Abstract
Gerbera represents a valuable commodity in the global cut flower industry. However, commercial production is hampered by low propagation rates using conventional methods. Hence, the current contribution investigated the application of silver nanoparticles (AgNPs: Argovit™) in temporary immersion bioreactors to promote plant growth. The results showed that AgNPs at the tested concentrations displayed minimal promotive effects in terms of biomass accumulation (with the highest biomass recorded in control plants and those exposed to 25.0 mg L−1 AgNP) and resulted in a reduction in the levels of iron and molybdenum in treated plants. Interesting results testing 50.0 mg L−1 AgNPs yielded plants with elevated levels of chlorophylls a and b and total chlorophyll compared with control plants. This effect was similarly observed in the levels of free and cell wall bound phenolics which were present at more than a two-fold higher concentration in AgNP-treated plants (329.00 to 482.10 Trolox equivalents (TE) g−1 DW) than in control plants (154.02 TE g−1 DW). The trends observed indicated a hormetic response in terms of the biochemical indicators assessed where elicitation occurred between 50 and 75 mg L−1 AgNP and inhibition at 100.0 mg L−1. This hormetic effect of AgNPs was also observed in the antioxidant capacity of phenolics. It is proposed that the accumulation of the abovementioned biochemical compounds is indicative of a stress response elicited by the AgNPs that is mediated through the secondary metabolite biosynthetic pathway. It was further shown that this response displayed a classic hormetic effect. Future work will further investigate this interesting outcome which will be valuable in the context of biotic and abiotic stress research.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author (ME) upon reasonable request.
References
Abdul-Sahib AM, Golbashy M, Abbass J (2023) Effect of date palm wastes, perlite and magnesium on growth and flowering in gerbera plants (Gerbera jamesonii L.). Int J Horticult Sci Technol 10:375–386
Akter N, Hoque M, Sarker R (2012) In vitro propagation in three varieties of gerbera (Gerbera jamesonii Bolus.) from flower bud and flower stalk explants. Plant Tiss Cult Biotechnol 22:143–152
Akter N, Sarkar S, Hasan N, Rahman SM, Sarkar MAR (2022) Development of in vitro mass propagation protocol for gerbera (Gerbera jamesonii Bolus) var Orange. Plant Tiss Cult Biotechnol 32:217–226
Alcántar-González G, Sandoval-Villa M (1999) Procedimientos analíticos. In: Alcántar-González G, Sandoval-Villa M (eds) Manual de Análisis Químicos de Tejido Vegetal. Sociedad Mexicana de la Ciencia del Suelo, AC México D F:40-42
Alp FN, Arikan B, Ozfidan-Konakci C, Gulenturk C, Yildiztugay E, Turan M, Cavusoglu H (2023) Hormetic activation of nano-sized rare earth element terbium on growth, PSII photochemistry, antioxidant status and phytohormone regulation in Lemna minor. Plant Physiol Biochem 194:361–373
Anand M, Sankari A, Arulmozhiyan R (2013) Evaluation of commercial cultivars of cut gerbera (Gerbera jamesonii Bolus ex Hooker F.) under polyhouse in Shevaroy condition of Eastern Ghats. J Horticult Sci 8:199–203
Andújar I, González M, García-Ramos JC, Hajari E, Bogdanchikova N, Pestryakov A, Concepción O, Lorenzo JC, Escalona M (2023) Are silver nanoparticles the “silver bullet” to promote diterpene production in Stevia rebaudiana? Plant Cell Tiss Org Cult. https://doi.org/10.1007/s11240-023-02450-5
Andújar I, González N, García-Ramos JC, Bogdanchikova N, Pestryakov A, Escalona M, Concepción O (2020) Argovit™ silver nanoparticles reduce contamination levels and improve morphological growth in the in vitro culture of Psidium friedrichsthalianum (O. Berg) Nied. SN Appl Sci 2:1–9
