Skip to main content
Log in

Engineered magnetic nanoparticles enhance chlorophyll content and growth of barley through the induction of photosystem genes

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

This study investigates the impact of an engineered magnetic nanoparticle (MNP) on a crop plant. For this purpose, a sonochemical synthetic approach was utilized in order to dope magnetic elements (Co and Nd) into technologically important iron oxide NPs. After being characterized by using TEM, SEM, and XRD instruments, the MNPs were hydroponically applied to barley plants with varying doses (from 125 to 1000 mg/L) both in germination (4 days) and early growing stages (3 weeks). Physiological responses, as well as expression of photosystem marker genes, were assessed. Compared to the untreated control, MNP treatment enhanced germination rate (~ 31%), tissue growth (8% in roots, 16% in shoots), biomass (~ 21%), and chlorophyll (a, b) (~ 20%), and carotenoids (~ 22%) pigments. In general, plants showed the highest growth enhancement at 125 or 250 mg/L treatment. However, higher doses diminished the growth indices. Compared to the control, the catalase activity was significantly reduced in the leaves (~ 33%, p < 0.005) but stimulated in the roots (~ 46%, p < 0.005). All tested photosystem marker genes (BCA, psbA, and psaA) were overexpressed in MNP-treated leaves than non-treated control. Moreover, the gene expressions were found to be proportionally increased with increasing MNP doses, indicating a positive correlation between MNPs and the photosynthetic machinery, which could contribute to the enhancement of plant growth.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

MNPs:

magnetic nanoparticles

NPs:

nanoparticles

ROS:

reactive oxygen species

H2O2 :

hydrogen peroxide

RWC:

relative water content

Ms:

saturation magnetization

Hc:

coercivity

Mr:

remanent magnetization

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126 Academic Press

    Article  CAS  Google Scholar 

  • Almessiere MA, Slimani Y, Korkmaz AD, Sertkol M, Baykal A, Ercan I, Özçelik B (2019) Sonochemical synthesis of CoFe2-xNdxO4 nanoparticles: structural, optical, and magnetic investigation. J Supercond Nov Magn:1–8. https://doi.org/10.1007/s10948-019-05147-z

  • Atak Ç, Çelik Ö, Olgun A, Alikamanoğlu S, Rzakoulieva A (2007) Effect of magnetic field on peroxidase activities of soybean tissue culture. Biotechnol Biotechnol Equip 21(2):166–171

    Article  CAS  Google Scholar 

  • BCC Research (2018) https://www.bccresearch.com/market-research/nanotechnology/nanocomposites-nanoparticles-nanoclays-and-nanotubes-global-markets.html

  • Bhavani P, Manikandan A, Paulraj P, Dinesh A, Durka M, Antony SA (2018) Okra (Abelmoschus esculentus) plant extract-assisted combustion synthesis and characterization studies of spinel ZnAl2O4 nano-catalysts. J Nanosci Nanotechnol 18(6):4072–4081

    Article  CAS  Google Scholar 

  • Bideskan AE, Mohammadipour A, Fazel A, Haghir H, Rafatpanah H, Hosseini M, Rajabzadeh A (2017) Maternal exposure to titanium dioxide nanoparticles during pregnancy and lactation alters offspring hippocampal mRNA BAX and Bcl-2 levels, induces apoptosis and decreases neurogenesis. Exp Toxicol Pathol 69(6):329–337

    Article  CAS  Google Scholar 

  • Bostancioglu SM, Tombuloglu G, Tombuloglu H (2018) Genome-wide identification of barley MCs (metacaspases) and their possible roles in boron-induced programmed cell death. Mol Biol Rep 45(3):211–225

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    Article  CAS  Google Scholar 

  • Briat JF, Dubos C, Gaymard F (2015) Iron nutrition, biomass production, and plant product quality. Trends Plant Sci 20:33–40

