Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Nitric oxide overcomes copper and copper oxide nanoparticle-induced toxicity in Sorghum vulgare seedlings through regulation of ROS and proline metabolism

Swati Singh A , Nidhi Kandhol B , Sangeeta Pandey https://orcid.org/0000-0001-9044-3144 C , Vijay Pratap Singh https://orcid.org/0000-0002-5772-5438 D * , Durgesh Kumar Tripathi B * and Devendra Kumar Chauhan A *
+ Author Affiliations
- Author Affiliations

A D D Pant Interdisciplinary Research Lab, Department of Botany, University of Allahabad, Prayagraj 211002, India.

B Crop Nanobiology and Molecular Stress Physiology Lab, Amity Institute of Organic Agriculture (AIOA) Amity University Uttar Pradesh, Noida, Sector 125, Noida, Uttar Pradesh 201313, India.

C Plant and Microbe Interaction Lab, Amity Institute of Organic Agriculture (AIOA) Amity University Uttar Pradesh, Noida, Sector 125, Noida, Uttar Pradesh 201313, India.

D Plant Physiology Laboratory, Department of Botany, C.M.P. Degree Collage, A Constituent Post Graduate College of University of Allahabad, Prayagraj 211002, India.


Handling Editor: Suleyman Allakhverdiev

Functional Plant Biology - https://doi.org/10.1071/FP22021
Submitted: 9 February 2022  Accepted: 28 July 2022   Published online: 11 October 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

This study aimed to investigate the phytotoxic effect of copper (Cu) and copper nanoparticles (CuONPs) and ameliorative potential of nitric oxide (NO) against these toxic materials in Sorghum vulgare Pers. seedlings. Data suggested that exposure of Cu and CuONPs significantly reduced growth, chlorophyll, carotenoids and protein in root and shoot, which coincided with increased Cu accumulation. However, addition of sodium nitroprusside (SNP, a donor of NO) lowered Cu and CuONPs mediated toxicity through restricting Cu accumulation and improving photosynthetic pigments and total soluble protein contents. Data further suggested that exposure of Cu and CuONPs significantly increased hydrogen peroxide (H2O2), superoxide radicals (O2•−), and malondialdehyde (MDA) contents. Enhanced level of oxidative stress severely inhibited the enzymatic activities of glutathione reductase (GR), ascorbate peroxidase (APX), dehydroascorbate reductase (DHAR) and monodehydroascorbate reductase (MDHAR) but enhanced superoxide dismutase (SOD) and catalase (CAT) activity. However, addition of SNP positively regulated antioxidants enzymes activity, particularly the enzymes involved in the ascorbate-glutathione cycle to overcome Cu- and CuONPs-induced stress in Sorghum seedlings. Further, Cu and CuONPs enhanced accumulation of free proline through inducing Δ1-pyrroline-5-carboxylate synthetase (P5CS) activity while lowering the proline dehydrogenase (PDH) activity. However, addition of SNP reversed these responses. Therefore, overall results revealed that SNP has enough potential of reducing the toxicity of Cu and CuONPs in Sorghum seedlings through regulation of proline metabolism and activity of enzymes of the ascorbate-glutathione cycle. These findings can be employed in developing new resistant varieties of Sorghum having enhanced tolerance against Cu or CuONP stress and improved productivity.

Keywords: CuONPs, enzymes, nitric oxide, oxidative stress, photosynthesis, proline metabolism, sodium nitroprusside, sorghum.


References

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.
Catalase in vitro.Crossref | GoogleScholarGoogle Scholar |

Aguirre G, Pilon M (2016) Copper delivery to chloroplast proteins and its regulation. Frontiers in Plant Science 6, 1250
Copper delivery to chloroplast proteins and its regulation.Crossref | GoogleScholarGoogle Scholar |

Ahsan N, Lee D-G, Lee S-H, Kang KY, Lee JJ, Kim PJ, Yoon H-S, Kim J-S, Lee B-H (2007) Excess copper induced physiological and proteomic changes in germinating rice seeds. Chemosphere 67, 1182–1193.
Excess copper induced physiological and proteomic changes in germinating rice seeds.Crossref | GoogleScholarGoogle Scholar |

Ali MA, Fahad S, Haider I, Ahmed N, Ahmad S, Hussain S, Arshad M (2019) Oxidative stress and antioxidant defense in plants exposed to metal/metalloid toxicity. In ‘Reactive oxygen, nitrogen and sulfur species in plants: production, metabolism, signaling and defense mechanisms’. (Eds M Hasanuzzaman, V Fotopoulos, K Nahar, M Fujita) pp. 353–370. (John Wiley & Sons Ltd.)

