Abstract
In vitro, shoot apices cultures provide an alternative means for producing secondary metabolites of medicinal and pharmaceutical importance. In this study, the major objective was to investigate the effect of Copper (Cu) and Methyl Jasmonate elicitors on basil 'Grecco a Palla' shoot apex growth, on the volatile chemical composition, and biological and enzymatic activities. Stem apex, from seedlings grown in vitro, were used as explant for plant propagation. Murashige—Skoog medium, supplemented with five elicitors concentrations (T1: 0 µM, 0 µM; T2: 25 µM, 0 µM; T3: 0 µM, 5 µM, T4: 25 µM, 5 µM; T5: 75 µM, 5 µM de Cu and MeJa, respectively) was used for the inoculation. Cooper in combination with MeJa (T3 and T4) reduced the occurrence of oxidation (20%) and hyperhydricity (77%) in the shoot when compared to the control treatment. 25 µM Cu and 5 µM MeJa increased the antioxidant activity by 72.5% (DPPH), the enzymatic activity of Phenylalanine ammonia-lyase (PAL) by 95%, the total phenolic compounds by 33,33%, and superoxide dismutase (SOD) enzymatic activity by 37%. In the 75 µM Cu and 5 µM MeJa treatment resulted in an increase of 20% in the ascorbate peroxidase enzyme activity. Those treatments promoted a higher number of volatile compounds to T4 (20) and T5 (28), of which α-bergamotene, methyl eugenol, and linalool were found to be the majority. β-Pinene, Myrcene, γ-Cadinene, and δ-Cadinene were only identified in T5. Therefore, the above-mentioned elicitors might be used in combination with the described concentrations, in order to improve the compound synthesis and antioxidant activity.
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References
Aftab T, Khan M, Idrees M, Naeem M, Hashmi N (2011) Methyl jasmonate counteracts boron toxicity by preventing oxidative stress and regulating antioxidant enzyme activities and artemisinin biosynthesis in Artemisia annua L. Protoplasma 248:601–612. https://doi.org/10.1007/s00709-010-0218-5
Beatovic D, Krstic-Milosevic D, Trifunovic S, Siljegovic J, Glamoclija J, Ristic M et al (2015) Chemical composition, antioxidant and antimicrobial activities of the essential oils of twelve Ocimum basilicum L. cultivars grown in Serbia. Rec Nat Prod 9:62–75
Bhaduri-Anwesha M, Fulekar MH (2012) Antioxidant enzyme responses of plant to heavy metal stress. Environ Sci Technol 11:55–69. https://doi.org/10.1007/s11157-011-9251-x
Biswas T (2020) Elicitor induced increased rosmarinic acid content of in vitro root cultures of Ocimum basilicum L. (Sweet Basil). Plant Sci Today 7:157–163. https://doi.org/10.14719/pst.2020.7.2.690
Bonacina C, Trevizan CB, Stracieri J, dos Santos TB, Gonçalves JE, Gazim ZC et al (2017) Changes in growth, oxidative metabolism and essential oil composition of lemon balm (Melissa officinalis L.) subjected to salt stress. Aust J Crop Sci 12:1665–1674. https://doi.org/10.3316/informit.402502203155099
Cardoso JC, Oliveira ME, Cardoso FDC (2019) Advances and challenges on the in vitro production of secondary metabolites from medicinal plants. Hortic Bras 37:124–132. https://doi.org/10.1590/S0102-053620190201
Comar CG, Barbosa EM, Pereira VSR, de Lima JD, Santana TT, Magalhães HM (2019) Zinc as promoter of growth and biochemical activity in basil cultivars under in vitro conditions. Sci Agraria Par 18:342–350. https://doi.org/10.18188/sap.v18i4.21909
de Araújo Couto HGS, Blank AF, Silva AMDO, de Lima Nogueira PC, de Fátima A-B, de Castro Nizio DA, de Oliveira Pinto JA (2019) Essential oils of basil chemotypes: major compounds, binary mixtures, and antioxidant activity. Food Chem 293:446–454. https://doi.org/10.1016/j.foodchem.2019.04.078
Dias MI, Sousa MJ, Alves RC, Ferreira IC (2016) Exploring plant tissue culture to improve the production of phenolic compounds: a review. Ind Crops Prod 82:9–22. https://doi.org/10.1016/j.indcrop.2015.12.016
Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2003) Response of the ascorbate–glutathione cycle to excess copper in Arabidopsis thaliana (L.). Plant Sci 164:195–202. https://doi.org/10.1016/S0168-9452(02)00383-7
