Abstract
Using nanoparticles in agriculture requires a positive and eco-friendly response and a better understanding of their effects on plant cultures. Micropropagation is a recourse for the mass production and rescue of plant species that uses biotechnological tools in which it is possible to include nanoparticles for different purposes. In this study, zinc oxide nanoparticles (ZNPs) with an average size of 70 nm were biosynthesized with cell-free filtrate (CFF) from Mucor fragilis, the addition of ZNPs to the shoots of Agave salmiana var. Ayoteco, in their multiplication stage, was evaluated. Agave seedlings treated with ZNPs generally showed organogenesis after 20 days, with an optimal production of 18 shoots. Depending on the treatment applied, the combination of NPs and intermediate concentrations of the studied regulators caused a modification of the structures in the shoots and seedlings, mainly in the stomata, without the accumulation of ZnO. The antioxidant activity in shoots and seedlings depended on the stress generated by abiotic agents, such as growth regulators and NPs, to which they were exposed.
Key message
The combination of extracellular biogenic zinc oxide nanoparticles and growth regulators reduced the time required for shoot generation in A. salmiana while simultaneously preventing microbial contamination of the culture medium.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Enquiries about data availability should be directed to the authors.
References
Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Agarwal H, Venkat Kumar S, Rajeshkumar S (2017) A review on green synthesis of zinc oxide nanoparticles- An eco-friendly approach. Resour-Effic Technol 3:406–413. https://doi.org/10.1016/j.reffit.2017.03.002
Alharby HF, Metwali E, Fuller MP, Aldhebian AY (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. Arch Biol Sci 68(4):723–735. https://doi.org/10.2298/ABS151105017A
Al-Qurainy F, Khan S, Alansi S, Nadeem M, Alshameri A, Gaafar AR, Tarroum M, Shaikhaldein HO, Salih AM, Alenezi NA, Alfarraj NS (2021) Impact of phytomediated zinc oxide nanoparticles on growth and oxidative stress response of in vitro raised shoots of ochradenus arabicus. Biomed Res Int 6829806. https://doi.org/10.1155/2021/6829806
Álvarez-Duarte MC, Suárez-Espinosa J, Luna-Cavazos M, Rodríguez-Acosta M (2018) Traditional knowledge, cultivation and use of maguey pulquero in municipalities of Puebla and Tlaxcala. Polibotanica 45:205–222. https://doi.org/10.18387/polibotanica.45.15
Amiri H, Mousavi M, Torahi A (2016) Improving date palm (Phoenix dactyfera L. CV. Estamaran) callogenesis by the use of zinc oxide nanoparticles. J Exp Biol Agric Sci 4(5):556–563. https://doi.org/10.18006/2016.4
Ángeles-Espino A, Valencia-Botin AJ, Virgen-Calleros G, Ramírez-Serrano C, Paredes-Gutierres L, Hurtado-de la Piña S (2012) Micropropagation of agave (Agave tequilana weber. Var. Azul) through axilary buds. Trop Subtrop Agroecosystems 15:693–698. http://dx.doi.org/urn:ISSN:1870-0462-tsaes.v15i3.1355
Awad K, Al-Mayahi W, Mahdi A, Al-Asasi M, Abass AM (2020) In vitro assessment of ZnO nanoparticles on Phoenix dactylifera L. micropropagation. Sci J King Faisal Un. https://doi.org/10.37575/b/agr/2000
Barrales-Fernández C, Monfil-Briones P, Sandoval-Salas F (2018) In vitro induction of Agave salmiana. Sci Technol Innov 1:1–9
Bejines Ramos G, González Eguiarte DR, Rodríguez Mendoza MN, Rodríguez Macías R (2017) Penetration pathways for a foliar fertilizer in Agave tequilana Weber var. Azul Rev Mex Cien Agríc 8(4):985–991
Cassells AC (2012) Pathogen and biological contamination management in plant tissue culture: Phytopathogens, vitro phathogens and vitro pests. Methods Mol Biol 877:57–80. https://doi.org/10.1007/978-1-61779-818-4_6
Cioffi N, Rai M (2012) Nano-Antimicrobials: Progress and prospects. Springer, Germany
Devaisa J, Muniswamy B, Misha MK (2020) Investigation of ZnO nanoparticles on in vitro cultures of coffee (Coffea Arabica L.). Int J Nanosci Nanotechnol 16(4):271–277
Dhindsa RA, Plumb DP, Thorpe TA (1981) Leaf senescence: correlated with increased permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. Exp Bot 32:93–101. https://doi.org/10.1093/jxb/32.1.93
