Hydroponic grown tobacco plants respond to zinc oxide nanoparticles and bulk exposures by morphological, physiological and anatomical adjustments
Maryam Mazaheri Tirani A , Maryam Madadkar Haghjou
A C and Ahmad Ismaili B
+ Author Affiliations
- Author Affiliations
A Department of Biology, Plant Physiology, Faculty of Science, Lorestan University, Khoramabad-Tehran Road (5th K), Iran.
B Department of Agronomy and Plant Breeding, Faculty of Agriculture, Lorestan University, Iran.
C Corresponding author. Emails: madadkar.m@lu.ac.ir; m_madadkar@yahoo.com
Functional Plant Biology 46(4) 360-375 https://doi.org/10.1071/FP18076
Submitted: 28 March 2018 Accepted: 18 December 2018 Published: 8 February 2019
Abstract
Zinc oxide nanoparticles (NPs) are the third highest in terms of global production among the various inorganic nanoparticles, and there are concerns because of their worldwide availability and accumulation in the environment. In contrast, zinc is an essential element in plant growth and metabolism, and ZnO NPs (nano-ZnO) may have unknown interactions with plants due to their small sizes as well as their particular chemical and physical characteristics. The present study examined the effect of nano-ZnO (25 nm) and bulk or natural form (<1000 nm, bulk-ZnO), compared with zinc in the ionic form (ZnSO4) on Nicotiana tabacum seedlings in a nutrient solution supplemented with either nano-ZnO, bulk-ZnO (0.2, 1, 5 and 25 µM) or ZnSO4 (control) for 21 days. Results showed that nano-ZnO at most of the levels and 1 µM bulk-ZnO positively affected growth (root and shoot length/dry weight), leaf surface area and its metabolites (auxin, phenolic compounds, flavonoids), leaf enzymatic activities (CAT, APX, SOD, POX, GPX, PPO and PAL) and anatomical properties (root, stem, cortex and central cylinder diameters), while bulk-ZnO caused decreases at other levels. The activities of enzymes were induced to a greater extent by intermediate nano-ZnO levels than by extreme concentrations, and were higher in nano-ZnO treated than in bulk treated tobacco. As the ZnO level increased, the vascular expansion and cell wall thickening of the collenchyma/parenchyma cells occurred, which was more pronounced when treated by NPs than by its counterpart. The Zn content of root and leaf increased in most of ZnO treatments, whereas the Fe content of leaves decreased. Our findings indicate that tobacco responded positively to 1 µM bulk-ZnO and to nearly all nano-ZnO levels (with the best levels being at 0.2 µM and 1 µM) by morphological, physiological and anatomical adjustments.
Additional keywords: antioxidative response, auxin, chlorophyll deficiency, flavonoids, zinc uptake.
References
Aslani F, Bagheri S, Julkapli NM, Juraimi AS, Hashemi FSG, Baghdadi A (2014) Effects of engineered nanomaterials on plants growth: an overview. Planta 104, 66–77.Aydaş SB, Ozturk S, Aslım B (2013) Phenylalanine ammonialyase (PAL) enzyme activity and antioxidant properties of some cyanobacteria isolates. Food Chemistry 136, 164–169.
| Phenylalanine ammonialyase (PAL) enzyme activity and antioxidant properties of some cyanobacteria isolates.Crossref | GoogleScholarGoogle Scholar |
Babaei K, Sharifi RS, Pirzad A, Khalilzadeh R (2017) Effects of biofertilizer and nano Zn-Fe oxide on physiological traits, antioxidant enzymes activity and yield of wheat (Triticum aestivum L.) under salinity stress. Plant-Environment Interactions 12, 381–389.
| Effects of biofertilizer and nano Zn-Fe oxide on physiological traits, antioxidant enzymes activity and yield of wheat (Triticum aestivum L.) under salinity stress.Crossref | GoogleScholarGoogle Scholar |
Bachelard EP (1969) Effects of gibberellic acid on internode growth and starch contents of Eucalyptus camaldulensis seedlings. New Phytologist 68, 1017–1022.
| Effects of gibberellic acid on internode growth and starch contents of Eucalyptus camaldulensis seedlings.Crossref | GoogleScholarGoogle Scholar |
Bae YS, Oh H, Rhee SG, Yoo YD (2011) Regulation of reactive oxygen species generation in cell signaling. Molecules and Cells 32, 491–509.