Elansary HO, Szopa A, Kubica P, Ekiert H, El-Ansary DO, Al-Mana FA et al (2020) Saudi Rosmarinus officinalis and Ocimum basilicum L. polyphenols and biological activities. Processes 8:2–15. https://doi.org/10.3390/pr8040446
Fazal H, Abbasi BH, Ahmad N, Ali M (2016) Elicitation of medicinally important antioxidant secondary metabolites with silver and gold nanoparticles in callus cultures of Prunella vulgaris L. Appl Biochem Biotechnol 180:1076–1092. https://doi.org/10.1007/s12010-016-2153-1
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Cien Agrot 35:1039–1042. https://doi.org/10.1590/S1413-70542011000600001
Folli-Pereira MDS, Meira-Haddad LSA, Bazzolli DMS, Kasuya MCM (2012) Micorriza arbuscular e a tolerância das plantas ao estresse. Rev Bras Cienc Sol 36:1663–1679. https://doi.org/10.1590/S0100-06832012000600001
Giannopolitis I, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314. https://doi.org/10.1104/pp.59.2.309
Górski F, Gerotti GM, Magalhães HM (2021) Relationship between auxins and cytokinins in the growth and organogenesis of Ocimum basilicum L. ‘Grecco a Palla.’ Can J Plant Sci 101:1–16. https://doi.org/10.1139/cjps-2020-0067
Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455. https://doi.org/10.1104/pp.84.2.450
Ibrahim AS, Fahmy AH, Ahmed SS (2019) Copper nanoparticles elevate regeneration capacity of (Ocimum basilicum L.) plant via somatic embryogenesis. Plant Cell Tiss Org 136:41–50. https://doi.org/10.1007/s11240-018-1489-3
Isah T, Umar S (2022) Influence of silver nitrate and copper sulfate on somatic embryogenesis, shoot morphogenesis, multiplication, and associated physiological biochemical changes in Gladiolus hybridus L. Plant Cell Tiss Org 149:1–25. https://doi.org/10.1007/s11240-022-02309-1
Juang KW, Lo YC, Chen TH, Chen BC (2019) Effects of copper on root morphology, cations accumulation, and oxidative stress of grapevine seedlings. Bull Environ Contam Toxicol 102:873–879. https://doi.org/10.1007/s00128-019-02616-y
Khatun S, Ali MB, Hahn EJ, Paek KY (2008) Copper toxicity in Withania somnifera: growth and antioxidant enzymes responses of in vitro grown plants. Environ Exp Bot 64:279–285. https://doi.org/10.1016/j.envexpbot.2008.02.004
Kim YB, Kim JK, Uddin MR, Xu H, Park WT, Tuan PA et al (2013) Metabolomics analysis and biosynthesis of rosmarinic acid in Agastache rugosa Kuntze treated with methyl jasmonate. PLoS One 8:1–8. https://doi.org/10.1371/journal.pone.0064199
Koca N, Karaman Ş (2015) The effects of plant growth regulators and L-phenylalanine on phenolic compounds of sweet basil. Food Chem 166:515–521. https://doi.org/10.1016/j.foodchem.2014.06.065
Korkor AM, Mohamed SA, Abd El-kafie OM, Gohar AA (2017) Adaptation of the in vitro culture of Origanum majorana L. for production of phenolic acids. IOSR J Pharm Biol Sci 12:30–38. https://doi.org/10.9790/3008-1202013038
Kumar V, Pandita S, Sidhu GPS, Sharma A, Khanna K, Kaur P, Setia R (2021) Copper bioavailability, uptake, toxicity and tolerance in plants: a comprehensive review. Chemosphere 262:1–25. https://doi.org/10.1016/j.chemosphere.2020.127810
Larrauri JA, Rupérez P, Saura-Calixto F (1997) Effect of drying temperature on the stability of polyphenols and antioxidant activity of red grape pomace peels. J Agric Food Chem 45:1390–1393. https://doi.org/10.1021/jf960282f
Li QX, Chang CL (2016) Basil (Ocimum basilicum L.) oils. Essential oils in food preservation flavor and safety. Academic Press, Cambridge, Massachusetts
Luciano ÁJ, Irineo TP, Virginia OVR, Feregrino-Pérez AA, Hernández AC, Gerardo GGR (2017) Integrating plant nutrients and elicitors for production of secondary metabolites, sustainable crop production and human health: a review. Int J Agric Biol 19:391–402. https://doi.org/10.17957/IJAB/15.0297
Maksymiec W, Krupa Z (2006) Effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57:187–194. https://doi.org/10.1016/j.envexpbot.2005.05.006
Manan AA, Taha RM, Mubarak EE, Elias H (2016) In vitro flowering, glandular trichomes ultrastructure, and essential oil accumulation in micropropagated Ocimum basilicum L. In Vitro Cell Dev-Plant 52:303–314. https://doi.org/10.1007/s11627-016-9755-8
