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Combined effects of carbon nanotubes and cadmium on the photosynthetic capacity and antioxidant response of wheat seedlings

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Abstract

A detailed study of nanomaterials has revealed their broad application prospects. However, the presence of carbon nanotubes (CNTs) in the environment has been increasing and has aroused concerns regarding their toxicity to crops when combined with heavy metals. In the present study, the effects of Cd on the photosynthetic capacity and antioxidant activity of wheat seedlings in the presence of single-walled CNTs (SW) and multi-walled CNTs (MW) were investigated. Our results indicated that SW (5–40 mg L−1) and MW (10–40 mg L−1) significantly increased the oxidative stress response of wheat seedlings to Cd. Compared with Cd alone, CNTs combined with Cd decreased net photosynthetic rate, stomatal conductance, transpiration rate, primary maximum photochemical efficiency of photosystem II, actual quantum yield, photosynthetic electron transport rate, root canal protein, and ribulose-1,5-bisphosphate carboxylase/oxygenase content. Moreover, combined treatments increased the content of superoxide anion, superoxide dismutase, guaiacol peroxidase, cytochrome, and malondialdehyde in wheat seedlings. Moreover, membrane lipid peroxidation was aggravated, causing serious damage to the wheat membrane system. In addition, the toxicity of the SW treatment and the combined treatment with SW and Cd was higher than that of the MW treatment.

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References

  • Baughman RH, Zakhidov AA, de Heer WA (2002) Carbon nanotubes - the route toward applications. Science 297(5582):787–792

    Article  CAS  Google Scholar 

  • Baun A, Hartmann NB, Grieger K, Kusk KO (2008a) Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing. Ecotoxicology 17(5):387–395

    Article  CAS  Google Scholar 

  • Baun A, Sorensen SN, Rasmussen RF, Hartmann NB, Koch CB (2008b) Toxicity and bioaccumulation of xenobiotic organic compounds in the presence of aqueous suspensions of aggregates of nano-C-60. Aquat Toxicol 86(3):379–387

    Article  CAS  Google Scholar 

  • Boncel S, Kyziol-Komosinska J, Krzyewska I, Czupiol J (2015) Interactions of carbon nanotubes with aqueous/aquatic media containing organic/inorganic contaminants and selected organisms of aquatic ecosystems - a review. Chemosphere 136:211–221

    Article  CAS  Google Scholar 

  • Burzynski M, Klobus G (2004) Changes of photosynthetic parameters in cucumber leaves under Cu, Cd, and Pb stress. Photosynthetica 42(4):505–510

    Article  CAS  Google Scholar 

  • Camejo D, Guzman-Cedeno A, Moreno A (2016) Reactive oxygen species, essential molecules, during plant-pathogen interactions. Plant Physiol Biochem 103:10–23

    Article  CAS  Google Scholar 

  • Canas JE, Long M, Nations S, Vadan R, Dai L, Luo M, Ambikapathi R, Lee EH, Olszyk D (2008) Effects of functionalized and nonfunctionalized single-walled carbon nanotubes on root elongation of select crop species. Environ Toxicol Chem 27(9):1922–1931

    Article  CAS  Google Scholar 

  • Chen G, Qiu J, Liu Y, Jiang R, Cai S, Liu Y, Zhu F, Zeng F, Luan T, Ouyang G (2015) Carbon nanotubes act as contaminant carriers and translocate within plants. Sci Rep 5:15682

    Article  CAS  Google Scholar 

  • Chen D, Chen D, Xue R, Long J, Lin X, Lin Y, Jia L, Zeng R, Song Y (2019) Effects of boron, silicon and their interactions on cadmium accumulation and toxicity in rice plants. J Hazard Mater 367:447–455

    Article  CAS  Google Scholar 

  • Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57(5):779–795

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Deng Y, Eitzer B, White JC, Xing BS (2017b) Impact of multiwall carbon nanotubes on the accumulation and distribution of carbamazepine in collard greens (Brassica oleracea). Environ Sci Nano 4:149–159

    Article  CAS  Google Scholar 

  • Feng J, Shi Q, Wang X, Wei M, Yang F, Xu H (2010) Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci Hortic 123(4):521–530