Andresen E, Peiter E, Küpper H (2018) Trace metal metabolism in plants. Journal of Experimental Botany 69, 909–954.
Trace metal metabolism in plants.Crossref | GoogleScholarGoogle Scholar |

Apodaca SA, Tan W, Dominguez OE, Hernandez-Viezcas JA, Peralta-Videa JR, Gardea-Torresdey JL (2017) Physiological and biochemical effects of nanoparticulatecopper, bulk copper, copper chloride, and kinetin in bush bean (Phaseolus vulgaris) plants. Science of The Total Environment 599-600, 2085–2094.
Physiological and biochemical effects of nanoparticulatecopper, bulk copper, copper chloride, and kinetin in bush bean (Phaseolus vulgaris) plants.Crossref | GoogleScholarGoogle Scholar |

Arif N, Yadav V, Singh S, Tripathi DK, Dubey NK, Chauhan DK, Giorgetti L (2018) Interaction of copper oxide nanoparticles with plants: uptake, accumulation, and toxicity. In ‘Nanomaterials in plants, algae, and microorganisms’. (Eds DK Tripathi, P Ahmad, S Sharma, DK Chauhan, NK Dubey) pp. 297–310. (Academic Press)

Aruoja V, Dubourguier H-C, Kasemets K, Kahru A (2009) Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Science of The Total Environment 407, 1461–1468.
Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata.Crossref | GoogleScholarGoogle Scholar |

Bajguz A (2014) Nitric oxide: role in plants under abiotic stress. In ‘Physiological mechanisms and adaptation strategies in plants under changing environment.’ pp. 137–159. (Springer: New York, NY)

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar |

Bhuyan MHMB, Hasanuzzaman M, Parvin K, Mohsin SM, Al Mahmud J, Nahar K, Fujita M (2020) Nitric oxide and hydrogen sulfide: two intimate collaborators regulating plant defense against abiotic stress. Plant Growth Regulation 90, 409–424.
Nitric oxide and hydrogen sulfide: two intimate collaborators regulating plant defense against abiotic stress.Crossref | GoogleScholarGoogle Scholar |

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 |

Chaki M, Begara-Morales JC, Barroso JB (2020) Oxidative stress in plants. Antioxidants 9, 481
Oxidative stress in plants.Crossref | GoogleScholarGoogle Scholar |

Chen J, Liu X, Wang C, Yin S-S, Li X-L, Hu W-J, Simon M, Shen Z-J, Xiao Q, Chu C-C, Peng X-X, Zheng H-L (2015) Nitric oxide ameliorates zinc oxide nanoparticles-induced phytotoxicity in rice seedlings. Journal of Hazardous Materials 297, 173–182.
Nitric oxide ameliorates zinc oxide nanoparticles-induced phytotoxicity in rice seedlings.Crossref | GoogleScholarGoogle Scholar |

Cota-Ruiz K, Hernández-Viezcas JA, Varela-Ramírez A, Valdés C, Núñez-Gastélum JA, Martínez-Martínez A, Delgado-Rios M, Peralta-Videa JR, Gardea-Torresdey JL (2018) Toxicity of copper hydroxide nanoparticles, bulk copper hydroxide, and ionic copper to alfalfa plants: a spectroscopic and gene expression study. Environmental Pollution 243, 703–712.
Toxicity of copper hydroxide nanoparticles, bulk copper hydroxide, and ionic copper to alfalfa plants: a spectroscopic and gene expression study.Crossref | GoogleScholarGoogle Scholar |

de la Rosa G, García-Castañeda C, Vázquez-Núñez E, Alonso-Castro AJ, Basurto-Islas G, Mendoza A, Cruz-Jimenez G, Molina C (2017) Physiological and biochemical response of plants to engineered NMs: implications on future design. Plant Physiology and Biochemistry 110, 226–235.
Physiological and biochemical response of plants to engineered NMs: implications on future design.Crossref | GoogleScholarGoogle Scholar |

De La Torre-Roche R, Hawthorne J, Musante C, Xing B, Newman LA, Ma X, White JC (2013) Impact of Ag nanoparticle exposure on p,p′-DDE bioaccumulation by Cucurbita pepo (zucchini) and Glycine max (soybean). Environmental Science and Technology 47, 718–725.
Impact of Ag nanoparticle exposure on p,p′-DDE bioaccumulation by Cucurbita pepo (zucchini) and Glycine max (soybean).Crossref | GoogleScholarGoogle Scholar |

del Río LA (2015) ROS and RNS in plant physiology: an overview. Journal of Experimental Botany 66, 2827–2837.
ROS and RNS in plant physiology: an overview.Crossref | GoogleScholarGoogle Scholar |