Duhan JS, Kumar R, Kumar N, Kaur P, Nehra SD (2017) Nanotechnology: the new perspective in precision agriculture. Biotechnol Rep 15:11–23. https://doi.org/10.1016/j.btre.2017.03.002
Fakhari S, Jamzad M, Hassan F (2019) Green synthesis of zinc oxide nanoparticles: a comparison. Green Chem Lett Rev 12(1):19–24. https://doi.org/10.1080/17518253.2018.1547925
García Mendoza AJ (2007) The agaves of Mexico. Science 1(87):14–23
García-Aguilar MG (2016) Sociocultural importance of the production process of mezcal in the ejido of San Pedro Chichicasco, Malinalco, Mexico. Textual 67:119–137
Giannopolities CN, Ries SK (1997) Superoxide dismutase. Plant physiol 59:309–314. https://doi.org/10.1104/pp.59.2.309
Gottschalk F, Nowack B (2011) The release of engineered nanomaterials to the environment. J Environ Monit 13(5):1145–1155. https://doi.org/10.1039/C0EM00547A
Gudkov SV, Burmistrov DE, Serov DA, Rebezov MB, Semenova AA, Lisitsyn AB (2021) A Mini Review of Antibacterial Properties of ZnO Nanoparticles. Front Phys 9:641481. https://doi.org/10.3389/fphy.2021.641481
Habib D, Fayyaz M, Zia M (2013) The study of ascorbate peroxidase, catalase and peroxidase during in vitro regeneration of Argyrolobium roseum. Appl Biochem Biotechnol 172:1070–1084. https://doi.org/10.1007/s12010-013-0591-6
Helaly MN, El-Metwally MA, El-Hoseiny H, Samar A, El-Sheery NH (2014) Effect of nanoparticles on biological contamination of in vitro cultures and organogenic regeneration of banana. Aust J Crop Sci 8(4):612–624
Kalpana VN, Kataru BA, Sravini N, Vigneshwari T, Panneerselvam A, Devi Rajeswari V (2018) Biosynthesis of zinc oxide nanoparticles using culture filtrates of Aspergillus niger: antimicrobial textiles and dye degradation studies. Open nano 3:48–55. https://doi.org/10.1016/j.onano.2018.06.001
Kim DH, Gopal J, Sivanesan I (2017) Nanomaterials in plant tissue culture: the disclosed and undisclosed. RSC Adv 7:36492–36505. https://doi.org/10.1039/C7RA07025J
Krishnamoorthy R, Athinarayanan J, Periyasamy VS, Alshuniaber MA, Alshammari G, Hakeem MJ, Ahmed MA, Alshatwi AA (2022) Antibacterial mechanisms of zinc oxide nanoparticle against bacterial food pathogens resistant to beta-lactam antibiotics. Molecules 27(8):2489. https://doi.org/10.3390/molecules27082489
Kulus D (2014) Micropropagation of selected Agave species. PhD Interdisciplinary Journal 1(1):75–84. https://doi.org/10.13140/2.1.1482.6565
Lee W, Kwak J, An Y (2012) Effect of silver nanoparticles in crop plants Phaseolus radiatus and Sorghum bicolor: media effect on phytotoxicity. Chemosphere 86:491–499. https://doi.org/10.1016/j.chemosphere.2011.10.013
Ling AP, Tan KP, Hussein S (2013) Comparative effects of plant growth regulators on leaf and stem explants of Labisia pumila var. Alata. J Zhejiang Univ Sci B 14(7):621–631. https://doi.org/10.1631/jzus.B1200135PMID: 23825148; PMCID: PMC3709067
Méndez-Argüello B, Vera-Reyes I, Mendoza-Mendoza E, García-Cerda LA, Puente-Urbina BA, Lira-Saldívar RH (2016) Growth promotion of Capsicum annuum plants by zinc oxide nanoparticles. Nova Scientia 8:140–156
Miri A, Mahdinejad N, Ebrahimy O, Khatami M, Sarani M (2019) Zinc oxide nanoparticles: biosynthesis, characterization, antifungal and cytotoxic activity. Mater Sci Eng C 104:1–7. https://doi.org/10.1016/j.msec.2019.109981
Mohd Yusof H, Abdul Rahman N, Mohamad R et al (2020) Biosynthesis of zinc oxide nanoparticles by cell-biomass and supernatant of Lactobacillus plantarum TA4 and its antibacterial and biocompatibility properties. Sci Rep 10:19996. https://doi.org/10.1038/s41598-020-76402-w
Mora-López JL, Reyes-Agüero JA, Flores-Flores JL, Peña-Valdivia CB, Aguirre-Rivera JR (2011) Morphological variation and humanization of Agave genus, salmianae section. Agrociencia 45(4):465–477 ISSN 2521–9766
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Acta Physiol Plant 15:473–497
Nava-Cruz NY, Medina-Morales MA, Martínez JL, Rodríguez L, Aguilar C (2014) Agave biotechnology: an overview. Crit Rev Biotechnol 1:1–13. https://doi.org/10.3109/07388551.2014.923813
Pandey AC, Sanjay SS, Yadav RS (2010) Application of ZnO nanoparticles in influencing the growth rate of Cicer arietinum. J Exp Nanosci 5:488–497. https://doi.org/10.1080/17458081003649648
Panwar GS, Guru SK (2012) Influence of gibberellic acid and seed coat removal on the seed germination behavior of Rauwolfia serpentina L. under controlled environment. J Non-Timber For Prod 19:1–4
