ranf S, Hückelhoven R (2021) The Arabidopsis leucine-rich repeat receptor-like kinase MIK2 is a crucial component of early immune responses to a fungal-derived elicitor. New Phytol 229(6):3453–3466
Cope KR, Prates ET, Miller JI, Demerdash ON, Shah M, Kainer D, Kalluri UC (2023) Exploring the role of plant lysin motif receptor-like kinases in regulating plant-microbe interactions in the bioenergy crop Populus. Comput Struct Biotechnol J 21:1122–1139
Cuéllar-Torres EA, Aguilera-Aguirre S, Hernández-Oñate MÁ, López-García UM, Vega-Arreguín J, Montalvo-González E, Chacón-López A (2023) Molecular aspects revealed by omics technologies related to the defense system activation in fruits in response to elicitors: a review. Horticulturae 9(5):558
Dheeranupattana S, Wangprapa M, Jatisatienr A (2007) Effect of sodium acetate on stevioside production of Stevia rebaudiana. Acta Hortic. https://doi.org/10.17660/ActaHortic.2008.786.31
Ebadollahi R, Jafarirad S, Kosari-Nasab M, Mahjouri S (2019) Effect of explant source, perlite nanoparticles and TiO2/perlite nanocomposites on phytochemical composition of metabolites in callus cultures of Hypericum perforatum. Sci Rep 9(1):12998
El-Saber MM, Diab M, Hendawey M, Farroh K (2021) Magnetite nanoparticles different sizes effectiveness on growth and secondary metabolites in Ginkgo biloba L. callus. Egypt J Chem 64(9):4523–5432
Ferrusquía-Jiménez NI, González-Arias B, Rosales A, Esquivel K, Escamilla-Silva EM, Ortega-Torres AE, Guevara-González RG (2022) Elicitation of bacillus cereus-amazcala (Bc-A) with SiO2 nanoparticles improves its role as a plant growth-promoting bacteria (PGPB) in Chili pepper plants. Plants 11(24):3445
Fróna D, Szenderák J, Harangi-Rákos M (2021) Economic effects of climate change on global agricultural production. Nat Conserv 44:117–139
Gadzovska Simic S, Tusevski O, Maury S, Delaunay A, Joseph C, Hagège D (2014) Effects of polysaccharide elicitors on secondary metabolite production and antioxidant response in Hypericum perforatum L. shoot cultures. Sci World J 2014:10
Garcia-Caparros P, De Filippis L, Gul A, Hasanuzzaman M, Ozturk M, Altay V, Lao MT (2021) Oxidative stress and antioxidant metabolism under adverse environmental conditions: a review. Bot Rev 87:421–466
García-García AL, Matos AR, Feijão E, Cruz de Carvalho R, Boto A, Marques da Silva J, Jiménez-Arias D (2023) The use of chitosan oligosaccharide to improve artemisinin yield in well-watered and drought-stressed plants. Front Plant Sci 14:1200898
Garcia-Mier L et al (2019) Strategies that influence the production of secondary metabolites in plants. In: Jaiwal P, Chhillar A, Chaudhary D, Jaiwal R (eds) Nutritional quality improvement in plants: concepts and strategies in plant sciences. Springer, Cham
Gohari G, Mohammadi A, Akbari A, Panahirad S, Dadpour MR, Foto-poulos V, Kimura S (2020) Titanium dioxide nanoparticles (TiO2 NPs) promote growth and ameliorate salinity stress efects on essential oil profle and biochemical attributes of Dracocepha-lum moldavica. Sci Rep 10(1):1–14
Gómez-Merino FC, Trejo-Téllez LI (2018) The role of beneficial elements in triggering adaptive responses to environmental stressors and improving plant performance. In: Vats S (ed) Biotic and abiotic stress tolerance in plants. Springer, Singapore, pp 137–172
Goossens A, Häkkinen ST, Laakso I, Seppänen-Laakso T, Biondi S, De Sutter V, Oksman-Caldentey KM (2003) A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc Natl Acad Sci 100(14):8595–8600
Grover JK, Yadav SP (2004) Pharmacological actions and potential uses of Momordica charantia: a review. J Ethnopharmacol 93(1):123–132
Gupta S, Chaturvedi P (2019) Enhancing secondary metabolite production in medicinal plants using endophytic elicitors: a case study of Centella asiatica (Apiaceae) and asiaticoside. In: Hodkinson TR, Doohan FM, Saunders MJ, Murphy BR (eds) Endophytes for a growing world. Cambridge University Press, Cambridge, pp 310–323