    Article  CAS  Google Scholar 

  • Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Function of nutrients: micronutrients. In: Marschner’s mineral nutrition of higher plants. Academic Press, pp 191–248

  • Ding Y, Bai X, Ye Z, Ma L, Liang L (2019) Toxicological responses of Fe3O4 nanoparticles on Eichhornia crassipes and associated plant transportation. Sci Total Environ 671:558–567

    Article  CAS  Google Scholar 

  • Ghafariyan MH, Malakouti MJ, Dadpour MR, Stroeve P, Mahmoudi M (2013) Effects of magnetite nanoparticles on soybean chlorophyll. Environ Sci Technol 47(18):10645–10652

    CAS  Google Scholar 

  • Giraldo JP, Landry MP, Faltermeier SM, McNicholas TP, Iverson NM, Boghossian AA, Strano MS (2014) Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat Mater 13(4):400–408

    Article  CAS  Google Scholar 

  • Govindjee U (2014) In: Demmig-Adams B, Garab G, Adams W III (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria, vol 40. Springer Netherlands, Dordrecht

    Google Scholar 

  • Harwood WA (2018) Methods in molecular biology barley:1–5

  • Hernandez-Viezcas JA, Castillo-Michel H, Andrews JC, Cotte M, Rico C, Peralta-Videa JR, Gardea-Torresdey JL (2013) In situ synchrotron X-ray fluorescence mapping and speciation of CeO2 and ZnO nanoparticles in soil cultivated soybean (Glycine max). ACS Nano 7(2):1415–1423

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular California agricultural experiment station, 347(2nd edit)

  • Hu J, Guo H, Li J, Wang Y, Xiao L, Xing B (2017) Interaction of γ-Fe2O3 nanoparticles with Citrus maxima leaves and the corresponding physiological effects via foliar application. J Nanobiotechnol 15(1):51

    Article  CAS  Google Scholar 

  • Kim JH, Lee Y, Kim EJ, Gu S, Sohn EJ, Seo YS, An HJ, Chang YS (2014) Exposure of iron nanoparticles to Arabidopsis thaliana enhances root elongation by triggering cell wall loosening. Environ Sci Technol 48(6):3477–3485

    Article  CAS  Google Scholar 

  • Konate A, He X, Zhang Z, Ma Y, Zhang P, Alugongo G, Rui Y (2017) Magnetic (Fe3O4) nanoparticles reduce heavy metals uptake and mitigate their toxicity in wheat seedling. Sustainability 9(5):790

    Article  CAS  Google Scholar 

  • Le N, Rui Y, Gui X, Li X, Liu S, Han Y (2014) Uptake, transport, distribution and bio-effects of SiO2 nanoparticles in Bt-transgenic cotton. J Nanobiotechnol 12(1):50

    Article  CAS  Google Scholar 

  • Libralato G, Devoti AC, Zanella M, Sabbioni E, Mičetić I, Manodori L, Ghirardini AV (2016) Phytotoxicity of ionic, micro-and nano-sized iron in three plant species. Ecotoxicol Environ Saf 123:81–88

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11(5):591–592

    Article  CAS  Google Scholar 

  • Lisjak D, Mertelj A (2018) Anisotropic magnetic nanoparticles: a review of their properties, syntheses and potential applications. Prog Mater Sci 95:286–328

    Article  CAS  Google Scholar 

  • López-Millán AF, Duy D, Philippar K (2016) Chloroplast iron transport proteins–function and impact on plant physiology. Front Plant Sci 7:178

    Article  Google Scholar 

  • Lugojan C, Ciulca S (2011) Evaluation of relative water content in winter wheat. J Hortic Forest Biotechnol 15:173–177

    Google Scholar 

  • Maher BA, Ahmed IA, Karloukovski V, MacLaren DA, Foulds PG, Allsop D et al (2016) Magnetite pollution nanoparticles in the human brain. Proc Natl Acad Sci U S A 113(39):10797–10801