| Regulation of reactive oxygen species generation in cell signaling.Crossref | GoogleScholarGoogle Scholar | 22207195PubMed |
Bandyopadhyay S, Plascencia-Villa G, Mukherjee A, Rico CM, José-Yacamán M, Peralta-Videa JR, Gardea-Torresdey JL (2015) Comparative phytotoxicity of ZnO NPs, bulk ZnO, and ionic zinc onto the alfalfa plants symbiotically associated with Sinorhizobium meliloti in soil. Science of the Total Environment 515–516, 60–69.
| Comparative phytotoxicity of ZnO NPs, bulk ZnO, and ionic zinc onto the alfalfa plants symbiotically associated with Sinorhizobium meliloti in soil.Crossref | GoogleScholarGoogle Scholar | 25698520PubMed |
Barabasz A, Klimecka M, Kendziorek M, Weremczuk A, Ruszczyńska A, Bulska E, Antosiewicz DM (2016) The ratio of Zn to Cd supply as a determinant of metalhomeostasis gene expression in tobacco and its modulation by overexpressing the metal exporter AtHMA4. Journal of Experimental Botany 67, 6201–6214.
| The ratio of Zn to Cd supply as a determinant of metalhomeostasis gene expression in tobacco and its modulation by overexpressing the metal exporter AtHMA4.Crossref | GoogleScholarGoogle Scholar | 27811086PubMed |
Barceló J, Poschenrieder C (1990) Plant water relations as affected by heavy metal stress: a review. Journal of Plant Nutrition 13, 1–37.
| Plant water relations as affected by heavy metal stress: a review.Crossref | GoogleScholarGoogle Scholar |
Begum MC, Islam M, Sarkar MR, Azad MAS, Nazmul Huda AKM, Kabir AH (2016) Auxin signaling is closely associated with Zn-efficiency in rice (Oryza sativa L.). Plant-Environment Interactions 11, 124–129.
| Auxin signaling is closely associated with Zn-efficiency in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Biemelt S, Tschiersch H, Sonnewald U (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiology 135, 254–265.
| Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants.Crossref | GoogleScholarGoogle Scholar | 15122040PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |
Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytologist 173, 677–702.
| Zinc in plants.Crossref | GoogleScholarGoogle Scholar | 17286818PubMed |
Cakmak I, Marschner H, Bangerth F (1989) Effect of zinc nutritional status on growth, protein metabolism and levels of indole-3-acetic acid and other phytohormones in bean (Phaseolus vulgaris L.). Journal of Experimental Botany 40, 405–412.
| Effect of zinc nutritional status on growth, protein metabolism and levels of indole-3-acetic acid and other phytohormones in bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar |
Carillo P, Gibon Y (2011) ‘Protocol: extraction and determination of proline.’ (Prometheus Wiki) Available at http://prometheuswiki.org/tiki-=Extractionanddeterminationofproline [Accessed 16 September 2018]
Carroll MD, Loneragan JF (1969) Response of plant species to concentrations of zinc in solution. II. Rates of zinc absorption and their relation to growth. Australian Journal of Agricultural Research 20, 457–463.
| Response of plant species to concentrations of zinc in solution. II. Rates of zinc absorption and their relation to growth.Crossref | GoogleScholarGoogle 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. Journal of Nanoparticle Research 13, 2443–2449.
| The effects of nano-TiO2 on seed germination, development and mitosis of root tip cells of Vicia narbonensis L. and Zea mays L.Crossref | GoogleScholarGoogle Scholar |
Chang CC, Yang MH, Wen HM, Chern JC (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Yao Wu Shi Pin Fen Xi 10, 178–182.
Cui Y, Zhao N (2011) Oxidative stress and change in plant metabolism of maize (Zea mays L.) growing in contaminated soil with elemental sulfur and toxic effect of zinc. Plant, Soil and Environment 57, 34–39.
| Oxidative stress and change in plant metabolism of maize (Zea mays L.) growing in contaminated soil with elemental sulfur and toxic effect of zinc.Crossref | GoogleScholarGoogle Scholar |
D’souzar RM, Devaraj VR (2012) Induction of oxidative stress and antioxidative mechanisms in hyacinth bean under zinc stress. African Crop Science Journal 20, 17–29.