Gupta P, Sharma S, Saxena S (2015) Biomass yield and steviol glycoside production in callus and suspension culture of Stevia rebaudiana treated with proline and polyethylene glycol. Appl Biochem Biotechnol 176:863–874
Guru A, Dwivedi P, Kaur P, Pandey DK (2022) Exploring the role of elicitors in enhancing medicinal values of plants under in vitro condition. S Afr J Bot 149:1029–1043
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(12):880–895
Hassanen SA, Hegazi GA, Diab MI, Mahdi AA, Hendawey MH, Farroh KY (2021) Effect of coumarin and phenylalanine conjugated with chitosan nanoparticles on secondary metabolites synthesis in callus of Silybium marianum. Plant Cell Biotechnol Mol Biol 22(71):112–130
Hidangmayum A, Dwivedi P, Katiyar D, Hemantaranjan A (2019) Application of chitosan on plant responses with special reference to abiotic stress. Physiol Mol Biol Plants 25:313–326
Humbal A, Pathak B (2023) Influence of exogenous elicitors on the production of secondary metabolite in plants: a review (“VSI: secondary metabolites”). Plant Stress 8:100166
Hussain MS, Fareed S, Ansari S, Rahman MA, Ahmad IZ, Saeed M (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 4(1):10
Hussain F, Hadi F, Akbar F (2019) Magnesium oxide nanoparticles and thidiazuron enhance lead phytoaccumulation and antioxidative response in Raphanus sativus L. Environ Sci Pollut Res 26:30333–30347
Iqbal Z, Iqbal MS, Hashem A, Abd-Allah EF, Ansari MI (2021) Plant defense responses to biotic stress and its interplay with fluctuating dark/light conditions. Front Plant Sci 12:631810
Isah T (2019) Stress and defense responses in plant secondary metabolites production. Biol Res. https://doi.org/10.1186/s40659-019-0246-3
Islek C, Ustun AS, Koc ESRA (2014) The effects of cellulase on capsaicin production in freely suspended cells and immobilized cell cultures of Capsicum annuum L. Pak J Bot 46(5):1883–1887
Jain C, Khatana S, Vijayvergia R (2019) Bioactivity of secondary metabolites of various plants: a review. Int J Pharm Sci Res 10(2):494–504
Jalal A, da Silva Oliveira CE, Galindo FS, Rosa PAL, Gato IMB, de Lima BH, Teixeira Filho MCM (2023) Regulatory mechanisms of plant growth-promoting rhizobacteria and plant nutrition against abiotic stresses in brassicaceae family. Life 13(1):211
Jaleel CA, Manivannan P, Sankar B, Kishorekumar A, Gopi R, Somasundaram R, Panneerselvam R (2007) Pseudomonas fluorescens enhances biomass yield and ajmalicine production in Catharanthus roseus under water deficit stress. Colloids Surf B 60(1):7–11
Jaleel CA, Gopi R, Gomathinayagam M, Panneerselvam R (2009) Traditional and non-traditional plant growth regulators alters phytochemical constituents in Catharanthus roseus. Process Biochem 44(2):205–209
Jan R, Asaf S, Numan M, Kim KM (2021) Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy 11(5):968
Jiang J, Ling WF, Wei HW (2005) Evidences for involvement of endogenous cAMP in Arabidopsis defense responses to Verticillium toxins. Cell Res 15(8):585–592
Jiao J, Gai QY, Wang X, Qin QP, Wang ZY, Liu J, Fu YJ (2018) Chitosan elicitation of Isatis tinctoria L. hairy root cultures for enhancing flavonoid productivity and gene expression and related antioxidant activity. Ind Crops Prod 124:28–35
Jimenez-Garcia SN, Vazquez-Cruz MA, Guevara-Gonzalez RG, Torres-Pacheco I, Cruz-Hernandez A, Feregrino-Perez AA (2013) Current approaches for enhanced expression of secondary metabolites as bioactive compounds in plants for agronomic and human health purposes—a review. Pol J Food Nutr Sci 63(2):67
Jogawat A, Yadav B, Lakra N, Singh AK, Narayan OP (2021) Crosstalk between phytohormones and secondary metabolites in the drought stress tolerance of crop plants: a review. Physiol Plant 172(2):1106–1132
Jurić S, Sopko Stracenski K, Król-Kilińska Ż, Žutić I, Uher SF, Đermić E, Vinceković M (2020) The enhancement of plant secondary metabolites content in Lactuca sativa L. by encapsulated bioactive agents. Sci Rep 10(1):1–12
