Skip to main content
Book cover

Inorganic Nanopesticides and Nanofertilizers pp 123–152Cite as

Biological Barriers, Processes, and Transformations at the Soil–Plant–Atmosphere Interfaces Driving the Uptake, Translocation, and Bioavailability of Inorganic Nanoparticles to Plants

  • 520 Accesses

Abstract

The development of nanotechnologies for more sustainable agriculture is an innovative strategy proposed to increase food production while decreasing material inputs and reducing environmental impacts. Nanoparticles (NPs) applied to seeds, soil, or leaves interact with plants at two major interfaces: the rhizoplane (root–rhizosphere interface) or the phylloplane (atmosphere–leaf interface). NP transformations occurring at these interfaces control their bioavailability, while plant structures are barriers to NP absorption and bottlenecks for their translocation. This chapter focuses on the complex interplays driving NP uptake, translocation, and accumulation into plant tissues. Foliar treatments appear to present advantages over soil application for the delivery of NPs to certain compartments. The adjustment for nanoparticle’s shape and surface properties could allow specific targeting (e.g., apoplast, symplast, organelles) and designed mobility to freely reach the phloem or accumulate in the mesophyll. This chapter highlights the knowledge gaps that need to be overcome for the safe and efficient development of nano-enabled agriculture. The parameters influencing for NP movement across cuticle barriers, cell walls, and cell membranes are still to be identified. Consequently, NP mobility in the root cortex and through the endodermis before entering the xylem or in the mesophyll before loading the phloem is not predictable yet. The processes that drive NP movement from the mesophyll cells to the sinks and their capacity to load the phloem are also poorly characterized. In addition, plant physiological responses and in vivo transformations, such as dissolution rates, or protein corona formation around NPs, remain important knowledge gaps that need to be addressed to understand, predict, and regulate NP translocation in plants and their bioavailability, thus enabling safe and efficient, targeted delivery of NPs for agricultural purposes.

Keywords

  • Target
  • Fate
  • Nanobiotechnology
  • Plant-nanoparticle interaction

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-3-030-94155-0_4
  • Chapter length: 30 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   149.00
Price excludes VAT (USA)
  • ISBN: 978-3-030-94155-0
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Hardcover Book
USD   199.99
Price excludes VAT (USA)
Learn about institutional subscriptions
Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Adisa, I. O., Pullagurala, V. L. R., Peralta-Videa, J. R., Dimkpa, C. O., Elmer, W. H., Gardea-Torresdey, J. L., & White, J. C. (2019). Recent advances in nano-enabled fertilizers and pesticides: A critical review of mechanisms of action. Environmental Science: Nano, 6, 2002–2030. https://doi.org/10.1039/c9en00265k

    CrossRef  CAS  Google Scholar 

  • Ahmed, E., & Holmström, S. J. M. (2014). Siderophores in environmental research: Roles and applications. Microbial Biotechnology, 7, 196–208. https://doi.org/10.1111/1751-7915.12117

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson, A., McLean, J., McManus, P., & Britt, D. (2017). Soil chemistry influences the phytotoxicity of metal oxide nanoparticles. International Journal of Nanotechnology, 14, 15–21. https://doi.org/10.1504/IJNT.2017.082438

    CrossRef  CAS  Google Scholar 

  • Avellan, A., Schwab, F., Masion, A., Chaurand, P., Borschneck, D., Vidal, V., Rose, J., Santaella, C., & Levard, C. (2017). Nanoparticle uptake in plants: Gold nanomaterial localized in roots of Arabidopsis thaliana by X-ray computed Nanotomography and hyperspectral imaging - Environmental Science & Technology (ACS publications). Environmental Science and Technology, 51, 8682–8691. https://doi.org/10.1021/acs.est.7b01133

    CrossRef  CAS  PubMed  Google Scholar 

  • Avellan, A., Yun, J., Zhang, Y., Spielman-Sun, E., Unrine, J. M. J. M., Thieme, J., Li, J., Lombi, E., Bland, G., & Lowry, G. V. G. V. (2019). Nanoparticle size and coating chemistry control foliar uptake pathways, translocation, and leaf-to-rhizosphere transport in wheat. ACS Nano, 13, 5291–5305. https://doi.org/10.1021/acsnano.8b09781

    CrossRef  CAS  PubMed  Google Scholar 

  • Belhaj Abdallah, B., Andreu, I., Chatti, A., Landoulsi, A., & Gates, B. D. (2020). Size fractionation of Titania nanoparticles in wild Dittrichia viscosa grown in a native environment. Environmental Science and Technology, 54, 8649–8657. https://doi.org/10.1021/acs.est.9b07267

    CrossRef  CAS  PubMed  Google Scholar 

  • Berhin, A., de Bellis, D., Franke, R. B., Buono, R. A., Nowack, M. K., & Nawrath, C. (2019). The root cap cuticle: A Cell Wall structure for seedling establishment and lateral root formation. Cell, 176, 1367–1378.e8. https://doi.org/10.1016/j.cell.2019.01.005

    CrossRef  CAS  PubMed  Google Scholar 

  • Bindraban, P. S., Dimkpa, C., Nagarajan, L., Roy, A., & Rabbinge, R. (2015). Revisiting fertilisers and fertilisation strategies for improved nutrient uptake by plants. Biology and Fertility of Soils, 51, 897–911. https://doi.org/10.1007/s00374-015-1039-7

    CrossRef  CAS  Google Scholar 

  • Bombo, A. B., Pereira, A. E. S., Lusa, M. G., De Medeiros, O. E., De Oliveira, J. L., Campos, E. V. R., De Jesus, M. B., Oliveira, H. C., Fraceto, L. F., & Mayer, J. L. S. (2019). A mechanistic view of interactions of a Nanoherbicide with target organism. Journal of Agricultural and Food Chemistry, 67, 4453–4462. https://doi.org/10.1021/acs.jafc.9b00806

    CrossRef  CAS  PubMed  Google Scholar 

  • Borgatta, J., Ma, C., Hudson-smith, N., Elmer, W., David, C., Pe, P., La, T.-r. R. D., Zuverza-mena, N., Haynes, C. L., White, J. C., & Hamers, R. J. (2018). Copper based nanomaterials suppress root fungal disease in watermelon (Citrullus lanatus): Role of particle morphology, composition and dissolution behavior. ACS Sustainable Chemistry & Engineering, 6, 14847–14856.

