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Differentially charged nanoplastics demonstrate distinct accumulation in Arabidopsis thaliana

Nature Nanotechnology volume 15, pages 755–760 (2020)Cite this article

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Abstract

Although the fates of microplastics (0.1–5 mm in size) and nanoplastics (<100 nm) in marine environments are being increasingly well studied1,2, little is known about the behaviour of nanoplastics in terrestrial environments3,4,5,6, especially agricultural soils7. Previous studies have evaluated the consequences of nanoplastic accumulation in aquatic plants, but there is no direct evidence for the internalization of nanoplastics in terrestrial plants. Here, we show that both positively and negatively charged nanoplastics can accumulate in Arabidopsis thaliana. The aggregation promoted by the growth medium and root exudates limited the uptake of amino-modified polystyrene nanoplastics with positive surface charges. Thus, positively charged nanoplastics accumulated at relatively low levels in the root tips, but these nanoplastics induced a higher accumulation of reactive oxygen species and inhibited plant growth and seedling development more strongly than negatively charged sulfonic-acid-modified nanoplastics. By contrast, the negatively charged nanoplastics were observed frequently in the apoplast and xylem. Our findings provide direct evidence that nanoplastics can accumulate in plants, depending on their surface charge. Plant accumulation of nanoplastics can have both direct ecological effects and implications for agricultural sustainability and food safety.

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Fig. 1: Nanoplastic characterization and physiological effects of nanoplastics on A. thaliana.
Fig. 2: ROS distribution and tissue morphology in roots.
Fig. 3: Uptake of nanoplastics and root response.

Data availability

The processed RNA-Seq data have been deposited in the Gene Expression Omnibus database under accession code GSE123369. All the other data are available from the corresponding author upon reasonable request.

References

  1. Galloway, T. S., Cole, M. & Lewis, C. Interactions of microplastic debris throughout the marine ecosystem. Nat. Ecol. Evol. 1, 0116 (2017).

    Article  Google Scholar 

  2. Dawson, A. L. et al. Turning microplastics into nanoplastics through digestive fragmentation by Antarctic krill. Nat. Commun. 9, 1001 (2018).

    Article  Google Scholar 

  3. Weithmann, N. et al. Organic fertilizer as a vehicle for the entry of microplastic into the environment. Sci. Adv. 4, 8060 (2018).

    Article  Google Scholar 

  4. Huerta Lwanga, E. et al. Microplastics in the terrestrial ecosystem: implications for Lumbricus terrestris (Oligochaeta, Lumbricidae). Environ. Sci. Technol. 50, 2685–2691 (2016).

    Article  CAS  Google Scholar 

  5. Hodson, M. E., Duffus-Hodson, C. A., Clark, A., Prendergast-Miller, M. T. & Thorpe, K. L. Plastic bag derived-microplastics as a vector for metal exposure in terrestrial invertebrates. Environ. Sci. Technol. 51, 4714–4721 (2017).

    Article  CAS  Google Scholar 

  6. de Souza Machado, A. A., Kloas, W., Zarfl, C., Hempel, S. & Rillig, M. C. Microplastics as an emerging threat to terrestrial ecosystems. Glob. Chang. Biol. 24, 1405–1416 (2018).

    Article  Google Scholar 

  7. Nizzetto, L., Langaas, S. & Futter, M. Pollution: do microplastics spill on to farm soils? Nature 537, 488 (2016).

    Article  CAS  Google Scholar 

  8. Duis, K. & Coors, A. Microplastics in the aquatic and terrestrial environment: sources (with a specific focus on personal care products), fate and effects. Environ. Sci. Eur. 28, 2 (2016).

    Article  Google Scholar 

  9. Besseling, E., Wang, B., Lurling, M. & Koelmans, A. A. Nanoplastic affects growth of S. obliquus and reproduction of D. magna. Environ. Sci. Technol. 48, 12336–12343 (2014).

    Article  CAS  Google Scholar 

  10. della Torre, C. et al. Accumulation and embryotoxicity of polystyrene nanoparticles at early stage of development of sea urchin embryos Paracentrotus lividus. Environ. Sci. Technol. 48, 12302–12311 (2014).

    Article  Google Scholar 

  11. Rillig, M. C., Lehmann, A., de Souza Machado, A. A. & Yang, G. Microplastic effects on plants. New Phytol. 223, 1066–1070 (2019).