Kabiri R, Naghizadeh M, Hatami A (2016) Protective role of arginine against oxidative damage induced by osmotic stress in ajwain (Trachyspermum ammi) seedlings under hydroponic culture. J Plant Physiol Breed 6(1):13–22
Kandoudi W, Nemeth-Zamborine E (2022) Stimulating secondary compound accumulation by elicitation: is it a realistic tool in medicinal plants in vivo? Phytochem Rev 21:1–19
Kandoudi W, Radácsi P, Gosztola B, Zámboriné Németh É (2022) Elicitation of medicinal plants in vivo—is it a realistic tool? The effect of methyl jasmonate and salicylic acid on lamiaceae species. Horticulturae 8(1):5
Kang SM, Min JY, Kim YD, Kang YM, Park DJ, Jung HN, Choi MS (2006) Effects of methyl jasmonate and salicylic acid on the production of bilobalide and ginkgolides in cell cultures of Ginkgo biloba. In Vitro Cell Dev Biol Plant 42:44–49
Kanthaliya B, Joshi A, Arora J, Alqahtani MD, Abd-Allah EF (2023) Effect of biotic elicitors on the growth, antioxidant activity and metabolites accumulation in in vitro propagated shoots of Pueraria tuberosa. Plants 12(6):1300
Karpiński TM (2020) Essential oils of Lamiaceae family plants as antifungals. Biomolecules 10(1):103
Kaur H, Kaur H, Kaur H, Srivastava S (2022a) The beneficial roles of trace and ultratrace elements in plants. Plant Growth Regul 2022:1–18
Kaur S, Tiwari V, Kumari A, Chaudhary E, Sharma A, Ali U, Garg M (2022b) Protective and defensive role of anthocyanins under plant abiotic and biotic stresses: an emerging application in sustainable agriculture. J Biotechnol 361:12
Keshavan B, Srinivas NS, Tamizh MM, Vairamani M, Pachaiappan R (2022) In vitro elicitation of Camptothecin by challenging with biotic elicitors in Nothapodytes nimmoniana (J. Graham) Mabb. S Afr J Bot 144:325–331
Khan AK, Kousar S, Tungmunnithum D, Hano C, Abbasi BH, Anjum S (2021) Nano-elicitation as an effective and emerging strategy for in vitro production of industrially important flavonoids. Appl Sci 11(4):1694
Khezerluo M, Hosseini B, Amiri J (2018) Sodium nitroprusside stimulated production of tropane alkaloids and antioxidant enzymes activity in hairy root culture of Hyoscyamus reticulatus L. Acta Biol Hung 69(4):437–448
Kim HJ, Chen F, Wang X, Rajapakse NC (2006) Effect of methyl jasmonate on secondary metabolites of sweet basil (Ocimum basilicum L.). J Agric Food Chem 54(6):2327–2332
Knez M, Ranic M, Gurinovic M, Glibetic M, Savic J, Mattas K, Yercan M (2023) Causes and conditions for reduced cultivation and consumption of underutilized crops: is there a solution? Sustainability 15(4):3076
Kochan E, Balcerczak E, Lipert A, Szymańska G, Szymczyk P (2018) Methyl jasmonate as a control factor of the synthase squalene gene promoter and ginsenoside production in American ginseng hairy root cultured in shake flasks and a nutrient sprinkle bioreactor. Ind Crops Prod 115:182–193
Kolenčík M, Ernst D, Urík M, Ďurišová Ľ, Bujdoš M, Šebesta M, Kratošová G (2020) Foliar application of low concentrations of titanium dioxide and zinc oxide nanoparticles to the common sunflower under field conditions. Nanomaterials 10(8):1619
Komaraiah P, Ramakrishna SV, Reddanna P, Kishor PK (2003) Enhanced production of plumbagin in immobilized cells of Plumbago rosea by elicitation and in situ adsorption. J Biotechnol 101(2):181–187
Koza NA, Adedayo AA, Babalola OO, Kappo AP (2022) Microorganisms in plant growth and development: roles in abiotic stress tolerance and secondary metabolites secretion. Microorganisms 10(8):1528
Kruszka D, Sawikowska A, Selvakesavan RK, Krajewski P, Kachlicki P, Franklin G (2020) Silver nanoparticles affect phenolic and phytoalexin composition of Arabidopsis thaliana. Sci Total Environ 716:135361
Kruszka D, Selvakesavan RK, Kachlicki P, Franklin G (2022) Untargeted metabolomics analysis reveals the elicitation of important secondary metabolites upon treatment with various metal and metal oxide nanoparticles in Hypericum perforatum L. cell suspension cultures. Ind Crops Prod 178:114561