Deng R, Lin D, Zhu L, Majumdar S, White JC, Gardea-Torresdey JL, Xing B (2017) Nanoparticle interactions with co-existing contaminants: joint toxicity, bioaccumulation and risk. Nanotoxicology 11, 591–612.
Nanoparticle interactions with co-existing contaminants: joint toxicity, bioaccumulation and risk.Crossref | GoogleScholarGoogle Scholar |

Dimkpa CO, McLean JE, Latta DE, Manangon 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 |

Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2004) Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. Biometals 17, 379–387.
Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Droppa M, Horvàth G (1990) The role of copper in photosynthesis. Critical Reviews in Plant Sciences 9, 111–123.
The role of copper in photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Du W, Tan W, Peralta-Videa JR, Gardea-Torresdey JL, Ji R, Yin Y, Guo H (2017) Interaction of metal oxide nanoparticles with higher terrestrial plants: physiological and biochemical aspects. Plant Physiology and Biochemistry 110, 210–225.
Interaction of metal oxide nanoparticles with higher terrestrial plants: physiological and biochemical aspects.Crossref | GoogleScholarGoogle Scholar |

Dubey S, Shri M, Gupta A, Rani V, Chakrabarty D (2018) Toxicity and detoxification of heavy metals during plant growth and metabolism. Environmental Chemistry Letters 16, 1169–1192.
Toxicity and detoxification of heavy metals during plant growth and metabolism.Crossref | GoogleScholarGoogle Scholar |

Elisa B, Marsano F, Cavaletto M, Berta G (2007) Copper stress in Cannabis sativa roots: morphological and proteomic analysis. Caryologia 60, 96–101.
Copper stress in Cannabis sativa roots: morphological and proteomic analysis.Crossref | GoogleScholarGoogle Scholar |

Fancy NN, Bahlmann A-K, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant, Cell & Environment 40, 462–472.
Nitric oxide function in plant abiotic stress.Crossref | GoogleScholarGoogle Scholar |

Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiology 155, 93–100.
Understanding oxidative stress and antioxidant functions to enhance photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Frahry G, Schopfer P (2001) NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 212, 175–183.
NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay.Crossref | GoogleScholarGoogle Scholar |

García-Ríos M, Fujita T, LaRosa PC, Locy RD, Clithero JM, Bressan RA, Csonka LN (1997) Cloning of a polycistronic cDNA from tomato encoding γ-glutamyl kinase and γ-glutamyl phosphate reductase. Proceedings of the National Academy of Sciences of the United States of America 94, 8249–8254.
Cloning of a polycistronic cDNA from tomato encoding γ-glutamyl kinase and γ-glutamyl phosphate reductase.Crossref | GoogleScholarGoogle Scholar |

Ghori N-H, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, Ozturk M (2019) Heavy metal stress and responses in plants. International Journal of Environmental Science and Technology 16, 1807–1828.
Heavy metal stress and responses in plants.Crossref | GoogleScholarGoogle Scholar |

Ghosh S (2020) Protective role of sodium nitroprusside in overcoming diverse environmental stresses in plants. In ‘Protective chemical agents in the amelioration of plant abiotic stress: biochemical and molecular perspectives’. (Eds A Roychoudhury, DK Tripathi) pp. 238–253. (John Wiley & Sons Ltd)

Ghosh UK, Islam MN, Siddiqui MN, Cao X, Khan MAR (2022) Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms. Plant Biology 24, 227–239.
Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms.Crossref | GoogleScholarGoogle Scholar |

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 |

Gjorgieva Ackova D (2018) Heavy metals and their general toxicity on plants. Plant Science Today 5, 14–18.
Heavy metals and their general toxicity on plants.Crossref | GoogleScholarGoogle Scholar |

Guo Y, Marschner H (1995) Uptake, distribution, and binding of cadmium and nickel in different plant species. Journal of Plant Nutrition 18, 2691–2706.
Uptake, distribution, and binding of cadmium and nickel in different plant species.Crossref | GoogleScholarGoogle Scholar |

Hameed A, Farooq T, Hameed A, Sheikh MA (2021) Sodium nitroprusside mediated priming memory invokes water-deficit stress acclimation in wheat plants through physio-biochemical alterations. Plant Physiology and Biochemistry 160, 329–340.
Sodium nitroprusside mediated priming memory invokes water-deficit stress acclimation in wheat plants through physio-biochemical alterations.Crossref | GoogleScholarGoogle Scholar |

Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In ‘Crop stress and its management: perspectives and strategies.’ (pp. 261–315). (Springer: Dordrecht)

Hasanuzzaman M, Bhuyan MHMB, Anee TI, Parvin K, Nahar K, Mahmud JA, Fujita M (2019) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8, 384
Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress.Crossref | GoogleScholarGoogle Scholar |

Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar |

Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station, 347(2nd edn).

Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant and Cell Physiology 25, 385–395.
Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide.Crossref | GoogleScholarGoogle Scholar |

Hong J, Peralta-Videa JR, Rico C, Sahi S, Viveros MN, Bartonjo J, Zhao L, Gardea-Torresdey JL (2014) Evidence of translocation and physiological impacts of foliar applied CeO2 nanoparticles on cucumber (Cucumis sativus) plants. Environmental Science & Technology 48, 4376–4385.
Evidence of translocation and physiological impacts of foliar applied CeO2 nanoparticles on cucumber (Cucumis sativus) plants.Crossref | GoogleScholarGoogle Scholar |

Hong J, Rico CM, Zhao L, Adeleye AS, Keller AA, Peralta-Videa JR, Gardea-Torresdey JL (2015) Toxic effects of copper-based nanoparticles or compounds to lettuce (Lactuca sativa) and alfalfa (Medicago sativa). Environmental Science: Processes & Impacts 17, 177–185.
Toxic effects of copper-based nanoparticles or compounds to lettuce (Lactuca sativa) and alfalfa (Medicago sativa).Crossref | GoogleScholarGoogle Scholar |

Jabeen Z, Fayyaz HA, Irshad F, Hussain N, Hassan MN, Li J, Rehman S, Haider W, Yasmin H, Mumtaz S, Bukhari SAH, Khalofah A, Al-Qthanin RN, Alsubeie MS (2021) Sodium nitroprusside application improves morphological and physiological attributes of soybean (Glycine max L.) under salinity stress. PLoS ONE 16, e0248207
Sodium nitroprusside application improves morphological and physiological attributes of soybean (Glycine max L.) under salinity stress.Crossref | GoogleScholarGoogle Scholar |

Kumar V, Pandita S, Sidhu GPS, Sharma A, Khanna K, Kaur P, Bali AS, Setia R (2021) Copper bioavailability, uptake, toxicity and tolerance in plants: a comprehensive review. Chemosphere 262, 127810
Copper bioavailability, uptake, toxicity and tolerance in plants: a comprehensive review.Crossref | GoogleScholarGoogle Scholar |

Lasso-Robledo JL, Torres B, Peralta-Videa JR (2022) Do all Cu nanoparticles have similar applications in nano-enabled agriculture? Plant Nano Biology 1, 100006
Do all Cu nanoparticles have similar applications in nano-enabled agriculture?Crossref | GoogleScholarGoogle Scholar |

Lee W-M, An Y-J, Yoon H, Kweon H-S (2008) Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles. Environmental Toxicology and Chemistry 27, 1915–1921.
Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles.Crossref | GoogleScholarGoogle Scholar |

Lehotai N, Pető A, Weisz M, Erdei L, Kolbert Z (2011) Generation of reactive oxygen and nitrogen species in pea cultivars under copper exposure. Acta Biologica Szegediensis 55, 273–278.

Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxidants & Redox Signaling 19, 998–1011.
Proline mechanisms of stress survival.Crossref | GoogleScholarGoogle Scholar |

Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.Crossref | GoogleScholarGoogle Scholar |

Maksymiec W (2007) Signaling responses in plants to heavy metal stress. Acta Physiologiae Plantarum 29, 177–187.
Signaling responses in plants to heavy metal stress.Crossref | GoogleScholarGoogle Scholar |

Małkowski E, Sitko K, Zieleźnik-Rusinowska P, Gieroń Ż, Szopiński M (2019) Heavy metal toxicity: physiological implications of metal toxicity in plants. In ‘Plant metallomics and functional omics.’ (pp. 253–301). (Springer: Cham)

Medina-Velo IA, Peralta-Videa JR, Gardea-Torresdey JL (2017) Assessing plant uptake and transport mechanisms of engineered nanomaterials from soil. MRS Bulletin 42, 379–384.
Assessing plant uptake and transport mechanisms of engineered nanomaterials from soil.Crossref | GoogleScholarGoogle Scholar |

Migocka M, Malas K (2018) Plant responses to copper: molecular and regulatory mechanisms of copper uptake, distribution and accumulation in plants. In ‘Plant micronutrient use efficiency.’ pp. 71–86. (Academic Press)

