Advertisement

Plant and Soil

, Volume 431, Issue 1–2, pp 333–345 | Cite as

Copper oxide nanoparticle effects on root growth and hydraulic conductivity of two vegetable crops

  • Andrew J. Margenot
  • Devin A. Rippner
  • Matt R. Dumlao
  • Sareh Nezami
  • Peter G. Green
  • Sanjai J. Parikh
  • Andrew J. McElrone
Regular Article
  • 90 Downloads

Abstract

Aims

Root growth and water transport were evaluated for two vegetable crops of contrasting root architecture (lettuce, carrot) exposed to copper oxide nanoparticles (CuO NPs).

Methods

10-day seedling root growth assays were evaluated for 16 nanometer (nm) diameter CuO NP and CuCl2 control (0.8 – 798.9 mg Cu L-1). In a separate experiment, hydraulic conductivity (Kh) of root systems not previously exposed to NP was tested using 16 and 45 nm CuO NP (798.9 mg Cu L-1) relative to CuO NP-free controls, and xylem sap was assessed by TEM-EDS for presence of CuO NPs.

Results

16 nm CuO NP produced dose-dependent increases in root diameter for lettuce (+52%) and carrot (+26%) seedlings, whereas CuCl2 did not affect (lettuce) or marginally increased (carrot) root diameter. Root Kh was similarly reduced by 16 and 45 nm CuO NPs for lettuce (-46%) but not for carrot, and no Cu was identified by TEM-EDS in xylem sap.

Conclusions

Adverse effects of CuO NPs on root physiology and function in the early stages of growth of two key food crops are not necessarily due to Cu2+ toxicity and can be specific to crop species. In addition to triggering root thickening, reduction of root Kh signifies that CuO NPs can compromise root water transport and thus crop performance.

Keywords

Copper oxide Nanoparticles Roots Hydraulic conductivity Lettuce Carrot 

Abbreviations

CuO

copper oxide

NP

nanoparticle

Kh

hydraulic conductivity

Notes

Acknowledgements

This material is based upon work that is supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture, under award number Grant #2013-67017-21211. We thank Professor Wendy Silk (Department of Land, Air and Water Resources, University of California-Davis) for providing intellectual support, laboratory resources and student advising. We thank Professor Thomas Young (Department of Civil and Environmental Engineering, University of California-Davis) for providing access to and support for ICP-MS analysis. Finally, we would like to thank Fred Hayes at the Applied Materials Characterization Facility at UC Davis for his support in collecting STEM data.

Supplementary material

11104_2018_3741_MOESM1_ESM.docx (146 kb)
ESM 1 (DOCX 146 kb)
11104_2018_3741_MOESM2_ESM.docx (49 kb)
ESM 2 (DOCX 49.3 kb)
11104_2018_3741_MOESM3_ESM.docx (159 kb)
ESM 3 (DOCX 158 kb)

