Skip to main content
SpringerLink
Log in

Zinc oxide nanoparticles-mediated changes in ultrastructure and macromolecules of pomegranate callus cells

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

The dramatic increase in the usage of nanoparticles (NPs) in a variety of applications extensively expanded the possibility regarding the release of NPs into our ecosystem. Pomegranate is a tropical and subtropical countries’ shrub, as offers food supplement and more pharmaceutical and medicinal applications. Here, we investigated the effects concerning different concentrations regarding each of ZnO NPs and its bulk on growth, uptake of Zn, potassium (K), phosphorus (P), proline, ascorbic acid, total phenolic compounds, total antioxidant, localization of Zn in callus cells by transmission electron microscope (TEM) and changes in macromolecules by Fourier transform infrared spectroscopy (FT-IR) in pomegranate (Punica granatum cv. Hegazy) callus. Growth parameters in callus exposure to high concentrations of ZnO (50–200 µg mL−1) were reduced. Different concentrations of ZnO NPs and bulk did not affect the content of K and P. In comparison according to control, uptake of Zn was increased in pomegranate callus exposed to both ZnO NPs and its bulk. Moreover, TEM images showed small cells with the tortuous cell wall, disintegrated cytoplasmic content and Zn deposition in the cell walls at low concentration of ZnO NPs. However, the high concentration of ZnO NPs showed a further Zn influx in the cytoplasm and attachment to the tonoplast. The FT-IR analysis confirmed variations in the peaks corresponding to the most macromolecules, phenolic compounds, lipids, proteins, carbohydrates, cellulose, and hemicellulose. From these results, we could consider the toxicity effects concerning ZnO NPs and its bulk.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

AsA:

Ascorbic acid

2,4-D:

2,4-dichlorophenoxyacetic acid

FT-IR:

Fourier transform infrared spectroscopy

ROS:

Reactive oxygen species

NPs:

Nanoparticles

TEM:

Transmission electron microscope

References

  • Alia A, Pardha-Saradhi P, Prasanna Mohanty P (1997) Involvement of proline in protecting thylakoid membranes against free radical-induced photodamage. J Photochem Photobiol B 38:253–257

    Article  CAS  Google Scholar 

  • Bates L, Waldren PP, Teare JD (1973) Rapid determination of free proline of water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beal T, Massiot E, Arsenault JE, Smith MR, Hijmans RJ (2017) Global trends in dietary micronutrient supplies and estimated prevalence of inadequate intakes. PLoS ONE 12:e0175554

    Article  Google Scholar 

  • Bonyanpour A, Khosh-Khui M (2013) Callus induction and plant regeneration in Punica granatum L. ‘Nana’ from leaf explants. J Cent Eur Agric 14:75–83.

    Article  Google Scholar 

  • Bozzola JJ, Russell LD (1991) Electron microscopy: principles and techniques for biologists. Jones and Bartlett Publishers, Boston

    Google Scholar 

  • Cakmak I, Marschner H (1988) Increase in membrane permeability and exudation in roots of zinc deficient plants. J Plant Physiol 132:356–361

    Article  CAS  Google Scholar 

  • Castiglione MR, Giorgetti L, Geri C, Cremonini R (2011) The effects of nano-TiO2 on seed germination, development and mitosis of root tip cells of Vicia narbonensis L. and Zea mays L. J Nanopart Res 13:2443–2449

    Article  Google Scholar 

  • Caverzan A, Casassola A, Brammer SP (2016) Reactive oxygen species and antioxidant enzymes involved in plant tolerance to stress. In Shanker AK, Shanker C (eds) Agricultural and biological sciences “abiotic and biotic stress in plants-recent advances and future perspectives”. Intech Open Agricultural and Biological Sciences, Rijeka

    Google Scholar 

  • Chung I-M, Rekha K, Rajakumar G, Thiruvengadam M (2018) Production of bioactive compounds and gene expression alterations in hairy root cultures of chinese cabbage elicited by copper oxide nanoparticles. Plant Cell Tissue Organ Cult 134:95–106

    Article  CAS  Google Scholar 

  • Dokken KM, Davis LC (2007) Infrared imaging of sunflower and maize root anatomy. J Agric Food Chem 55:10517–10530

    Article  CAS  Google Scholar 

  • Dorado J, Almendros G, Field JA, Sierra-Álvarez R (2001) Infrared spectroscopy analysis of hemp (Cannabis sativa) after selective delignification by Bjerkandera sp. at different nitrogen levels. Enzyme Microb Technol 28:550–559