Miller G, Honig A, Stein H, Suzuki N, Mittler R, Zilberstein A (2009) Unraveling Δ1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. Journal of Biological Chemistry 284, 26482–26492.
Unraveling Δ1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes.Crossref | GoogleScholarGoogle Scholar |

Mir AR, Pichtel J, Hayat S (2021) Copper: uptake, toxicity and tolerance in plants and management of Cu-contaminated soil. Biometals 34, 737–759.
Copper: uptake, toxicity and tolerance in plants and management of Cu-contaminated soil.Crossref | GoogleScholarGoogle Scholar |

Mittal S, Kumari N, Sharma V (2012) Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiology and Biochemistry 54, 17–26.
Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes.Crossref | GoogleScholarGoogle Scholar |

Morales MI, Rico CM, Hernandez-Viezcas JA, Nunez JE, Barrios AC, Tafoya A, Flores-Marges JP, Peralta-Videa JR, Gardea-Torresdey JL (2013) Toxicity assessment of cerium oxide nanoparticles in cilantro (Coriandrum sativum L.) plants grown in organic soil. Journal of Agricultural and Food Chemistry 61, 6224–6230.
Toxicity assessment of cerium oxide nanoparticles in cilantro (Coriandrum sativum L.) plants grown in organic soil.Crossref | GoogleScholarGoogle Scholar |

Moustakas M, Malea P, Haritonidou K, Sperdouli I (2017) Copper bioaccumulation, photosystem II functioning, and oxidative stress in the seagrass Cymodocea nodosa exposed to copper oxide nanoparticles. Environmental Science and Pollution Research 24, 16007–16018.
Copper bioaccumulation, photosystem II functioning, and oxidative stress in the seagrass Cymodocea nodosa exposed to copper oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar |

Musante C, White JC (2012) Toxicity of silver and copper to Cucurbita pepo: differential effects of nano and bulk size particles. Environmental Toxicology 27, 510–517.
Toxicity of silver and copper to Cucurbita pepo: differential effects of nano and bulk size particles.Crossref | GoogleScholarGoogle Scholar |

Nair PMG, Chung IM (2014) A mechanistic study on the toxic effect of copper oxide nanoparticles in soybean (Glycine max L.) root development and lignification of root cells. Biological Trace Element Research 162, 342–352.
A mechanistic study on the toxic effect of copper oxide nanoparticles in soybean (Glycine max L.) root development and lignification of root cells.Crossref | GoogleScholarGoogle Scholar |

Nair PMG, Chung IM (2015) Study on the correlation between copper oxide nanoparticles induced growth suppression and enhanced lignification in Indian mustard (Brassica juncea L.). Ecotoxicology and Environmental Safety 113, 302–313.
Study on the correlation between copper oxide nanoparticles induced growth suppression and enhanced lignification in Indian mustard (Brassica juncea L.).Crossref | GoogleScholarGoogle Scholar |

Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867–880.
Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.Crossref | GoogleScholarGoogle Scholar |

Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311, 622–627.
Toxic potential of materials at the nanolevel.Crossref | GoogleScholarGoogle Scholar |

Ochoa L, Medina-Velo IA, Barrios AC, Bonilla-Bird NJ, Hernandez-Viezcas JA, Peralta-Videa JR, Gardea-Torresdey JL (2017) Modulation of CuO nanoparticles toxicity to green pea (Pisum sativum Fabaceae) by the phytohormone indole-3-acetic acid. Science of The Total Environment 598, 513–524.
Modulation of CuO nanoparticles toxicity to green pea (Pisum sativum Fabaceae) by the phytohormone indole-3-acetic acid.Crossref | GoogleScholarGoogle Scholar |

Peng C, Duan D, Xu C, Chen Y, Sun L, Zhang H, Yuan X, Zheng L, Yang Y, Yang J, Zhen X (2015) Translocation and biotransformation of CuO nanoparticles in rice (Oryza sativa L.) plants. Environmental Pollution 197, 99–107.
Translocation and biotransformation of CuO nanoparticles in rice (Oryza sativa L.) plants.Crossref | GoogleScholarGoogle Scholar |

Perreault F, Samadani M, Dewez D (2014) Effect of soluble copper released from copper oxide nanoparticles solubilisation on growth and photosynthetic processes of Lemna gibba L. Nanotoxicology 8, 374–382.
Effect of soluble copper released from copper oxide nanoparticles solubilisation on growth and photosynthetic processes of Lemna gibba L.Crossref | GoogleScholarGoogle Scholar |

Printz B, Lutts S, Hausman J-F, Sergeant K (2016) Copper trafficking in plants and its implication on cell wall dynamics. Frontiers in Plant Science 7, 601
Copper trafficking in plants and its implication on cell wall dynamics.Crossref | GoogleScholarGoogle Scholar |