    CrossRef  CAS  Google Scholar 

  • Camara, M. C., Campos, E. V. R., Monteiro, R. A., do Espirito Santo Pereira, A., de Freitas Proença, P. L., & Fraceto, L. F. (2019). Development of stimuli-responsive nano-based pesticides: Emerging opportunities for agriculture. Journal of Nanobiotechnology, 17, 100. https://doi.org/10.1186/s12951-019-0533-8

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Cerutti, A., Jauneau, A., Laufs, P., Leonhardt, N., Schattat, M. H., Berthomé, R., Routaboul, J.-M., & Noël, L. D. (2019). Annual review of phytopathology mangroves in the leaves: Anatomy. Physiology, and Immunity of Epithemal Hydathodes. https://doi.org/10.1146/annurev-phyto-082718

  • Cocozza, C., Perone, A., Giordano, C., Salvatici, M. C., Pignattelli, S., Raio, A., Schaub, M., Sever, K., Innes, J. L., Tognetti, R., & Cherubini, P. (2019). Silver nanoparticles enter the tree stem faster through leaves than through roots. Tree Physiology, 39, 1251–1261. https://doi.org/10.1093/treephys/tpz046

    CrossRef  CAS  PubMed  Google Scholar 

  • Cornelis, G., Hund-Rinke, K., Kuhlbusch, T., Van Den Brink, N., & Nickel, C. (2014). Fate and bioavailability of engineered nanoparticles in soils: A Review,Interactions within natural soils have often been neglectedwhen assessing fate and bioavailability of engineered nanomaterials (ENM) in soils. This review combines patchwise ENM resea. Critical Reviews in Environmental Science and Technology, 44, 2720–2764. https://doi.org/10.1080/10643389.2013.829767

    CrossRef  CAS  Google Scholar 

  • Dahle, J. T., Livi, K., & Arai, Y. (2015). Effects of pH and phosphate on CeO2 nanoparticle dissolution. Chemosphere. https://doi.org/10.1016/j.chemosphere.2014.02.027

  • DeRosa, M. C., Monreal, C., Schnitzer, M., Walsh, R., Sultan, Y., Nair, R., Varghese, S. H., Nair, B. G., Maekawa, T., Yoshida, Y., Kumar, D. S., Singh Sekhon, B., O’Sullivan, J. N., Asher, C. J., Blarney, C., Stampoulis, D., Sinha, S. K., White, J. C., Nanocomposix, T. M. A., … Gardea-Torresdey, J. L. (2015). Copper nanoparticles/compounds impact agronomic and physiological parameters in cilantro (Coriandrum sativum). Environmental Science: Processes & Impacts, 17, 1783–1793. https://doi.org/10.1039/C5EM00329F

    CrossRef  CAS  Google Scholar 

  • Dimkpa, C. O. (2018). Soil properties influence the response of terrestrial plants to metallic nanoparticles exposure. Current Opinion in Environmental Science and Health, 6, 1–8. https://doi.org/10.1016/j.coesh.2018.06.007

    CrossRef  Google Scholar 

  • Dimkpa, C. O., White, J. C., Elmer, W. H., & Gardea-Torresdey, J. (2017). Nanoparticle and ionic Zn promote nutrient loading of sorghum grain under low NPK fertilization. Journal of Agricultural and Food Chemistry, 65, 8552–8559. https://doi.org/10.1021/acs.jafc.7b02961

    CrossRef  CAS  PubMed  Google Scholar 

  • do Espirito Santo Pereira, A., Caixeta Oliveira, H., Fernandes Fraceto, L., & Santaella, C. (2021). Nanotechnology potential in seed priming for sustainable agriculture. Nanomaterials, 11, 267. https://doi.org/10.3390/nano11020267

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Doolette, C. L., Read, T. L., Howell, N. R., Cresswell, T., & Lombi, E. (2020). Zinc from foliar-applied nanoparticle fertiliser is translocated to wheat grain: A 65Zn radiolabelled translocation study comparing conventional and novel foliar fertilisers. Science of the Total Environment, 749. https://doi.org/10.1016/j.scitotenv.2020.142369

  • Dotaniya, M. L., & Meena, V. D. (2015). Rhizosphere effect on nutrient availability in soil and its uptake by plants: A review. Proceedings of the National Academy of Sciences India Section B – Biological Sciences, 85, 1–12. https://doi.org/10.1007/s40011-013-0297-0

    CrossRef  CAS  Google Scholar 

  • Eichert, T., & Goldbach, H. E. (2008). Equivalent pore radii of hydrophilic foliar uptake routes in stomatous and astomatous leaf surfaces—Further evidence for a stomatal pathway. Physiologia Plantarum, 132, 491–502. https://doi.org/10.1111/j.1399-3054.2007.01023.x

    CrossRef  CAS  PubMed  Google Scholar 

  • Eichert, T., Kurtz, A., Steiner, U., & Goldbach, H. E. (2008). Size exclusion limits and lateral heterogeneity of the stomatal foliar uptake pathway for aqueous solutes and water-suspended nanoparticles. Physiologia Plantarum, 134, 151–160. https://doi.org/10.1111/j.1399-3054.2008.01135.x

    CrossRef  CAS  PubMed  Google Scholar 

  • El-shetehy, M., Moradi, A., Maceroni, M., Reinhardt, D., Petri-fink, A., Rothen-rutishauser, B., Mauch, F., & Schwab, F. (2020). Silica nanoparticles enhance disease resistance in Arabidopsis plants. Nature Nanotechnology. https://doi.org/10.1038/s41565-020-00812-0

  • Fischer, J., Beckers, S. J., Yiamsawas, D., Thines, E., Landfester, K., Wurm, F. R. (2019). Targeted drug delivery in plants: Enzyme-responsive Lignin nanocarriers for the curative treatment of the worldwide grapevine trunk disease Esca. https://doi.org/10.1002/advs.201802315.