Pérez-Ramos A, Rodríguez-Ortega A, Nieto-Aquino JC, Callejas-Hernández J, Portillo-Márquez L (2017) Comparison of two Maguey planting systems (Agave salmiana). Universidad Politécnica de F.I. Madero. Edo. Hidalgo. México
Phillips GC, Collins GB (1979) In vitro tissue culture of selected legumes and plant regeneration from callus cultures of red clover. Crop Sci 19:59–64. https://doi.org/10.2135/cropsci1979.0011183X001900010014x
Puente-Garza C, Gutiérrez-Mora A, García-Lara S (2015) Microprogation of Agave salmiana: means to production of antioxidant and bioactive principles. Front Plant Sci 6:1–9. https://doi.org/10.3389/fpls.2015.01026
Ramírez-Tobías HM, Peña-Valdivia CB, Aguirre JR, Reyes-Agüero JA, Sánchez-Urdaneta AB, Valle-Guadarrama S (2011) Seed germination temperatures of eight mexican Agave species with economic importance. Plant Species Biol 27:124–137. https://doi.org/10.1111/j.1442-1984.2011.00341.x
Rodriguez-Garay B, Rodríguez-Domínguez JM (2018) Micropropagation of Agave species. In: Loyola-Vargas V, Ochoa-Alejo N (eds) Plant Cell Culture Protocols. Methods in Molecular Biology, vol 1815. Humana Press, New York, NY, pp 151–159. https://doi.org/10.1007/978-1-4939-8594-4_8
Saeed F, Younas M, Fazal H, Mushtaq S, Rahman F, Shah M, Anjum S, Ahmad N, Ali M, Hano C, Abbasi BH (2021) Green and chemically synthesized zinc oxide nanoparticles: effects on in vitro seedlings and callus cultures of Silybum marianum and evaluation of their antimicrobial and anticancer potential. Artif Cells Nanomed Biotechnol 49:450–460. https://doi.org/10.1080/21691401.2021.1926274
Shaikhaldein HO, Al-Qurainy F, Nadeem M et al (2020) Biosynthesis and characterization of silver nanoparticles using Ochradenus arabicus and their physiological effect on Maerua oblongifolia raised in vitro. Sci Rep 10:17569. https://doi.org/10.1038/s41598-020-74675-9
Sharma D, Kanchi S, Bisetty K (2019) Biogenic synthesis of nanoparticles: an review. Arab J Chem 12(8):3576–3600. https://doi.org/10.1016/j.arabjc.2015.11.002
Shen L, Sun P, Bonnell VC, Edwards KJ, Hetherington AM, McAinsh MR, Roberts MR (2015) Measuring stress signaling responses of stomata in isolated epidermis of graminaceous species. Front Plant Sci 5:1–7. https://doi.org/10.3389/fpls.2015.00533
Sosa M, Alemán S, Pérez Y, Abreu E, Sosa D, González G (2014) Characterization of leaf area of Agave fourcroydes Lem. Plants obtained from asexual propagation. Biotecnol Veg 14(1):37–44
Talukdar M, Swain KD, Bhadoria PBS (2022) Effect of IAA and BAP application in varying concentration on seed yield and oil quality of Guizotia abyssinica (L.f.) Cass. Ann Agric Sci 67(1):15–23. https://doi.org/10.1016/j.aoas.2022.02.002
Tymoszuk A, Wojnarowicz J (2020) Zinc oxide and zinc oxide nanoparticles impact on in vitro germination and seedling growth in allium cepa L. Materials (Basel) 13(12):2784. https://doi.org/10.3390/ma13122784
Acknowledgements
We thank MM R. Gonzalez-Montes de Oca and Dr. M.A. Hernández Pérez for SEM and XRD analysis. We also thank the National Council for Science and Technology (CONACYT-Mexico) for A.I. Canales-Mendoza scholarship (813864).
Funding
No funding was received to assist with the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
AICM - conceptualization, implementation of the experimental methodology, research, and writing of the original draft. MVI - conceptualization, design of the experimental methodology, research, supervision, validation, writing—revision, and editing. XTJ - supervision, validation, statistical analysis. JAC - supervision, validation of experimental methodology. All authors discussed the results and contributed to the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflicts of interest.
Additional information
Communicated by Melekşen Akın.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
Canales-Mendoza, A.I., Villanueva-Ibáñez, M., Tovar-Jiménez, X. et al. Effect of the addition of fungal extracellular biogenic zinc oxide nanoparticles on the in vitro multiplication of Agave salmiana shoots. Plant Cell Tiss Organ Cult 155, 479–491 (2023). https://doi.org/10.1007/s11240-023-02589-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-023-02589-1