The effect of zinc oxide nanoparticles on the growth and development of Stevia plants cultured in vitro

Anna Krzepiłko

Department of Biotechnology, Microbiology and Human Nutrition, Faculty of Food Sciences and Biotechnology, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland
https://orcid.org/0000-0001-9409-9897

Roman Prażak

Institute of Plant Genetics, Breeding and Biotechnology, University of Life Sciences in Lublin, University of Life Sciences in Lublin, Akademicka 15, 20-950 Lublin, Poland
https://orcid.org/0000-0002-6920-1017

Katarzyna Matyszczuk

Department of Biotechnology, Microbiology and Human Nutrition, Faculty of Food Sciences and Biotechnology, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland
https://orcid.org/0000-0003-2085-0574

Magdalena Dyduch-Siemińska

Institute of Plant Genetics, Breeding and Biotechnology, University of Life Sciences in Lublin, University of Life Sciences in Lublin, Akademicka 15, 20-950 Lublin, Poland
https://orcid.org/0000-0002-6549-7391


Abstrakt

Stevia (Stevia rebaudiana Bertoni) is an essential herbal plant used as a sweetener. The demand for stevia is growing due to its low caloric and medicinal value, hence the need for a more thorough investigation of its nutritional and biological properties. Nanoparticles of metal oxides have been found to have broad applications in agriculture for the stimulation of plant growth and development. The study aimed to assess the effect of various zinc oxide nanoparticles (ZnONPs) concentrations on stevia plants’ quantitative and qualitative traits obtained in in vitro cultures. Micropropagation of two stevia varieties, Candy and Morita, was carried out using explants of shoot tips placed on MS medium supplemented with 1.0 mg dm–3 BA and 0.1 mg dm–3 IBA and with ZnONPs at concentrations of 0 (control), 10, 20, 30 and 40 mg dm–3. The obtained results indicated that high concentrations of ZnONPs stimulated the propagation of shoots. On the other hand, they negatively influenced shoot length, root number and length, and the fresh weight of the plantlets. The presence of zinc oxide nanoparticles in the medium increased the potassium, calcium, magnesium, and zinc content while decreasing the sodium and iron content in the regenerated stevia plantlets. The total phenolic content in the Candy variety was higher in the treatments with ZnONPs than in the control plants, while it was varied in the Morita variety. In both varieties, total antioxidant content measured by the ABTS method showed significantly higher in the treatments with 20–30 mg dm–3 ZnONPs than in the control. The content of chlorophyll a, chlorophyll b and chlorophyll a + b in the Morita variety was higher in the treatments with 10 and 20 mg dm–3 ZnONPs than in the control. On the other hand, high concentrations of ZnONPs negatively affected the content of carotenoids in both varieties. The study showed that stevia plants obtained in in vitro cultures on control media and media containing ZnONPs had a high content of valuable minerals, phytocompounds with antioxidant properties, and photosynthetic pigments.

Słowa kluczowe:

ZnONPs, Stevia rebaudiana Bertoni, in vitro culture, photosynthetic pigments, antioxidants, content of metals

Adhikari, S., Adhikari, A., Ghosh, S., Roy, D., Azahar, I., Basuli, D., Hossain, Z. (2020). Assessment of ZnONPs toxicity in maize: An integrative microRNAomic approach. Chemosphere, 249, 126197. https://doi.org/10.1016/j.chemosphere.2020.126197 DOI: https://doi.org/10.1016/j.chemosphere.2020.126197

Al-Taweel, S.K., Azzam, C.R., Khaled, K.A., Abdel-Aziz, R.M. (2021). Improvement of stevia (Stevia rebaudiana Bertoni) and steviol glycoside through traditional breeding and biotechnological approaches. SABRAO J. Breed. Genet., 53(1), 88–111

Alharby, H.F., Metwali, E.M.R., Fuller, M.P., Aldhebiani, A.Y. (2016). Impact of application of zinc oxide nanoparticles on callus induction, plant regeneration, element content, and antioxidant enzyme activity in tomato (Solanum lycopersicum MILL) under salt stress. Acta Sci. Biol. Sci., 68, 723–735. https://doi.org/10.2298/ABS151105017A DOI: https://doi.org/10.2298/ABS151105017A

Al-Mayahi, A.M.W. (2021). The effect of humic acid (HA) and zinc oxide nanoparticles (ZnONPs) on in vitro regeneration of date palm (Phoenix dactylifera L.) cv. Quntar. Plant Cell Tiss. Organ Cult., 145, 445–456. https://doi.org/10.1007/s11240-021-02020-7 DOI: https://doi.org/10.1007/s11240-021-02020-7