    Article  Google Scholar 

  12. Rochman, C. M. Microplastics research—from sink to source. Science 360, 28–29 (2018).

    Article  CAS  Google Scholar 

  13. Scheurer, M. & Bigalke, M. Microplastics in Swiss floodplain soils. Environ. Sci. Technol. 52, 3591–3598 (2018).

    Article  CAS  Google Scholar 

  14. Zubris, K. A. & Richards, B. K. Synthetic fibers as an indicator of land application of sludge. Environ. Pollut. 138, 201–211 (2005).

    Article  CAS  Google Scholar 

  15. Fuller, S. & Gautam, A. A procedure for measuring microplastics using pressurized fluid extraction. Environ. Sci. Technol. 50, 5774–5780 (2016).

    Article  CAS  Google Scholar 

  16. Etxeberria, E., Gonzalez, P., Baroja-Fernandez, E. & Romero, J. P. Fluid phase endocytic uptake of artificial nano-spheres and fluorescent quantum dots by sycamore cultured cells: evidence for the distribution of solutes to different intracellular compartments. Plant Signal. Behav. 1, 196–200 (2006).

    Article  Google Scholar 

  17. Huang, C. et al. Transformation of 14C-labeled graphene to 14CO2 in the shoots of a rice plant. Angew. Chem. Int. Ed. 130, 9907–9911 (2018).

    Article  Google Scholar 

  18. Slomberg, D. L. & Schoenfisch, M. H. Silica nanoparticle phytotoxicity to Arabidopsis thaliana. Environ. Sci. Technol. 46, 10247–10254 (2012).

    CAS  Google Scholar 

  19. Wang, Z. et al. CuO nanoparticle interaction with Arabidopsis thaliana: toxicity, parent-progeny transfer, and gene expression. Environ. Sci. Technol. 50, 6008–6016 (2016).

    Article  CAS  Google Scholar 

  20. Zhang, M., Ellis, E. A., Cisneros-Zevallos, L. & Akbulut, M. Uptake and translocation of polymeric nanoparticulate drug delivery systems into ryegrass. RSC Adv. 2, 9679–9686 (2012).

    Article  CAS  Google Scholar 

  21. Rice-Evans, C., Miller, N. & Paganga, G. Antioxidant properties of phenolic compounds. Trends Plant Sci. 2, 152–159 (1997).

    Article  Google Scholar 

  22. Paré, P. W. & Tumlinson, J. H. Plant volatiles as a defense against insect herbivores. Plant Physiol. 121, 325–332 (1999).

    Article  Google Scholar 

  23. Dodd, A. N. et al. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630–633 (2005).

    Article  CAS  Google Scholar 

  24. Tsukagoshi, H., Busch, W. & Benfey, P. N. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143, 606–616 (2010).

    Article  CAS  Google Scholar 

  25. García-Sánchez, S., Bernales, I. & Cristobal, S. Early response to nanoparticles in the Arabidopsis transcriptome compromises plant defence and root-hair development through salicylic acid signalling. BMC Genom. 16, 341 (2015).

    Article  Google Scholar 

  26. Pan, J. W. et al. Root border cell development is a temperature-insensitive and Al-sensitive process in barley. Plant Cell Physiol. 45, 751–760 (2004).

    Article  CAS  Google Scholar 

  27. Liu, Q. et al. Study of the inhibitory effect of water-soluble fullerenes on plant growth at the cellular level. ACS Nano 4, 5743–5748 (2010).

    Article  CAS  Google Scholar 

  28. Ma, C., White, J. C., Dhankher, O. P. & Xing, B. Metal-based nanotoxicity and detoxification pathways in higher plants. Environ. Sci. Technol. 49, 7109–7122 (2015).

    Article  CAS  Google Scholar 

  29. Wang, Z. et al. Xylem- and phloem-based transport of CuO nanoparticles in maize (Zea mays L.). Environ. Sci. Technol. 46, 4434–4441 (2012).

    Article  CAS  Google Scholar 

  30. Mitrano, D. M. et al. Synthesis of metal-doped nanoplastics and their utility to investigate fate and behaviour in complex environmental systems. Nat. Nanotechnol. 14, 362–368 (2019).

    Article  CAS  Google Scholar 

  31. Avellan, A. et al. Nanoparticle uptake in plants: gold nanomaterial localized in roots of Arabidopsis thaliana by X-ray computed nanotomography and hyperspectral imaging. Environ. Sci. Technol. 51, 8682–8691 (2017).

    Article  CAS  Google Scholar 

  32. Klug, B. & Horst, W. J. Oxalate exudation into the root-tip water free space confers protection from aluminum toxicity and allows aluminum accumulation in the symplast in buckwheat (Fagopyrum esculentum). New Phytol. 187, 380–391 (2010).