Mandoulakani BA, Eyvazpour E, Ghadimzadeh M (2017) The effect of drought stress on the expression of key genes involved in the biosynthesis of phenylpropanoids and essential oil components in basil (Ocimum basilicum L.). Phytochemistry 139:1–7. https://doi.org/10.1016/j.phytochem.2017.03.006
Mehring A, Haffelder J, Chodorski J, Stiefelmaier J, Strieth D, Ulber R (2020) Establishment and triterpenoid production of Ocimum basilicum cambial meristematic cells. Plant Cell Tiss Org 143:573–581. https://doi.org/10.1007/s11240-020-01942-y
Milan EB, Mandoulakani BA, Kheradmand F (2017) The effect of methyl jasmonate on the expression of phenylalanine ammonia lyase and eugenol-o-methyl transferase genes in basil. Philipp Agric Sci 100:163–167
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 3:426–428
Murashige T, Skoog FA (1962) Revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216. https://doi.org/10.1007/s10311-010-0297-8
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Narayani M, Srivastava S (2017) Elicitation: a stimulation of stress in vitro plant cell/tissue cultures for enhancement of secondary metabolite production. Phytochem Rev 16:1227–1252. https://doi.org/10.1007/s11101-017-9534-0
Nazir M, Tungmunnithum D, Bose S, Drouet S, Garros L, Giglioli-Guivarc’h N, Hano C (2019) Differential production of phenylpropanoid metabolites in callus cultures of Ocimum basilicum L. with distinct in vitro antioxidant activities and in vivo protective effects against UV stress. J Agric Food Chem 67:1847–1859
Nezami-Alanagh E, Garoosi GA, Landín M, Gallego PP (2019) Computer-based tools provide new insight into the key factors that cause physiological disorders of pistachio rootstocks cultured in vitro. Sci Rep 9:1–15. https://doi.org/10.1021/acs.jafc.8b05647
Pandey P, Singh S, Banerjee S (2019) Ocimum basilicum suspension culture as resource for bioactive triterpenoids: yield enrichment by elicitation and bioreactor cultivation. Plant Cell Tiss Org 137:65–75. https://doi.org/10.1007/s11240-018-01552-9
Redman RS, Freeman S, Clifton DR, Morrel J, Brown G, Rodriguez RJ (1999) Biochemical analysis of plant protection afforded by a nonpathogenic endophytic mutant of Colletotrichum magna. Plant Physiol 119:795–804. https://doi.org/10.1104/pp.119.2.795
Rufino MS, Fernandes FA, Alves RE, de Brito ES (2009) Free radical-scavenging behaviour of some north-east Brazilian fruits in a DPPH system. Food Chem 114:693–695. https://doi.org/10.1016/j.foodchem.2008.09.098
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 Plants 23:229–237. https://doi.org/10.1007/s12298-016-0406-7
Sami F, Yusuf M, Faizan M, Faraz A, Hayat S (2016) Role of sugars under abiotic stress. Plant Physiol Biochem 109:54–61. https://doi.org/10.1016/j.plaphy.2016.09.005
Santos AAD, Deoti JR, Müller G, Dário MG, Stambuk BU, Alves Junior SL (2017) Microwell plate-based method for the determination of reducing sugars with the DNS reagent. Braz J Food Tech 20:1–29
Santos STD, Oliveira FDAD, Oliveira G, Sá FVDS, Costa JPDM, Fernandes PD (2020) Photochemical efficiency of basil cultivars fertigated with salinized nutrient solutions. Rev Bras Eng Agr Amb 24:319–324. https://doi.org/10.1590/1807-1929/agriambi.v24n5p319-324
Senji BM, Mandoulakani BA (2018) The impact of cold stress on genes expression pattern of mono-and sesquiterpene biosynthesis and their contents in Ocimum basilicum L. Phytochem 156:250–256. https://doi.org/10.1016/j.phytochem.2018.09.006
Shoja AA, Çirak C, Ganjeali A, Cheniany M (2022) Stimulation of phenolic compounds accumulation and antioxidant activity in in vitro culture of Salvia tebesana Bunge in response to nano-TiO2 and methyl jasmonate elicitors. Plant Cell Tiss Org 149:423–440. https://doi.org/10.1007/s11240-022-02251-2
Statsoft (2020) Statistica for windows (computer program manual). [Online]. Available from http://www.statsoftcom. Accessed 1 Aug 2021
Tahsili J, Sharifi M, Behmanesh M, Pourbozorgi-Rudsari N, Ziaei M (2012) Expression of 4 genes in Ocimum basilicum and their relationship with phenylpropanoids content. J Med Plants By-Prod 1:23–34
Talebi M, Moghaddam M, Pirbalouti AG (2018) Methyl jasmonate effects on volatile oil compounds and antioxidant activity of leaf extract of two basil cultivars under salinity stress. Acta Physiol Plant 40:1–11. https://doi.org/10.1007/s11738-018-2611-1