Aqeel M, Khalid N, Nazir A, Irshad MK, Hakami O, Basahi MA, Alamri S, Hashem M, Noman A (2023) Foliar application of silver nanoparticles mitigated nutritional and biochemical perturbations in chilli pepper fertigated with domestic wastewater. Plant Physiol Biochem 194:470–479
Asgari-Targhi G, Iranbakhsh A, Ardebili ZO, Tooski AH (2021) Synthesis and characterization of chitosan encapsulated zinc oxide (ZnO) nanocomposite and its biological assessment in pepper (Capsicum annuum) as an elicitor for in vitro tissue culture applications. Int J Biol Macromol 189:170–182
Baghele R, Pusdekar M (2022) Evaluation of gerbera (Gerbera jamesonii L.) cultivars grown under fan and pad cooled polyhouse conditions. The Pharma Innovat Int J 11:647–650
Barooah L, Talukdar MC (2009) Evaluation of different gerbera (Gerbera jamessonii Bolus ex Hooker F.) cultivars under agro climatic conditions of Jorhat. Assam. J Ornam Horticult 12:106–110
Barreto MR, Aleixo NA, Silvestre RB, Fregonezi NF, Barud HS, Dias DS, Ribeiro CA, Resende FA (2020) Genotoxicological safety assessment of puree-only edible films from onion bulb (Allium cepa L.) for use in food packaging-related applications. J Food Sci 85:201–208
Bello-Bello JJ, Castillo JLS (2023) Utilización de nanopartículas de plata en la micropropagación de plantas. Mundo Nano Revista Interdisciplinaria en Nanociencias y Nanotecnología 16:1e–14e
Bello-Bello JJ, Chavez-Santoscoy RA, Lecona-Guzman CA, Bogdanchikova N, Salinas-Ruíz J, Gomez-Merino FC, Pestryakov A (2017) Hormetic response by silver nanoparticles on in vitro multiplication of sugarcane (Saccharum spp. Cv. Mex 69-290) using a temporary immersion system. Dose-Response 15:1559325817744945
Bello-Bello JJ, Spinoso-Castillo JL, Arano-Avalos S, Martínez-Estrada E, Arellano-García ME, Pestryakov A, Toledano-Magaña Y, García-Ramos JC, Bogdanchikova N (2018) Cytotoxic, genotoxic, and polymorphism effects on Vanilla planifolia Jacks ex Andrews after long-term exposure to Argovit® silver nanoparticles. Nanomaterials 8:754
Ben Y, Cheng M, Liu Y, Wang L, Yang Q, Huang X, Zhou Q (2023) The stimulatory effect and mechanism of low-dose lanthanum on soybean leaf cells. J Hazard Mat 441:129924
Bernela M, Seth M, Kaur N, Sharma S, Pati PK (2023) Harnessing the potential of nanobiotechnology in medicinal plants. Ind Crops Prod 194:116266
Bhatia R, Singh K, Sharma T, Jhang T (2011) Evaluation of the genetic fidelity of in vitro-propagated gerbera (Gerbera jamesonii Bolus) using DNA-based markers. Plant Cell Tiss Org Cult 104:131–135
Calabrese EJ, Baldwin LA (2003) Hormesis: the dose-response revolution. Ann Rev Pharmacol Toxicol 43:175–197
Cardoso JC, da Silva JAT (2013) Gerbera micropropagation. Biotechnol Adv 31:1344–1357
Castro-González CG, Sánchez-Segura L, Gómez-Merino FC, Bello-Bello JJ (2019) Exposure of stevia (Stevia rebaudiana B.) to silver nanoparticles in vitro: transport and accumulation. Scient Rep 9:1–10
Chahardoli A, Sharifan H, Karimi N, Kakavand SN (2022) Uptake, translocation, phytotoxicity, and hormetic effects of titanium dioxide nanoparticles (TiO2NPs) in Nigella arvensis L. Sci The Total Environ 806:151222
Chopra L (2023) Photo-degradation of dyes and drugs using aloe vera synthesized zinc oxide nanoparticles–a review. Mat Today Proceed 72:1613–1617
Chung I-M, 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 9:2165
Cioć M, Kalisz A, Żupnik M, Pawłowska B (2019) Different LED light intensities and 6-benzyladenine concentrations in relation to shoot development, leaf architecture, and photosynthetic pigments of Gerbera jamesonii Bolus in vitro. Agronomy 9:358