    Article  CAS  Google Scholar 

  33. Feng, L. J. et al. Role of extracellular polymeric substances in the acute inhibition of activated sludge by polystyrene nanoparticles. Environ. Pollut. 238, 859–865 (2018).

    Article  CAS  Google Scholar 

  34. Holzapfel, V., Musyanovych, A., Landfester, K., Lorenz, M. R. & Mailänder, V. Preparation of fluorescent carboxyl and amino functionalized polystyrene particles by miniemulsion polymerization as markers for cells. Macromol. Chem. Phys. 206, 2440–2449 (2005).

    Article  CAS  Google Scholar 

  35. Feng, L. J. et al. Short-term exposure to positively charged polystyrene nanoparticles causes oxidative stress and membrane destruction in cyanobacteria. Environ. Sci. Nano 6, 3072–3079 (2019).

    Article  CAS  Google Scholar 

  36. Wintermans, J. F. G. M. & de Mots, A. Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochim. Biophys. Acta Biophys. Incl. Photsynth. 109, 448–453 (1965).

    Article  CAS  Google Scholar 

  37. Napsucialy-Mendivil, S., Alvarez-Venegas, R., Shishkova, S. & Dubrovsky, J. G. Arabidopsis homolog of trithorax1 (ATX1) is required for cell production, patterning, and morphogenesis in root development. J. Exp. Bot. 65, 6373–6384 (2014).

    Article  CAS  Google Scholar 

  38. Liu, X. et al. Arsenic induced phytate exudation, and promoted FeAsO4 dissolution and plant growth in As-hyperaccumulator Pteris vittata. Environ. Sci. Technol. 50, 9070–9077 (2016).

    Article  CAS  Google Scholar 

  39. Kong, X. et al. PHB3 maintains root stem cell niche identity through ROS-responsive AP2/ERF transcription factors in Arabidopsis. Cell Rep. 22, 1350–1363 (2018).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (21776163, 21676161 and U196224), Shandong Provincial Natural Science Foundation (ZR2019JQ18), Youth Interdisciplinary Science and Innovative Research Groups of Shandong University (2020QNQT014), the Fundamental Research Funds of Shandong University (2017JC021), the Qilu Youth Talent Program of Shandong University, the USDA-NIFA Hatch program (MAS 00549) and the UMass Amherst Conti Fellowship.

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Authors and Affiliations

  1. Shandong Key Laboratory of Water Pollution Control and Resource Reuse, School of Environmental Science and Engineering, Shandong University, Qingdao, People’s Republic of China

    Xiao-Dong Sun, Xian-Zheng Yuan, Li-Juan Feng, Fan-Ping Zhu, Shang-Shang Dong, Jian-Lu Duan & Shu-Guang Wang

  2. The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Science, Shandong University, Qingdao, People’s Republic of China

    Yuebin Jia, Jiajia Liu, Xiangpei Kong, Huiyu Tian & Zhaojun Ding

  3. Shandong Provincial Key Laboratory of Plant Stress Research, School of Life Science, Shandong Normal University, Jinan, People’s Republic of China

    Yuebin Jia

  4. State Key Laboratory of Microbial Technology, Shandong University, Qingdao, China

    Zhaojun Ding

  5. Stockbridge School of Agriculture, University of Massachusetts , Amherst, MA, USA

    Baoshan Xing

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  1. Xiao-Dong Sun
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Contributions

X.-Z.Y., S.-G.W. and B.X. designed the study. X.-Z.Y. and X.-D.S. wrote the manuscript. X.-Z.Y. and X.-D.S. analysed the results. Y.-B.J., H.T., X.K. and L.-J.F. performed the transcriptomics experiments. Y.-B.J. and J.-J.L. contributed to histological stains. F.-P.Z. contributed to high-performance liquid chromatography analyses. J.-L.D. and S.-S.D. synthesized nanoplastics. X.-Z.Y., X.-D.S., S.-G.W. and B.X. evaluated and revised the manuscript. Z.D. proofread the manuscript.

Corresponding authors

Correspondence to Xian-Zheng Yuan, Shu-Guang Wang or Baoshan Xing.

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Peer review information Nature Nanotechnology thanks Catherine Santaella, Geraldine Sarret and Fabienne Schwab for their contribution to the peer review of this work.

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Supplementary Information

Supplementary Tables 1–8, Figs. 1–15 and refs. 1–22.

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Sun, XD., Yuan, XZ., Jia, Y. et al. Differentially charged nanoplastics demonstrate distinct accumulation in Arabidopsis thaliana. Nat. Nanotechnol. 15, 755–760 (2020). https://doi.org/10.1038/s41565-020-0707-4

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