Awad, K.M., Al-Mayahi, A.M.W., Mahdi, M.A., Al-Asadi, A.S.M., Abas, M.H. (2020). In vitro assessment of ZnO nanoparticles on Phoenix dactylifera L. micropropagation. Basic Appl. Sci., 21(1), 149–160. https://doi.org/10.37575/b/agr/2000 DOI: https://doi.org/10.37575/b/agr/2000

Bagheri, H., Hashemabadi, D., Pasban Eslam, B., Sedaghathoor, S. (2023). Effects of zinc-nanooxide, salicylic acid, and sodium nitroprusside on physiological properties, antioxidant enzyme activities, and secondary metabolites of Viola odorata under drought stress. Acta Sci. Pol. Hortorum Cultus, 22(6), 29–41. https://doi.org/10.24326/asphc.2023.4778 DOI: https://doi.org/10.24326/asphc.2023.4778

Befa, A., Gebre, A., Bekele, T. (2020). Evaluation of dried stevia (Stevia rebaudiana Bertoni) leaf and its infusion nutritional profile. Int. J. Med. Aromat. Plants, 9(6), 360. https://doi.org/10.35248/2167-0412.20.9.360 DOI: https://doi.org/10.23880/fsnt-16000270

Devasia, J., Muniswamy, B., Mishra, M.K. (2020). Investigation of ZnO nanoparticles on in vitro cultures of coffee (Coffea arabica L.). Int. J. Nanosci. Nanotechnol., 16, 271–277.

Doliński, R., Kowalczyk, K. (2019). Fast direct regeneration of plants from nodal explants of Stevia rebaudiana Bert. Acta Sci. Pol. Hortorum Cultus., 18(5), 95–103. https://doi.org/10.24326/asphc.2019.5.9 DOI: https://doi.org/10.24326/asphc.2019.5.9

Doliński, R., Jabłońska, E. 2015. Mikrorozmnażanie stewii (Stevia rebaudiana Bertoni) z eksplantatów węzłowych izolowanych z roślin wytworzonych in vitro [Micropropagation of stevia (Stevia rebaudiana Bert.) through node explants isolated from in vitro produced plants]. Agron. Sci., 70(4), 13–24. https://doi.org/10.24326/as.2015.4.2 DOI: https://doi.org/10.24326/as.2015.4.2

Dyduch-Siemińska, M., Najda, A., Gawroński, J., Balant, S., Świca, K., Żaba, A. (2020). Stevia rebaudiana Bertoni, a source of high-potency natural sweetener: Biochemical and genetic characterization. Molecules, 25(4), 767. https://doi.org/10.3390/molecules25040767 DOI: https://doi.org/10.3390/molecules25040767

Dyduch-Siemińska, M. (2021). A fast and effective protocol for obtaining genetically diverse stevia (Stevia rebaudiana Bertoni) regenerants through indirect organogenesis. Agron. Sci., 76(4), 47–63. https://doi.org/10.24326/as.2021.4.4 DOI: https://doi.org/10.24326/as.2021.4.4

El-Tohamy, W.A., Khalid, A.Kh., El-Abagy, H.M., Abou-Hussein, S.D. (2009). Essential oil, growth and yield of onion (Allium cepa L.) in response to foliar application of some micronutrients. Austral. J. Basic Appl. Sci., 3(1), 201–205.

Erenoglu, B., Nikolic, M., Romheld, V., Cakmak, I. (2002). Uptake and transport of foliar applied zinc (65Zn) in bread and durum wheat cultivars differing in zinc efficiency. Plant Soil, 241, 251–257. https://doi.org/10.1023/A:1016148925918 DOI: https://doi.org/10.1023/A:1016148925918

Galo, E.V. (2019). In vitro propagation of Stevia rebaudiana (Bert.) using different media and explant. Ciencia, 38, 77–85. Available: www.wmsu.edu.ph/research_journal [10 July 2017].

Gantait, S., Das, A., Mandal, N. (2015). Stevia: a comprehensive review on ethnopharmacological properties and in vitro regeneration. Sugar Tech., 17, 95–106. https://doi.org/10.1007/s12355-014-0316-3 DOI: https://doi.org/10.1007/s12355-014-0316-3

Gerdzihiova, M., Pavlov, D., Grozeva, N., Tzanova, M., Dimanov, D., Terziewa, S., Krastanov, J. (2018). Chemical composition content in vitro gas production and relative feed value of Stevia rebaudiana Bertoni. Bulg. J. Agric. Sci., 24 (Suppl. 1), 40–46.