  • Gao, X., Avellan, A., Laughton, S., Vaidya, R., Rodrigues, S. M., Casman, E. A., & Lowry, G. V. (2018). CuO nanoparticle dissolution and toxicity to wheat (Triticum aestivum) in rhizosphere soil. Environmental Science and Technology, 52. https://doi.org/10.1021/acs.est.7b05816

  • Gao, X., Rodrigues, S. M., Spielman-Sun, E., Lopes, S., Rodrigues, S., Zhang, Y., Avellan, A., Duarte, R. M. B. O., Duarte, A., Casman, E. A., & Lowry, G. V. (2019). Effect of soil organic matter, soil pH, and moisture content on solubility and dissolution rate of CuO NPs in soil. Environmental Science and Technology, 53. https://doi.org/10.1021/acs.est.8b07243

  • Gao, X., Spielman-Sun, E., Rodrigues, S. M., Casman, E. A., & Lowry, G. V. (2017). Time and nanoparticle concentration affect the extractability of cu from CuO NP-amended soil. Environmental Science & Technology, 51, 2226–2234. https://doi.org/10.1021/acs.est.6b04705

    CrossRef  CAS  Google Scholar 

  • Geisler-Lee, J., Wang, Q., Yao, Y., Zhang, W., Geisler, M., Li, K., Huang, Y., Chen, Y., Kolmakov, A., & Ma, X. (2013). Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thaliana. Nanotoxicology, 7, 323–337. https://doi.org/10.3109/17435390.2012.658094

    CrossRef  CAS  PubMed  Google Scholar 

  • Gilbertson, L. M., Pourzahedi, L., Laughton, S., Gao, X., Zimmerman, J. B., Theis, T. L., Westerhoff, P., & Lowry, G. V. (2020). Guiding the design space for nanotechnology to advance sustainable crop production. Nature Nanotechnology, 15, 801–810. https://doi.org/10.1038/s41565-020-0706-5

    CrossRef  CAS  PubMed  Google Scholar 

  • Giraldo, J. P., Landry, M. P., Faltermeier, S. M., McNicholas, T. P., Iverson, N. M., Boghossian, A. A., Reuel, N. F., Hilmer, A. J., Sen, F., Brew, J. A., & Strano, M. S. (2014). Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nature Materials, 13, 400–408. https://doi.org/10.1038/nmat3890

    CrossRef  CAS  PubMed  Google Scholar 

  • Gollan, T., Schurr, U., & Schulze, E.-D. (1992). Stomatal response to drying soil in relation to changes in the xylem sap composition of Helianthus annuus. I. the concentration of cations, anions, amino acids in, and pH of, the xylem sap. Plant, Cell & Environment, 15, 551–559. https://doi.org/10.1111/j.1365-3040.1992.tb01488.x

    CrossRef  CAS  Google Scholar 

  • Hetherington, A., Woodward, I. (2003). The role of stomata in sensing and driving environmental change. London.

    Google Scholar 

  • Hofmann, T., Lowry, G. V., Ghoshal, S., Tufenkji, N., Brambilla, D., Dutcher, J. R., Gilbertson, L. M., Giraldo, J. P., Kinsella, J. M., Landry, M. P., Lovell, W., Naccache, R., Paret, M., Pedersen, J. A., Unrine, J. M., White, J. C., & Wilkinson, K. J. (2020). Technology readiness and overcoming barriers to sustainably implement nanotechnology-enabled plant agriculture. Nature Food, 1, 416–425. https://doi.org/10.1038/s43016-020-0110-1

    CrossRef  CAS  Google Scholar 

  • Hong, J., Peralta-Videa, J. R., Rico, C., Sahi, S., Viveros, M. N., Bartonjo, J., Zhao, L., & Gardea-Torresdey, J. L. (2014). Evidence of translocation and physiological impacts of foliar applied CeO2 nanoparticles on cucumber (Cucumis sativus) plants. Environmental Science & Technology, 48, 4376–4385. https://doi.org/10.1021/es404931g

    CrossRef  CAS  Google Scholar 

  • Hong, J., Wang, L., Sun, Y., Zhao, L., Niu, G., Tan, W., Rico, C. M., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2016). Foliar applied nanoscale and microscale CeO 2 and CuO alter cucumber (Cucumis sativus) fruit quality. Science of the Total Environment, 563, 904–911.

    CrossRef  Google Scholar 

  • Hu, P., An, J., Faulkner, M. M., Wu, H., Li, Z., Tian, X., & Giraldo, J. P. (2020). Nanoparticle charge and size control foliar delivery efficiency to plant cells and organelles. ACS Nano, 14, 7970–7986. https://doi.org/10.1021/acsnano.9b09178

    CrossRef  CAS  PubMed  Google Scholar 

  • Hülskamp, M. (2004). Plant trichomes: A model for cell differentiation. Nature Reviews Molecular Cell Biology, 5, 471–480. https://doi.org/10.1038/nrm1404

    CrossRef  CAS  PubMed  Google Scholar 

  • Hussain, B., Lin, Q., Hamid, Y., Sanaullah, M., Di, L., Hashmi, M. L. u. R., Khan, M. B., He, Z., & Yang, X. (2020). Foliage application of selenium and silicon nanoparticles alleviates cd and Pb toxicity in rice (Oryza sativa L.). Science of the Total Environment, 712, 136497. https://doi.org/10.1016/j.scitotenv.2020.136497

    CrossRef  CAS  PubMed  Google Scholar 

  • Javelle, M., Vernoud, V., Rogowsky, P. M., & Ingram, G. C. (2011). Epidermis: The formation and functions of a fundamental plant tissue. New Phytologist, 189, 17–39. https://doi.org/10.1111/j.1469-8137.2010.03514.x

    CrossRef  CAS  PubMed  Google Scholar 

  • Jensen, K. H., Berg-Sørensen, K., Bruus, H., Holbrook, N. M., Liesche, J., Schulz, A., Zwieniecki, M. A., & Bohr, T. (2016). Sap flow and sugar transport in plants. Reviews of Modern Physics, 88. https://doi.org/10.1103/RevModPhys.88.035007

  • Jia, X., Sheng, W. B., Li, W., Bin, T. Y., Liu, Z. Y., & Zhou, F. (2014). Adhesive polydopamine coated avermectin microcapsules for prolonging foliar pesticide retention. ACS Applied Materials and Interfaces, 6, 19552–19558. https://doi.org/10.1021/am506458t

    CrossRef  CAS  PubMed  Google Scholar 

  • Kah, M., Navarro, D., Kookana, R. S., Kirby, J. K., Santra, S., Ozcan, A., & Kabiri, S. (2019b). Impact of (nano)formulations on the distribution and wash-off of copper pesticides and fertilisers applied on citrus leaves. Environmental Chemistry, 16, 401. https://doi.org/10.1071/EN18279