Cioć M, Tokarz K, Dziurka M, Pawłowska B (2021) Energy-saving led light affects the efficiency of the photosynthetic apparatus and carbohydrate content in Gerbera jamesonii bolus ex hook. f. axillary shoots multiplied in vitro. Biology 10:1035
de Souza CP, Guedes TA, Fontanetti CS (2016) Evaluation of herbicides action on plant bioindicators by genetic biomarkers: a review. Environ Monit Assessm 188:1–12
Escalona M, Lorenzo JC, González B, Daquinta M, Borroto C, González JL, Desjardines Y (1999) Pineapple micropropagation in temporary immersion systems. Plant Cell Rep 18:743–748. https://doi.org/10.1007/s002990050653
Feizi S (2023) Role of nanomaterials in plant cell and tissue culture. In: Al-Khayri JM, Alnaddaf LM, Jain SM (eds) Nanomaterial interactions with plant cellular mechanisms and macromolecules and agricultural implications. Springer, Cham, pp 359–397. https://doi.org/10.1007/978-3-031-20878-2_14
Frómeta OM, Morgado MME, da Silva JAT, Morgado DTP, Gradaille MAD (2017) In vitro propagation of Gerbera jamesonii Bolus ex Hooker f. in a temporary immersion bioreactor. Plant Cell Tiss Org Cult 129:543–551
Gurr S, McPherson J, Bowles D (1992) Lignin and associated phenolic acids in cell walls. In: Wilkinson DL (ed) Molecular plant pathology. Oxford Press, Oxford, pp 51–56
Harborne J (1973) Chlorophyll extraction. In: Harbone J (ed) Phytochemical methods recommended technique. Chapman and Hall, London, pp 205–207
Hasanin M, Hashem AH, Lashin I, Hassan SA (2021) In vitro improvement and rooting of banana plantlets using antifungal nanocomposite based on myco-synthesized copper oxide nanoparticles and starch. Biomass Conv Bioref. https://doi.org/10.1007/s13399-021-01784-4:1-11
Hasbullah NA, Taha RM, Saleh A, Mahmad N (2012) Irradiation effect on in vitro organogenesis, callus growth and plantlet development of Gerbera jamesonii. Horticult Brasil 30:252–257
Hatano T, Kagawa H, Yasuhara T, Okuda T (1988) Two new flavonoids and other constituents in licorice root: their relative astringency and radical scavenging effects. Chem Pharm Bull 36:2090–2097
Horwitz W (1975) Official methods of analysis Association of Official Analytical Chemists, Washington, DC
Kanwar J, Kumar S (2008) In vitro propagation of gerbera-a review. Hort Sci 35:35–44
Kendig EL, Le HH, Belcher SM (2010) Defining hormesis: evaluation of a complex concentration response phenomenon. Int J Toxicol 29:235–246
Khafri AZ, Zarghami R, Ma’mani L, Ahmadi B (2022) Enhanced efficiency of in vitro rootstock micro-propagation using silica-based nanoparticles and plant growth regulators in myrobalan 29C (Prunus cerasifera L.). J Plant Grow Reg 42:1457–1471
Khalili S, Niazian M, Arab M, Norouzi M (2020) In vitro chromosome doubling of African daisy, Gerbera jamesonii Bolus cv Mini Red. Nucleus 63:59–65
Kirby AJ, Schmidt RJ (1997) The antioxidant activity of Chinese herbs for eczema and of placebo herbs. J Ethnopharmacol 56:103–108
Klimek A, Kletkiewicz H, Siejka A, Wyszkowska J, Maliszewska J, Klimiuk M, Jankowska M, Seckl J, Rogalska J (2022) New view on the impact of the low-frequency electromagnetic field (50 Hz) on stress responses–hormesis effect. Neuroendocrinology 113:423–441
Kolbert Z, Szőllősi R, Rónavári A, Molnár Á (2022) Nanoforms of essential metals: from hormetic phytoeffects to agricultural potential. J Exp Bot 73:1825–1840
Kumar A, Saha SK, Kumar KR, Rakshit D (2022) Study of melting of paraffin dispersed with copper nanoparticles in square cavity subjected to external magnetic field. J Energy Stor 50:104338
