Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Soil mobility of synthetic and virus-based model nanopesticides

Nature Nanotechnology volume 14, pages 712–718 (2019)Cite this article

Subjects

Abstract

Large doses of chemical pesticides are required to achieve effective concentrations in the rhizosphere, which results in the accumulation of harmful residues. Precision farming is needed to improve the efficacy of pesticides, but also to avoid environmental pollution, and slow-release formulations based on nanoparticles offer one solution. Here, we tested the mobility of synthetic and virus-based model nanopesticides by combining soil column experiments with computational modelling. We found that the tobacco mild green mosaic virus and cowpea mosaic virus penetrate soil to a depth of at least 30 cm, and could therefore deliver nematicides to the rhizosphere, whereas the Physalis mosaic virus remains in the first 4 cm of soil and would be more useful for the delivery of herbicides. Our experiments confirm that plant viruses are superior to synthetic mesoporous silica nanoparticles and poly(lactic-co-glycolic acid) for the delivery and controlled release of pesticides, and could be developed as the next generation of pesticide delivery systems.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The combined experimental and computational approach to assess nanopesticide transport through soil.
Fig. 2: Cargo release from nanoparticles during dialysis.
Fig. 3: Experimental transport of nanopesticides and pesticides through soil.
Fig. 4: Theoretical transport of nanoparticles through soil.
Fig. 5: Theoretical transport of Cy5 through soil.
Fig. 6: Theoretical treatment of a crop infected with nematodes using TMGMV–abamectin.

Similar content being viewed by others

Data availability

The following raw data can be found in the Supplementary Information: the composition of the soil used to produce all experimental data (Supplementary Tables 2 and 3); the SDS PAGE required to reproduce the data presented in Fig. 3 (Supplementary Fig. 5); the Matlab code required to reproduce the data presented in Figs. 4–6 (Supplementary Code 1).

Code availability

These dimensionless equations were solved using partial differential equation solver function ‘pdepe’ (Matlab). All code was made available in Supplementary Code 1.

References

  1. Aktar, M. W., Sengupta, D. & Chowdhury, A. Impact of pesticides use in agriculture: their benefits and hazards. Interdisc. Toxicol. 2, 1–12 (2009).

    Article  Google Scholar 

  2. Lamberth, C., Jeanmart, S., Luksch, T. & Plant, A. Current challenges and trends in the discovery of agrochemicals. Science 341, 742–746 (2013).

    Article  Google Scholar 

  3. Atwood, D. & Paisley-Jones, C. Pesticide Industry Sales and Usage: 2008–2012 Market Estimates (US Environmental Protection Agency, 2017).

  4. Damalas, C. A. & Eleftherohorinos, I. G. Pesticide exposure, safety issues, and risk assessment indicators. Int. J. Environ. Res. Pub. He. 8, 1402–1419 (2011).

    Article  CAS  Google Scholar 

  5. Nuruzzaman, M., Rahman, M. M., Liu, Y. & Naidu, R. Nanoencapsulation, nano-guard for pesticides: a new window for safe application. J. Agr. Food Chem. 64, 1447–1483 (2016).

    Article  CAS  Google Scholar 

  6. Vurro, M., Miguel-Rojas, C. & Pérez-de-Luque, A. Safe nanotechnologies for increasing the effectiveness of environmentally friendly natural agrochemicals. Pest. Manag. Sci. https://doi.org/10.1002/ps.5348 (2019).

  7. Kah, M., Kookana, R. S., Gogos, A. & Bucheli, T. D. A critical evaluation of nanopesticides and nanofertilizers against their conventional analogues. Nat. Nanotechnol. 13, 677–684 (2018).

    Article  CAS  Google Scholar 

  8. Kookana, R. S. et al. Nanopesticides: guiding principles for regulatory evaluation of environmental risks. J. Agr. Food Chem. 62, 4227–4240 (2014).

    Article  CAS  Google Scholar 

  9. Walker, G. W. et al. Ecological risk assessment of nano-enabled pesticides: perspective on problem formulation. J. Agr. Food Chem. 66, 6480–6486 (2018).

    Article  CAS  Google Scholar 

  10. Chariou, P. L. & Steinmetz, N. F. Delivery of pesticides to plant parasitic nematodes using tobacco mild green mosaic virus as a nanocarrier. ACS Nano 11, 4719–4730 (2017).

    Article  CAS  Google Scholar 

  11. Cao, J. et al. Development of abamectin loaded plant virus nanoparticles for efficacious plant parasitic nematode control. ACS Appl. Mater. Interfaces 7, 9546–9553 (2015).

    Article  CAS  Google Scholar 

  12. Guenther, R. H., Lommel, S. A., Opperman, C. H. & Sit, T. L. in Virus-Derived Nanoparticles for Advanced Technologies: Methods and Protocols (eds Wege, C. & Lomonossoff, G. P.) 203–214 (Springer, 2018).

  13. Charudattan, R., Pettersen, M. & Hiebert, E. Use of tobacco mild green mosaic virus (TMGMV) mediated lethal hypersensitive response (HR) as a novel method of weed control. US patent 6689718 (2009).

  14. Charudattan, R. & Hiebert, E. A plant virus as a bioherbicide for tropical soda apple, Solanum viarum. Outlook Pest Manag. 18, 167–171 (2007).

    Article  Google Scholar 

  15. Umekawa, M. & Oshima, N. Sensitivity of tobacco mosaic virus to ultraviolet irradiation. Jpn J. Microbiol. 16, 441–443 (1972).

    Article  CAS  Google Scholar 

  16. Rae, C. et al. Chemical addressability of ultraviolet-inactivated viral nanoparticles (VNPs). PLoS ONE 3, e3315 (2008).