    CrossRef  CAS  Google Scholar 

  • Kah, M., Tufenkji, N., & White, J. C. (2019a). Nano-enabled strategies to enhance crop nutrition and protection. Nature Nanotechnology, 14, 532–540. https://doi.org/10.1038/s41565-019-0439-5

    CrossRef  CAS  PubMed  Google Scholar 

  • Karas, I., & McCully, M. E. (1973). Further studies of the histology of lateral root development in Zea mays. Protoplasma: An. International Journal of Cell Biology, 77, 243–269. https://doi.org/10.1007/BF01276762

    CrossRef  Google Scholar 

  • Kopittke, P. M., Lombi, E., Wang, P., Schjoerring, J. K., & Husted, S. (2019). Nanomaterials as fertilizers for improving plant mineral nutrition and environmental outcomes. Environmental Science: Nano, 6, 3513–3524. https://doi.org/10.1039/c9en00971j

    CrossRef  CAS  Google Scholar 

  • Kühn, C., Franceschi, V. R., Schulz, A., Lemoine, R., & Frommer, W. B. (1997). Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science. https://doi.org/10.1126/science.275.5304.1298

  • Kwak, S.-Y. Y., Giraldo, J. P., Wong, M. H., Koman, V. B., Lew, T. T. S., Ell, J., Weidman, M. C., Sinclair, R. M., Landry, M. P., Tisdale, W. A., & Strano, M. S. (2017). A Nanobionic light-emitting plant. Nano Letters, 17, 7951–7961. https://doi.org/10.1021/acs.nanolett.7b04369

    CrossRef  CAS  PubMed  Google Scholar 

  • Larue, C., Castillo-Michel, H., Sobanska, S., Cécillon, L., Bureau, S., Barthès, V., Ouerdane, L., Carrière, M., & Sarret, G. (2014a). Foliar exposure of the crop Lactuca sativa to silver nanoparticles: Evidence for internalization and changes in ag speciation. Journal of Hazardous Materials, 264, 98–106. https://doi.org/10.1016/j.jhazmat.2013.10.053

    CrossRef  CAS  PubMed  Google Scholar 

  • Larue, C., Castillo-Michel, H., Sobanska, S., Trcera, N., Sorieul, S., Cécillon, L., Ouerdane, L., Legros, S., & Sarret, G. (2014b). Fate of pristine TiO2 nanoparticles and aged paint-containing TiO2 nanoparticles in lettuce crop after foliar exposure. Journal of Hazardous Materials, 273, 17–26. https://doi.org/10.1016/j.jhazmat.2014.03.014

    CrossRef  CAS  PubMed  Google Scholar 

  • Larue, C., Laurette, J., Herlin-Boime, N., Khodja, H., Fayard, B., Flank, A.-M., Brisset, F., & Carriere, M. (2012). Accumulation, translocation and impact of TiO2 nanoparticles in wheat (Triticum aestivum spp.): Influence of diameter and crystal phase. Science of the Total Environment, 431, 197–208. https://doi.org/10.1016/j.scitotenv.2012.04.073

    CrossRef  CAS  PubMed  Google Scholar 

  • Laughton, S., Laycock, A., Bland, G., von der Kammer, F., Hofmann, T., Casman, E. A., & Lowry, G. V. (2020). Methanol-based extraction protocol for insoluble and moderately water-soluble nanoparticles in plants to enable characterization by single particle ICP-MS. Analytical and Bioanalytical Chemistry, 1–16. https://doi.org/10.1007/s00216-020-03014-8

  • Layet, C., Auffan, M., Santaella, C., Chevassus-Rosset, C., Montes, M., Ortet, P., Barakat, M., Collin, B., Legros, S., & Bravin, M. N. (2017). Evidence that soil properties and organic coating drive the Phytoavailability of cerium oxide nanoparticles. Environmental Science & Technology, 51, 9756–9764. https://doi.org/10.1021/acs.est.7b02397

    CrossRef  CAS  Google Scholar 

  • Lew, T. T. S., Wong, M. H., Kwak, S. Y., Sinclair, R., Koman, V. B., & Strano, M. S. (2018). Rational design principles for the transport and subcellular distribution of nanomaterials into plant protoplasts. Small, 14, 1802086. https://doi.org/10.1002/smll.201802086

    CrossRef  CAS  Google Scholar 

  • Li, C., Wang, P., Lombi, E., Cheng, M., Tang, C., Howard, D. L., Menzies, N. W., & Kopittke, P. M. (2018). Absorption of foliar-applied Zn fertilizers by trichomes in soybean and tomato. Journal of Experimental Botany, 69, 2717–2729. https://doi.org/10.1093/jxb/ery085

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, J., Tappero, R. V., Acerbo, A. S., Yan, H., Chu, Y., Lowry, G. V., & Unrine, J. M. (2019). Effect of CeO 2 nanomaterial surface functional groups on tissue and subcellular distribution of Ce in tomato (Solanum lycopersicum). Environmental Science: Nano, 6, 273–285. https://doi.org/10.1039/c8en01287c

    CrossRef  CAS  Google Scholar 

  • Li, L., Luo, Y., Li, R., Zhou, Q., Peijnenburg, W. J. G. M., Yin, N., Yang, J., Tu, C., & Zhang, Y. (2020). Effective uptake of submicrometre plastics by crop plants via a crack-entry mode. Nature Sustainability, 3, 929–937. https://doi.org/10.1038/s41893-020-0567-9

    CrossRef  Google Scholar 

  • Lian, J., Zhao, L., Wu, J., Xiong, H., Bao, Y., Zeb, A., Tang, J., & Liu, W. (2020). Foliar spray of TiO2 nanoparticles prevails over root application in reducing cd accumulation and mitigating cd-induced phytotoxicity in maize (Zea mays L.). Chemosphere, 239, 124794. https://doi.org/10.1016/j.chemosphere.2019.124794

    CrossRef  CAS  PubMed  Google Scholar 

  • Liang, J., Yu, M., Guo, L., Cui, B., Zhao, X., Sun, C., Wang, Y., Liu, G., Cui, H., & Zeng, Z. (2018). Bioinspired development of P(St-MAA)-Avermectin nanoparticles with high affinity for foliage to enhance folia retention. Journal of Agricultural and Food Chemistry, 66, 6578–6584. https://doi.org/10.1021/acs.jafc.7b01998

    CrossRef  CAS  PubMed  Google Scholar 

  • Liu, R., & Lal, R. (2015). Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Science of the Total Environment, 514, 131–139.