    Article  CAS  Google Scholar 

  • Manikandan A, Durka M, Antony SA (2015) Hibiscus rosa-sinensis leaf extracted green methods, magneto-optical and catalytic properties of spinel CuFe 2 O 4 nano-and microstructures. J Inorg Organomet Polym Mater 25(5):1019–1031

    Article  CAS  Google Scholar 

  • Manikandan A, Durka M, Amutha Selvi M, Arul Antony S (2016) Sesamum indicum plant extracted microwave combustion synthesis and opto-magnetic properties of spinel MnxCo1-xAl2O4 nano-catalysts. J Nanosci Nanotechnol 16(1):448–456

    Article  CAS  Google Scholar 

  • Marmiroli M, Pagano L, Savo Sardaro ML, Villani M, Marmiroli N (2014) Genome-wide approach in Arabidopsis thaliana to assess the toxicity of cadmium sulfide quantum dots. Environ Sci Technol 48(10):5902–5909

    Article  CAS  Google Scholar 

  • Mohammadipour A, Hosseini M, Fazel AR, Haghir H, Rafatpanah H, Pourganji M, Ebrahimzadeh Bideskan A (2016) The effects of exposure to titanium dioxide nanoparticles during lactation period on learning and memory of rat offspring. Toxicol Ind Health 32(2):221–228

    Article  CAS  Google Scholar 

  • Ooi A, Wong A, Ng TK, Marondedze C, Gehring C, Ooi BS (2016) Growth and development of Arabidopsis thaliana under single-wavelength red and blue laser light. Sci Rep 6:33885

    Article  CAS  Google Scholar 

  • Pagano L, Servin AD, De La Torre-Roche R, Mukherjee A, Majumdar S, Hawthorne J, Dhankher OP (2016) Molecular response of crop plants to engineered nanomaterials. Environ Sci Technol 50(13):7198–7207

    Article  CAS  Google Scholar 

  • Pagano L, Pasquali F, Majumdar S, De la Torre-Roche R, Zuverza-Mena N, Villani M, Maestri E (2017) Exposure of Cucurbita pepo to binary combinations of engineered nanomaterials: physiological and molecular response. Environ Sci Nano 4(7):1579–1590

    Article  CAS  Google Scholar 

  • Pagano L, Maestri E, Caldara M, White JC, Marmiroli N, Marmiroli M (2018) Engineered nanomaterial activity at the organelle level: impacts on the chloroplasts and mitochondria. ACS Sustain Chem Eng 6(10):12562–12579

    Article  CAS  Google Scholar 

  • Pariona N, Martínez AI, Hernandez-Flores H, Clark-Tapia R (2017) Effect of magnetite nanoparticles on the germination and early growth of Quercus macdougallii. Sci Total Environ 575:869–875

    Article  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29(9):e45

    Article  CAS  Google Scholar 

  • Qian H, Zhu K, Lu H, Lavoie M, Chen S, Zhou Z, Deng Z, Chen J, Fu Z (2016) Contrasting silver nanoparticle toxicity and detoxification strategies in Microcystis aeruginosa and Chlorella vulgaris: new insights from proteomic and physiological analyses. Sci Total Environ 572:1213–1221

    Article  CAS  Google Scholar 

  • Racuciu M, Creanga D (2007) TMA-OH-coated magnetic nanoparticles internalized in vegetal tissue. Rom J Physiol 52(3/4):395

    CAS  Google Scholar 

  • Rajput VD, Minkina TM, Behal A, Sushkova SN, Mandzhieva S, Singh R, Movsesyan HS (2018) Effects of zinc-oxide nanoparticles on soil, plants, animals and soil organisms: a review. Environ Nanotechnol Monitor Manag 9:76–84

    Article  Google Scholar 

  • Rastogi A, Zivcak M, Sytar O, Kalaji HM, He X, Mbarki S, Brestic M (2017) Impact of metal and metal oxide nanoparticles on plant: a critical review. Front Chem 5:78