References

  1. Adams J, Wright M, Wagner H, Valiente J, Britt D, Anderson A (2017) Cu from dissolution of CuO nanoparticles signals changes in root morphology. Plant Physiol Biochem 110:108–117.  https://doi.org/10.1016/j.plaphy.2016.08.005 CrossRefPubMedGoogle Scholar
  2. Asli S, Neumann PM (2009) Colloidal suspensions of clay or titanium dioxide nanoparticles can inhibit leaf growth and transpiration via physical effects on root water transport. Plant Cell Environ 32:577–584.  https://doi.org/10.1111/j.1365-3040.2009.01952.x CrossRefPubMedGoogle Scholar
  3. Atha DH, Wang H, Petersen EJ, Cleveland D, Holbrook RD, Jaruga P, Dizdaroglu M, Xing B, Nelson BC (2012) Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environ Sci Technol 46:1819–1827.  https://doi.org/10.1021/es202660k CrossRefPubMedGoogle Scholar
  4. Bengough AG, Bransby MF, Hans J, McKenna SJ, Roberts TJ, Valentine TA (2006) Root responses to soil physical conditions; growth dynamics from field to cell. J Exp Bot 57:437–447.  https://doi.org/10.1093/jxb/erj003 CrossRefPubMedGoogle Scholar
  5. Bernard Tinker P, Reed L, Legg C, Højer-Pederson S (1977) The effects of chloride in fertiliser salts on crop seed germination. J Sci Food Agric 28:1045–1051.  https://doi.org/10.1002/jsfa.2740281202 CrossRefGoogle Scholar
  6. Brar SK, Verma M, Tyagi RD, Surampalli RY (2010) Engineered nanoparticles in wastewater and wastewater sludge – evidence and impacts. Waste Manag 30:504–520.  https://doi.org/10.1016/j.wasman.2009.10.012 CrossRefPubMedGoogle Scholar
  7. Chaignon V, Sanchez-Neira I, Herrmann P, Jaillard B, Hinsinger P (2003) Copper bioavailability and extractability as related to chemical properties of contaminated soils from a vine-growing area. Environ Pollut 123:229–238.  https://doi.org/10.1016/S0269-7491(02)00374-3 CrossRefPubMedGoogle Scholar
  8. Davis RA, Rippner DA, Hausner SH, Parikh SJ, McElrone AJ, Sutcliffe JL (2017) In vivo tracking of copper-64 radiolabeled nanoparticles in lactuca sativa. Environ Sci Technol 51:12537–12546.  https://doi.org/10.1021/acs.est.7b03333 CrossRefPubMedGoogle Scholar
  9. 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. J Nanopart Res 14:1125.  https://doi.org/10.1007/s11051-012-1125-9 CrossRefGoogle Scholar
  10. Dimkpa CO, McLean JE, Britt DW, Anderson AJ (2015) Nano-CuO and interaction with nano-ZnO or soil bacterium provide evidence for the interference of nanoparticles in metal nutrition of plants. Ecotoxicology 24:119–129.  https://doi.org/10.1007/s10646-014-1364-x CrossRefPubMedGoogle Scholar
  11. Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2004) Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. Biometals 17:379–387.  https://doi.org/10.1023/b:biom.0000029417.18154.22 CrossRefPubMedGoogle Scholar
  12. Du W, Tan W, Peralta-Videa JR, Gardea-Torresdey JL, Ji R, Yin Y, Guo H (2016) Interaction of metal oxide nanoparticles with higher terrestrial plants: Physiological and biochemical aspects. Plant Physiol Biochem.  https://doi.org/10.1016/j.plaphy.2016.04.024
  13. Eduok S, Coulon F (2017) Engineered nanoparticles in the environments: interactions with microbial systems and microbial activity. In: Cravo-Laureau C, Cagnon C, Lauga B, Duran R (eds) Microbial ecotoxicology. Springer International Publishing, ChamGoogle Scholar
  14. Elmer WH, White JC (2016) The use of metallic oxide nanoparticles to enhance growth of tomatoes and eggplants in disease infested soil or soilless medium. Environ Sci Nano 3:1072–1079.  https://doi.org/10.1039/C6EN00146G CrossRefGoogle Scholar