    CrossRef  CAS  Google Scholar 

  • Lowry, G. V., Avellan, A., & Gilbertson, L. M. (2019). Opportunities and challenges for nanotechnology in the Agri-tech revolution. Nature Nanotechnology, 14, 517–522. https://doi.org/10.1038/s41565-019-0461-7

    CrossRef  CAS  PubMed  Google Scholar 

  • Lucas, W. J., & Lee, J. (2004). Plasmodesmata as a supracellular control network in plants. Nature Reviews Molecular Cell Biology, 5, 712–726. https://doi.org/10.1038/nrm1470

    CrossRef  CAS  PubMed  Google Scholar 

  • Lv, J., Christie, P., & Zhang, S. (2019). Uptake, translocation, and transformation of metal-based nanoparticles in plants: Recent advances and methodological challenges. Environmental Science Nano, 41, 41–59. https://doi.org/10.1039/C8EN00645H

    CrossRef  Google Scholar 

  • Lv, J., Zhang, S., Luo, L., Zhang, J., Yang, K., Christie, P., & Christied, P. (2015). Accumulation, speciation and uptake pathway of ZnO nanoparticles in maize. Environmental Science: Nano, 2, 68–77. https://doi.org/10.1039/C4EN00064A

    CrossRef  CAS  Google Scholar 

  • Ma, C., Borgatta, J., Hudson, B. G., Tamijani, A. A., Torre-roche, R. D. L., Zuverza-mena, N., Shen, Y., Elmer, W., Xing, B., Mason, S. E., Hamers, R. J., & White, J. C. (2020). Advanced material modulation of nutritional and phytohormone status alleviates damage from soybean sudden death syndrome. Nature Nanotechnology, 15, 1033.

    CrossRef  CAS  Google Scholar 

  • Ma, X., Geiser-Lee, J., Deng, Y., & Kolmakov, A. (2010). Interactions between engineered nanoparticles (ENPs) and plants: Phytotoxicity, uptake and accumulation. Science of the Total Environment, 408, 3053–3061. https://doi.org/10.1016/j.scitotenv.2010.03.031

    CrossRef  CAS  PubMed  Google Scholar 

  • Ma, Y., He, X., Zhang, P., Zhang, Z., Ding, Y., Zhang, J., Wang, G., Xie, C., Luo, W., Zhang, J., Zheng, L., Chai, Z., & Yang, K. (2017). Xylem and phloem based transport of CeO2 nanoparticles in hydroponic cucumber plants. Environmental Science and Technology, 51, 5215–5221. https://doi.org/10.1021/acs.est.6b05998

    CrossRef  CAS  PubMed  Google Scholar 

  • Mauricio, R., & Rausher, M. D. (1997). Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant Defense. Evolution, 51, 1435–1444. https://doi.org/10.1111/j.1558-5646.1997.tb01467.x

    CrossRef  PubMed  Google Scholar 

  • McManus, P., Hortin, J., Anderson, A. J., Jacobson, A. R., Britt, D. W., Stewart, J., & McLean, J. E. (2018). Rhizosphere interactions between copper oxide nanoparticles and wheat root exudates in a sand matrix: Influences on copper bioavailability and uptake. Environmental Toxicology and Chemistry, 37, 2619–2632. https://doi.org/10.1002/etc.4226

    CrossRef  CAS  PubMed  Google Scholar 

  • Nadiminti, P. P., Dong, Y. D., Sayer, C., Hay, P., Rookes, J. E., Boyd, B. J., & Cahill, D. M. (2013). Nanostructured liquid crystalline particles as an alternative delivery vehicle for plant agrochemicals. ACS Applied Materials & Interfaces, 5, 1818–1826. https://doi.org/10.1021/am303208t

    CrossRef  CAS  Google Scholar 

  • Navarro, D. A., Bisson, M. A., & Aga, D. S. (2012). Investigating uptake of water-dispersible CdSe/ZnS quantum dot nanoparticles by Arabidopsis thaliana plants. Journal of Hazardous Materials, 211–212, 427–435. https://doi.org/10.1016/j.jhazmat.2011.12.012

    CrossRef  CAS  PubMed  Google Scholar 

  • O’Leary, B. M., Neale, H. C., Geilfus, C. M., Jackson, R. W., Arnold, D. L., & Preston, G. M. (2016). Early changes in apoplast composition associated with defence and disease in interactions between Phaseolus vulgaris and the halo blight pathogen pseudomonas syringae Pv. Phaseolicola. Plant Cell and Environment, 39, 2172–2184. https://doi.org/10.1111/pce.12770

    CrossRef  CAS  Google Scholar 

  • Oburger, E., Gruber, B., Schindlegger, Y., Schenkeveld, W. D. C., Hann, S., Kraemer, S. M., Wenzel, W. W., & Puschenreiter, M. (2014). Root exudation of phytosiderophores from soil-grown wheat. New Phytologist, 203, 1161–1174. https://doi.org/10.1111/nph.12868

    CrossRef  CAS  PubMed  Google Scholar 

  • Onelli, E., Prescianotto-Baschong, C., Caccianiga, M., & Moscatelli, A. (2008). Clathrin-dependent and independent endocytic pathways in tobacco protoplasts revealed by labelling with charged nanogold. Journal of Experimental Botany, 59, 3051–3068. https://doi.org/10.1093/jxb/ern154

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng, C., Chen, S., Shen, C., He, M., Zhang, Y., Ye, J., Liu, J., & Shi, J. (2018). Iron plaque: A barrier layer to the uptake and translocation of copper oxide nanoparticles by Rice plants. Environmental Science and Technology, 52, 12244–12254. https://doi.org/10.1021/acs.est.8b02687

    CrossRef  CAS  PubMed  Google Scholar 

  • Prasad, T. N. V. K. V., Sudhakar, P., Sreenivasulu, Y., Latha, P., Munaswamy, V., Raja Reddy, K., Sreeprasad, T. S., Sajanlal, P. R., & Pradeep, T. (2012). Effect of nanoscale zinc oxide particles on the germination, growth and yield of peanut. Journal of Plant Nutrition, 35, 905–927. https://doi.org/10.1080/01904167.2012.663443