Kumari S, Chhillar H, Chopra P, Khanna RR, Khan MIR (2021) Potassium: A track to develop salinity tolerant plants. Plant Physiol Biochem 167:1011–1023
Kuzel S, Vydra JAN, Triska JAN, Vrchotova N, Hruby M, Cigler P (2009) Elicitation of pharmacologically active substances in an intact medical plant. J Agric Food Chem 57(17):7907–7911
Largia MJV, Shilpha J, Satish L, Swamy MK, Ramesh M (2023) Elicitation: an efficient strategy for enriched production of plant secondary metabolites. Phytochemical genomics: plant metabolomics and medicinal plant genomics. Springer, Cham, pp 477–497
Le KC, Im WT, Paek KY, Park SY (2018) Biotic elicitation of ginsenoside metabolism of mutant adventitious root culture in Panax ginseng. Appl Microbiol Biotechnol 102:1687–1697
Lei Z, Mingyu S, Chao L, Liang C, Hao H, Xiao W, Xiaoqing L, Fan Y, Fengqing G, Fashui H (2007) Efects of nanoanatase TiO 2 on photosynthesis of spinach chloroplasts under diferent light illumination. Biol Trace Elem Res 119(1):68–76
Li B, Wang B, Li H, Peng L, Ru M, Liang Z, 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
Linh TM, Mai NC, Hoe PT, Ngoc NT, Thao PTH, Ban NK, Van NT (2021) Development of a cell suspension culture system for promoting alkaloid and vinca alkaloid biosynthesis using endophytic fungi isolated from local Catharanthus roseus. Plants 10(4):672
Liu CZ, Guo C, Wang YC, Ouyang F (2002) Effect of light irradiation on hairy root growth and artemisinin biosynthesis of Artemisia annua L. Process Biochem 38(4):581–585
López-Vargas ER, Ortega-Ortíz H, Cadenas-Pliego G, de Alba Romenus K, Cabrera de la Fuente M, Benavides-Mendoza A, Juárez-Maldonado A (2018) Foliar application of copper nanoparticles increases the fruit quality and the content of bioactive compounds in tomatoes. Appl Sci 8(7):1020
Mahfouz SA, Shamf-Eldin MA (2007) Effect of mineral vs. biofertilizer on growth, yield, and essential oil content of fennel (Foeniculum vulgare Mill.). Int Agrophys 21:361–366. https://doi.org/10.1055/s-2007-987419
Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Gene 26(4):403–410
Marchev AS, Yordanova ZP, Georgiev MI (2020) Green (cell) factories for advanced production of plant secondary metabolites. Crit Rev Biotechnol 40(4):443–458
Memelink J, Kijne JW, van der Heijden R, Verpoorte R (2001) Genetic modification of plant secondary metabolite pathways using transcriptional regulators. Plant Cells. https://doi.org/10.1007/3-540-45302-4_4
Mishra UN, Saha D, Chauhan J, Kumar V, Jatav HS, Lal D, Chandra K (2022) Emerging roles of osmoprotectants in response to multiple abiotic stress tolerance in plants. In: Aftab T (ed) Omics analysis of plants under abiotic stress. Apple Academic Press, Boca Raton, pp 179–206
Mithöfer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566(1–3):1–5
Moharrami F, Hosseini B, Sharafi A, Farjaminezhad M (2017) Enhanced production of hyoscyamine and scopolamine from genetically transformed root culture of Hyoscyamus reticulatus L. elicited by iron oxide nanoparticles. In Vitro Cell Dev Biol Plant 53:104–111
Morteza E, Moaveni P, Farahani HA, Kiyani M (2013) Study of photosynthetic pigments changes of maize (Zea mays L.) under nano TiO2 spraying at various growth stages. Springerplus 2(1):1–5
Mostofa MG, Rahman MM, Ghosh TK, Kabir AH, Abdelrahman M, Khan MAR, Tran LSP (2022) Potassium in plant physiological adaptation to abiotic stresses. Plant Physiol Biochem. https://doi.org/10.1016/j.plaphy.2022.07.011
Mun BG, Lee WH, Kang SM, Lee SU, Lee SM, Lee DY, Lee IJ (2020) Streptomyces sp. LH 4 promotes plant growth and resistance against Sclerotinia sclerotiorum in cucumber via modulation of enzymatic and defense pathways. Plant Soil 448:87–103
Murugaragavan Ramasamy TG, Yuvaraj M (2020) Role of biofertilizers in plant growth and soil health. In: Rigobelo EC, Serra AP (eds) Nitrogen fixation. IntechOpen, London, p 1