    Article  CAS  Google Scholar 

  • Rico CM, Majumdar 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 

  • Ritchie SW, Nguyan HT, Holaday AS (1990) Leaf water content and gas exchange parameters of two wheat genotypes differing in drought resistance. Crop Sci 30:105–111

    Article  Google Scholar 

  • Sade N, Galkin E, Moshelion M (2015) Measuring Arabidopsis, tomato and barley leaf relative water content (RWC). Bio-Protocols 5:1–4

    Google Scholar 

  • Servin AD, Morales MI, Castillo-Michel H, Hernandez-Viezcas JA, Munoz B, Zhao L, Gardea-Torresdey JL (2013) Synchrotron verification of TiO2 accumulation in cucumber fruit: a possible pathway of TiO2 nanoparticle transfer from soil into the food chain. Environ Sci Technol 47(20):11592–11598

    Article  CAS  Google Scholar 

  • Silva T, Pokhrel LR, Dubey B, Tolaymat TM, Maier KJ, Liu X (2014) Particle size, surface charge and concentration dependent ecotoxicity of three organo-coated silver nanoparticles: comparison between general linear model-predicted and observed toxicity. Sci Total Environ 468:968–976

    Article  CAS  Google Scholar 

  • Subramanian V, Semenzin E, Hristozov D, Zabeo A, Malsch I, McAlea E, Linkov I (2016) Sustainable nanotechnology decision support system: bridging risk management, sustainable innovation and risk governance. J Nanopart Res 18(4):89

    Article  Google Scholar 

  • Swift TA, Oliver TA, Galan MC, Whitney HM (2019) Functional nanomaterials to augment photosynthesis: evidence and considerations for their responsible use in agricultural applications. Interface Focus 9(1):20180048

    Article  Google Scholar 

  • Tombuloglu H, Semizoglu N, Sakcali S, Kekec G (2012) Boron induced expression of some stress-related genes in tomato. Chemosphere 86(5):433–438

    Article  CAS  Google Scholar 

  • Tombuloglu H, Kekec G, Sakcali MS, Unver T (2013) Transcriptome-wide identification of R2R3-MYB transcription factors in barley with their boron responsive expression analysis. Mol Gen Genomics 288(3–4):141–155

    Article  CAS  Google Scholar 

  • Tombuloglu G, Tombuloglu H, Sakcali MS, Unver T (2015) High-throughput transcriptome analysis of barley (Hordeum vulgare) exposed to excessive boron. Gene 557(1):71–81

    Article  CAS  Google Scholar 

  • Tombuloglu H, Ozcan I, Tombuloglu G, Sakcali S, Unver T (2016) Aquaporins in boron-tolerant barley: identification, characterization, and expression analysis. Plant Mol Biol Report 34(2):374–386

    Article  CAS  Google Scholar 

  • Tombuloglu H, Tombuloglu G, Slimani Y, Ercan I, Sozeri H, Baykal (2018) Impact of manganese ferrite (MnFe2O4) nanoparticles on growth and magnetic character of barley (Hordeum vulgare L). Environ Pollut 243:872–881

    Article  CAS  Google Scholar 

  • Tombuloglu H, Slimani Y, Tombuloglu G, Demir-Korkmaz A, Baykal A, Almessiere M, Ercan I (2019a) Impact of superparamagnetic iron oxide nanoparticles (SPIONs) and ionic iron on physiology of summer squash (Cucurbita pepo): a comparative study. Plant Physiol Biochem 139:56–65

    Article  CAS  Google Scholar 

  • Tombuloglu H, Slimani Y, Tombuloglu G, Almessiere M, Baykal A (2019b) Uptake and translocation of magnetite (Fe3O4) nanoparticles and its impact on photosynthetic genes in barley (Hordeum vulgare L). Chemosphere 226:110–122

