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Secondary metabolites induction in plantain (Plantago major L.) via abiotic stresses in liquid medium

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Abstract

Plantain (Plantago major L.) is a valuable medicinal plant that contains a high level of secondary metabolites. The objective of this research is to examine the oxidative stress, such as drought and heavy metals, on the production of these metabolites in liquid medium. Drought stress was induced by using polyethylene glycol 6000 at three levels of 0%, 6%, and 12%. Heavy metal stress was induced by using HgCl2 at three levels of 0, 4 and 8 µM on 21-day -old plants immersed in liquid MS medium. Sampling was performed at 0, 2, 4, and 6 days after stress from treated and control plants. The Total content of secondary metabolites, including phenol, flavonoid, terpene, alkaloid, and anthocyanin, was evaluated using spectrophotometry methods. Additionally, the correlation between the levels of these metabolites and the expression of crucial genes involved in their biosynthesis, such as phenylalanine ammonia-lyase synthesize (PAL), 3-deoxy-D-arabino-heptulosonate-7-phosphate-synthase (DAHPS), 3-hydroxy-3-methylglutaryl coenzyme A (HMG-CoAR), caffeic acid o-methyl transferase (COMT), and squalene epoxidase (SQE), was examined using Real-Time PCR. The results of the variance analysis for phenol, flavonoid, terpene, alkaloid, and anthocyanin, which were affected by PEG and HgCl2, showed significant changes in secondary metabolites in treated plants compared to control plants. Although the patterns of gene expression and secondary metabolite production did not always follow the same pattern, the effect of stresses on increasing the expression of some genes related to phenol and terpenoid production pathway was significant.

Key message

Both HgCl2 and PEG can increase the biosynthesis of secondary metabolites in Plantain immersed in a culture medium.

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References

  • Babalola TI, Shode FO (2013) Ubiquitous ursolic acid: a potential pentacyclic triterpene natural product. J Pharmacogn Phytochem 2(2):214–222

    CAS  Google Scholar 

  • Beara IN, Lesjak MM, Jovin ED, Balog KJ, Anackov GT, Orcic DZ, Mimica-Dukic NM (2009) Plantain (Plantago major L.) species as novel sources of flavonoid antioxidants. J Agric Food Chem 57(19):9268–9273

    Article  CAS  PubMed  Google Scholar 

  • Bhatti MZ, Ismail H, Kayani WK (2022) Plant secondary metabolites: therapeutic potential and pharmacological properties. Trends and Reviews, Secondary Metabolites, p 201

    Google Scholar 

  • Bjørklund G, Dadar M, Mutter J, Aaseth J (2017) The toxicology of mercury: current research and emerging trends. Environ Res 159:545–554

    Article  PubMed  Google Scholar 

  • Boening DW (2000) Ecological effects, transport, and fate of mercury: a general review. Chemosphere 40(12):1335–1351

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Yan J, Lei J, Li J, Zhu J, Zhang H (2017) De novo transcriptome sequencing of MeJA-induced Taraxacum koksaghyz Rodin to identify genes related to rubber formation. Sci Rep 7(1):15697

    Article  PubMed  PubMed Central  Google Scholar 

  • Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ (2013) Balancing metabolites in drought: the sulfur assimilation conundrum. Trends Plant Sci 18:18–29

    Article  CAS  PubMed  Google Scholar 

  • Chen JY, He LH, Jiang YM, Wang Y, Joyce DC, Ji ZL, Lu WJ (2008) Role of phenylalanine ammonia-lyase in heat pretreatment induced chilling tolerance in banana fruit. Physiol Plant 132:318–328

    Article  CAS  PubMed  Google Scholar 

  • Chun OK, Kim DO, Lee CY (2003) Superoxide radical scavenging activity of the major polyphenols in fresh plums. J Agric Food Chem 51:8067–8072

    Article  CAS  PubMed  Google Scholar 

  • de Matos YMLS, Rocha JE, Souza CES, Al Yafawi TT, de Araújo Neto JB, Campina FF, Pinheiro JCA, de Freitas TS, Sousa AK, Tintino SR, Braga MFBM (2021) FTIR analysis and reduction of the phytotoxic effect of mercury dichloride by rutin. Rhizosphere 19:100393

    Article  Google Scholar 

  • Ebrahimi FS, Kumleh SH, Rezadoost MH (2019) Morphological changes and the expression of oxidoreductase genes of Brassica napus in deep culture media containing PEG. Proc Natl Acad Sci India Sect B Biol Sci 89:1311–1318

