The Effect of Magnetic Iron Oxide Nanoparticles and Ferric Chloride on the Expression of Some Rosmarinic Acid Biosynthetic Genes in Melissa Officinalis L.

Document Type : Research Paper

Authors

1 Department of Agricultural Biotechnology, Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran

2 Assistant Professor, Department of Plant Genetics and Production Engineering, Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran

Abstract

Objective
Rosmarinic acid (RA), an anticancer, antiallergic, and antimicrobial agent, is a secondary metabolite in many plants of the family Lamiaceae including M. officinalis L. The application of nanoparticles (NPs) as a novel elicitor for the biosynthesis of bioactive compounds shown that the NPs could affect the secondary metabolites in plants by eliciting the expression of biosynthetic pathway genes. The present paper aimed to assess the effect of Magnetic Iron Oxide Nanoparticles (MIONPs) in comparison with their dissolved counterpart.
Materials and methods
Foliar application of different concentrations: including 5, 10, 25, and 50 mg/L Fe of ferric chloride and MIONPs on the plant leaves was performed. The relative mRNA levels of TAT, RAS, and HPPR were evaluated with quantitative real-time PCR (qRT-PCR) and compared between treated and untreated samples.
Results
This study showed the positive effects of ferric chloride and MIONPs on the expression of genes involved in the biosynthesis pathway of RA. The highest expression level of TAT, HPPR, and RAS genes was observed in plants treated with MIONPs at the concentration of 25 mg/L and the expression of genes decreased as the concentration increased to 50 mg/L. However, the genes expression was still higher compared to the control plant.
Conclusions
The results showed that the exposure of plants to ferric chloride and magnetic iron oxide nanoparticles led to an increase in the expression of the genes under study compared to control samples. However, the application of nano-scale iron particles had more effect than ferric chloride on the expression levels. An increase in the expression of genes involved in the biosynthesis pathway of RA through treatment with MIONPs provides an opportunity for induction of synthesis and accumulation of RA. Therefore, we hope to be able to enhance the production of RA in M. officinalis L. by using these NPs.