    Article  CAS  Google Scholar 

  • Gao ML, Liu Y, Dong YM, Song ZG (2018) Photosynthetic and antioxidant response of wheat to di(2-ethylhexyl) phthalate (DEHP) contamination in the soil. Chemosphere 209:258–267

    Article  CAS  Google Scholar 

  • Gao ML, Yang YJ, Song ZG (2019) Effects of graphene oxide on cadmium uptake and photosynthesis performance in wheat seedlings. Ecotoxicol Environ Saf 173:165–173

    Article  CAS  Google Scholar 

  • Hu X, Kang J, Lu K, Zhou R, Mu L, Zhou Q (2014) Graphene oxide amplifies the phytotoxicity of arsenic in wheat. Sci Rep 4:6122

    Article  CAS  Google Scholar 

  • Jia G, Wang HF, Yan L, Wang X, Pei RJ, Yan T, Zhao YL, Guo XB (2005) Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environ Sci Technol 39(5):1378–1383

    Article  CAS  Google Scholar 

  • Jong AJD, Yakimova ET, Kapchina VM, Woltering EJ (2002) A critical role for ethylene in hydrogen peroxide release during programmed cell death in tomato suspension cells. Planta 214(4):537–545

    Article  CAS  Google Scholar 

  • Kasson TMD, Barry BA (2012) Reactive oxygen and oxidative stress: N-formyl kynurenine in photosystem II and non-photosynthetic proteins. Photosynth Res 114(2):97–110

    Article  CAS  Google Scholar 

  • Khodakovskaya MV, de Silva K, Biris AS, Dervishi E, Villagarcia H (2012) Carbon nanotubes induce growth enhancement of tobacco cells. ACS Nano 6(3):2128–2135

    Article  CAS  Google Scholar 

  • Kojima K, Oshita M, Nanjo Y, Kasai K, Tozawa Y, Hayashi H, Nishiyama Y (2007) Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II. Mol Microbiol 65(4):936–947

    Article  CAS  Google Scholar 

  • Lavres J, Rabelo FHS, Capaldi FR, Reis ARD, Rosssi ML, Franco MR, Azevedo RA, Abreu CH, Nogueira ND (2019) Investigation into the relationship among Cd bioaccumulation, nutrient composition, ultrastructural changes and antioxidative metabolism in lettuce genotypes under Cd stress. Ecotoxicol Environ Saf 170:578–589

    Article  CAS  Google Scholar 

  • Liu Q, Chen B, Wang Q, Shi X, Xiao Z, Lin J, Fang X (2009a) Carbon nanotubes as molecular transporters for walled plant cells. Nano Lett 9(3):1007–1010

    Article  CAS  Google Scholar 

  • Liu W, Ai XZ, Liang WJ, Wang HT, Liu SX, Zheng N (2009b) Effects of salicylic acid on the leaf photosynthesis and antioxidant enzyme activities of cucumber seedlings under low temperature and light intensity. Chin J Appl Ecol 20(2):441–445

    CAS  Google Scholar 

  • Liu Y, Nie YG, Wang JJ, Wang J, Wang X, Chen SP, Zhao GP, Wu LJ, Xu A (2018) Mechanisms involved in the impact of engineered nanomaterials on the joint toxicity with environmental pollutants. Ecotoxicol Environ Saf 162:92–102

    Article  CAS  Google Scholar 

  • Long ZF, Ji J, Yang K, Lin DH, Wu FC (2014) Systematic and quantitative investigation of the mechanism of carbon nanotubes’ toxicity toward algae. Environ Sci Technol 48(8):4634–4634

    Article  CAS  Google Scholar 

  • Lopez-Luna J, Silva-Silva MJ, Martinez-Vargas S, Mijangos-Ricardez OF, Gonzalez-Chavez MC, Solis-Dominguez FA, Cuevas-Diaz MC (2016) Magnetite nanoparticle (NP) uptake by wheat plants and its effect on cadmium and chromium toxicological behavior. Sci Total Environ 565:941–950

    Article  CAS  Google Scholar 

  • Lu LT, Chang IC, Hsiao TY, Yu YH, Ma HW (2007) Identification of pollution source of cadmium in soil - application of material flow analysis and a case study in Taiwan. Environ Sci Pollut Res 14(1):49–59