    Article  CAS  Google Scholar 

  • Elbaz A, Wei YY, Meng Q, Zheng Q, Yang ZM (2010) Mercury-induced oxidative stress and impact on antioxidant enzymes in Chlamydomonas reinhardtii. Ecotoxicology 19:1285–1293

    Article  CAS  PubMed  Google Scholar 

  • Entus R, Poling M, Herrmann KM (2002) Redox regulation of Arabidopsis 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase. Plant Physiol 129(4):1866–1871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furdui C, Zhou L, Woodard RW, Anderson KS (2004) Insights into the mechanism of 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase (phe) from Escherichia coli using a transient kinetic analysis. J Biol Chem 279(44):45618–45625

    Article  CAS  PubMed  Google Scholar 

  • Gammoudi N, Nagaz K, Ferchichi A (2022) Establishment of optimized in vitro disinfection protocol of Pistacia vera L. explants mediated a computational approach: multilayer perceptron–multi – objective genetic algorithm. BMC Plant Biol 22:324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gelinas P, McKinnon CM (2006) Effect of wheat variety, farming site, and bread-baking on total phenolics. Int J Food Sci 41(3):329–332

    Article  CAS  Google Scholar 

  • Gho YS, Kim SJ, Jung KH (2020) Phenylalanine ammonia-lyase family is closely associated with response to phosphate deficiency in rice. Genes Genomics 42(1):67–76

    Article  CAS  PubMed  Google Scholar 

  • Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351

    Article  CAS  PubMed  Google Scholar 

  • Hura T, Hura K, Grzesiak S (2008) Contents of total phenolics and ferulic acids, and PAL activity during water potental changes in leaves of maize single-cross hybrids of different drought tolerance. J Agron Crop Sci 194(2):104–112

    Article  Google Scholar 

  • Isah T (2019) Stress and defense responses in plant secondary metabolites production. Biol Res 52:39

    Article  PubMed  PubMed Central  Google Scholar 

  • Jain D, Tripathi PC (2021) R Chapter one the impact of various environmental factors on secondary metabolites. The life of plants in a changing Environment, 1

  • Jing P, Bomser JA, Schwartz SJ, He J, Magnuson BA, Giusti MM (2008) Structure – function relationships of anthocyanins from various anthocyanin-rich extracts on the inhibition of colon cancer cell growth. J Agric Food Chem 56(20):9391–9398

    Article  CAS  PubMed  Google Scholar 

  • Jung C, Maeder V, Funk F, Frey B, Sticher H, Frossard E (2003) Release of phenols from Lupinus albus L. roots exposed to Cu and their possible role in Cu detoxification. Plant Soil 252(2):301–312

    Article  CAS  Google Scholar 

  • Kim J, Choi B, Cho B, Lim H, Kim J, Natarajan S, Kwak E, Bae H (2013) Molecular cloning, characterization and expression of caffeic acid O-methyltransferase (COMT) ortholog from kenaf (Hibiscus cannabinus). Plant Omics Journal 6(4):246–253

    CAS  Google Scholar 

  • Kirby J, Keasling JD (2009) Biosynthesis of plant isoprenoids: perspectives for microbial engineering. Annu Rev Plant Biol 60(1):335–355

    Article  CAS  PubMed  Google Scholar 

  • Kleine S, Müller C (2014) Drought stress and leaf herbivory affect root terpenoid concentrations and growth of Tanacetum vulgare. J Chem Ecol 40:1115–1125

    Article  CAS  PubMed  Google Scholar 

  • Kleinwächter M, Selmar D (2015) New insights explain that drought stress enhances the quality of spice and medicinal plants: potential applications. Agron Sustain Dev 35:121–131

    Article  Google Scholar 

  • Konczak I, Zhang W (2004) Anthocyanins – more than nature’s colours. J Biomed Biotechnol 5:239–240

    Article  Google Scholar 

  • Kumar S, Bhushan B, Wakchaure GC, Meena KK, Kumar M, Meena NL, Rane J (2020) Plant phenolics under water-deficit conditions: biosynthesis, accumulation, and physiological roles in water stress alleviation. Plant Phenolics in Sustainable Agriculture. Springer, Singapore, pp 451–465

    Chapter  Google Scholar 

  • Leivar P, Antolín-Llovera M, Arró M, Ferrer A, Boronat A, Campos N (2011) Modulation of plant HMG-CoA reductase by protein phosphatase 2a. Plant Signal Behav 6:1127–1131

