Effective uptake of submicrometre plastics by crop plants via a crack-entry mode

Abstract

Most microplastics are emitted, either directly or via the degradation of plastics, to the terrestrial environment and accumulate in large amounts in soils, representing a potential threat to terrestrial ecosystems. It is very important to evaluate the uptake of microplastics by crop plants because of the ubiquity of microplastics in wastewaters often used for agricultural irrigation worldwide. Here, we analyse the uptake of different microplastics by crop plants (wheat (Triticum aestivum) and lettuce (Lactuca sativa)) from treated wastewater in hydroponic cultures and in sand matrices or a sandy soil. Our results provide evidence in support of submicrometre- and micrometre-sized polystyrene and polymethylmethacrylate particles penetrating the stele of both species using the crack-entry mode at sites of lateral root emergence. This crack-entry pathway and features of the polymeric particles lead to the efficient uptake of submicrometre plastic. The plastic particles were subsequently transported from the roots to the shoots. Higher transpiration rates enhanced the uptake of plastic particles, showing that the transpirational pull was the main driving force of their movement. Our findings shed light on the modes of plastic particle interaction with plants and have implications for crops grown in fields contaminated with wastewater treatment discharges or sewage sludges.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Accumulation of 0.2 μm fluorescently labelled PS beads by wheat plants.
Fig. 2: Accumulation of 0.2 μm fluorescently labelled PS beads by lettuce.
Fig. 3: SEM images of 0.2 μm PS bead localization in the root, stem and leaf of a wheat plant.
Fig. 4: SEM images of 0.2 μm PS bead localization in the root and leaf of a lettuce plant.
Fig. 5: SEM images of 2.0 μm PS microbead localization in the root, stem and leaf of a wheat plant.
Fig. 6: SEM images of 2.0 μm PS bead localization in the root and leaf of a lettuce plant.

Data availability

The data that support the findings of this study are available in the paper and its Supplementary Information or from the corresponding author upon request.

References

  1. 1.

    Jambeck, J. R. et al. Plastic waste inputs from land into the ocean. Science 347, 768–771 (2015).

    CAS  Google Scholar 

  2. 2.

    Barnes, D. K. A. et al. Accumulation and fragmentation of plastic debris in global environments. Phil. Trans. R. Soc. B 364, 1985–1998 (2009).

    CAS  Google Scholar 

  3. 3.

    Wallace, H. Presence of microplastics and nanoplastics in food, with particular focus on seafood. EFSA J. 14, e04501 (2016).

    Google Scholar 

  4. 4.

    Wardrop, P. et al. Chemical pollutants sorbed to ingested microbeads from personal care products accumulate in fish. Environ. Sci. Technol. 50, 4037–4044 (2016).

    CAS  Google Scholar 

  5. 5.

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

    CAS  Google Scholar 

  6. 6.

    Seltenrich, N. New link in the food chain? marine plastic pollution and seafood safety. Environ. Health Persp. 123, A34-41 (2015).

    Google Scholar 

  7. 7.

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

    CAS  Google Scholar 

  8. 8.

    Zhou, Q. et al. The distribution and morphology of microplastics in coastal soils adjacent to the Bohai Sea and the Yellow Sea. Geoderma 322, 201–208 (2018).

    CAS  Google Scholar 

  9. 9.

    Weithmann, N. et al. Organic fertilizer as a vehicle for the entry of microplastic into the environment. Sci. Adv. 4, EAAP8060 (2018).

    Google Scholar 

  10. 10.

    Nizzetto, L., Futter, M. & Langaas, S. Are agricultural soils dumps for microplastics of urban origin? Environ. Sci. Technol. 50, 10777–10779 (2016).

    CAS  Google Scholar 

  11. 11.

    van Sebille, E. A global inventory of small floating plastic debris. Environ. Res. Lett. 10, 124006 (2015).

    Google Scholar 

  12. 12.

    Rodriguez-Seijo, A. et al. Histopathological and molecular effects of microplastics in Eisenia andrei Bouché. Environ. Pollut. 220, 495–503 (2017).

    CAS  Google Scholar 

  13. 13.

    Huerta Lwanga, E. et al. Field evidence for transfer of plastic debris along a terrestrial food chain. Sci. Rep. 7, 14071 (2017).

    Google Scholar 

  14. 14.