    CrossRef  CAS  Google Scholar 

  • Qiu, H., & Smolders, E. (2017). Nanospecific phytotoxicity of CuO nanoparticles in soils disappeared when bioavailability factors were considered. Environmental Science and Technology, 51, 11976–11985. https://doi.org/10.1021/acs.est.7b01892

    CrossRef  CAS  PubMed  Google Scholar 

  • Raliya, R., Franke, C., Chavalmane, S., Nair, R., Reed, N., & Biswas, P. (2016). Quantitative understanding of nanoparticle uptake in watermelon plants. Frontiers in Plant Science, 7, 1288. https://doi.org/10.3389/fpls.2016.01288

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Raliya, R., Nair, R., Chavalmane, S., Wang, W.-N., & Biswas, P. (2015). Mechanistic evaluation of translocation and physiological impact of titanium dioxide and zinc oxide nanoparticles on the tomato (Solanum lycopersicum L.) plant. Metallomics, 7, 1584–1594. https://doi.org/10.1039/C5MT00168D

    CrossRef  CAS  PubMed  Google Scholar 

  • Raliya, R., Saharan, V., Dimkpa, C., & Biswas, P. (2018). Nanofertilizer for precision and sustainable agriculture: Current state and future perspectives. Journal of Agricultural and Food Chemistry, 66, 6487–6503.

    CrossRef  CAS  Google Scholar 

  • Rodrigues, S., Bland, G. D., Gao, X., Rodrigues, S. M., & Lowry, G. V. (2020). Investigation of pore water and soil extraction tests for characterizing the fate of poorly soluble metal-oxide nanoparticles. Chemosphere, 128885. https://doi.org/10.1016/j.chemosphere.2020.128885

  • Rodrigues, S. M., Demokritou, P., Dokoozlian, N., Hendren, C. O., Karn, B., Mauter, M. S., Sadik, O. A., Safarpour, M., Unrine, J. M., Viers, J., Welle, P., White, J. C., Wiesner, M. R., & Lowry, G. V. (2017). Nanotechnology for sustainable food production: Promising opportunities and scientific challenges. Environmental Science: Nano, 4, 767–781. https://doi.org/10.1039/C6EN00573J

    CrossRef  CAS  Google Scholar 

  • Rodrigues, S. M., Trindade, T., Duarte, A. C., Pereira, E., Koopmans, G. F., & Römkens, P. F. A. M. (2016). A framework to measure the availability of engineered nanoparticles in soils: Trends in soil tests and analytical tools. TrAC – Trends in Analytical Chemistry, 75, 129–140.

    CrossRef  CAS  Google Scholar 

  • Santana, I., Wu, H., Hu, P., & Giraldo, J. P. (2020). Targeted delivery of nanomaterials with chemical cargoes in plants enabled by a biorecognition motif. Nature Communications, 11, 1–12. https://doi.org/10.1038/s41467-020-15731-w

    CrossRef  CAS  Google Scholar 

  • Schreck, E., Foucault, Y., Sarret, G., Sobanska, S., Cécillon, L., Castrec-Rouelle, M., Uzu, G., & Dumat, C. (2012). Metal and metalloid foliar uptake by various plant species exposed to atmospheric industrial fallout: Mechanisms involved for lead. Science of the Total Environment, 427, 253–262. https://doi.org/10.1016/j.scitotenv.2012.03.051

    CrossRef  CAS  PubMed  Google Scholar 

  • Schwab, F., Zhai, G., Kern, M., Turner, A., Schnoor, J. L., & Wiesner, M. R. (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

    CrossRef  CAS  PubMed  Google Scholar 

  • Shang, Y., Hasan, M. K., Ahammed, G. J., Li, M., Yin, H., & Zhou, J. (2019). Applications of nanotechnology in plant growth and crop protection: A review. Molecules (Basel, Switzerland), 24, 2558. https://doi.org/10.3390/molecules24142558

    CrossRef  CAS  PubMed Central  Google Scholar 

  • Sharma, S., Muddassir, M., Muthusamy, S., Vaishnav, P. K., Singh, M., Sharma, D., Kanagarajan, S., & Shanmugam, V. (2020). A non-classical route of efficient plant uptake verified with fluorescent nanoparticles and root adhesion forces investigated using AFM. Scientific Reports, 10, 1–13. https://doi.org/10.1038/s41598-020-75685-3

    CrossRef  CAS  Google Scholar 

  • Shen, Y., Borgatta, J., Ma, C., Elmer, W., Hamers, R. J., & White, J. C. (2020). Copper nanomaterial morphology and composition control foliar transfer through the cuticle and mediate resistance to root fungal disease in tomato (Solanum lycopersicum). Journal of Agricultural and Food Chemistry. https://doi.org/10.1021/acs.jafc.0c04546

  • Singh, A., Singh, N. B., Afzal, S., Singh, T., & Hussain, I. (2018). Zinc oxide nanoparticles: A review of their biological synthesis, antimicrobial activity, uptake, translocation and biotransformation in plants. Journal of Materials Science, 53, 185–201. https://doi.org/10.1007/s10853-017-1544-1

    CrossRef  CAS  Google Scholar 

  • Singh, S., Dosani, T., Karakoti, A. S., Kumar, A., Seal, S., & Self, W. T. (2011). A phosphate-dependent shift in redox state of cerium oxide nanoparticles and its effects on catalytic properties. Biomaterials, 32, 6745–6753. https://doi.org/10.1016/j.biomaterials.2011.05.073

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Spielman-Sun, E., Avellan, A., Bland, G. D., Clement, E. T., Tappero, R. V., Acerbo, A. S., & Lowry, G. V. (2020). Protein coating composition targets nanoparticles to leaf stomata and trichomes. Nanoscale, 12, 3630–3636. https://doi.org/10.1039/c9nr08100c

    CrossRef  CAS  PubMed  Google Scholar 

  • Spielman-Sun, E., Avellan, A., Bland, G. D., Tappero, R. V., Acerbo, A. S., Unrine, J. M., Giraldo, J. P., & Lowry, G. V. (2019). Nanoparticle surface charge influences translocation and leaf distribution in vascular plants with contrasting anatomy. Environmental Science: Nano, 6, 2508–2519. https://doi.org/10.1039/c9en00626e

    CrossRef  CAS  Google Scholar 

  • Spielman-Sun, E., Lombi, E., Donner, E., Avellan, A., Etschmann, B., Howard, D., & Lowry, G. V. (2018). Temporal evolution of copper distribution and speciation in roots of Triticum aestivum exposed to CuO, cu(OH)2, and CuS nanoparticles. Environmental Science and Technology, 52, 9777–9784. https://doi.org/10.1021/acs.est.8b02111

    CrossRef  CAS  PubMed  Google Scholar 

  • Spielman-Sun, E., Lombi, E., Donner, E., Howard, D. L., Unrine, J. M., Lowry, G. V. (2017). Impact of surface charge on cerium oxide nanoparticle uptake and translocation by wheat (Triticum aestivum). Environmental Science & Technology, 51(13), 7361–7368.