    Article  PubMed  PubMed Central  Google Scholar 

  • Li HY, Deng ZY, Zhu HH, Hu CL, Liu RH, Young JC (2012) Highly pigmented vegetables: anthocyanin compositions and their role in antioxidant activities. Food Res Int 46:250–259

    Article  CAS  Google Scholar 

  • Li W, Liu W, Wei H, He Q, Chen J, Zhang B, Zhu Sh (2014) Species-specific expansion and molecular evolution of the 3-hydroxy-3-methylglutaryl coenzyme a reductase (HMGR) gene family in plants. PLOS 9(4):e94172

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Loreto F, Dicke M, Schnitzler JP, Turlings TC (2014) Plant volatiles and the environment. Plant Cell Environ 37:1905–1908

    Article  PubMed  Google Scholar 

  • Marinova D, Ribarova F, Atanassova M (2005) Total phenolics and flavonoids in bulgarian fruits and vegetables. JU Chem Metal 40:255–260

    CAS  Google Scholar 

  • Midzi J, Jeffery DW, Baumann U, Rogiers S, Tyerman SD, Pagay V (2022) Stress-Induced Volatile Emissions and Signalling in Inter-Plant Communication. Plants (Basel) 11(19):29

    Google Scholar 

  • Nemeikaitė-Čėnienė A, Imbrasaitė A, Sergedienė E, Čėnas N (2005) Quantitative structure–activity relationships in prooxidant cytotoxicity of polyphenols: role of potential of phenoxyl radical/phenol redox couple. Arch Biochem Biophys 441(2):182–190

    Article  PubMed  Google Scholar 

  • Neto CC (2011) Ursolic acid and other pentacyclic triterpenoids: anticancer activities and occurrence in berries. Berries and cancer prevention. Springer, New York, NY, pp 41–49

    Chapter  Google Scholar 

  • Nogués I, Medori M, Calfapietra C (2015a) Limitations of monoterpene emissions and their antioxidant role in Cistus sp. under mild and severe treatments of drought and warming. Environ Exp Bot 119:76–86

    Article  Google Scholar 

  • Pandey S, Gupta K, Mukherjee AK (2007) Impact of cadmium and lead on Catharanthus roseus-A phytoremediation study. J Environ Biol 28(3):655–662

    CAS  PubMed  Google Scholar 

  • Piasecka A, Jedrzejczak-Rey N, Bednarek P (2015) Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol 206:948–964

    Article  PubMed  Google Scholar 

  • Possell M, Loreto F (2013) The role of volatile organic compounds in plant resistance to abiotic stresses: responses and mechanisms. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions. Springer, Berlin, Germany, pp 209–235

    Chapter  Google Scholar 

  • Rasbery JM, Shan H, LeClair RJ, Norman M, Matsuda SPT, Bartel B (2007) Arabidopsis thaliana squalene epoxidase 1 is essential for root and seed development. J Biol Chem 282(23):17002–17013

    Article  CAS  PubMed  Google Scholar 

  • Sakihama Y, Cohen MF, Grace SC, Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177(1):67–80

    Article  CAS  PubMed  Google Scholar 

  • Sangtarash MH, Qaderi MM, Chinnappa CC, Reid DM (2009b) Carotenoid differential sensitivity of canola (Brassica napus) seedlings to ultraviolet-B radiation, water stress and abscisic acid. Environ Exp Bot 66(2):212–219

    Article  CAS  Google Scholar 

  • Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53(372):1351–1365

    CAS  PubMed  Google Scholar 

  • Selmar D, Kleinwächter M (2013) Stress enhances the synthesis of secondary plant products: the impact of stress-related over-reduction on the accumulation of natural products. Plant Cell Physiol 54:817–826

    Article  CAS  PubMed  Google Scholar 

  • Seyoum A, Asres K, El-Fiky FK (2006) Structure radical scavenging activity relationships of flavonoid. Phytochemistry 67(18):2058–2070

    Article  CAS  PubMed  Google Scholar 

  • Shao HB, Chu LY, Lu ZH, Kang CM (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4(1):8–14

    Article  CAS  Google Scholar 

  • Shao JW, Dai YC, Xue JP, Wang JC, Lin FP, Guo YH (2011) In vitro and in vivo anticancer activity evaluation of ursolic acid derivatives. Eur J Med Chem 46(7):2652–2661

    Article  CAS  PubMed  Google Scholar 

  • Sobral-Souza CE, Silva ARP, Leite NF, Rocha JE, Sousa AK, Costa JGM, Menezes IRA, Cunha FAB, Rolim LA, Coutinho HDM (2019) Phytotoxicity reduction of the mercury chloride effect by natural products from Eugenia jambolana Lam.: a new strategy against the toxic metal pollution. Ecotoxicol Environ Saf 15(170):461–467