Daneshbakhsh B, Khoshgoftarmanesh AH, Shariatmadari H, Cakmak I (2013) Effect of zinc nutrition on salinity-induced oxidative damages in wheat genotypes differing in zinc deficiency tolerance. Acta Physiologiae Plantarum 35, 881–889.
| Effect of zinc nutrition on salinity-induced oxidative damages in wheat genotypes differing in zinc deficiency tolerance.Crossref | GoogleScholarGoogle Scholar |
Dayan J, Voronin N, Gong F, Sun T-p, Hedden P, Fromm H, Aloni R (2012) Leaf-induced gibberellin signaling is essential for internode elongation, cambial activity, and fiber differentiation in tobacco stems. The Plant Cell 24, 66–79.
| Leaf-induced gibberellin signaling is essential for internode elongation, cambial activity, and fiber differentiation in tobacco stems.Crossref | GoogleScholarGoogle Scholar | 22253226PubMed |
Dimkpa CO, McLean JE, Latta DE, Manangón E, Britt DW, Johnson WP, Boyanov MI, Anderson AJ (2012) CuO and ZnO nanoparticles: phytotoxicity, metal speciation, and induction of oxidative stress in sand-grown wheat. Journal of Nanoparticle Research 14, 1125
| CuO and ZnO nanoparticles: phytotoxicity, metal speciation, and induction of oxidative stress in sand-grown wheat.Crossref | GoogleScholarGoogle Scholar |
El-Beltagi HS, Salama ZA, El Hariri DM (2008) Some biochemical markers for evaluation of flax cultivars under salt stress conditions. Journal of Natural Fibers 5, 316–330.
| Some biochemical markers for evaluation of flax cultivars under salt stress conditions.Crossref | GoogleScholarGoogle Scholar |
Elobeid M, Gobel C, Feussner I, Polle A (2012) Cadmium interferes with auxin physiology and lignification in Poplar. Journal of Experimental Botany 63, 1413–1421.
| Cadmium interferes with auxin physiology and lignification in Poplar.Crossref | GoogleScholarGoogle Scholar | 22140243PubMed |
Franklin NM, Rogers NJ, Apte SC, Batley GE, Gadd GE, Casey PS (2007) Comparative toxicity of nanoparticulate ZnO, Bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environmental Science & Technology 41, 8484–8490.
| Comparative toxicity of nanoparticulate ZnO, Bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility.Crossref | GoogleScholarGoogle Scholar |
Fukaki H, Okushima Y, Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. International Review of Cytology 256, 111–137.
| Auxin-mediated lateral root formation in higher plants.Crossref | GoogleScholarGoogle Scholar | 17241906PubMed |
Fukuda H (2004) Signals that control plant vascular cell differentiation. Nature Reviews. Molecular Cell Biology 5, 379–391.
| Signals that control plant vascular cell differentiation.Crossref | GoogleScholarGoogle Scholar | 15122351PubMed |
Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Science 121, 151–159.
| Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress.Crossref | GoogleScholarGoogle Scholar |
Gechev T, Gadjev I, Van Breusegem F, Inzé D, Dukiandjiev S, Toneva V, Minkov I (2002) Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cellular and Molecular Life Sciences 59, 708–714.
| Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes.Crossref | GoogleScholarGoogle Scholar | 12022476PubMed |
Ghamsari L, Keyhani E, Golkhoo S (2007) Kinetics properties of guaiacol peroxidase activity in Crocus sativus L. corm during rooting. Iranian Biomedical Journal 11, 137–146.
Ghormade V, Deshpande MV, Paknikar KM (2011) Perspectives for nano-biotechnology enabled protection and nutrition of plants. Biotechnology Advances 29, 792–803.
| Perspectives for nano-biotechnology enabled protection and nutrition of plants.Crossref | GoogleScholarGoogle Scholar | 21729746PubMed |
Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiology 59, 309–314.
| Superoxide dismutases I. Occurrence in higher plants.Crossref | GoogleScholarGoogle Scholar | 16659839PubMed |
Gopalakrishnan Nair PM, Kim SH, Chung IM (2014) Copper oxide nanoparticle toxicity in mung bean (Vigna radiata L.) seedlings: physiological and molecular level responses of in vitro grown plants. Acta Physiologiae Plantarum 36, 2947–2958.