Lala S (2020) Enhancement of secondary metabolites in Bacopa monnieri (L.) Pennell plants treated with copper-based nanoparticles in vivo. IET Nanobiotechnol 14:78–85
Leme DM, Marin-Morales MA (2009) Allium cepa test in environmental monitoring: a review on its application. Mut Res/Gen Toxicol Environ Mutag 682:71–81. https://doi.org/10.1016/j.mrrev.2009.06.002
Li C, Lin Y, Li X, Cheng JJ, Yang C (2023) Dynamic hormesis inducing by cupric ions in duckweed systems for swine wastewater treatment: quantification, modelling and mechanisms. Sci Total Environ 866:161411
Lorenzo JC, Yabor L, Medina N, Quintana N, Wells V (2015) Coefficient of variation can identify the most important effects of experimental treatments. Not Bot Horti Agrobo Cluj-Nap 43:287–291. https://doi.org/10.15835/NBHA4319881
Mahajan S, Kadam J, Dhawal P, Barve S, Kakodkar S (2022) Application of silver nanoparticles in in-vitro plant growth and metabolite production: revisiting its scope and feasibility. Plant Cell Tiss Org Cult 150:15–39
Mahanta M, Gantait S, Mukherjee E, Bhattacharyya S (2023) Meta-Topolin-induced mass propagation, acclimatization and cyto-genetic fidelity assessment of gerbera (Gerbera jamesonii Bolus ex Hooker f.). South African J Bot 153:236–245
Majeed S, Saravanan M, Danish M, Zakariya NA, Ibrahim MNM, Rizvi EH, Un NisaAndrabi S, Barabadi H, Mohanta YK, Mostafavi E (2023) Bioengineering of green-synthesized TAT peptide-functionalized silver nanoparticles for apoptotic cell-death mediated therapy of breast adenocarcinoma. Talanta 253:124026
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 5:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nghia LT, Tung HT, Huy NP, Luan VQ, Nhut DT (2017) The effects of silver nanoparticles on growth of Chrysanthemum morifolium Ramat. cv. “Jimba” in different cultural systems. Vietnam J Sci Technol 55:503–503
Parthasarathy V, Nagaraju V (1999) In-vitro propagation in Gerbera jamesonii Bolus. Indian J Horticult 56:82–85
Ramírez-Mosqueda MA, Sánchez-Segura L, Hernández-Valladolid SL, Bello-Bello JJ (2020) Influence of silver nanoparticles on a common contaminant isolated during the establishment of Stevia rebaudiana Bertoni culture. Plant Cell Tiss Org Cult 143:609–618
Rico-Chávez AK, Franco JA, Fernandez-Jaramillo AA, Contreras-Medina LM, Guevara-González RG, Hernandez-Escobedo Q (2022) Machine learning for plant stress modeling: a perspective towards hormesis management. Plants 11:970
Rivero-Montejo SJ, Vargas-Hernandez M, Torres-Pacheco I (2021) Nanoparticles as novel elicitors to improve bioactive compounds in plants. Agriculture 11:134
Sangma SM, Kumar S, Collis J, Momin BC (2017) Performance of gerbera (Gerbera jamesonii Bolus ex Hooker F) cultivars for growth, flowering and yield characters under naturally ventilated polyhouse. J Ornam Horticult 20:108–112
Shah MA, Pirzada BM, Price G, Shibiru AL, Qurashi A (2022) Applications of nanotechnology in smart textile industry: a critical review. J Adv Res 38:55–75
Spinoso-Castillo J, Chavez-Santoscoy R, Bogdanchikova N, Pérez-Sato J, Morales-Ramos V, Bello-Bello J (2017) Antimicrobial and hormetic effects of silver nanoparticles on in vitro regeneration of vanilla (Vanilla planifolia Jacks. ex Andrews) using a temporary immersion system. Plant Cell Tiss Org Cult 129:195–207
Stapulionytė A, Kleizaitė V, Šiukšta R, Žvingila D, Taraškevičius R, Čėsnienė T (2019) Cyto/genotoxicological evaluation of hot spots of soil pollution using Allium bioassays in relation to geochemistry. Mut Res/Gen Toxicol Environ Mutag 842:102–110
Teeri TH, Elomaa P, Kotilainen M, Albert VA (2006) Mining plant diversity: gerbera as a model system for plant developmental and biosynthetic research. BioEssays 28:756–767