    Sato, T. et al. Global, regional, and country level need for data on wastewater generation, treatment, and use. Agric. Water Manage. 130, 1–13 (2013).

    Google Scholar 

  15. 15.

    Kalčíková, G. et al. Wastewater treatment plant effluents as source of cosmetic polyethylene microbeads to freshwater. Chemosphere 188, 25–31 (2017).

    Google Scholar 

  16. 16.

    Schwab, F. et al. Barriers, pathways and processes for uptake, translocation and accumulation of nanomaterials in plants - critical review. Nanotoxicology 10, 257–278 (2016).

    CAS  Google Scholar 

  17. 17.

    Robardsa, W. & Jackson, M. in Perspectives in Experimental Biology Vol. 2 (ed. Sunderland, N.) 413–422 (Pergamon, 1976).

  18. 18.

    Karas, I. & Mccully, M. E. Further studies of the histology of lateral root development in Zea mays. Protoplasma 77, 243–269 (1973).

    Google Scholar 

  19. 19.

    Huang, J. Ultrastructure of bacterial penetration in plants. Annu. Rev. Phytopathol. 24, 141–157 (1986).

    Google Scholar 

  20. 20.

    Vega-Hernández, M. C. et al. Novel infection process in the indeterminate root nodule symbiosis between Chamaecytisus proliferus (tagasaste) and Bradyrhizobium sp. New Phytol. 150, 707–721 (2001).

    Google Scholar 

  21. 21.

    Marschner, H. Mineral Nutrition of Higher Plants 2nd edn (Academic, 1995).

  22. 22.

    Carpita, N. et al. Determination of the pore size of cell walls of living plant cells. Science 205, 1144–1147 (1979).

    CAS  Google Scholar 

  23. 23.

    Smith, H. The Molecular Biology of Plant Cells (Univ. of California Press, 1978).

  24. 24.

    Enstone, D. E. & Peterson, C. A. Suberin lamella development in maize seedling roots grown in aerated and stagnant conditions. Plant Cell Environ. 28, 444–455 (2005).

    Google Scholar 

  25. 25.

    Gouin, T. et al. Use of micro-plastics beads in cosmetics products in Europe and their estimated emissions to the North Sea environment. SOFW J. 141, 40–46 (2015).

    Google Scholar 

  26. 26.

    Plastic in Cosmetics (UNEP, 2015).

  27. 27.

    Fendall, L. S. & Sewell, M. A. Contributing to marine pollution by washing your face: microplastics in facial cleansers. Mar. Pollut. Bull. 58, 1225–1228 (2009).

    CAS  Google Scholar 

  28. 28.

    Fahn, A. Plant Anatomy (Pergamon, 1982).

  29. 29.

    Ristroph, K. D. et al. Zein nanoparticles uptake by hydroponically grown soybean plants. Environ. Sci. Technol. 51, 14065–14071 (2017).

    CAS  Google Scholar 

  30. 30.

    González-Melendi, P. et al. Nanoparticles as smart treatment-delivery systems in plants: assessment of different techniques of microscopy for their visualization in plant tissues. Ann. Bot. 101, 187–195 (2008).

    Google Scholar 

  31. 31.

    Taylor, A. F. et al. Investigating the toxicity, uptake, nanoparticle formation and genetic response of plants to gold. PLoS ONE 9, e93793 (2014).

    Google Scholar 

  32. 32.

    Larue, C. et al. Accumulation, translocation and impact of TiO2 nanoparticles in wheat (Triticum aestivum spp.): influence of diameter and crystal phase. Sci. Total Environ. 431, 197–208 (2012).

    CAS  Google Scholar 

  33. 33.

    Zhang, M. & Akbulut, M. Adsorption, desorption, and removal of polymeric nanomedicine on and from cellulose surfaces: effect of size. Langmuir 27, 12550–12559 (2011).

    CAS  Google Scholar 

  34. 34.

    Wen, F. et al. Extracellular proteins in pea root tip and border cell exudates. Plant Physiol. 143, 773–783 (2007).

    CAS  Google Scholar 

  35. 35.

    Driouich, A. et al. Root border cells and secretions as critical elements in plant host defense. Curr. Opin. Plant Biol. 16, 489–495 (2013).

    CAS  Google Scholar 

  36. 36.

    Nel, A. E. et al. Understanding biophysicochemical interactions at the nano-bio interface. Nat. Mater. 8, 543–557 (2009).