Rejeb KB, Abdelly C, Savouré A (2014) How reactive oxygen species and proline face stress together. Plant Physiology and Biochemistry 80, 278–284.
How reactive oxygen species and proline face stress together.Crossref | GoogleScholarGoogle Scholar |

Rena AB, Splittstoesser WE (1975) Proline dehydrogenase and pyrroline-5-carboxylate reductase from pumpkin cotyledons. Phytochemistry 14, 657–661.
Proline dehydrogenase and pyrroline-5-carboxylate reductase from pumpkin cotyledons.Crossref | GoogleScholarGoogle Scholar |

Rousk J, Ackermann K, Curling SF, Jones DL (2012) Comparative toxicity of nanoparticulate CuO and ZnO to soil bacterial communities. PLoS ONE 7, e34197
Comparative toxicity of nanoparticulate CuO and ZnO to soil bacterial communities.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Fahad S, Khan SU, Din M, Ullah A, Sabagh AEL, Hossain A, Llanes A, Liu L (2020) Copper-induced oxidative stress, initiation of antioxidants and phytoremediation potential of flax (Linum usitatissimum L.) seedlings grown under the mixing of two different soils of China. Environmental Science and Pollution Research 27, 5211–5221.
Copper-induced oxidative stress, initiation of antioxidants and phytoremediation potential of flax (Linum usitatissimum L.) seedlings grown under the mixing of two different soils of China.Crossref | GoogleScholarGoogle Scholar |

Sami F, Faizan M, Faraz A, Siddiqui H, Yusuf M, Hayat S (2018) Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide 73, 22–38.
Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress.Crossref | GoogleScholarGoogle Scholar |

Sandeep G, Vijayalatha KR, Anitha T (2019) Heavy metals and its impact in vegetable crops. International Journal of Chemical Studies 7, 1612–1621.

Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiology 59, 1011–1012.
Chloroplast glutathione reductase.Crossref | GoogleScholarGoogle Scholar |

Servin AD, White JC (2016) Nanotechnology in agriculture: next steps for understanding engineered nanoparticle exposure and risk. NanoImpact 1, 9–12.
Nanotechnology in agriculture: next steps for understanding engineered nanoparticle exposure and risk.Crossref | GoogleScholarGoogle Scholar |

Servin A, Elmer W, Mukherjee A, De la Torre-Roche R, Hamdi H, White JC, Bindraban P, Dimkpa C (2015) A review of the use of engineered nanomaterials to suppress plant disease and enhance crop yield. Journal of Nanoparticle Research 17, 92
A review of the use of engineered nanomaterials to suppress plant disease and enhance crop yield.Crossref | GoogleScholarGoogle Scholar |

Shabbir Z, Sardar A, Shabbir A, Abbas G, Shamshad S, Khalid S, Murtaza G, Dumat C, Shahid M (2020) Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment. Chemosphere 259, 127436
Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment.Crossref | GoogleScholarGoogle Scholar |

Shaw AK, Hossain Z (2013) Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere 93, 906–915.
Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings.Crossref | GoogleScholarGoogle Scholar |

Siddique A, Kandpal G, Kumar P (2018) Proline accumulation and its defensive role under diverse stress condition in plants: an overview. Journal of Pure and Applied Microbiology 12, 1655–1659.
Proline accumulation and its defensive role under diverse stress condition in plants: an overview.Crossref | GoogleScholarGoogle Scholar |

Siddiqui MH, Alamri SA, Al-Khaishany MYY, Al-Qutami MA, Ali HM, Khan MN (2017) Sodium nitroprusside and indole acetic acid improve the tolerance of tomato plants to heat stress by protecting against DNA damage. Journal of Plant Interactions 12, 177–186.
Sodium nitroprusside and indole acetic acid improve the tolerance of tomato plants to heat stress by protecting against DNA damage.Crossref | GoogleScholarGoogle Scholar |

Simontacchi M, Galatro A, Ramos-Artuso F, Santa-María GE (2015) Plant survival in a changing environment: the role of nitric oxide in plant responses to abiotic stress. Frontiers in Plant Science 6, 977
Plant survival in a changing environment: the role of nitric oxide in plant responses to abiotic stress.Crossref | GoogleScholarGoogle Scholar |

Singh VP, Srivastava PK, Prasad SM (2013) Nitric oxide alleviates arsenic-induced toxic effects in ridged Luffa seedlings. Plant Physiology and Biochemistry 71, 155–163.
Nitric oxide alleviates arsenic-induced toxic effects in ridged Luffa seedlings.Crossref | GoogleScholarGoogle Scholar |