    Article  CAS  Google Scholar 

  • Luo S, Ishida H, Makino A, Mae T (2002) Fe2+-catalyzed site-specific cleavage of the large subunit of ribulose 1,5-bisphosphate carboxylase close to the active site. J Biol Chem 277(14):12382–12387

    Article  CAS  Google Scholar 

  • Ma XM, Geisler-Lee J, Deng Y, Kolmakov A (2014) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 481:635–635

    Article  CAS  Google Scholar 

  • Mauter MS, Elimelech M (2008) Environmental applications of carbon-based nanomaterials. Environ Sci Technol 42(16):5843–5859

    Article  CAS  Google Scholar 

  • Miralles P, Johnson E, Church TL, Harris AT (2012) Multiwalled carbon nanotubes in alfalfa and wheat: toxicology and uptake. J R Soc Interface 9(77):3514–3527

    Article  CAS  Google Scholar 

  • Mueller NC, Nowack B (2008) Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42(12):4447–4453

    Article  CAS  Google Scholar 

  • Murtaza G, Javed W, Hussain A, Wahid A, Murtaza B, Owens G (2015) Metal uptake via phosphate fertilizer and city sewage in cereal and legume crops in Pakistan. Environ Sci Pollut Res Int 22(12):9136–9147

    Article  CAS  Google Scholar 

  • Naeem A, Saifullah, Rehman MZ-u, Akhtar T, Ok YS, Rengel Z (2016) Genetic variation in cadmium accumulation and tolerance among wheat cultivars at the seedling stage. Commun Soil Sci Plant Anal 47(5):554–562

    Article  CAS  Google Scholar 

  • Nath RG, Sonawane BR, Vulimiri SV, Lin YS (2015) Mechanisms of cadmium carcinogenesis. Cancer Res 75:1

    Google Scholar 

  • Nawrot T, Plusquin M, Hogervorst J, Roels HA, Celis H, Thijs L, Vangronsveld J, Van Hecke E, Staessen JA (2006) Environmental exposure to cadmium and risk of cancer: a prospective population-based study. Lancet Oncol 7(2):119–126

    Article  CAS  Google Scholar 

  • Petersen EJ, Zhang L, Mattison NT, O'Carroll DM, Whelton AJ, Uddin N, Tinh N, Huang Q, Henry TB, Holbrook RD, Chen KL (2011) Potential release pathways, environmental fate, and ecological risks of carbon nanotubes. Environ Sci Technol 45(23):9837–9856

    Article  CAS  Google Scholar 

  • Rizwan M, Ali S, Adrees M, Ibrahim M, Tsang DCW, Zia-Ur-Rehman M, Zahir ZA, Rinklebe J, Tack FMG, Ok YS (2017) A critical review on effects, tolerance mechanisms and management of cadmium in vegetables. Chemosphere 182:90–105

    Article  CAS  Google Scholar 

  • Salin ML (1991) Chloroplast and mitochondrial mechanisms for protection against oxygen toxicity. Free Radic Res Commun 12–13 Pt 2:851–858

    Article  Google Scholar 

  • Singh OV, Labana S, Pandey G, Budhiraja R, Jain RK (2003) Phytoremediation: an overview of metallic ion decontamination from soil. Appl Microbiol Biotechnol 61(5–6):405–412

    Article  CAS  Google Scholar 

  • Skórzyńska-Polit E, Drążkiewicz M, Krupa Z (2009) Lipid peroxidation and antioxidative response in Arabidopsis thaliana exposed to cadmium and copper. Acta Physiol Plant 32(1):169–175

    Article  CAS  Google Scholar 

  • Soo RK, Seung CH (2005) Cadmium toxicity and calcium effect on growth and photosynthesis of tobacco. J Life Sci 3:453–460

    Google Scholar 

  • Spurgeon DJ, Rowland P, Ainsworth G, Rothery P, Long S, Black HIJ (2008) Geographical and pedological drivers of distribution and risks to soil fauna of seven metals (Cd, Cu, Cr, Ni, Pb, V and Zn) in British soils. Environ Pollut 153(2):273–283