Naik PM, Al-Khayri JM (2016) Impact of abiotic elicitors on in vitro production of plant secondary metabolites: a review. J Adv Res Biotechnol 1(2):1–7
Nair PMG, Chung IM (2014) Impact of copper oxide nanoparticles exposure on Arabidopsis thaliana growth, root system development, root lignificaion, and molecular level changes. Environ Sci Pollut Res 21:12709–12722
Narayani M, Srivastava S (2017) Elicitation: a stimulation of stress in in vitro plant cell/tissue cultures for enhancement of secondary metabolite production. Phytochem Rev 16:1227–1252
Nourozi E, Hosseini B, Maleki R, Abdollahi Mandoulakani B (2019) Iron oxide nanoparticles: a novel elicitor to enhance anticancer flavonoid production and gene expression in Dracocephalum kotschyi hairy-root cultures. J Sci Food Agric 99(14):6418–6430
Nourozi E, Hosseini B, Maleki R, Mandoulakani BA (2021) Inductive effect of titanium dioxide nanoparticles on the anticancer compounds production and expression of rosmarinic acid biosynthesis genes in Dracocephalum kotschyi transformed roots. Plant Physiol Biochem 167:934–945
Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10(2):79–87
Pande D, Iqbal M, Srivastava PS (2000) Effect of ZnSO4 and CuSO4 on regeneration and lepidine content in Lepidium sativum L. Biol Plant 43:253–256
Paramo LA, Feregrino-Pérez AA, Guevara R, Mendoza S, Esquivel K (2020) Nanoparticles in agroindustry: applications, toxicity, challenges, and trends. Nanomaterials 10(9):1654
Patil JG, Ahire ML, Nitnaware KM, Panda S, Bhatt VP, Kishor PBK, 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
Pu X, Gao HC, Wang MJ, Zhang JH, Shan JH, Chen MH, Huang QM (2022) Integrative analysis of elicitor-induced camptothecin biosynthesis in Camptotheca acuminata plantlets through a combined omics approach. Front Plant Sci 13:851077
Radman R, Saez T, Bucke C, Keshavarz T (2003) Elicitation of plants and microbial cell systems. Biotechnol Appl Biochem 37(1):91–102
Rafiee H, Naghdi Badi HA, Mehrafarin A, Qaderi A, Zarinpanjeh N, Sękara A, Zand E (2016) Application of plant biostimulants as new approach to improve the biological responses of medicinal plants—a critical review. J Med Plants 15(59):6–39
Rai A, Sanjeev K, Kuldeep B, Nandita S, Rana PS (2017) Improvement in growth and alkaloid content of Rauwolfia serpentina on application of organic matrix entrapped biofertilizers (Azotobacter chroococcum, Azospirillum brasilense and Pseudomonas putida). J Plant Nutr 41:1–11
Rajput VD, Singh RK, Verma KK, Sharma L, Quiroz-Figueroa FR, Meena M, Mandzhieva S (2021) Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress. Biology 10(4):267
Ramadan T, Sayed SA, Abd-Elaal AK, Amro A (2022) The combined efect of water defcit stress and TiO2 nanoparticles on cell membrane and antioxidant enzymes in Helianthus annuus L. Physiol Mol Biol Plants 28(2):391–409
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(2):182
Rastogi R, Saxena M, Chaturvedi DK, Gupta M, Jain P, Jain R, Garg P (2022) Indian science of Yajna and Mantra to cure different diseases: an analysis amidst pandemic with a simulated approach. Bioinformatics and medical applications: big data using deep learning algorithms. Wiley, Hoboken, pp 235–267
Sachdev S, Ansari SA, Ansari MI (2023) ROS as signaling molecule under unfavorable conditions. Reactive oxygen species in plants: the right balance. Springer Nature Singapore, Singapore, pp 203–222
Salam U, Ullah S, Tang ZH, Elateeq AA, Khan Y, Khan J, Ali S (2023) Plant metabolomics: an overview of the role of primary and secondary metabolites against different environmental stress factors. Life 13(3):706
Salehi M, Moieni A, Safaie N, Farhadi S (2020) Whole fungal elicitors boost paclitaxel biosynthesis induction in Corylus avellana cell culture. PLoS ONE 15(7):e0236191
Sardar T, Maqbool M, Ishtiaq M, Mazhar MW, El-Sheikh MA, Casini R, Elansary HO (2023) Synergistic influence of yeast extract and calcium oxide nanoparticles on the synthesis of bioactive antioxidants and metabolites in Swertia chirata in vitro callus cultures. Molecules 28(12):4607