    CAS  Google Scholar 

  37. 37.

    Wang, C. X. et al. Modelling the mechanical properties of single suspension-cultured tomato cells. Ann. Bot. 93, 443–453 (2004).

    CAS  Google Scholar 

  38. 38.

    Yu, M. et al. Rapid transport of deformation-tuned nanoparticles across biological hydrogels and cellular barriers. Nat. Commun. 9, 2607 (2018).

    Google Scholar 

  39. 39.

    Li, L. Z. et al. Uptake and accumulation of microplastics in an edible plant. Chin. Sci. Bull. 64, 928–934 (2019).

    Google Scholar 

  40. 40.

    White, P. J. Long-Distance Transport in the Xylem and Phloem (Elsevier, 2011).

  41. 41.

    Production/Crops (FAO Statistics Division, 2017); http://faostat3.fao.org/browse/Q/QC/E.

  42. 42.

    GEMS/Food Regional Diets: Regional Per Capita Consumption of Raw and Semi-processed Agricultural Commodities (WHO, 2003).

  43. 43.

    Lehner, R. et al. Emergence of nanoplastic in the environment and possible impact on human health. Environ. Sci. Technol. 53, 1748–1765 (2019).

    CAS  Google Scholar 

  44. 44.

    Ter Halle, A. et al. Nanoplastic in the North Atlantic subtropical gyre. Environ. Sci. Technol. 51, 13689–13697 (2017).

    CAS  Google Scholar 

  45. 45.

    Lambert, S. & Wagner, M. Characterisation of nanoplastics during the degradation of polystyrene. Chemosphere 145, 265–268 (2016).

    CAS  Google Scholar 

  46. 46.

    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).

    CAS  Google Scholar 

  47. 47.

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

    CAS  Google Scholar 

  48. 48.

    Lu, S., Qu, R. & Forcada, J. Preparation of magnetic polymeric composite nanoparticles by seeded emulsion polymerization. Mater. Lett. 63, 770–772 (2009).

    CAS  Google Scholar 

  49. 49.

    Peng, B. et al. Synthesis of monodisperse, highly cross-linked, fluorescent PMMA particles by dispersion polymerization. Langmuir 28, 6776–6785 (2012).

    CAS  Google Scholar 

  50. 50.

    Hoagland, D. R. & Arnon, D. I. The Water-Culture Method for Growing Plants without Soil Circular No. 347 (Univ. of California, College of Agriculture, 1938).

  51. 51.

    Jiao, L. et al. Improving the brightness and photostability of NIR fluorescent silica nanoparticles through rational fine-tuning of the covalent encapsulation methods. J. Mater. Chem. B 5, 5278–5283 (2017).

  52. 52.

    Stanghellini, C. & Van Meurs, W. T. M. Environmental control of greenhouse crop transpiration. J. Agric. Eng. Res. 51, 297–311 (1992).

    Google Scholar 

Download references

Acknowledgements

We acknowledge the financial support by the National Nature Science Foundation of China (grant nos 41877142 and 41991330), the Key Research Program of Frontier Sciences, CAS (grant no. QYZDJ-SSW-DQC015) and the External Cooperation Program of BIC, Chinese Academy of Sciences (grant no. 133337KYSB20160003). We thank P. Christie from the Institute of Soil Science, Chinese Academy of Sciences, China, for contributing to language polishing.

Author information

Affiliations

Authors

Contributions

Y.L. managed the whole project, designed all the experiments and jointly wrote the manuscript. L.L. conducted the uptake experiments and wrote the manuscript. R.L. inspected the plant tissue using a confocal laser scanning microscope and collected the images. N.Y. and J.Y. examined the samples with a scanning electron microscope and collected the images. R.L. and Y.Z. conducted the X-ray computed microtomography using a high-resolution X-ray computed microtomography system. Q.Z. and N.Y. analysed the mechanical properties of the PS beads using a Dimension Icon atomic force microscope system and collected the images. W.J.G.M.P. and C.T. helped with the manuscript revising and data analysis.

Corresponding author

Correspondence to Yongming Luo.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–37.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, L., Luo, Y., Li, R. et al. Effective uptake of submicrometre plastics by crop plants via a crack-entry mode. Nat Sustain (2020). https://doi.org/10.1038/s41893-020-0567-9

Download citation

Further reading