    Article  CAS  Google Scholar 

  • Faizan M, Faraz A, Yusuf M, Khan ST, Hayat S (2018) Zinc oxide nanoparticle-mediated changes in photosynthetic efficiency and antioxidant system of tomato plants. Photosynthetica 56:678–686

    Article  CAS  Google Scholar 

  • Fawzy MA (2016) Phycoremediation and adsorption isotherms of cadmium and copper ions by Merismopedia tenuissima and their effect on growth and metabolism. Environ Toxicol Pharmacol 46:116–121

    Article  CAS  Google Scholar 

  • Feng YZ, Chen DJ, Song MT, Zhao YL, Li ZH (1998) Assessment and utilization of pomegranate varieties resources. J Fruit Sci 15:370–373

    Google Scholar 

  • Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide-and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254

    Article  CAS  Google Scholar 

  • Fukui H, Iwahashi H, Nishio K, Hagihara Y, Yoshida Y, Horie M (2017) Ascorbic acid prevents zinc oxide nanoparticle-induced intracellular oxidative stress and inflammatory responses. Toxicol Ind Health 33:687–695

    Article  CAS  Google Scholar 

  • Gangwar S, Singh VP, Tripathi DK, Chauhan DK, Prasad SM, Maurya JN (2014) Plant responses to metal stress: the emerging role of plant growth hormones in toxicity alleviation. In: Ahmad P, Rasool S (eds) Emerging technologies and management of crop stress tolerance, 1st edn. Academic Press, San Diego, pp 215–248

    Chapter  Google Scholar 

  • Ghosh M, Jana A, Sinha S, Jothiramajayam M, Nag A, Chakraborty A, Mukherjee A (2016) Effects of ZnO nanoparticless in plants: cytotoxicity, genotoxicity, deregulation of antioxidant defenses, and cell-cycle arrest. Mutat Res Genet Toxicol Environ Mutagen 807:25–32

    Article  CAS  Google Scholar 

  • Grace SC, Logan BA (2000) Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Philos Trans R Soc Lond B 355:1499–1510

    Article  CAS  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466

    Article  CAS  Google Scholar 

  • Helaly MN, El-Hosieny H, Tobias N, Alsudays I, Omar SA, Elsheery NI (2014) In vitro studies on regeneration and transformation of some pomegranate genotypes. Aust J Crop Sci 8:307–316

    Google Scholar 

  • Javed R, Mohamed A, Yücesan B, Gürel E, Kausar R, Zia M (2017) CuO nanoparticles significantly influence in vitro culture, steviol glycosides, and antioxidant activities of Stevia rebaudiana Bertoni. Plant Cell Tissue Organ Cult 131:611–620

    Article  CAS  Google Scholar 

  • Kampfenkel K, Van Montagu M, Inzé D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225:165–167

    Article  CAS  Google Scholar 

  • Khalil MI, Al-Qunaibit MM, Al-zahem AM, Labis JP (2014) Synthesis and characterization of ZnO nanoparticles by thermal decomposition of a curcumin zinc complex. Arab J Chem 7:1178–1184

    Article  CAS  Google Scholar 

  • Khan GA, Bouraine S, Wege S, Li Y, de Carbonnel M, Berthomieu P, Poirier Y, Rouached H (2014) Coordination between zinc and phosphate homeostasis involves the transcription factor PHR1, the phosphate exporter PHO1, and its homologue PHO1;H3 in Arabidopsis. J Exp Bot 65:871–874

    Article  CAS  Google Scholar 

  • Kofalvi SA, Nassuth A (1995) Influence of wheat streak mosaic virus infection on phenyl propanoid metabolism and the accumulation of phenolics and lignin in wheat. Physiol Mol Plant Pathol 47:365–377

    Article  CAS  Google Scholar 

  • Kulbat K (2016) The role of phenolic compounds in plant resistance. Biotechnol Food Sci 80:97–108

    Google Scholar 

  • Kumssa DB, Joy EJ, Ander EL, Watts MJ, Young SD, Walker S, Broadley MR (2015) Dietary calcium and zinc deficiency risks are decreasing but remain prevalent. Sci Rep 5:10974

    Article  Google Scholar 

  • Lee S, Kim S, Lee I (2013) Assessment of phytotoxicity of ZnO NPs on a medicinal plant, Fagopyrum esculentum. Environ Sci Pollut Res Int 20:848–854