Timoteo CO, Paiva R, dos Reis MV, Claro PIC, da Silva DPC, Marconcini JM, de Oliveira JE (2019) Silver nanoparticles in the micropropagation of Campomanesia rufa (O. Berg) Nied. Plant Cell Tiss Org Cult 137:359–368
Tortella G, Pieretti J, Rubilar O, Fernández-Baldo M, Benavides-Mendoza A, Diez M, Seabra A (2022) Silver, copper and copper oxide nanoparticles in the fight against human viruses: progress and perspectives. Crit Rev Biotechnol 42:431–449
Tung HT, Bao HG, Cuong DM, Ngan HTM, Hien VT, Luan VQ, Phuong HTN, Nam NB, Trieu LN, Truong NK (2021) Silver nanoparticles as the sterilant in large-scale micropropagation of chrysanthemum. In Vitro Cell Dev Biol - Plant 57:897–906
Tymoszuk A, Miler N (2019) Silver and gold nanoparticles impact on in vitro adventitious organogenesis in chrysanthemum, gerbera and Cape Primrose. Sci Hort 257:108766
Valenzuela-Salas LM, Girón-Vázquez NG, García-Ramos JC, Torres-Bugarín O, Gómez C, Pestryakov A, Villarreal-Gómez LJ, Toledano-Magaña Y, Bogdanchikova N (2019) Antiproliferative and antitumour effect of nongenotoxic silver nanoparticles on melanoma models. Oxid Med Cell Long 2019. https://doi.org/10.1155/2019/4528241
Vasyukova I, Gusev A, Zakharova O, Baranchikov P, Yevtushenko N (2021) Silver nanoparticles for enhancing the efficiency of micropropagation of gray poplar (Populus × canescens Aiton. Sm.). In: IOP Conference Series: Earth and Environmental Science. IOP Publishing, p 012053
Wang B, Li Z, Sebesta C, Hinojosa DT, Zhang Q, Robinson JT, Bao G, Peterchev AV, Goetz SM (2022) Multichannel power electronics and magnetic nanoparticles for selective thermal magnetogenetics. J Neural Eng 19:026015
Wen H, Shi H, Jiang N, Qiu J, Lin F, Kou Y (2023) Antifungal mechanisms of silver nanoparticles on mycotoxin producing rice false smut fungus. Iscience 26:105763
Winarto B, Yuniarto K, Soehendi R (2020) Young capitulum as important explant in in vitro mass propagation of gerbera (Gerbera jamesonii). Not Sci Biol 12:264–276
Winarto B, Yuniarto K, Wegadara DM (2019) Axillary shoots derived from thin cell layer and adenine sulphate application in in vitro mass propagation of gerbera [Gerbera jamesonii (H. bolus ex bolus f.)]. Not Sci Biol 11:63–76
Zhang Y, Qi G, Yao L, Huang L, Wang J, Gao W (2022) Effects of metal nanoparticles and other preparative materials in the environment on plants: from the perspective of improving secondary metabolites. J Agricult Food Chem 70:916–933
Acknowledgements
This research was supported by the Bioplant Center (University of Ciego de Ávila Máximo Gómez Báez, Cuba); Colegio de Postgraduados (Veracruz, México); Colegio de Postgraduados (Ciudad México, México); Agricultural Research Council-Tropical and Subtropical Crops (South Africa); and Centro de Nanociencias y Nanotecnología (Universidad Nacional Autónoma de México, Mexico).
Author information
Authors and Affiliations
Contributions
OMF, JBB, FCGM, EH, NB, OC, JCL, and ME designed the research; OMF, JBB, and FCGM conducted the experiment; OMF, JBB, EH, NB, JCL, and ME analyzed the data and wrote the paper; and JCL and ME had primary responsibility for the final content. All authors have read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
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
Mosqueda-Frómeta, O., Bello-Bello, J., Gómez-Merino, F.C. et al. Argovit mediates a hormetic response in biochemical indicators in Gerbera jamesonii. In Vitro Cell.Dev.Biol.-Plant 59, 507–515 (2023). https://doi.org/10.1007/s11627-023-10365-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11627-023-10365-1