Keywords


 
Al-Dhabi NA, Arasu MV, Park CH, Park SU (2014) Recent studies on rosmarinic acid and its biological and pharmacological activities. EXCLI J 13, 1192.
Alkhatib R, Alkhatib B, Abdo N et al. (2019) Physio-biochemical and ultrastructural impact of (Fe3O4 ) nanoparticles on tobacco. BMC Plant Biol 19, 253.
Allahverdiyev A, Duran N, Ozguven M, Koltas S (2004) Antiviral activity of the volatile oils of Melissa officinalis L. against Herpes simplex virus type-2. Phytomedicine 11(7-8), 657-661.
Aminizadeh M, Riahi MA, Mohammadi M (2016) Nano-Metal oxides induced sulforaphane production and peroxidase activity in seedlings of Lepidium draba (Brassicaceae). Prog Biol Sci 6 (1), 75-83.
Bounihi A, Hajjaj G, Alnamer R et al. (2013) In vivo potential anti-inflammatory activity of Melissa officinalis L. essential oil. Adv Pharmacol Sci 2013.
Buzea C, Pacheco II, Robbie K (2007) Nanomaterials and nanoparticles: Sources and toxicity. Biointerphases 2, MR17–MR71.
Cardoso V, Francesko A, Ribeiro C et al. (2018) Advances in magnetic nanoparticles for biomedical applications. Adv Healthc Mater 7, 1700845.
Cvjetko P, Milosic A, Domijan AM et al. (2017) Toxicity of silver ions and differently coated silver nanoparticles in Allium cepa roots. Ecotoxicol Environ Saf 137, 18e28.
Dastmalchi K, Dorman HD, Oinonen PP et al. (2008) Chemical composition and in vitro antioxidative activity of a lemon balm (Melissa officinalis L.) extract. LWT - Food Sci Technol 41(3), 391-400.
De Oliveira JL, Campos EV, Bakshi M et al. (2014) Application of nanotechnology for the encapsulation of botanical insecticides for sustainable agriculture: prospects and promises. Biotechnol Adv 32(8), 1550-1561.
Grabherr MG, Haas BJ, Yassour M et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7), 644-652.
Hossain Z, Mustafa G, Komatsu S (2015) Plant responses to nanoparticle stress. Int J Mol Sci 16 (11), 26644e26653.
Huang B, Yi B, Duan Y et al. (2008) Characterization and expression profiling of tyrosine aminotransferase gene from Salvia miltiorrhiza (Dan-shen) in rosmarinic acid biosynthesis pathway. Mol Biol Rep 35(4), 601-612.
Jiang HS, Qiu XN, Li GB et al. (2014) Silver nanoparticles induced accumulation of reactive oxygen species and alteration of antioxidant systems in the aquatic plant Spirodela polyrhiza. Environ Toxicol Chem 33, 1398e1405.
Kim KH, Petersen M (2002) cDNA-cloning and functional expression of hydroxyphenylpyruvate dioxygenase from cell suspension cultures of Coleus blumei. Plant Sci 163(5), 1001-1009.
Konate A, Wang Y, He X et al. (2018) Comparative effects of nano and bulk-Fe3O4 on the growth of cucumber (Cucumis sativus). Ecotoxicol Environ Saf 165, 547–554.
Kumari S, Khan S (2018) Effect of Fe3O4 NPs application on fluoride (F) accumulation efficiency of Prosopis juliflora. Ecotoxicol Environ Saf 166, 419–426.
Lapaz ADM, Yoshida CHP, Gorni PH et al. (2022) Iron toxicity: effects on the plants and detoxification strategies. Acta Bot Brasilica 36, e2021abb0131.
Li M, Zhang P, Adeel M et al. (2021) Physiological impacts of zero valent iron, Fe3O4 and Fe2O3 nanoparticles in rice plants and their potential as Fe fertilizers. Environ Pollut 269, 116134.
Liu WT (2006) Nanoparticles and their biological and environmental applications. J Biosci Bioeng 102(1), 1-7.
Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408, 3053–3061.
Mansouri M, Mohammadi F (2021) Transcriptome analysis to identify key genes involved in terpenoid and rosmarinic acid biosynthesis in lemon balm (Melissa officinalis). Gene 773, 145417.
Miraj S, Rafieian-Kopaei, Kiani S (2017) Melissa officinalis L: A Review study with an antioxidant prospective. J Evid Based Complementary Altern Med 22(3), 385-394.
Mizukami H, Ogawa T, Ohashi H, Ellis BE (1992) Induction of rosmarinic acid biosynthesis in Lithospermum erythrorhizon cell suspension cultures by yeast extract. Plant Cell Rep 11(9), 480-483.
Mohammadabadi MR (2019) Expression of calpastatin gene in Raini Cashmere goat using Real-Time PCR. Agric Biotechnol J 11, 219-235.
Mohammadabadi MR, Asadollahpour Nanaei H (2021) Leptin gene expression in Raini Cashmere goat using Real-Time PCR. Agric Biotechnol J 13, 197-214.
Mohammadabadi MR, Kord M, Nazari M (2018) Studying expression of leptin gene in different tissues of Kermani Sheep using Real Time PCR. Agric Biotechnol J 10, 111-122.
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(2), 104-111.
Munns R (2013) Hoagland’s nutrient solution. (https://prometheusprotocols.net/experimental-design-and-analysis/experimental-treatments/salinity/hoaglands-nutrient-solution/).
Nasiri-Bezenjani MA, Riahi-Madvar A, Baghizadeh A, Ahmadi AR (2014) Rosmarinic acid production and expression of tyrosine aminotransferase gene in Melissa officinalis seedlings in response to yeast extract. J Agric Sci Technol 16(4), 921-930.