| Copper oxide nanoparticle toxicity in mung bean (Vigna radiata L.) seedlings: physiological and molecular level responses of in vitro grown plants.Crossref | GoogleScholarGoogle Scholar |
Górecka K, Cvikrová M, Kowalska U, Eder J, Szafrańska K, Górecki R, Janas KM (2007) The impact of Cu treatment on phenolic and polyamine levels in plant material regenerated from embryos obtained in another culture of carrot. Plant Physiology and Biochemistry 45, 54–61.
| The impact of Cu treatment on phenolic and polyamine levels in plant material regenerated from embryos obtained in another culture of carrot.Crossref | GoogleScholarGoogle Scholar | 17303431PubMed |
Hajiboland R, Farhanghi F, Aliasgharpour M (2012) Morphological and anatomical modifications in leaf, stem and roots of four plant species under boron deficiency conditions. Anales de Biología 34, 15–29.
Hoffmann WA, Franco AC, Moreira MZ, Haridasan M (2005) Specific leaf area explains differences in leaf traits between congeneric savanna and forest trees. Functional Ecology 19, 932–940.
| Specific leaf area explains differences in leaf traits between congeneric savanna and forest trees.Crossref | GoogleScholarGoogle Scholar |
Jensen WA (1962) ‘Botanical histochemistry: principles and practice.’ (WH Freeman & Co.: San Francisco, CA, USA)
Kalra Y (1997) ‘Handbook of reference methods for plant analysis.’ (CRC Press: Boca Raton, FL, USA)
Kisan B, Shruthi H, Sharanagouda H, Revanappa SB, Pramod NK (2015) Effect of nano-zinc oxide on the leaf physical and nutritional quality of spinach. Agrotechnology 4, 1–3.
Kleckerova A, Sobrova P, Krystofova O, Sochor J, Zitka O, Babula P, Adam V, Docekalova H, Kizek R (2011) Cadmium (II) and zinc (II) ions effects on maize plants revealed by spectroscopy and electrochemistry. International Journal of Electrochemical Science 6, 6011–6031.
Ko KS, Koh DC, Kong IC (2017) Evaluation of the effects of nanoparticle mixtures on Brassica seed germination and bacterial bioluminescence activity based on the theory of probability. Nanomaterials (Basel, Switzerland) 7, 344
| Evaluation of the effects of nanoparticle mixtures on Brassica seed germination and bacterial bioluminescence activity based on the theory of probability.Crossref | GoogleScholarGoogle Scholar |
Kołodziejczak-Radzimska A, Jesionowski T (2014) Zinc oxide-from synthesis to application: a review. Materials (Basel) 7, 2833–2881.
| Zinc oxide-from synthesis to application: a review.Crossref | GoogleScholarGoogle Scholar | 28788596PubMed |
Kumar S, Patra AK, Datta SC, Rosin KG, Purakayastha TJ (2015) Phytotoxicity of nanoparticles to seed germination of plants. International Journal of Advanced Research 3, 854–865.
Laware SL, Raskar S (2014) Influence of zinc oxide nanoparticles on growth, flowering and seed productivity in onion. International Journal of Current Microbiology and Applied Sciences 3, 874–881.
Le Gall H, Philippe F, Domon J-M, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4, 112–166.
| Cell wall metabolism in response to abiotic stress.Crossref | GoogleScholarGoogle Scholar | 27135320PubMed |
Li J (2016) Comparative behaviour of nano ZnO, bulk ZnO and ionic Zinc in marine environment and effect upon biological target organisms such as primary producers (marine algae Tetraselmis suecica and Phaeodactylum tricornutum) and filter feeder (Mediterranean mussels, Mytilus galloprovincialis) chronically exposed. Thesis, Università degli Studi di Napoli “Federico II”.
Libralato G, Devoti AC, Zanella M, Sabbioni E, Mičetić I, Manodori L, Pigozzo A, Manenti S, Groppi F, Ghirardini AV (2016) Phytotoxicity of ionic, micro-and nano-sized iron in three plant species. Ecotoxicology and Environmental Safety 123, 81–88.
| Phytotoxicity of ionic, micro-and nano-sized iron in three plant species.Crossref | GoogleScholarGoogle Scholar | 26232851PubMed |
Lin D, Xing B (2007) Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environmental Pollution 150, 243–250.
| Phytotoxicity of nanoparticles: inhibition of seed germination and root growth.Crossref | GoogleScholarGoogle Scholar | 17374428PubMed |
Lin D, Tian X, Wu F, Xing B (2010) Fate and transport of engineered nanomaterials in the environment. Journal of Environmental Quality 39, 1896–1908.