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. https://doi.org/10.1016/j.jarmap.2018.11.004
Tijjani CE, Luka DC (2018) Phytochemistry. Biosynthesis of phytochemicals. Apple Academic Press, Palm Bay, Florida
Trettel JR, Gazim ZC, Gonçalves JE, Stracieri J, Magalhães HM (2017) Volatile essential oil chemical composition of basil (Ocimum basilicum L. ‘Green’) cultivated in a greenhouse and micropropagated on a culture medium containing copper sulfate. Plant Cell Tiss Org 6:631–640. https://doi.org/10.1007/s11627-017-9868-8
Trettel JR, Gazim ZC, Goncalves JE, Stracieri J, Magalhaes HM (2018) Effects of copper sulphate (CuSO4) elicitation on the chemical constitution of volatile compounds and the in vitro development of Basil. Sci Hortic 234:19–26. https://doi.org/10.1016/j.scienta.2018.01.062
Trettel JR, Queiroz MDS, Andrade MM, Magalhães HM (2020) In vitro effects of regulators on growth and morphogenesis of Ocimum basilicum L. “Alfavaca Green” stem apexes. Agron Res 18:603–618. https://doi.org/10.15159/ar.20.039
Trivellini A, Lucchesini M, Maggini R, Mosadegh H, Villamarin TSS, Vernieri P et al (2016) Lamiaceae phenols as multifaceted compounds: bioactivity, industrial prospects and role of “positive-stress.” Ind Crop Prod 83:241–254. https://doi.org/10.1016/j.indcrop.2015.12.039
Umesha S (2006) Note: phenylalanine ammonia lyase activity in tomato seedlings and its relationship to bacterial canker disease resistance. Phytoparasitica 34:68–71. https://doi.org/10.1007/BF02981341
Van den Dries N, Giannì S, Czerednik A, Krens FA, de Klerk GJM (2013) Flooding of the apoplast is a key factor in the development of hyperhydricity. J Exp Bot 64:5221–5230. https://doi.org/10.1093/jxb/ert315
Wasternack C, Hause B (2019) The missing link in jasmonic acid biosynthesis. Nat Plant 5:776–777. https://doi.org/10.1038/s41477-019-0492-y
Waterhouse AL (2002) Determination of total phenolics. Curr Protoc Food Anal Chem 6:1–1
Welz VFF, Trettel JR, Nascimento AB, Barbosa LN, Magalhães HM (2020a) Effects of photoperiod, potassium, and growth regulators on micropropagation of Ocimum basilicum L. ‘Genovese.’ Aust J Crop Sci 14:1645–1653. https://doi.org/10.3316/informit.796708603218908
Welz VFF, Trettel JR, Nascimento AB, Magalhães H (2020b) Growth, enzymatic activity, and antioxidant activity of sweet basil grown in vitro. Rev Caatinga 33:660–667. https://doi.org/10.1590/1983-21252020v33n309rc
Yu X, Zhang W, Zhang Y, Zhang X, Lang D, Zhang X (2018) The roles of methyl jasmonate to stress in plants. Funct Plant Biol 46:197–212. https://doi.org/10.1071/FP18106
Zare-Hassani E, Motafakkerazad R, Razeghi J, Kosari-Nasab M (2019) The effects of methyl jasmonate and salicylic acid on the production of secondary metabolites in organ culture of Ziziphora persica. Plant Cell Tiss Org 138:437–444. https://doi.org/10.1007/s11240-019-01639-x
Złotek U, Michalak-Majewska M, Szymanowska U (2016) Effect of jasmonic acid elicitation on the yield, chemical composition, and antioxidant and anti-inflammatory properties of essential oil of lettuce leaf basil (Ocimum basilicum L.). Food Chem 213:1–7. https://doi.org/10.1016/j.foodchem.2016.06.052
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We would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) n° 001 for funding this work. And Universidade Paranaense (UNIPAR) for financial support.
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HM and ZC supervised the project. HM and FG conceived and designed the experiments and FG, GG, and JE performed the experiments. FG wrote the paper. HM and JE revised the paper. All authors read and approved the final paper.
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Górski, F., Gerotti, G.M., Gonçalves, J.E. et al. Methyl jasmonate and copper activate volatiles and antioxidant mechanisms in 'Grecco a Palla' basil produced in vitro. J. Crop Sci. Biotechnol. 26, 615–629 (2023). https://doi.org/10.1007/s12892-023-00206-3
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DOI: https://doi.org/10.1007/s12892-023-00206-3