    Article  CAS  Google Scholar 

  • Minocha R, Jain SM (2000) Tissue culture of woody plants and its relevance to molecular biology. In: Jain SM, Minocha SC (eds) Molecular biology of woody plants, vol 1. Kluwer, The Netherlands, pp 315–339

    Chapter  Google Scholar 

  • Mongkhonsin B, Nakbanpote W, Hokura A, Nuengchamnong N, Maneechai S (2016) Phenolic compounds responding to zinc and/or cadmium treatments in Gynura pseudochina (L.) DC. extracts and biomass. Plant Physiol Biochem 109:549–560

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Panda KK, Dambaru Golari D, Venugopal A, Achary VM, Phaomei G, Parinandi NL, Sahu HK, Panda BB (2017) Green synthesized zinc oxide (ZnO) nanoparticles induce oxidative stress and DNA damage in Lathyrus sativus L. root bioassay system. Antioxidants (Basel) 6:35

    Article  Google Scholar 

  • Patil VM, Dhande GA, Thigale DM, Rajput JC (2011) Micropropagation of pomegranate (Punica granatum L.) ‘Bhagava’ cultivar from nodal explant. Afr J Biotechnol 10:18130–18136

    CAS  Google Scholar 

  • Prasad KV, Paradha S, Sharmila P (1999) Concerted action of antioxidant enzymes and curtailed growth under zinc toxicity in Brassica juncea. Environ Exp Bot 42:1–10

    Article  CAS  Google Scholar 

  • Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269:337–341

    Article  CAS  Google Scholar 

  • Rai M, Ingle A (2012) Role of nanotechnology in agriculture with special reference to management of insect pests. Appl Microbiol Biotechnol 94:287–293

    Article  CAS  Google Scholar 

  • Rajendran SP, Sengodan K (2017) Synthesis and characterization of zinc oxide and iron oxide nanoparticles using Sesbania grandiflora leaf extract as reducing agent. J Nanosci 2017:1–7

    Article  Google Scholar 

  • Rico CM, Majumadar S, Duarte-Gardea M, Peralta-Videa JR, Gardea-Torresdey JL (2011) Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric Food Chem 59:3485–3498

    Article  CAS  Google Scholar 

  • Rico CM, Peralta-Videa JR, Gardea-Torresdey JL (2015) Differential effects of cerium oxide nanoparticles on rice, wheat, and barley roots: a Fourier transform infrared (FT-IR) microspectroscopy study. Appl Spectrosc 69:287–295

    Article  CAS  Google Scholar 

  • Sabir S, Arshad M, Chaudhari SK (2014) Zinc oxide nanoparticles for revolutionizing agriculture: synthesis and applications. Sci World J 2014:925494

    Article  Google Scholar 

  • Saha N, Gupta DS (2018) Promotion of shoot regeneration of Swertia chirata by biosynthesized silver nanoparticles and their involvement in ethylene interceptions and activation of antioxidant activity. Plant Cell Tissue Organ Cult 134:289–300

    Article  CAS  Google Scholar 

  • Santhoshkumar J, Venkat Kumar S, Rajeshkumar S (2017) Synthesis of zinc oxide nanoparticles using plant leaf extract against urinary tract infection pathogen. Resour Eff Technol 3:459–465

    Google Scholar 

  • Scott N, Chen H (2012) Nanoscale science and engineering for agriculture and food systems. Ind Biotechnol 8:340–343

    Article  Google Scholar 

  • Sharma SS, Schat H, Vooijs R (1998) In vitro alleviation of heavy metal-induced enzyme inhibition by proline. Phytochemistry 49:1531–1535

    Article  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 26:26

    Google Scholar 

  • Sillanpää M (1990) Micronutrient assessment at the country level: an international study. FAO Soils Bull 63:1990

    Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060

    Article  CAS  Google Scholar 

  • Song ZZ, Ma RJ, Yu ML (2015) Genome-wide analysis and identification of KT/HAK/KUP potassium transporter gene family in peach (Prunus persica). Genet Mol Res 14:774–787

    Article  CAS  Google Scholar 

  • Spinoso-Castillo JL, Chavez-Santoscoy RA, Bogdanchikova N, Pérez-Sato JA, Morales-Ramos V, Bello-Bello JJ (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 Tissue Organ Cult 129:195–207