| Fate and transport of engineered nanomaterials in the environment.Crossref | GoogleScholarGoogle Scholar | 21284287PubMed |
Liochev SI, Fridovich I (2002) Copper, zinc superoxide dismutase and H2O2. Effects of bicarbonate on inactivation and oxidations of NADPH and Urate, and on consumption of H2O2. Journal of Biological Chemistry 277, 34674–34678.
| Copper, zinc superoxide dismutase and H2O2. Effects of bicarbonate on inactivation and oxidations of NADPH and Urate, and on consumption of H2O2.Crossref | GoogleScholarGoogle Scholar | 12107177PubMed |
Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. International Journal of Molecular Science 19, 335
| Lignins: biosynthesis and biological functions in plants.Crossref | GoogleScholarGoogle Scholar |
López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology 6, 280–287.
| The role of nutrient availability in regulating root architecture.Crossref | GoogleScholarGoogle Scholar | 12753979PubMed |
Lwin KM, Myint MM, Tar T, Aung WZM (2012) Isolation of plant hormone (indole-3-acetic acid-IAA) producing rhizobacteria and study on their effects on maize seedling. Engineering Journal (New York) 16, 137–144.
Ma Y, Kuang L, He X, Bai W, Ding Y, Zhang Z, Zhao Y, Chai Z (2010) Effects of rare earth oxide nanoparticles on root elongation of plants. Chemosphere 78, 273–279.
| Effects of rare earth oxide nanoparticles on root elongation of plants.Crossref | GoogleScholarGoogle Scholar | 19897228PubMed |
Manivannan P, Jaleel CA, Somasundaram R, Panneerselvam R (2008) Osmoregulation and antioxidant metabolism in drought-stressed Helianthus annuus under triadimefon drenching. Comptes Rendus Biologies 331, 418–425.
| Osmoregulation and antioxidant metabolism in drought-stressed Helianthus annuus under triadimefon drenching.Crossref | GoogleScholarGoogle Scholar | 18510994PubMed |
Marinou E, Chrysargyris A, Tzortzakis N (2013) Use of sawdust, coco soil and pumice in hydroponically grown strawberry. Plant, Soil and Environment 59, 452–459.
| Use of sawdust, coco soil and pumice in hydroponically grown strawberry.Crossref | GoogleScholarGoogle Scholar |
Martínez-Fernández D, Barroso D, Komárek M (2016) Root water transport of Helianthus annuus L. under iron oxide nanoparticle exposure. Environmental Science and Pollution Research International 23, 1732–1741.
| Root water transport of Helianthus annuus L. under iron oxide nanoparticle exposure.Crossref | GoogleScholarGoogle Scholar | 26396006PubMed |
Meziane D, Shipley B (2001) Direct and indirect relationships between specific leaf area, leaf nitrogen and leaf gas exchange. Effects of irradiance and nutrient supply. Annals of Botany 88, 915–927.
| Direct and indirect relationships between specific leaf area, leaf nitrogen and leaf gas exchange. Effects of irradiance and nutrient supply.Crossref | GoogleScholarGoogle Scholar |
Michael PI, Krishnaswamy M (2014) Membrane damage and activity of antioxidant enzymes in response to zinc and high irradiance stress in cowpea plant. International Journal of Current Research and Academic Review 2, 112–128.
Mousavi Kouhi SM, Lahouti M, Ganjeali A, Entezari MH (2014) Comparative phytotoxicity of ZnO nanoparticles, ZnO microparticles, and Zn2+ on rapeseed (Brassica napus L.): investigating a wide range of concentrations. Toxicological and Environmental Chemistry 96, 861–868.
| Comparative phytotoxicity of ZnO nanoparticles, ZnO microparticles, and Zn2+ on rapeseed (Brassica napus L.): investigating a wide range of concentrations.Crossref | GoogleScholarGoogle Scholar |
Nair PMG, Chung IM (2017) Regulation of morphological, molecular and nutrient status in Arabidopsis thaliana seedlings in response to ZnO nanoparticles and Zn ion exposure. The Science of the Total Environment 575, 187–198.
| Regulation of morphological, molecular and nutrient status in Arabidopsis thaliana seedlings in response to ZnO nanoparticles and Zn ion exposure.Crossref | GoogleScholarGoogle Scholar | 27741454PubMed |
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880.
Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology (London, England) 17, 372–386.
| Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi.Crossref | GoogleScholarGoogle Scholar |
O’Sullivan JN, Asher CJ, Blamey FPC (1997) ‘Nutrient disorders of sweet potato. ACIAR Monograph No. 48.’ (Australian Centre for International Agricultural Research: Canberra)
Prasad R, Shivay YS, Kumar D (2016) Interactions of zinc with other nutrients in soils and plants – a Review. Indian Journal of Fertilisers 12, 16–26.
Raddy R (2014) ‘Efficiency of nano zinc particle on growth and yield of crop plants.’ (University of Agricultural Sciences, Crop Physiology: Bangalore, India)
Radotić K, Dučić T, Mutavdžić D (2000) Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentrations of cadmium. Environmental and Experimental Botany 44, 105–113.
| Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentrations of cadmium.Crossref | GoogleScholarGoogle Scholar | 10996363PubMed |
Rahmani F, Peymani A, Daneshvand E, Biparva P (2016) Impact of zinc oxide and copper oxide nano-particles on physiological and molecular processes in Brassica napus. Indian Journal of Plant Physiology / Official Publication of the Indian Society for Plant Physiology 21, 122–128.
| Impact of zinc oxide and copper oxide nano-particles on physiological and molecular processes in Brassica napus.Crossref | GoogleScholarGoogle Scholar |
Raho G, Cassano N, D’Argento V, Vena GA, Zanotti F (2003) Over-expression of Mn-superoxide dismutase as a marker of oxidative stress in lesional skin of chronic idiopathic urticaria. Clinical and Experimental Dermatology 28, 318–320.
| Over-expression of Mn-superoxide dismutase as a marker of oxidative stress in lesional skin of chronic idiopathic urticaria.Crossref | GoogleScholarGoogle Scholar | 12780723PubMed |
Raskar SV, Laware SL (2014) Effect of zinc oxide nanoparticles on cytology and seed germination in onion. International Journal of Current Microbiology and Applied Sciences 3, 467–473.
Ray PC, Yu H, Fu PP (2009) Toxicity and environmental risks of nanomaterials: challenges and future needs. Journal of Environmental Science and Health. Part C, Environmental Carcinogenesis & Ecotoxicology Reviews 27, 1–35.
| Toxicity and environmental risks of nanomaterials: challenges and future needs.Crossref | GoogleScholarGoogle Scholar |
Resende MD, Nojosa GBA, Cavalcanti LS, Aguilar MAG, Silva LHCP, Perez JO, Andrade GCG, Carvalho GA, Castro RM (2002) Induction of resistance in cocoa against Crinipellis perniciosa and Verticillium dahliae by acibenzolar‐S‐methyl (ASM). Plant Pathology 51, 621–628.
| Induction of resistance in cocoa against Crinipellis perniciosa and Verticillium dahliae by acibenzolar‐S‐methyl (ASM).Crossref | GoogleScholarGoogle Scholar |
Ronen E 2007
Rui M, Ma C, Hao Y, Guo J, Rui Y, Tang X, Zhao Q, Fan X, Zhang Z, Hou T, Zhu S (2016) Iron oxide nanoparticles as a potential iron fertilizer for Peanut (Arachis hypogaea). Frontiers of Plant Science 7, 815
| Iron oxide nanoparticles as a potential iron fertilizer for Peanut (Arachis hypogaea).Crossref | GoogleScholarGoogle Scholar |
Sadeghzadeh B (2013) A review of zinc nutrition and plant breeding. Journal of Soil Science and Plant Nutrition 13, 905–927.
Salama ZA, Gaafar AA, El Fouly MM (2015) Genotypic variations in phenolic, flavonoids and their antioxidant activities in maize plants treated with Zn (II) HEDTA grown in salinized media. Agricultural Sciences 6, 397
| Genotypic variations in phenolic, flavonoids and their antioxidant activities in maize plants treated with Zn (II) HEDTA grown in salinized media.Crossref | GoogleScholarGoogle Scholar |
Samreen T, Humaira , Shah HU, Ullah S, Javid M (2017) Zinc effect on growth rate, chlorophyll, protein and mineral contents of hydroponically grown mungbeans plant (Vigna radiata). Arabian Journal of Chemistry 10, S1802–S1807.
| Zinc effect on growth rate, chlorophyll, protein and mineral contents of hydroponically grown mungbeans plant (Vigna radiata).Crossref | GoogleScholarGoogle Scholar |
Sanjay SS, Pandey AC, Singh M, Prasad MS (2015) Effects of functionalized ZnO nanoparticles on the phytohormones: growth and development of Solanum melongena L. (Brinjal) plant. World Journal of Pharmaceutical Research 5, 1990–2009.