Sato F, Hashimoto T, Hachiya A, Tamura KI, Choi KB, Morishige T, Yamada Y (2001) Metabolic engineering of plant alkaloid biosynthesis. Proc Natl Acad Sci 98(1):367–372
Savitha BC, Thimmaraju R, Bhagyalakshmi N, Ravishankar GA (2006) Different biotic and abiotic elicitors influence betalain production in hairy root cultures of Beta vulgaris in shake-flask and bioreactor. Process Biochem 41(1):50–60
Saxena P, Ahlawat S, Ali A, Khan S, Abdin MZ (2017) Gene expression analysis of the withanolide biosynthetic pathway in hairy root cultures of Withania somnifera elicited with methyl jasmonate and the fungus Piriformospora indica. Symbiosis 71:143–154
Shaikh S, Shriram V, Khare T, Kumar V (2020) Biotic elicitors enhance diosgenin production in Helicteres isora L. suspension cultures via up-regulation of CAS and HMGR genes. Physiol Mol Biol Plants 26:593–604
Shameer S, Prasad TNVKV (2018) Plant growth promoting rhizobacterium for sustainable agricultural practices with special reference to biotic and abiotic stresses. Plant Growth Regul 84(3):603–615
Sharma M, Bhardwaj R, Saran M, Prajapat RK, Sharma D, Mathur M (2023) Secondary metabolites and bioprospecting. Plant growth promoting microorganisms of arid region. Springer Nature Singapore, Singapore, pp 229–255
Shenavaie Zare A, Ganjeali A, Vaezi Kakhki MR, Cheniany M, Mashreghi M (2022) Plant elicitation and TiO2 nanoparticles application as an effective strategy for improving the growth, biochemical properties, and essential oil of peppermint. Physiol Mol Biol Plants 10:1–16
Sheng S, Wu C, Xiang Y, Pu W, Duan S, Huang P, Liu L (2022) Polyamine: a potent ameliorator for plant growth response and adaption to abiotic stresses particularly the ammonium stress antagonized by urea. Front Plant Sci 13:104
Shibata S (2000) A drug over the millennia: pharmacognosy, chemistry, and pharmacology of licorice. Yakugaku Zasshi 120(10):849–862
Singh A, Singh N, Hussain I, Singh H, Yadav V, Singh S (2016) Green synthesis of nano zinc oxide and evaluation of its impact on germination and metabolic activity of Solanum lycopersicum. J Bio-Technol 233:84–94
Singh R, Parihar P, Singh M, Bajguz A, Kumar J, Singh S, Prasad SM (2017) Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospects. Front Microbiol 8:515
Sivanandhan G, Kapil Dev G, Jeyaraj M, Rajesh M, Arjunan A, Muthuselvam M, 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 Organ Cult 114:121–129
Smokvarska M (2020) Role of Rho GTP-ase nanodomains in regulation of plant’s cell signalization. Université Montpellier, Montpellier
Sofowora A, Ogunbodede E, Onayade A (2013) The role and place of medicinal plants in the strategies for disease prevention. Afr J Tradit Complement Altern Med 10(5):210–229
Song X, Wu H, Yin Z, Lian M, Yin C (2017) Endophytic bacteria isolated from Panax ginseng improves ginsenoside accumulation in adventitious ginseng root culture. Molecules 22(6):837
Souri MK (2016) Aminochelate fertilizers: the new approach to the old problem; a review. Open Agric 1(1):118–123
Srivastava M, Sharma S, Misra P (2016) Elicitation based enhancement of secondary metabolites in Rauwolfia serpentina and Solanum khasianum hairy root cultures. Pharmacogn Mag 12(Suppl 3):S315
Sumbul A, Ansari RA, Rizvi R, Mahmood I (2020) Azotobacter: a potential bio-fertilizer for soil and plant health management. Saudi J Biol Sci 27(12):3634–3640
Süntar I (2020) Importance of ethnopharmacological studies in drug discovery: role of medicinal plants. Phytochem Rev 19(5):1199–1209
Taghizadeh M, Nasibi F, Kalantari KM, Ghanati F (2019) Evaluation of secondary metabolites and antioxidant activity in Dracocephalum polychaetum Bornm. cell suspension culture under magnetite nanoparticles and static magnetic field elicitation. Plant Cell Tiss Organ Cult 136:489–498