    Article  Google Scholar 

  17. Mir, M., Ahmed, N. & ur Rehman, A. Recent applications of PLGA based nanostructures in drug delivery. Colloids Surf. B 159, 217–231 (2017).

    Article  CAS  Google Scholar 

  18. Torney, F., Trewyn, B. G., Lin, V. S.-Y. & Wang, K. Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nat. Nanotechnol. 2, 295–300 (2007).

    Article  CAS  Google Scholar 

  19. Hassan, M. E. M., Zawam, H. S., El-Nahas, S. E. M. & Desoukey, A. F. Comparison study between silver nanoparticles and two nematicides against Meloidogyne incognita on tomato seedlings. Plant Pathol. J. 15, 144–151 (2016).

    Article  CAS  Google Scholar 

  20. Pestovsky, Y. S. & Martínez-Antonio, A. The use of nanoparticles and nanoformulations in agriculture. J. Nanosci. Nanotechnol. 17, 8699–8730 (2017).

    Article  CAS  Google Scholar 

  21. Truong, N. P., Whittaker, M. R., Mak, C. W. & Davis, T. P. The importance of nanoparticle shape in cancer drug delivery. Expert Opin. Drug Deliv. 12, 129–142 (2015).

    Article  CAS  Google Scholar 

  22. Barua, S. & Mitragotri, S. Challenges associated with penetration of nanoparticles across cell and tissue barriers: a review of current status and future prospects. Nano Today 9, 223–243 (2014).

    Article  CAS  Google Scholar 

  23. Toy, R. The Effect of Particle Size and Shape on the in vivo Journey of Nanoparticles. PhD thesis, Case Western Reserve University (2014).

  24. OECD Guidelines Test for the Testing of Chemicals No. 312: Leaching in Soil Columns (OECD, 2004).

  25. Chen, Z., Li, N., Chen, L., Lee, J. & Gassensmith, J. J. Dual functionalized bacteriophage Qβ as a photocaged drug carrier. Small 12, 4563–4571 (2016).

    Article  CAS  Google Scholar 

  26. Quentin, M., Abad, P. & Favery, B. Plant parasitic nematode effectors target host defense and nuclear functions to establish feeding cells. Front. Plant Sci. 4, 53 (2013).

    Article  Google Scholar 

  27. Godfrey, G. H. The depth distribution of the root-knot nematode, Heterodera radicicola, in Florida soils. J. Agri. Res. 24, 93–98 (1924).

    Google Scholar 

  28. Putter, I. et al. Avermectins: novel insecticides, acaricides and nematicides from a soil microorganism. Experientia 37, 963–964 (1981).

    Article  CAS  Google Scholar 

  29. Schoenmakers, R. G., van de Wetering, P., Elbert, D. L. & Hubbell, J. A. The effect of the linker on the hydrolysis rate of drug-linked ester bonds. J. Control Release 95, 291–300 (2004).

    Article  CAS  Google Scholar 

  30. Steinmetz, N. F. & Manchester, M. Viral Nanoparticles: Tools for Materials Science and Medicine (Pan Stanford, 2015).

  31. Masarapu, H. et al. Physalis mottle virus-like particles as nanocarriers for imaging reagents and drugs. Biomacromolecules 18, 4141–4153 (2017).

    Article  CAS  Google Scholar 

  32. Ultman, J. S., Baskaran, H. & Saidel, G. M. Biomedical Mass Transport and Chemical Reaction: Physicochemical Principles and Mathematical Modeling (Wiley, 2016).

Download references

Acknowledgements

This work was supported by a grant from the National Science Foundation CAREER DMR 1841848 (to N.F.S.) and NIH EB021911 (to H.B.). We thank H. Hu for providing the PhMV particles used in this study.

Author information

Authors and Affiliations

  1. Department of Bioengineering, University of California-San Diego, La Jolla, CA, USA

    Paul L. Chariou & Nicole F. Steinmetz

  2. Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH, USA

    Paul L. Chariou, Alan B. Dogan, Gerald M. Saidel & Nicole F. Steinmetz

  3. Department of Chemical and Biomolecular Engineering, Case Western Reserve University, Cleveland, OH, USA

    Alexandra G. Welsh & Harihara Baskaran

  4. Department of NanoEngineering, University of California-San Diego, La Jolla, CA, USA

    Nicole F. Steinmetz

  5. Moores Cancer Center, University of California-San Diego, La Jolla, CA, USA

    Nicole F. Steinmetz

  6. Department of Radiology, University of California-San Diego, La Jolla, CA, USA

    Nicole F. Steinmetz

Authors
  1. Paul L. Chariou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alan B. Dogan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexandra G. Welsh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gerald M. Saidel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Harihara Baskaran
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nicole F. Steinmetz
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

N.F.S. devised the project, the main conceptual ideas and proof outline. P.L.C. developed the technical procedures and performed the experiments, and developed the mathematical model under the supervision of G.M.S. and H.B. A.B.D. and A.G.W. performed the gel electrophoresis technical work under the supervision of P.L.C. The numerical solution of the computational model was executed using Matlab by P.L.C., under the supervision of H.B. P.L.C. and N.F.S. wrote the manuscript; all the authors read or edited the manuscript.

Corresponding author

Correspondence to Nicole F. Steinmetz.

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. 1–13, Supplementary Tables 1–5, Matlab codes.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chariou, P.L., Dogan, A.B., Welsh, A.G. et al. Soil mobility of synthetic and virus-based model nanopesticides. Nat. Nanotechnol. 14, 712–718 (2019). https://doi.org/10.1038/s41565-019-0453-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41565-019-0453-7

This article is cited by

Search

Advanced search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research