  15. Fleischer A, O'Neill MA, Ehwald R (1999) The pore size of non-graminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiol 121:829–838.  https://doi.org/10.1104/pp.121.3.829 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Giannousi K, Avramidis I, Dendrinou-Samara C (2013) Synthesis, characterization and evaluation of copper based nanoparticles as agrochemicals against Phytophthora infestans. RSC Advances 3:21743–21752.  https://doi.org/10.1039/C3RA42118J CrossRefGoogle Scholar
  17. Hatami M, Kariman K, Ghorbanpour M (2016) Engineered nanomaterial-mediated changes in the metabolism of terrestrial plants. Sci Total Environ 571:275–291.  https://doi.org/10.1016/j.scitotenv.2016.07.184 CrossRefPubMedGoogle Scholar
  18. Jarbeau JA, Ewers FW, Davis SD (1995) The mechanism of water-stress-induced embolism in two species of chaparral shrubs. Plant Cell Environ 18:189–196.  https://doi.org/10.1111/j.1365-3040.1995.tb00352.x CrossRefGoogle Scholar
  19. Ko K-S, Kong IC (2014) Toxic effects of nanoparticles on bioluminescence activity, seed germination, and gene mutation. Appl Microbiol Biotechnol 98:3295–3303.  https://doi.org/10.1007/s00253-013-5404-x CrossRefPubMedGoogle Scholar
  20. Li Y, Yang D, Cui J (2017) Graphene oxide loaded with copper oxide nanoparticles as an antibacterial agent against Pseudomonas syringae pv. tomato. RSC Advances 7:38853–38860.  https://doi.org/10.1039/C7RA05520J CrossRefGoogle Scholar
  21. Lin D, Xing B (2007) Phytotoxicity of nanoparticles: Inhibition of seed germination and root growth. Environ Pollut 150:243CrossRefPubMedGoogle Scholar
  22. 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.  https://doi.org/10.1016/j.chemosphere.2009.10.050 CrossRefPubMedGoogle Scholar
  23. Maas EV, Hoffman G (1976) Crop salt tolerance-current assessment. Proc Region Saline-Seep Contr Symp 6:245–252Google Scholar
  24. Martínez-Fernández D, Komárek M (2016) Comparative effects of nanoscale zero-valent iron (nZVI) and Fe2O3 nanoparticles on root hydraulic conductivity of Solanum lycopersicum L. Environ Exp Bot 131:128–136.  https://doi.org/10.1016/j.envexpbot.2016.07.010 CrossRefGoogle Scholar
  25. Martínez-Fernández D, Barroso D, Komárek M (2016) Root water transport of Helianthus annuus L. under iron oxide nanoparticle exposure. Environ Sci Pollut Res 23:1732–1741.  https://doi.org/10.1007/s11356-015-5423-5 CrossRefGoogle Scholar
  26. Maurer-Jones MA, Gunsolus IL, Murphy CJ, Haynes CL (2013) Toxicity of engineered nanoparticles in the environment. Anal Chem 85:3036–3049.  https://doi.org/10.1021/ac303636s CrossRefPubMedPubMedCentralGoogle Scholar
  27. McShane HVA, Sunahara GI, Whalen JK, Hendershot WH (2014) Differences in soil solution chemistry between soils amended with nanosized CuO or Cu reference materials: implications for nanotoxicity tests. Environ Sci Technol 48:8135–8142.  https://doi.org/10.1021/es500141h CrossRefPubMedGoogle Scholar
  28. Melcher PJ, Michele Holbrook N, Burns MJ, Zwieniecki MA, Cobb AR, Brodribb TJ, Choat B, Sack L (2012) Measurements of stem xylem hydraulic conductivity in the laboratory and field. Methods Ecol Evol 3:685–694CrossRefGoogle Scholar
  29. Miralles P, Church TL, Harris AT (2012) Toxicity, uptake, and translocation of engineered nanomaterials in vascular plants. Environ Sci Technol 46:9224–9239.  https://doi.org/10.1021/es202995d CrossRefPubMedGoogle Scholar