Gęsiński, K., Majcherczak, E., Gozdecka, G. (2013). Stevia (Stevia rebaudiana Bertoni) as a source of selected microelements. Inż. Aparat. Chem., 52(2), 74–75.

Gharpure, S., Ankamwar, B. (2020). Synthesis and antimicrobial properties of zinc oxide nanoparticles. J. Nanosci. Nanotechnol., 20(10), 5977–5996. https://doi.org/10.1166/jnn.2020.18707 DOI: https://doi.org/10.1166/jnn.2020.18707

Hayat, F., Khanum, F., Li, J., Iqbal, S., Khan, U., Javed, H.U., Razzaq, M.K., Peng, Y., Ma, X., Li, C., Tu, P., Chen, J., Altaf, M.A. (2023). Nanoparticles and their potential role in plant adaptation to abiotic stress in horticultural crops. Sci. Hortic., 321, 112285. https://doi.org/10.1016/j.scienta.2023.112285 DOI: https://doi.org/10.1016/j.scienta.2023.112285

Hajiboland, R., Amirazad, F. (2010). Growth, photosynthesis and antioxidant defense system in Zn-deficient red cabbage plants. Plant Soil Environ., 56(5), 209–217. https://doi.org/10.17221/207/2009-PSE DOI: https://doi.org/10.17221/207/2009-PSE

Haslett, B.S., Reid, R.J., Rengel, Z. (2001). Zinc mobility in wheat: Uptake and distribution of zinc applied to leaves or roots. Ann. Bot., 87(3), 379–386. https://doi.org/10.1006/anbo.2000.1349 DOI: https://doi.org/10.1006/anbo.2000.1349

Hassan, M.U., Aamer, M., Chattha, M.U., Haiying, T., Shahzad, B., Barbanti, L., Nawaz, M., Rasheed, A., Afzal, A., Liu, Y., Guogin, H. (2020). The critical role of zinc in plants facing the drought stress. Agriculture, 10(9), 396. https://doi.org/10.3390/agriculture10090396 DOI: https://doi.org/10.3390/agriculture10090396

Javed, R., Yucesan, B., Zia, M., Ekrem, G. (2018). Elicitation of secondary metabolites in callus cultures of Stevia rebaudiana Bertoni grown under ZnO and CuO nanoparticles stress. Sugar Tech, 20(2), 194–201. https://doi.org/10.1007/s12355-017-0539-1 DOI: https://doi.org/10.1007/s12355-017-0539-1

Karimi, N., Behbahani, M., Dini, G., Razmjou, A. (2018). Enhancing the secondary metabolite and anticancer activity of Echinacea purpurea callus extracts by treatment with biosynthesized ZnO nanoparticles. Adv. Nat. Sci. Nanosci. Nanotechnol., 9, 045009. https://doi.org/10.1088/2043-6254/aaf1af DOI: https://doi.org/10.1088/2043-6254/aaf1af

Kumari, M., Khan, S.S., Pakrashi, S., Mukherjee, A., Chandrasekaran, N. (2011). Cytogenetic and genotoxic effects of zinc oxide nanoparticles on root cells of Allium cepa. J. Hazard. Mater., 190(1–3), 613–621. https://doi.org/10.1016/j.jhazmat.2011.03.095 DOI: https://doi.org/10.1016/j.jhazmat.2011.03.095

Lee, C.W., Mahendra, S., Zodrow, K., Li, D., Tsai, Y.C., Braam, J., Alvarez, P.J. (2010). Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ. Toxicol. Chem., 29(3), 669–675. https://doi.org/10.1002/etc.58 DOI: https://doi.org/10.1002/etc.58

Lichtenthaler, H.K., Wellburn, A.R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans., 11, 591–592. https://doi.org/10.1042/bst0110591 DOI: https://doi.org/10.1042/bst0110591

Lin, D., Xing, B. (2007). Phytotoxicity of nanoparticles: Inhibition of seed germination and root growth. Environ. Pollut., 150(2), 243–250. https://doi.org/10.1016/j.envpol.2007.01.016 DOI: https://doi.org/10.1016/j.envpol.2007.01.016

Murashige, T., Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol., 15, 473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x DOI: https://doi.org/10.1111/j.1399-3054.1962.tb08052.x

Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med., 26, 1231–1237. https://doi.org/10.1016/s0891-5849(98)00315-3 DOI: https://doi.org/10.1016/S0891-5849(98)00315-3