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.
Oloumi H, Soltaninejad R, Baghizadeh A (2015) The comparative effects of nano and bulk size particles of CuO and ZnO on glycyrrhizin and phenolic compounds contents in Glycyrrhiza glabra L. seedlings. Indian J Plant Physiol 20(2), 157-161.
Pacheco I, Buzea C (2018) Nanoparticle uptake by plants: beneficial or detrimental?. In Phytotoxicity of nanoparticles pp. 1-61.
Petersen M (2013) Rosmarinic acid: new aspects. Phytochem Rev 12(1), 207-227.
Petersen M, Häusler E, Karwatzki B, Meinhard J (1993) Proposed biosynthetic pathway for rosmarinic acid in cell cultures of Coleus blumei Benth. Planta 189(1), 10-14.
Petersen M, Abdullah Y, Benner J et al. (2009) Evolution of rosmarinic acid biosynthesis. Phytochemistry 70(15-16), 1663-1679.
Pezeshki S, Petersen M (2018) Rosmarinic acid and related metabolites. Biotechnology of Natural Products pp. 25-60.
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9), e36-e36.
Rastogi A (2019) Industrial nanoparticles and their influence on gene expression in plants. In Nanomaterials in plants, algae and microorganisms. Academic Press pp. 89-101.
Rastogi A, Zivcak M, Sytar O et al. (2017) Impact of metal and metal oxide nanoparticles on plant: a critical review. Front Chem 5, 78.
Rico CM, Majumdar S, Duarte-Gardea M et al. (2011). Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric Food Chem 59(8), 3485-3498.
Rui M, Ma C, Hao Y, et al. (2016) Iron oxide nanoparticles as a potential iron fertilizer for peanut (Arachis hypogaea). Front Plant Sci 7, 815.
Sahu R, Gangopadhyay M, Dewanjee S (2013) Elicitor-induced rosmarinic acid accumulation and secondary metabolism enzyme activities in Solenostemon scutellarioides. Acta Physiol Plant 35(5), 1473-1481.
Saraydin SU, Tuncer E, Tepe B et al. (2012) Antitumoral effects of Melissa officinalis on breast cancer in vitro and in vivo. Asian Pac J Cancer Prev 13(6), 2765-2770.
Sari AO, Ceylan A (2002) Yield characteristics and essential oil composition of lemon balm (Melissa officinalis L.) grown in the Aegean region of Turkey. Turk J Agric For 26(4), 217-224.
Shahsavari M, Mohammadabadi M, Khezri A, et al. (2021) Correlation between insulin-like growth factor 1 gene expression and fennel (Foeniculum vulgare) seed powder consumption in muscle of sheep. Anim Biotechnol 34, 1-11.
Sharafi E, Fotokian MH, Loo H (2013) Improvement of hypericin and hyperforin production using zinc and iron nano-oxides as elicitors in cell suspension culture of John’swort (Hypericum perforatum L). J Medicinal Plants By-products 2(2), 177-184.
Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14 (1), 43e50.
Shaw AK, Ghosh S, Kalaji HM et al. (2014) Nano-CuO stress induced modulation of antioxidative defense and photosynthetic performance of syrian barley (Hordeum vulgare L.). Environ Exp Bot 102, 37e47.
Siddiqui MH, Al-Whaibi MH, Firoz M, Al-Khaishany MY (2015) Role of nanoparticles in plants. Nanotechnology and plant sciences pp. 19-35.
Smetanska I (2008) Production of secondary metabolites using plant cell cultures. Food Biotechnol 111, 187-228.
Song G, Hou W, Gao Y et al. (2016) Effects of CuO nanoparticles on Lemna minor. Bot Stud 57, 3.
Taheri A, Pourseyedi S, Lohrasbi-Nejad A (2018) Green biosynthesis of magnetic iron oxide (Fe3O4) nanoparticles using leaf extract of Melissa officinalis L. Second National Conference on Nanostructures, Science and Nanotechnology. Feb. 14, 2018. Kashan, Iran (In persian).
Usman M, Farooq M, Wakeel A et al. (2020) Nanotechnology in agriculture: current status, challenges and future opportunities. Sci Total Environ 721,137778.
Wang HH, Kou XM, Pei ZG et al (2011) Physiological effects of magnetite (Fe3O4) nanoparticles on perennial ryegrass (Lolium perenne L.) and pumpkin (Cucurbita mixta) plants. Nanotoxicology 5, 30–42.
Wang J, Koo Y, Alexander A et al. (2013) Phytostimulation of poplars and Arabidopsis exposed to silver nanoparticles and Ag+ at sublethal concentrations. Environ Sci Technol 47, 5442–5449.
Xing B, Yang D, Guo W et al. (2014) Ag+ as a more effective elicitor for production of tanshinones than phenolic acids in Salvia miltiorrhiza hairy roots. Molecules 20(1), 309-324.
Yan Q, Shi M, Ng J, Wu JY (2006) Elicitor-induced rosmarinic acid accumulation and secondary metabolism enzyme activities in Salvia miltiorrhiza hairy roots. Plant Sci 170(4), 853-858.
Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23(4), 283-333.
Zhu H, Han J, Xiao JQ et al (2008) Uptake, translocation, and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. J Environ Monit 10, 713–717.
Zhu K, Ju Y, Xu J et al. (2018) Magnetic nanomaterials: Chemical design, synthesis, and potential applications. Chem Res 51, 404–413.