  30. Moon Y-S, Park E-S, Kim T-O, Lee H-S, Lee S-E (2014) SELDI-TOF MS-based discovery of a biomarker in Cucumis sativus seeds exposed to CuO nanoparticles. Environ Toxicol Pharmacol 38:922–931.  https://doi.org/10.1016/j.etap.2014.10.002 CrossRefPubMedGoogle Scholar
  31. Nair PMG, Chung IM (2014a) Impact of copper oxide nanoparticles exposure on Arabidopsis thaliana growth, root system development, root lignificaion, and molecular level changes. Environ Sci Pollut Res 21:12709–12722.  https://doi.org/10.1007/s11356-014-3210-3 CrossRefGoogle Scholar
  32. Nair PMG, Chung IM (2014b) A mechanistic study on the toxic effect of copper oxide nanoparticles in soybean (Glycine max L.) root development and lignification of root cells. Biol Trace Elem Res 162:342–352.  https://doi.org/10.1007/s12011-014-0106-5 CrossRefPubMedGoogle Scholar
  33. Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627.  https://doi.org/10.1126/science.1114397 CrossRefPubMedGoogle Scholar
  34. Norén H, Svensson P, Andersson B (2004) A convenient and versatile hydroponic cultivation system for Arabidopsis thaliana. Physiologia Plantarum 121:343–348.  https://doi.org/10.1111/j.0031-9317.2004.00350.x CrossRefGoogle Scholar
  35. Parfitt RL, Wilson A (1985) Estimation of allophane and halloysite in three sequences of volcanic soils, New Zealand. Catena Suppl 7:1–8Google Scholar
  36. Parisi C, Vigani M, Rodríguez-Cerezo E (2015) Agricultural Nanotechnologies: What are the current possibilities? Nano Today 10:124–127CrossRefGoogle Scholar
  37. Pérez-Rodríguez P, Paradelo M, Rodríguez-Salgado I, Fernández-Calviño D, López-Periago JE (2013) Modeling the influence of raindrop size on the wash-off losses of copper-based fungicides sprayed on potato (Solanum tuberosum L.) leaves. J Environ Sci Health B 48:737–746.  https://doi.org/10.1080/03601234.2013.780551 CrossRefPubMedGoogle Scholar
  38. 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.  https://doi.org/10.1021/jf104517j CrossRefPubMedPubMedCentralGoogle Scholar
  39. Rippner DA, Green PG, Young TM, Parikh SJ (2018) Dissolved organic matter reduces CuO nanoparticle toxicity to duckweed in simulated natural systems. Environmental Pollution 234: 692–698  https://doi.org/10.1016/j.envpol.2017.12.014
  40. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682CrossRefPubMedGoogle Scholar
  41. Schwab F, Zhai G, Kern M, Turner A, Schnoor JL, Wiesner MR (2016) Barriers, pathways and processes for uptake, translocation and accumulation of nanomaterials in plants – Critical review. Nanotoxicology 10:257–278.  https://doi.org/10.3109/17435390.2015.1048326 PubMedGoogle Scholar
  42. Sekhon BS (2014) Nanotechnology in agri-food production: an overview. Nanotechnol Sci Appl 7:31–53.  https://doi.org/10.2147/NSA.S39406 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Servin AD, White JC (2016) Nanotechnology in agriculture: Next steps for understanding engineered nanoparticle exposure and risk. NanoImpact 1:9–12.  https://doi.org/10.1016/j.impact.2015.12.002 CrossRefGoogle Scholar
  44. Shaw AK, Hossain Z (2013) Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere 93:906–915.  https://doi.org/10.1016/j.chemosphere.2013.05.044 CrossRefPubMedGoogle Scholar
  45. Shen C-X, Zhang Q-F, Li J, Bi F-C, Yao N (2010) Induction of programmed cell death in Arabidopsis and rice by single-wall carbon nanotubes. Am J Bot 97:1602–1609.  https://doi.org/10.3732/ajb.1000073 CrossRefPubMedGoogle Scholar
  46. Siddiqui MA, Alhadlaq HA, Ahmad J, Al-Khedhairy AA, Musarrat J, Ahamed M (2013) Copper oxide nanoparticles induced mitochondria mediated apoptosis in human hepatocarcinoma cells. PloS one 8:e69534CrossRefPubMedPubMedCentralGoogle Scholar