Rehman, F. U., Paker, N.P., Khan, M., Zainab, N., Ali, N., Munis, M.F.H., Chaudhary, H.J. (2023). Assessment of application of ZnO nanoparticles on physiological profile, root architecture, and antioxidant potential of Solanum lycopersicum. Biocatal. Agric. Biotechnol. 53, 102874. https://doi.org/10.1016/j.bcab.2023.102874 DOI: https://doi.org/10.1016/j.bcab.2023.102874

Riesen, O., Feller, U. (2005). Redistribution of nickel, cobalt, manganese, zinc, and cadmium via the phloem in young and maturing wheat. J. Plant Nutr., 28(3), 421–430. https://doi.org/10.1081/PLN-200049153 DOI: https://doi.org/10.1081/PLN-200049153

Rokosa, M.T., Kulpa, D. (2019). Micropropagation of Stevia rebaudiana plants. Ciência Rural, 50, e20181029. https://doi.org/10.1590/0103-8478cr20181029 DOI: https://doi.org/10.1590/0103-8478cr20181029

Rosales, C., Brenes, J., Salas, K., Arce-Solano, S., Abdelnour-Esquivel, A. (2018). Micropropagation of Stevia rebaudiana in the temporary immersion systems as an alternative horticultural production method. Rev. Chapingo Ser. Hortic., 24(1), 69–78. https://doi.org/10.5154/r.rchsh.2017.08.028 DOI: https://doi.org/10.5154/r.rchsh.2017.08.028

Samuel, P., Ayoob, K.T., Magnuson, B.A., Wölwer-Rieck, U., Jeppesen, P.B., Rogers, P.J., Rowland, I., Mathews, R. (2018). Stevia leaf to stevia sweetener. Exploring its science, benefits, and future potential. J. Nutr., 148(7), 1186S–1205S. https://doi.org/10.1093/jn/nxy102 DOI: https://doi.org/10.1093/jn/nxy102

Shahnawaz Pandey D.K., Konjengbam M., Dwivedi ., Kaur P., Kumar V., Dey A. (2021). Biotechnological interventions of in vitro propagation and production of valuable secondary metabolites in Stevia rebaudiana. Appl. Microbiol. Biotechnol., 1–22. https://doi.org/10.1007/s00253-021-11580-9 DOI: https://doi.org/10.1007/s00253-021-11580-9

Sheikhalipour, M., Esmaielpour, B., Gohari, G., Haghighi, M., Jafari, H., Farhadi, H., Kulak, M., Kalisz, A. (2021). Salt stress mitigation via the foliar application of chitosan-functionalized selenium and anatase titanium dioxide nanoparticles in stevia (Stevia rebaudiana Bertoni). Molecules, 26(13), 4090, https://doi.org/10.3390/molecules26134090 DOI: https://doi.org/10.3390/molecules26134090

Schaff, G., Ludwig, U., Erenoglu, B.E., Mori, S., Kitahara, T., von Wirén, N. (2004). ZmYS1 functions as a proton-coupled symporter for phytosiderophore-and nicotianamine-chelated metals. J. Biol. Chem., 279(10), 9091–9096. https://doi.org/10.1074/jbc.M311799200 DOI: https://doi.org/10.1074/jbc.M311799200

Shafique, N., Jabeen, K.S., Ahmad, S., Irum, S., Anwaar, N., Ahmad, S., Alam, M., Ilyas, T.F., Khan, S.Z., Hussain, S. (2020). Green fabricated zinc oxide nanoformulated media enhanced callus induction and regeneration dynamics of Panicum virgatum L. PLoS One, 15, e0230464. https://doi.org/10.1371/journal.pone.0230464 DOI: https://doi.org/10.1371/journal.pone.0230464

Singleton, V.L., Orthofer, R., Lamuela-Raventos, R.M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Meth. Enzymol., 299, 152–178. https://doi.org/10.1016/S0076-6879(99)99017-1 DOI: https://doi.org/10.1016/S0076-6879(99)99017-1

Singh, S., Garg, V., Yadav, D., Beg, M., Sharma, N. (2012). In vitro antioxidative and antibacterial activities of various parts of Stevia rebaudiana (Bertoni). Int. J. Pharm. Pharm. Sci., 4(3), 468–473.