Singh VP, Singh S, Kumar J, Prasad SM (2015a) Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate–glutathione cycle: possible involvement of nitric oxide. Journal of Plant Physiology 181, 20–29.
Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate–glutathione cycle: possible involvement of nitric oxide.Crossref | GoogleScholarGoogle Scholar |

Singh M, Singh VP, Dubey G, Prasad SM (2015b) Exogenous proline application ameliorates toxic effects of arsenate in Solanum melongena L. seedlings. Ecotoxicology and Environmental Safety 117, 164–173.
Exogenous proline application ameliorates toxic effects of arsenate in Solanum melongena L. seedlings.Crossref | GoogleScholarGoogle Scholar |

Singh VP, Singh S, Tripathi DK, Prasad SM, Chauhan DK (2021) ‘Plant responses to nanomaterials.’ (Springer International Publishing)

Sudo E, Itouga M, Yoshida-Hatanaka K, Ono Y, Sakakibara H (2008) Gene expression and sensitivity in response to copper stress in rice leaves. Journal of Experimental Botany 59, 3465–3474.
Gene expression and sensitivity in response to copper stress in rice leaves.Crossref | GoogleScholarGoogle Scholar |

Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant J 11, 1187–1194.
Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction.Crossref | GoogleScholarGoogle Scholar |

Thounaojam TC, Panda P, Mazumdar P, Kumar D, Sharma GD, Sahoo L, Sanjib P (2012) Excess copper induced oxidative stress and response of antioxidants in rice. Plant Physiology and Biochemistry 53, 33–39.
Excess copper induced oxidative stress and response of antioxidants in rice.Crossref | GoogleScholarGoogle Scholar |

Tiwari PK, Shweta , Singh AK, Singh VP, Prasad SM, Ramawat N, Tripathi DK, Chauhan DK, Rai AK (2019) Liquid assisted pulsed laser ablation synthesized copper oxide nanoparticles (CuO-NPs) and their differential impact on rice seedlings. Ecotoxicology Environmental Safety 176, 321–329.
Liquid assisted pulsed laser ablation synthesized copper oxide nanoparticles (CuO-NPs) and their differential impact on rice seedlings.Crossref | GoogleScholarGoogle Scholar |

Tripathi DK, Ahmad P, Sharma S, Chauhan DK, Dubey NK (Eds) (2017a) ‘Nanomaterials in plants, algae, and microorganisms: concepts and controversies. Vol. 1.’ (Academic Press)

Tripathi DK, Mishra RK, Singh S, Singh S, Vishwakarma K, Sharma S, Singh VP, Singh PK, Prasad SM, Dubey NK, Pandey AC, Sahi S, Chauhan DK (2017b) Nitric oxide ameliorates zinc oxide nanoparticles phytotoxicity in wheat seedlings: implication of the ascorbate–glutathione cycle. Frontiers in Plant Science 8, 1
Nitric oxide ameliorates zinc oxide nanoparticles phytotoxicity in wheat seedlings: implication of the ascorbate–glutathione cycle.Crossref | GoogleScholarGoogle Scholar |

Tripathi DK, Singh S, Singh S, et al. (2017c) An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity. Plant Physiology and Biochemistry 110, 2–12.
An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity.Crossref | GoogleScholarGoogle Scholar |

Trujillo-Reyes J, Majumdar S, Botez CE, Peralta-Videa JR, Gardea-Torresdey JL (2014) Exposure studies of core–shell Fe/Fe3O4 and Cu/CuO NPs to lettuce (Lactuca sativa) plants: are they a potential physiological and nutritional hazard? Journal of Hazardous Materials 267, 255–263.
Exposure studies of core–shell Fe/Fe3O4 and Cu/CuO NPs to lettuce (Lactuca sativa) plants: are they a potential physiological and nutritional hazard?Crossref | GoogleScholarGoogle Scholar |

Usman M, Farooq M, Wakeel A, Nawaz A, Cheema SA, ur Rehman H, Ashraf I, Sanaullah M (2020) Nanotechnology in agriculture: current status, challenges and future opportunities. Science of The Total Environment 721, 137778
Nanotechnology in agriculture: current status, challenges and future opportunities.Crossref | GoogleScholarGoogle Scholar |

Vatansever R, Ozyigit II, Filiz E (2017) Essential and beneficial trace elements in plants, and their transport in roots: a review. Applied Biochemistry and Biotechnology 181, 464–482.
Essential and beneficial trace elements in plants, and their transport in roots: a review.Crossref | GoogleScholarGoogle Scholar |

Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science 151, 59–66.
Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines.Crossref | GoogleScholarGoogle Scholar |

Wang Z, Li J, Zhao J, Xing B (2011) Toxicity and internalization of CuO nanoparticles to prokaryotic alga Microcystis aeruginosa as affected by dissolved organic matter. Environmental Science & Technology 45, 6032–6040.
Toxicity and internalization of CuO nanoparticles to prokaryotic alga Microcystis aeruginosa as affected by dissolved organic matter.Crossref | GoogleScholarGoogle Scholar |

Wang P, Lombi E, Sun S, Scheckel KG, Malysheva A, McKenna BA, Menzies NW, Zhao F-J, Kopittke PM (2017) Characterizing the uptake, accumulation and toxicity of silver sulfide nanoparticles in plants. Environmental Science: Nano 4, 448–460.
Characterizing the uptake, accumulation and toxicity of silver sulfide nanoparticles in plants.Crossref | GoogleScholarGoogle Scholar |

Wu SG, Huang L, Head J, Chen D-R, Kong I-C, Tang YJ (2012) Phytotoxicity of metal oxide nanoparticles is related to both dissolved metals ions and adsorption of particles on seed surfaces. Journal of Petroleum & Environmental Biotechnology 3, 126
Phytotoxicity of metal oxide nanoparticles is related to both dissolved metals ions and adsorption of particles on seed surfaces.Crossref | GoogleScholarGoogle Scholar |

Yasir TA, Khan A, Skalicky M, Wasaya A, Rehmani MIA, Sarwar N, Mubeen K, Aziz M, Hassan MM, Hassan FAS, Iqbal MA, Brestic M, Islam MS, Danish S, Sabagh AEL (2021) Exogenous sodium nitroprusside mitigates salt stress in lentil (Lens culinaris Medik.) by affecting the growth, yield, and biochemical properties. Molecules 26, 2576
Exogenous sodium nitroprusside mitigates salt stress in lentil (Lens culinaris Medik.) by affecting the growth, yield, and biochemical properties.Crossref | GoogleScholarGoogle Scholar |

Yuan H-M, Xu H-H, Liu W-C, Lu Y-T (2013) Copper regulates primary root elongation through PIN1-mediated auxin redistribution. Plant and Cell Physiology 54, 766–778.
Copper regulates primary root elongation through PIN1-mediated auxin redistribution.Crossref | GoogleScholarGoogle Scholar |

Zhang Z, Ke M, Qu Q, Peijnenburg WJGM, Lu T, Zhang Q, Ye Y, Xu P, Du B, Sun L, Qian H (2018) Impact of copper nanoparticles and ionic copper exposure on wheat (Triticum aestivum L.) root morphology and antioxidant response. Environmental Pollution 239, 689–697.
Impact of copper nanoparticles and ionic copper exposure on wheat (Triticum aestivum L.) root morphology and antioxidant response.Crossref | GoogleScholarGoogle Scholar |

Zhao X, Chen Q, Wang Y, Shen Z, Shen W, Xu X (2017) Hydrogen-rich water induces aluminum tolerance in maize seedlings by enhancing antioxidant capacities and nutrient homeostasis. Ecotoxicology and Environmental Safety 144, 369–379.
Hydrogen-rich water induces aluminum tolerance in maize seedlings by enhancing antioxidant capacities and nutrient homeostasis.Crossref | GoogleScholarGoogle Scholar |

Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. Journal of Experimental Botany 56, 3223–3228.
Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis.Crossref | GoogleScholarGoogle Scholar |

Zuverza-Mena N, Medina-Velo IA, Barrios AC, Tan W, Peralta-Videa JR, Gardea-Torresdey JL (2015) Copper nanoparticles/compounds impact agronomic and physiological parameters in cilantro (Coriandrum sativum). Environmental Science: Processes & Impacts 17, 1783–1793.
Copper nanoparticles/compounds impact agronomic and physiological parameters in cilantro (Coriandrum sativum).Crossref | GoogleScholarGoogle Scholar |

Zuverza-Mena N, Martínez-Fernández D, Du W, Hernandez-Viezcas JA, Bonilla-Bird N, López-Moreno ML, Komárek M, Peralta-Videa JR, Gardea-Torresdey JL (2017) Exposure of engineered nanomaterials to plants: insights into the physiological and biochemical responses – a review. Plant Physiology and Biochemistry 110, 236–264.
Exposure of engineered nanomaterials to plants: insights into the physiological and biochemical responses – a review.Crossref | GoogleScholarGoogle Scholar |