    Article  CAS  Google Scholar 

  • Tombuloglu H, Slimani Y, Güngüneş H, Tombuloglu G, Almessiere MA, Sozeri H, Ercan I (2019c) Tracking of SPIONs in barley (Hordeum vulgare L) plant organs during its growth. J Supercond Nov Magn 32:1–10. https://doi.org/10.1007/s10948-019-5059-7

    Article  CAS  Google Scholar 

  • Tombuloglu H, Slimani Y, Tombuloglu G, Almessiere M, Baykal A, Ercan I, Sozeri H (2019d) Tracking of NiFe2O4 nanoparticles in barley (Hordeum vulgare L) and their impact on plant growth, biomass, pigmentation, catalase activity, and mineral uptake. Environ Nanotechnol Monit Manag 11:100223

    Google Scholar 

  • Tombuloglu H, Slimani Y, Alshammari T, Tombuloglu G, Almessiere M, Baykal A, Demirci T (2019e) Magnetic behavior and nutrient content analyses of barley (Hordeum vulgare L) tissues upon CoNd02Fe1.8O4 magnetic nanoparticle treatment. J Soil Sci Plant Nutr:1–10. https://doi.org/10.1007/s42729-019-00115-x

  • Tosco T, Sethi R (2018) Human health risk assessment for nanoparticle-contaminated aquifer systems. Environ Pollut 239:242–252

    Article  CAS  Google Scholar 

  • USEPA (United States Environmental Protection Agency) (1996) Ecological effects test guidelines: seed germination/root elongation toxicity test. Prevention, Pesticides and Toxic Substances, Washington, DC, p 7101

    Google Scholar 

  • Wientjes E, Renger J, Curto AG, Cogdell R, Van Hulst NF (2014) Strong antenna-enhanced fluorescence of a single light-harvesting complex shows photon antibunching. Nat Commun 5(1):1–7

    Article  CAS  Google Scholar 

  • Xiong T, Dumat C, Dappe V, Vezin H, Schreck E, Shahid M, Sobanska S (2017) Copper oxide nanoparticle foliar uptake, phytotoxicity, and consequences for sustainable urban agriculture. Environ Sci Technol 51(9):5242–5251

    Article  CAS  Google Scholar 

  • Yuan J, Chen Y, Li H, Lu J, Zhao H, Liu M, Glushchenko NN (2018) New insights into the cellular responses to iron nanoparticles in Capsicum annuum. Sci Rep 8(1):3228

    Article  CAS  Google Scholar 

  • Zhang P, Ma Y, Zhang Z, He X, Zhang J, Guo Z, Chai Z (2012) Biotransformation of ceria nanoparticles in cucumber plants. ACS Nano 6(11):9943–9950

    Article  CAS  Google Scholar 

  • Zhao L, Sun Y, Hernandez-Viezcas JA, Servin AD, Hong J, Niu G, Gardea-Torresdey JL (2013) Influence of CeO2 and ZnO nanoparticles on cucumber physiological markers and bioaccumulation of Ce and Zn: a life cycle study. J Agric Food Chem 61(49):11945–11951

    Article  CAS  Google Scholar 

Download references

Funding

This study is supported by Deanship of Scientific Research (DSR) fund of Imam Abdulrahman Bin Faisal University (IAU) under the project numbers of 2018-139-IRMC and 2019-058-IRMC.

Author information

Authors and Affiliations

Authors

Contributions

The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript.

Corresponding author

Correspondence to Huseyin Tombuloglu.

Additional information

Responsible editor: Gangrong Shi

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 18.5 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tombuloglu, H., Slimani, Y., Tombuloglu, G. et al. Engineered magnetic nanoparticles enhance chlorophyll content and growth of barley through the induction of photosystem genes. Environ Sci Pollut Res 27, 34311–34321 (2020). https://doi.org/10.1007/s11356-020-09693-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-09693-1

Keywords

Navigation