Tardast Z, Iranbakhsh A, Ebadi M, Ardebili ZO (2023) Carboxylic acid-functionalized multiwalled carbon nanotubes (COOH-MWCNTs) improved production of atropine in callus of Datura inoxia by influencing metabolism, gene regulation, and DNA cytosine methylation; an in vitro biological assessment. Plant Physiol Biochem 2021:107975
Taurino M, Ingrosso I, D’amico L, De Domenico S, Nicoletti I, Corradini D, Giovinazzo G (2015) Jasmonates elicit different sets of stilbenes in Vitis vinifera cv. Negramaro cell cultures. Springerplus 4(1):1–11
Tripathi D, Raikhy G, Kumar D (2019) Chemical elicitors of systemic acquired resistance—Salicylic acid and its functional analogs. Curr Plant Biol 17:48–59
Tumova L, Poustkova J, Tuma J (2001) CoCl2 and NiCl2 elicitation and flavonoid production in Ononis arvensis L. culture in vitro. Acta Pharm (zagreb) 51(2):159–162
Tunsagool P, Wang X, Leelasuphakul W, Jutidamrongphan W, Phaonakrop N, Jaresitthikunchai J, Li L (2019) Metabolomic study of stress responses leading to plant resistance in mandarin fruit mediated by preventive applications of Bacillus subtilis cyclic lipopeptides. Postharvest Biol Technol 156:110946
Turan V, Schröder P, Bilen S, Insam H, Fernández-Delgado Juárez M (2019) Co-inoculation effect of Rhizobium and Achillea millefolium L. oil extracts on growth of common bean (Phaseolus vulgaris L.) and soil microbial-chemical properties. Sci Rep 9(1):15178
Ullah MA, Gul FZ, Khan T, Bajwa MN, Drouet S, Tungmunnithum D, Abbasi BH (2021) Differential induction of antioxidant and anti-inflammatory phytochemicals in agitated micro-shoot cultures of Ajuga integrifolia Buch. Ham. ex D. Don with biotic elicitors. AMB Express 11(1):1–13
Van Wyk BE, Wink M (2018) Medicinal plants of the world. CABI
Velázquez-Gamboa MC, Rodríguez-Hernández L, Abud-Archila M, Gutiérrez-Miceli FA, González-Mendoza D, Valdez-Salas B, Luján-Hidalgo MC (2021) Agronomic biofortification of Stevia rebaudiana with zinc oxide (ZnO) phytonanoparticles and antioxidant compounds. Sugar Tech 23(2):453–460
Verpoorte R, Memelink J (2002) Engineering secondary metabolite production in plants. Curr Opin Biotechnol 13(2):181–187
Vivek AS, Riyas CT, Swapna TS (2023) Enhanced secondary metabolite production for drug leads. In: Sukumaran ST (ed) Conservation and sustainable utilization of bioresources: sustainable development and biodiversity. Springer, Singapore
Vosoughi N, Gomarian M, Pirbalouti AG, Khaghani S, Malekpoor F (2018) Essential oil composition and total phenolic, flavonoid contents, and antioxidant activity of sage (Salvia officinalis L.) extract under chitosan application and irrigation frequencies. Ind Crops Prod 117:366–374
Walker TS, Bais HP, Vivanco JM (2002) Jasmonic acid-induced hypericin production in cell suspension cultures of Hypericum perforatum L. (St. John’s wort). Phytochemistry 60(3):289–293
Wang C, Wu J, Mei X (2001) Enhancement of taxol production and excretion in Taxus chinensis cell culture by fungal elicitation and medium renewal. Appl Microbiol Biotechnol 55:404–410
Wang SY, Bunce JA, Maas JL (2003) Elevated carbon dioxide increases contents of antioxidant compounds in field-grown strawberries. J Agric Food Chem 51(15):4315–4320
Wang H, Wang H, Shao H, Tang X (2016) Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 7:67
Wang B, Kumar V, Olson A, Ware D (2019) Reviving the transcriptome studies: an insight into the emergence of single-molecule transcriptome sequencing. Front Genet 10:384
Wang SH, Liang WX, Lu J, Yao L, Wang J, Gao WY (2020) Penicillium sp. YJM-2013 induces ginsenosides biosynthesis in Panax ginseng adventitious roots by inducing plant resistance responses. Chin Herbal Med 12(3):257–264
Williams RD, Bedard C, Chavarie C, Archambault J (1996) Production of sanguinarine by elicited plant cell culture II. Further nutritional aspects. J Biotechnol 46(2):107–120
Xie XG, Zhang ZZ, Chen L, Ming QL, Sheng KX, Chen X, Han T (2023) An endophytic fungus Schizophyllum commune isolated from Panax ginseng enhances hairy roots growth and ginsenoside biosynthesis. Can J Microbiol. https://doi.org/10.1139/cjm-2022-0194