    Article  CAS  Google Scholar 

  • Tajmir-Riahi HA (1991) Coordination chemistry of vitamin C. Part II. Interaction of L-ascorbic acid with Zn(II), Cd(II), Hg(II), and Mn(II) ions in the solid state and in aqueous solution. J Inorg Biochem 42:47–55

    Article  CAS  Google Scholar 

  • Türker-Kaya S, Huck CW (2017) A review of mid-infrared and near-infrared imaging: principles, concepts and applications in plant tissue analysis. Molecules 22:168. https://doi.org/10.3390/molecules22010168

    Article  CAS  Google Scholar 

  • Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14:7370–7390

    Article  CAS  Google Scholar 

  • Wei Z, Jiao D, Xu J (2015) Using Fourier transform infrared spectroscopy to study effects of magnetic field treatment on wheat (Triticum aestivum L.) seedlings. J Spectrosc 2015:1–6

    Google Scholar 

  • Welch RM, Webb MJ, Lonegaran JF (1982) Zinc in membrane function and its role in phosphorus toxicity. In: Proceedings of the 9th international plant nutrition colloquium (ed. A. Scaife). Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, UK, pp. 710–715

  • Williams CH, Twine JR (1960) Flame photometric method for sodium, potassium and calcium. In: Peach K, Tracey MV (eds) Modern methods of plant analysis, vol 5. Springer, Berlin, pp 3–5

    Google Scholar 

  • Wong MH, Misra RP, Giraldo JP, Kwak SY, Son Y, Landry MP, Swan JW, Blankschtein D, Strano MS (2016) Lipid exchange envelope penetration (LEEP) of nanoparticles for plant engineering: a universal localization mechanism. Nano Lett 16:1161–1172

    Article  CAS  Google Scholar 

  • Wood JT, Mellon MG (1941) Thiocyanate method for iron: a spectrophotometric study. Ind Eng Chem Anal Ed 13:551–554

    Article  Google Scholar 

  • Zafar H, Ali A, Ali JS, Haq IU, Zia M (2016) Effect of ZnO nanoparticles on Brassica nigra seedlings and stem explants: growth dynamics and antioxidative response. Front Plant Sci 7:535

    Article  Google Scholar 

  • Zhao H, Wu L, Chai T, Zhang Y, Tan J, Ma S (2012) The effects of copper, manganese and zinc on plant growth and elemental accumulation in the manganese-hyperaccumulator Phytolacca americana. J Plant Physiol 169:1243–1252

    Article  CAS  Google Scholar 

  • Zuverza-Mena N, Armendariz R, Peralta-Videa JR, Gardea-Torresdey JL (2016) Effects of silver nanoparticles on radish sprouts: root growth reduction and modifications in the nutritional value. Front Plant Sci 7:90

    Article  Google Scholar 

Download references

Acknowledgements

This work was carried out in Genetic Engineering and Tissue Culture Research Unit in Assiut University. Authors wish to thank Dr. Mokhtar Mamdouh Shaaban and all members of the unit for sharing experience considering tissue culture. The authors acknowledge the contribution of the Cellular Imaging Unit of Assiut University. Also, the authors are grateful to Prof. Allam Nafady and all members of the Electron Microscopy Unit for carrying out the transmission electron microscopy.

Author information

Authors and Affiliations

  1. Botany and Microbiology Department, Faculty of Science, Assiut University, Assiut, 71516, Egypt

    Abeer A. Radi, Fatma A. Farghaly & Afaf M. Hamada

  2. Biology Department, Faculty of Science, Ibb University, Ibb, Yemen

    Fatma A. Al-Kahtany

Authors
  1. Abeer A. Radi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fatma A. Farghaly
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fatma A. Al-Kahtany
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Afaf M. Hamada
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AR, FF, and AH conceived and designed research. AR, FF, and FA conducted experiments. AR, FF, FA and AH analyzed data and wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Afaf M. Hamada.

Ethics declarations

Conflict of interest

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Additional information

Communicated by Ming-Tsair Chan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Radi, A.A., Farghaly, F.A., Al-Kahtany, F.A. et al. Zinc oxide nanoparticles-mediated changes in ultrastructure and macromolecules of pomegranate callus cells. Plant Cell Tiss Organ Cult 135, 247–261 (2018). https://doi.org/10.1007/s11240-018-1460-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-018-1460-3

Keywords

Search

Navigation