  47. Stampoulis D, Sinha SK, White JC (2009) Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol 43:9473–9479.  https://doi.org/10.1021/es901695c CrossRefPubMedGoogle Scholar
  48. Sun TY, Gottschalk F, Hungerbühler K, Nowack B (2014) Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials. Environ Pollut 185:69–76.  https://doi.org/10.1016/j.envpol.2013.10.004 CrossRefPubMedGoogle Scholar
  49. Tang YJ, Wu SG, Huang L, Head J, Chen D, Kong IC (2013) Phytotoxicity of metal oxide nanoparticles is related to both dissolved metals ions and adsorption of particles on seed surfaces. J Pet Environ Biotechnol 2012.Google Scholar
  50. Theng BKG, Yuan G (2008) Nanoparticles in the soil environment. Elements 4:395–399.  https://doi.org/10.2113/gselements.4.6.395 CrossRefGoogle Scholar
  51. Thwala M, Klaine SJ, Musee N (2016) Interactions of metal-based engineered nanoparticles with aquatic higher plants: A review of the state of current knowledge. Environ ToxicolChem 35:1677–1694.  https://doi.org/10.1002/etc.3364 CrossRefGoogle Scholar
  52. Tracy SR, Black CR, Roberts JA, Sturrock C, Mairhofer S, Craigon J, Mooney SJ (2012) Quantifying the impact of soil compaction on root system architecture in tomato (Solanum lycopersicum) by X-ray micro-computed tomography. Ann Bot 110:511–519.  https://doi.org/10.1093/aob/mcs031 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Tyree MT, Alexander J, Machado J-L (1992) Loss of hydraulic conductivity due to water stress in intact juveniles of Quercus rubra and Populus deltoides. Tree Physiol 10:411–415.  https://doi.org/10.1093/treephys/10.4.411 CrossRefPubMedGoogle Scholar
  54. Wada K (1978) Chapter 4 Allophane and imogolite. In: Toshio S, Susumu S (eds) Developments in sedimentology. ElsevierGoogle Scholar
  55. Wang Z, Xie X, Zhao J, Liu X, Feng W, White JC, Xing B (2012) Xylem- and phloem-based transport of CuO nanoparticles in maize (Zea mays L.). Environ Sci Technol 46:4434–4441.  https://doi.org/10.1021/es204212z CrossRefPubMedGoogle Scholar
  56. Wang Z, Xu L, Zhao J, Wang X, White JC, Xing B (2016) CuO nanoparticle interaction with arabidopsis thaliana: toxicity, parent-progeny transfer, and gene expression. Environ Sci Technol 50:6008–6016.  https://doi.org/10.1021/acs.est.6b01017 CrossRefPubMedGoogle Scholar
  57. Yang L, Watts DJ (2005) Particle surface characteristics may play an important role in phytotoxicity of alumina nanoparticles. Toxicol Lett 158:122–132.  https://doi.org/10.1016/j.toxlet.2005.03.003 CrossRefPubMedGoogle Scholar
  58. Zhao L, Ortiz C, Adeleye AS, Hu Q, Zhou H, Huang Y, Keller AA (2016) Metabolomics to detect response of lettuce (Lactuca sativa) to Cu(OH)2 nanopesticides: oxidative stress response and detoxification mechanisms. Environ Sci Technol 50:9697–9707.  https://doi.org/10.1021/acs.est.6b02763 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Crop SciencesUniversity of Illinois Urbana-ChampaignUrbanaUSA
  2. 2.Department of Land, Air and Water ResourcesUniversity of California-DavisDavisUSA
  3. 3.California Council on Science and TechnologySacramentoUSA
  4. 4.Department of Soil ScienceRazi UniversityKermanshahIran
  5. 5.Department of Civil and Environmental EngineeringUniversity of California-DavisDavisUSA
  6. 6.Department of ViticultureUniversity of California-DavisDavisUSA
  7. 7.United States Department of Agriculture-Agricultural Research ServiceCrops Pathology and Genetics Research UnitDavisUSA

Personalised recommendations