    Article  Google Scholar 

  • Soczynska-Kordala M, Bakowska A, Oszmianski J, Gabrielska J (2001) Metal ion-flavonoid associations in bilayer phospholipid membranes. Cell Mol Biol Lett 6:277–281

    CAS  PubMed  Google Scholar 

  • Srivastava NK, Srivastava AK (2010) Influence of some heavy metals on growth, alkaloid content and composition in Catharanthus roseus L. Indian J Pharm Sci 72(6):775–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taga MS, Miller EE, Pratt DE (1984) Chia seeds as a source of natural lipid antioxidants. J Am Oil Chem Soc 61:928–931

    Article  CAS  Google Scholar 

  • Tahkorpi M (2010) Anthocyanins under drought and droughtrelanted stresses in Bilberry (Vaccinium myrtillus L.). Acta Universitatis Ouluensis: a Scientiae Rerum. Naturalium 556:1–46

    Google Scholar 

  • Turner GW, Croteau R (2004) Organization of monoterpene biosynthesis in Mentha. Immunocytochemical localizations of geranyl diphosphate synthase, limonene-6-hydroxylase, isopiperitenol dehydrogenase, and pulegone reductase. Plant physiol 136(4):4215–4227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valentao P, Fernandes E, Carvalho F, Andrade PB, Seabra RM, Bastos ML (2001) Antioxidant activity of Centaurium erythraea infusion evidenced by its superoxide radical scavenging and xanthine oxidase inhibitory activity. J Agric Food Chem 49(7):3476–3479

    Article  CAS  PubMed  Google Scholar 

  • Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3(1):2–20

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Zhu X, Wang K, Lu C, Shan T, Zhang Z (2018) A wheat caffeic acid 3-O-methyltransferase TaCOMT-3D positively contributes to both resistance to sharp eyespot disease and stem mechanical strength. Sci Rep 8:6543

    Article  PubMed  PubMed Central  Google Scholar 

  • Watkins JM, Chapman JM, Muday GK (2017) Abscisic acid-induced reactive oxygen species are modulated by flavonols to control stomata aperture. Plant Physiol 175:1807–1825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang L, Wen KS, Ruan X, Zhao YX, Wei F, Wang Q (2018)yxcc response of plant secondary metabolites to environmental factors. Molecules 23:762

  • Yoshikawa M, Luo W, Tanaka G, Konishi Y, Matsuura H, Takahashi K (2018) Wounding stress induces phenylalanine ammonia lyases, leading to the accumulation of phenylpropanoids in the model liverwort Marchantia polymorpha, vol 155. Phytochemistry, pp 30–36

  • Zaree R, Farhadi M, Mohammdzadeh Z, Goudarzi GR (2013) Extraction and comparison of alkaloids in different organs during different phonological periods of Nitraria schoberi. Ann Biol Res 4(2):130–135

    CAS  Google Scholar 

  • Zhang C, Wang X, Zhang F, Dong L, Wu J, Cheng Q, Qi D, Yan X, Jiang L, Fan S, Li N, Li D, Xu P, Zhang S (2017) Phenylalanine ammonia-lyase2.1 contributes to the soybean response towards Phytophthora sojae infection. Sci Rep 3(1):7242

    Article  Google Scholar 

  • Zhou ZS, Wang SJ, Yang ZM (2008) Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere 70:1500–1509

    Article  CAS  PubMed  Google Scholar 

  • Zhou Z, Guo K, Elbaz A, Yang Z (2009) Salicylic acid alleviates mercury toxicity by preventing oxidative stress in roots of Medicago sativa. Environ Exp Bot 65:27–34

    Article  CAS  Google Scholar 

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  1. Plant Biotechnology Department, University of Guilan, Rasht, 4199613776, Iran

    Elham Rajabzadeh Siadeni, Hassan Hassani Kumleh & Mohammad Hossein Rezadoost

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  1. Elham Rajabzadeh Siadeni
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  2. Hassan Hassani Kumleh
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Correspondence to Hassan Hassani Kumleh.

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Siadeni, E.R., Kumleh, H.H. & Rezadoost, M.H. Secondary metabolites induction in plantain (Plantago major L.) via abiotic stresses in liquid medium. Plant Cell Tiss Organ Cult 154, 493–505 (2023). https://doi.org/10.1007/s11240-023-02532-4

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