Xoca-Orozco LÁ, Cuellar-Torres EA, González-Morales S, Gutiérrez-Martínez P, López-García U, Herrera-Estrella L, Chacón-López A (2017) Transcriptomic analysis of avocado hass (Persea americana Mill.) in the interaction system fruit-chitosan-Colletotrichum. Front Plant Sci 8:956
Xu W, Jin X, Yang M, Xue S, Luo L, Cao X, Wang X (2021) Primary and secondary metabolites produced in Salvia miltiorrhiza hairy roots by an endophytic fungal elicitor from Mucor fragilis. Plant Physiol Biochem 160:404–412
Yakhin OI, Lubyanov AA, Yakhin IA, Brown PH (2017) Biostimulants in plant science: a global perspective. Front Plant Sci 7:2049
Yamaner O, Erdag B (2013) Effects of sucrose and polyethylene glycol on hypericins content in Hypericum adenotrichum. Eurasia J Biosci. https://doi.org/10.5053/ejobios.2013.7.0.12
Yin H, Fretté XC, Christensen LP, Grevsen K (2012) Chitosan oligosaccharides promote the content of polyphenols in Greek oregano (Origanum vulgare ssp. hirtum). J Agric Food Chem 60(1):136–143
Yuan G, Wang X, Guo R, Wang Q (2010) Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts. Food Chem 121(4):1014–1019
Zahir A, Nadeem M, Ahmad W, Giglioli-Guivarch N, Hano C, Abbasi BH (2019) Chemogenic silver nanoparticles enhance lignans and neolignans in cell suspension cultures of Linum usitatissimum L. Plant Cell Tiss Organ Cult 136:589–596
Zehra A, Raytekar NA, Meena M, Swapnil P (2021) Efficiency of microbial bio-agents as elicitors in plant defense mechanism under biotic stress: a review. Curr Res Microbial Sci 2:100054
Zhan X, Chen Z, Chen R, Shen C (2022) Environmental and genetic factors involved in plant protection-associated secondary metabolite biosynthesis pathways. Front Plant Sci 13:877304
Zhang C, Yan Q, Cheuk WK, Wu J (2004) Enhancement of tanshinone production in Salvia miltiorrhiza hairy root culture by Ag+ elicitation and nutrient feeding. Planta Med 70(02):147–151
Zhang Z, Zhao P, Zhang P, Su L, Jia H, Wei X, Jia H (2020) Integrative transcriptomics and metabolomics data exploring the effect of chitosan on postharvest grape resistance to Botrytis cinerea. Postharvest Biol Technol 167:111248
Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23(4):283–333
Zhong JJ (2001) Biochemical engineering of the production of plant-specific secondary metabolites by cell suspension cultures. Plant Cells. https://doi.org/10.1007/3-540-45302-4_1
Zhou LS, Tang K, Guo SX (2018) The plant growth-promoting fungus (PGPF) Alternaria sp. A13 markedly enhances Salvia miltiorrhiza root growth and active ingredient accumulation under greenhouse and field conditions. Int J Mol Sci 19(1):270
Złotek U (2017) Effect of jasmonic acid and yeast extract elicitation on low-molecular antioxidants and antioxidant activity of marjoram (Origanum majorana L.). Acta Sci Pol Technol Aliment 16(4):371–377
Zobayed SMA, Afreen F, Kozai T (2005) Temperature stress can alter the photosynthetic efficiency and secondary metabolite concentrations in St. John’s Wort. Plant Physiol Biochem 43(10–11):977–984
Funding
No funds, grants, or other support was received.
Author information
Authors and Affiliations
Contributions
Conceptualization: NS; equally contributed to writing the original draft: NS, SK; writing—review, editing, valuable feedback: NS, SK, UG, NA and MS; manuscript corrections and draft formatting: SK, UG, MS, NA; supervision, visualization: NS. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Competing interests
All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.
Additional information
Handling Editor: Ariel D. Arencibia.
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.
About this article
Cite this article
Selwal, N., Goutam, U., Akhtar, N. et al. Elicitation: “A Trump Card” for Enhancing Secondary Metabolites in Plants. J Plant Growth Regul (2024). https://doi.org/10.1007/s00344-024-11294-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00344-024-11294-y