    Article  CAS  Google Scholar 

  • Tiwari SC, Wick SM, Williamson RE, Gunning BE (1984) Cytoskeleton and integration of cellular function in cells of higher plants. J Cell Biol 99(1 Pt 2):63 s–69 s

    Article  CAS  Google Scholar 

  • Tiwari DK, Dasgupta-Schubert N, Cendejas LMV, Villegas J, Montoya LC, García SEB (2014) Interfacing carbon nanotubes (CNT) with plants: enhancement of growth, water and ionic nutrient uptake in maize (Zea mays) and implications for nanoagriculture. Appl Nanosci 4(5):577–591

    Article  CAS  Google Scholar 

  • van der Zande M, Junker R, Walboomers XF, Jansen JA (2011) Carbon nanotubes in animal models: a systematic review on toxic potential. Tissue Eng B Rev 17(1):57–69

    Article  CAS  Google Scholar 

  • Wang J, Luo Y, Teng Y, Ma W, Christie P, Li Z (2013) Soil contamination by phthalate esters in Chinese intensive vegetable production systems with different modes of use of plastic film. Environ Pollut 180:265–273

    Article  CAS  Google Scholar 

  • Wild E, Jones KC (2009) Novel method for the direct visualization of in vivo nanomaterials and chemical interactions in plants. Environ Sci Technol 43(14):5290–5294

    Article  CAS  Google Scholar 

  • Xiong JL, Li J, Wang HC, Zhang CL, Naeem MS (2018) Fullerol improves seed germination, biomass accumulation, photosynthesis and antioxidant system in Brassica napus L. under water stress. Plant Physiol Biochem 129:130–140

    Article  CAS  Google Scholar 

  • Ye ZP, Yu Q (2008) A coupled model of stomatal conductance and photosynthesis for winter wheat. Photosynthetica 46(4):637–640

    Article  Google Scholar 

  • Zhang R, Zhang Y, Zhang Q, Xie H, Qian W, Wei F (2014) Growth of half-meter long carbon nanotubes based on Schulz-Flory distribution. ACS Nano 8(3):3097–3097

    Article  CAS  Google Scholar 

  • Zhao HM, Du H, Xiang L, Chen YL, Lu LA, Li YW, Li H, Cai QY, Mo CH (2015) Variations in phthalate ester (PAE) accumulation and their formation mechanism in Chinese flowering cabbage (Brassica parachinensis L.) cultivars grown on PAE-contaminated soils. Environ Pollut 206:95–103

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful for the financial support received from the National Key Research and Development Program of China (No. 2016YFD0800806) and STU scientific research foundation for talents (NTF19026).

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Authors and Affiliations

  1. Department of Civil and Environmental Engineering, Shantou University, No. 243 Daxue Road, Shantou, 515063, China

    Minling Gao & Zhengguo Song

  2. School of Environmental Science and Engineering, Tianjin Polytechnic University, Tianjin, 300387, China

    Yalei Xu & Xipeng Chang

Authors
  1. Minling Gao
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  2. Yalei Xu
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  3. Xipeng Chang
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  4. Zhengguo Song
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Contributions

Minling Gao and Yalei Xu performed laboratory experiments. Xipeng Chang interpreted histological data and designed image analysis methods. Minling Gao and Zhengguo Song analyzed the data and prepared the manuscript; Zhengguo Song and Minling Gao conceived the idea of this study. All authors contributed substantially to revisions and approved the final manuscript draft.

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Correspondence to Zhengguo Song.

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Responsible editor: Gangrong Shi

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Highlights

1. CNTs significantly increase the oxidative stress response of wheat seedlings to Cd.

2. CNTs and Cd treatments contribute to the accumulation of ROS in wheat.

3. The toxicity of SW combined with Cd treatments is higher than that of MW.

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Gao, M., Xu, Y., Chang, X. et al. Combined effects of carbon nanotubes and cadmium on the photosynthetic capacity and antioxidant response of wheat seedlings. Environ Sci Pollut Res 28, 34344–34354 (2021). https://doi.org/10.1007/s11356-021-13024-3

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  • DOI: https://doi.org/10.1007/s11356-021-13024-3

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