Sorahinobar, M., Deldari, T., Bokaeei, Z.N., Mehdinia, A. (2023). Effect of zinc nanoparticles on the growth and biofortification capability of mungbean (Vigna radiata) seedlings. Biologia, 78, 951–960. https://doi.org/10.1007/s11756-022-01269-3 DOI: https://doi.org/10.1007/s11756-022-01269-3

Sun, Z., Xiong, T., Zhang, T., Wang, N., Chen, D., Li, S. (2019). Influences of zinc oxide nanoparticles on Allium cepa root cells and the primary cause of phytotoxicity. Ecotoxicology, 28, 175–188. https://doi.org/10.1007/s10646-018-2010-9 DOI: https://doi.org/10.1007/s10646-018-2010-9

Taheri, M., Mousavi, M., Mortazavi, S.M.H. (2024). Different reactions of olive explants in response to zinc oxide nanoparticles and zinc sulfate under in vitro conditions. Int. J. Hortic. Sci., 11(1), 107–124. https://doi.org/10.22059/ijhst.2023.360354.647

Thiyagarajan, M., Venkatachalam, P. (2012) Large scale in vitro propagation of Stevia rebaudiana (Bert) for commercial application: Pharmaceutically important and antidiabetic medicinal herb. Ind. Crops Prod., 7(1), 111–117. https://doi.org/10.1016/j.indcrop.2011.10.037 DOI: https://doi.org/10.1016/j.indcrop.2011.10.037

Topdemir, A., Buran, A. (2023). Determination of antioxidant activity and phenolic and flavonoid content of Ocimum basilicum L. callus cultures obtained by different plant growth regulators. Acta Sci. Pol. Hortorum Cultus, 22(2), 133–149. https://doi.org/10.24326/asphc.2023.1661 DOI: https://doi.org/10.24326/asphc.2023.1661

Tymoszuk, A., Sławkowska, N., Szałaj, U., Kulus, D., Antkowiak, M., Wojnarowicz, J. (2022). Synthesis, characteristics, and effect of zinc oxide and silver nanoparticles on the in vitro regeneration and biochemical profile of Chrysanthemum adventitious shoots. Materials, 15(22), 8192. https://doi.org/10.3390/ma15228192 DOI: https://doi.org/10.3390/ma15228192

Tymoszuk, A., Wojnarowicz, J. (2020). Zinc oxide and zinc oxide nanoparticles impact on in vitro germination and seedling growth in Allium cepa L. Materials, 13(12), 2784. https://doi.org/10.3390/ma13122784 DOI: https://doi.org/10.3390/ma13122784

Venkatachalam, P., Priyanka, N., Manikandan, K., Ganeshbabu, I., Indiraarulselvi, P., Geetha, N., Muralikrishna, K., Bhattacharya, R.C., Tiwari, M., Sharma, N., Sahi, S.V. (2017). Enhanced plant growth promoting role of phycomolecules coated zinc oxide nanoparticles with P supplementation in cotton (Gossypium hirsutum L.). Plant Physiol. Biochem., 110, 118–127. https://doi.org/10.1016/j.plaphy.2016.09.004 DOI: https://doi.org/10.1016/j.plaphy.2016.09.004

Wang, P., Menzies, N.W., Lombi, E., McKenna, B.A., Johannessen, B., Glover C.J., Kappen, P., Kopittke, P.M. (2013). Fate of ZnO nanoparticles in soils and cowpea (Vigna unguiculata). Environ. Sci. Technol., 47(23), 13822–13830. https://doi.org/10.1021/es403466p DOI: https://doi.org/10.1021/es403466p

Yeşil-Çeliktaş, O., Nartop, P., Gürel, A., Bedir, E., Vardar-Sukan, F. (2007). Determination of phenolic content and antioxidant activity of extracts obtained from Rosmarinus officinalis Cali. J. Plant Physiol., 164(11), 1536–1542. https://doi.org/10.1016/j.jplph.2007.05.013 DOI: https://doi.org/10.1016/j.jplph.2007.05.013


Opublikowane
2024-06-28



Anna Krzepiłko 
Department of Biotechnology, Microbiology and Human Nutrition, Faculty of Food Sciences and Biotechnology, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland https://orcid.org/0000-0001-9409-9897
Roman Prażak 
Institute of Plant Genetics, Breeding and Biotechnology, University of Life Sciences in Lublin, University of Life Sciences in Lublin, Akademicka 15, 20-950 Lublin, Poland https://orcid.org/0000-0002-6920-1017
Katarzyna Matyszczuk 
Department of Biotechnology, Microbiology and Human Nutrition, Faculty of Food Sciences and Biotechnology, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland https://orcid.org/0000-0003-2085-0574
Magdalena Dyduch-Siemińska 
Institute of Plant Genetics, Breeding and Biotechnology, University of Life Sciences in Lublin, University of Life Sciences in Lublin, Akademicka 15, 20-950 Lublin, Poland https://orcid.org/0000-0002-6549-7391



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