Sekimoto H, Hoshi M, Nomura T, Yokota T (1997) Zinc deficiency affects the levels of endogenous gibberellins in Zea mays L. Plant and Cell Physiology 38, 1087–1090.
| Zinc deficiency affects the levels of endogenous gibberellins in Zea mays L.Crossref | GoogleScholarGoogle Scholar |
Shah F, Watson C, Cabrera E (2002) Seed vigour testing of subtropical corn hybrids. Mississippi Agricultural and Forestry Experiment Station Research Report 23(2).
Shahriaripour R, Tajabadipour A (2010) Zinc nutrition of pistachio: Interaction of zinc with other trace elements. Communications in Soil Science and Plant Analysis 41, 1885–1888.
| Zinc nutrition of pistachio: Interaction of zinc with other trace elements.Crossref | GoogleScholarGoogle Scholar |
Siddiqi KS, Husen A (2017) Plant response to engineered metal oxide nanoparticles. Nanoscale Research Letters 12, 92
| Plant response to engineered metal oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar | 28168616PubMed |
Siddiqi MY, Glass AD, Ruth TJ, Fernando M (1989) Studies of the regulation of nitrate influx by barley seedlings using 13NO3 –. Plant Physiology 90, 806–813.
| Studies of the regulation of nitrate influx by barley seedlings using 13NO3 –.Crossref | GoogleScholarGoogle Scholar | 16666881PubMed |
Sirelkhatim A, Mahmud S, Seeni A, Kaus NHM, Ann LC, Bakhori SKM, Hasan H, Mohamad D (2015) Review on zinc oxide nanoparticles: antibacterial activity and toxicity mechanism. Nano-Micro Letters 7, 219–242.
| Review on zinc oxide nanoparticles: antibacterial activity and toxicity mechanism.Crossref | GoogleScholarGoogle Scholar | 30464967PubMed |
Soland S, Laima S (1999) Phenolics and cold tolerance of Brassica napus. Plant Agriculture 1, 1–5.
Somogyi M (1952) Notes on sugar determination. The Journal of Biological Chemistry 195, 19–23.
Taranto F, Pasqualone A, Mangini G, Tripodi P, Miazzi MM, Pavan S, Montemurro C (2017) Polyphenol oxidases in crops: biochemical, physiological and genetic aspects. International Journal of Molecular Sciences 18, 377
| Polyphenol oxidases in crops: biochemical, physiological and genetic aspects.Crossref | GoogleScholarGoogle Scholar |
Terzi R, Güler NS, Çalişkan NK, Kadioğlu A (2013) Lignification response for rolled leaves of Ctenanthe setosa under long-term. Turkish Journal of Biology 37, 614–619.
| Lignification response for rolled leaves of Ctenanthe setosa under long-term.Crossref | GoogleScholarGoogle Scholar |
Volschenk CG, Hunter JJ, Watts JE (1996) The effect of different zinc levels on the growth of grapevines. Journal of Plant Nutrition 19, 827–837.
| The effect of different zinc levels on the growth of grapevines.Crossref | GoogleScholarGoogle Scholar |
Wang X, Yang X, Chen S, Li Q, Wang W, Hou C, Gao X, Wang L, Wang S (2015) Zinc oxide nanoparticles affect biomass accumulation and photosynthesis in Arabidopsis. Frontiers of Plant Science 6, 1243
Yu Q, Rengel Z (1999) Micronutrient deficiency influences plant growth and activities of superoxide dismutases in narrow-leafed lupins. Annals of Botany 83, 175–182.
| Micronutrient deficiency influences plant growth and activities of superoxide dismutases in narrow-leafed lupins.Crossref | GoogleScholarGoogle 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. Frontiers of Plant Science 7, 535
| Effect of ZnO nanoparticles on Brassica nigra seedlings and stem explants: growth dynamics and antioxidative response.Crossref | GoogleScholarGoogle Scholar |