    Google Scholar 

  • Steudle, E., & Peterson, C. A. (1998). How does water get through roots? Journal of Experimental Botany, 49, 775–788. https://doi.org/10.1093/jxb/49.322.775

    CrossRef  CAS  Google Scholar 

  • Su, Y., Ashworth, V. E. T. M., Geitner, N. K., Wiesner, M. R., Ginnan, N., Rolshausen, P., Roper, C., & Jassby, D. (2020). Delivery, fate, and mobility of silver nanoparticles in citrus trees. ACS Nano, 14, 2966–2981. https://doi.org/10.1021/acsnano.9b07733

    CrossRef  CAS  PubMed  Google Scholar 

  • Sun, D., Hussain, H. I., Yi, Z., Siegele, R., Cresswell, T., Kong, L., & Cahill, D. M. (2014). Uptake and cellular distribution, in four plant species, of fluorescently labeled mesoporous silica nanoparticles. Plant Cell Reports, 33, 1389–1402. https://doi.org/10.1007/s00299-014-1624-5

    CrossRef  CAS  PubMed  Google Scholar 

  • Sun, X. D., Yuan, X. Z., Jia, Y., Feng, L. J., Zhu, F. P., Dong, S. S., Liu, J., Kong, X., Tian, H., Duan, J. L., Ding, Z., Wang, S. G., & Xing, B. (2020). Differentially charged nanoplastics demonstrate distinct accumulation in Arabidopsis thaliana. Nature Nanotechnology, 15, 755–760. https://doi.org/10.1038/s41565-020-0707-4

    CrossRef  CAS  PubMed  Google Scholar 

  • Tan, W., Gao, Q., Deng, C., Wang, Y., Lee, W. Y., Hernandez-Viezcas, J. A., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2018). Foliar exposure of cu(OH)2 Nanopesticide to basil (Ocimum basilicum): Variety-dependent copper translocation and biochemical responses. Journal of Agricultural and Food Chemistry, 66, 3358–3366. https://doi.org/10.1021/acs.jafc.8b00339

    CrossRef  CAS  PubMed  Google Scholar 

  • Turgeon, R., & Gowan, E. (1990). Phloem loading in coleus blumei in the absence of carrier-mediated uptake of export sugar from the apoplast. Plant Physiology. https://doi.org/10.1104/pp.94.3.1244

  • Vives-Peris, V., de Ollas, C., Gómez-Cadenas, A., & Pérez-Clemente, R. M. (2020). Root exudates: From plant to rhizosphere and beyond. Plant Cell Reports, 39, 3–17. https://doi.org/10.1007/s00299-019-02447-5

    CrossRef  CAS  PubMed  Google Scholar 

  • Wang, P., Lombi, E., Zhao, F.-J., & Kopittke, P. M. (2016). Nanotechnology: A new opportunity in plant sciences. Trends in Plant Science, 21, 699–712.

    CrossRef  CAS  Google Scholar 

  • Wang, Z., Xie, X., Zhao, J., Liu, X., Feng, W., White, J. C., & Xing, B. (2012). Xylem- and phloem-based transport of CuO nanoparticles in maize (Zea mays L.). Environmental Science & Technology, 46, 4434–4441. https://doi.org/10.1021/es204212z

    CrossRef  CAS  Google Scholar 

  • Wilkinson, S., Corlett, J. E., Oger, L., & Davies, W. J. (1998). Effects of xylem pH on transpiration from wild-type and flacca tomato leaves: A vital role for abscisic acid in preventing excessive water loss even from well-watered plants. Plant Physiology, 117, 703–709. https://doi.org/10.1104/pp.117.2.703

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Winter, H., Lohaus, G., & Heldt, H. W. (1992). Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiology, 99, 996–1004. https://doi.org/10.1104/pp.99.3.996

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong, M. H., Misra, R. P., Giraldo, J. P., Kwak, S. Y., Son, Y., Landry, M. P., Swan, J. W., Blankschtein, D., & Strano, M. S. (2016). Lipid exchange envelope penetration (LEEP) of nanoparticles for plant engineering: A universal localization mechanism. Nano Letters, 16, 1161–1172. https://doi.org/10.1021/acs.nanolett.5b04467

    CrossRef  CAS  PubMed  Google Scholar 

  • Wu, H., Nißler, R., Morris, V., Herrmann, N., Hu, P., Jeon, S. J., Kruss, S., & Giraldo, J. P. (2020). Monitoring plant health with near-infrared fluorescent H2O2 nanosensors. Nano Letters, 20, 2432–2442. https://doi.org/10.1021/acs.nanolett.9b05159

    CrossRef  CAS  PubMed  Google Scholar 

  • Wu, H., Tito, N., & Giraldo, J. P. (2017). Anionic cerium oxide nanoparticles protect plant photosynthesis from abiotic stress by scavenging reactive oxygen species. ACS Nano, 11, 11283–11297. https://doi.org/10.1021/acsnano.7b05723

    CrossRef  CAS  PubMed  Google Scholar 

  • Xiong, T., Dumat, C., Dappe, V., Vezin, H., Schreck, E., Shahid, M., Pierart, A., & Sobanska, S. (2017). Copper oxide nanoparticle foliar uptake, Phytotoxicity, and consequences for sustainable urban agriculture. Environmental Science & Technology, 51, 5242–5251. https://doi.org/10.1021/acs.est.6b05546

    CrossRef  CAS  Google Scholar 

  • Yeats, T. H., & Rose, J. K. C. (2013). The formation and function of plant cuticles. Plant Physiology, 163, 5–20. https://doi.org/10.1104/pp.113.222737

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhai, G., Walters, K. S., Peate, D. W., Alvarez, P. J. J., & Schnoor, J. L. (2014). Transport of gold nanoparticles through Plasmodesmata and precipitation of gold ions in Woody poplar. Environmental Science & Technology Letters, 1, 146–151. https://doi.org/10.1021/ez400202b

    CrossRef  CAS  Google Scholar 

  • Zhang, H., Chen, B., & Banfield, J. F. (2010). Particle size and pH effects on nanoparticle dissolution. Journal of Physical Chemistry C. https://doi.org/10.1021/jp1060842

  • Zhang, P., Ma, Y., Zhang, Z., He, X., Zhang, J., Guo, Z., Tai, R., Zhao, Y., & Chai, Z. (2012). Biotransformation of ceria nanoparticles in cucumber plants. ACS Nano, 6, 9943–9950. https://doi.org/10.1021/nn303543n

    CrossRef  CAS  PubMed  Google Scholar 

  • Zhang, W. (2018). Global pesticide use: Profile, trend, cost / benefit and more. Proceedings of the International Academy of Ecology and Environmental Sciences, 8, 1–27.

    Google Scholar 

  • Zhang, Y., Yan, J., Avellan, A., Gao, X., Matyjaszewski, K., Tilton, R. D., & Lowry, G. V. (2020). Temperature- and pH-responsive star polymers as Nanocarriers with potential for in vivo agrochemical delivery. ACS Nano, 14, 10954–10965. https://doi.org/10.1021/acsnano.0c03140

    CrossRef  CAS  PubMed  Google Scholar 

  • Zhang, Z., He, X., Zhang, H., Ma, Y., Zhang, P., Ding, Y., & Zhao, Y. (2011). Uptake and distribution of ceria nanoparticles in cucumber plants. Metallomics: Integrated biometal. Science, 3, 816–822. https://doi.org/10.1039/c1mt00049g

    CrossRef  CAS  Google Scholar 

  • Zhao, L., Ortiz, C., Adeleye, A. S., Hu, Q., Zhou, H., Huang, Y., & Keller, A. A. (2016). Metabolomics to detect response of lettuce (Lactuca sativa) to cu(OH)2 nanopesticides: Oxidative stress response and detoxification mechanisms. Environmental Science and Technology, 50, 9697–9707. https://doi.org/10.1021/acs.est.6b02763

    CrossRef  CAS  PubMed  Google Scholar 

  • Zhao, L., Sun, Y., Hernandez-Viezcas, J. A., Hong, J., Majumdar, S., Niu, G., Duarte-Gardea, M., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2015). Monitoring the environmental effects of CeO2 and ZnO nanoparticles through the life cycle of corn (Zea mays) plants and in situ μ-XRF mapping of nutrients in kernels. Environmental Science and Technology, 49, 2921–2928. https://doi.org/10.1021/es5060226

    CrossRef  CAS  PubMed  Google Scholar 

  • Zhu, Z.-J., Wang, H., Yan, B., Zheng, H., Jiang, Y., Miranda, O. R., Rotello, V. M., Xing, B., & Vachet, R. W. (2012). Effect of surface charge on the uptake and distribution of gold nanoparticles in four plant species. Environmental Science & Technology, 46, 12391–12398. https://doi.org/10.1021/es301977w

    CrossRef  CAS  Google Scholar 

Download references

Acknowledgments

Thanks are due to CESAM and FCT/MCTES for the financial support (UIDP/50017/2020 + UIDB/50017/2020) through national funds. Part of this work was supported by the project AgriTarget (POCI-01-0145-FEDER-029258 and PTDC/BAA-AGR/29258/2017) funded by FEDER, through COMPETE2020 - Programa Operacional Competitividade e Internacionalização (POCI), and by national funds (OE), through FCT/MCTES. Sandra Rodrigues and Bruno Morais acknowledge Ph.D. financial support from FCT (Grant: SFRH/BD/143646/2019 and BD/06247/BD, respectively). Part of this work is based upon work supported by the National Science Foundation (NSF) and the Environmental Protection Agency (EPA) under NSF Cooperative Agreement EF-0830093, CBET-1530563 (NanoFARM), and DBI-1266252 (CEINT).

Author information

Authors and Affiliations

  1. CESAM & Department of Chemistry, University of Aveiro, Aveiro, Portugal

    Astrid Avellan

  2. UMR Géosciences Environnement Toulouse (GET), CNRS, IRD, Université de Toulouse & Observatoire Midi Pyrénées (OMP), Toulouse, France

    Astrid Avellan

  3. CESAM & Department of Environment and Planning, University of Aveiro, Aveiro, Portugal

    Sónia M. Rodrigues & Sandra Rodrigues

  4. CICECO & Department of Chemistry, University of Aveiro, Aveiro, Portugal

    Bruno P. Morais

  5. CEE, Carnegie Mellon University, Pittsburgh, PA, USA

    Benjamin Therrien, Yilin Zhang & Gregory V. Lowry

Authors
  1. Astrid Avellan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sónia M. Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bruno P. Morais
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Benjamin Therrien
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yilin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sandra Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gregory V. Lowry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Astrid Avellan .

Editor information

Editors and Affiliations

  1. Instituto de Ciencia e Tecnologia, São Paulo State University, Sorocaba, São Paulo, Brazil

    Leonardo Fernandes Fraceto

  2. Universidade de Sao Paulo, Piracicaba, Brazil

    Hudson Wallace Pereira de Carvalho

  3. Dept de Biotecnologia, Universidade de Sorocaba, Sorocaba, Brazil

    Renata de Lima

  4. Department of Civil Engineering, McGill University, Montreal, QC, Canada

    Subhashis Ghoshal

  5. Biosciences and Biotechnology, Aix-Marseille University, Saint-Paul-lez-Durance, France

    Catherine Santaella

Rights and permissions

Reprints and Permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Verify currency and authenticity via CrossMark

Cite this chapter

Avellan, A. et al. (2022). Biological Barriers, Processes, and Transformations at the Soil–Plant–Atmosphere Interfaces Driving the Uptake, Translocation, and Bioavailability of Inorganic Nanoparticles to Plants. In: Fernandes Fraceto, L., Pereira de Carvalho, H.W., de Lima, R., Ghoshal, S., Santaella, C. (eds) Inorganic Nanopesticides and Nanofertilizers. Springer, Cham. https://doi.org/10.1007/978-3-030-94155-0_4

Download citation