Abstract
Plant nanobionics aims to embed non-native functions to plants by interfacing them with specifically designed nanoparticles. Here, we demonstrate that living spinach plants (Spinacia oleracea) can be engineered to serve as self-powered pre-concentrators and autosamplers of analytes in ambient groundwater and as infrared communication platforms that can send information to a smartphone. The plants employ a pair of near-infrared fluorescent nanosensors—single-walled carbon nanotubes (SWCNTs) conjugated to the peptide Bombolitin II to recognize nitroaromatics via infrared fluorescent emission, and polyvinyl-alcohol functionalized SWCNTs that act as an invariant reference signal—embedded within the plant leaf mesophyll. As contaminant nitroaromatics are transported up the roots and stem into leaf tissues, they accumulate in the mesophyll, resulting in relative changes in emission intensity. The real-time monitoring of embedded SWCNT sensors also allows residence times in the roots, stems and leaves to be estimated, calculated to be 8.3 min (combined residence times of root and stem) and 1.9 min mm−1 leaf, respectively. These results demonstrate the ability of living, wild-type plants to function as chemical monitors of groundwater and communication devices to external electronics at standoff distances.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Wheeler, T. D. & Stroock, A. D. The transpiration of water at negative pressures in a synthetic tree. Nature 455, 208–212 (2008).
Reischl, A., Reissinger, M., Thoma, H. & Hutzinger, O. Uptake and accumulation of PCDD/F in terrestrial plants: basic considerations. Chemosphere 19, 467–474 (1989).
Buckley, E. H. Accumulation of airbourne polychlorinated biphenyls in foliage. Science 216, 520–522 (1982).
Riederer, M. Estimating partitioning and transport of organic-chemicals in the foliage atmosphere system–discussion of a fugacity-based model. Environ. Sci. Technol. 24, 829–837 (1990).
McLachlan, M. S. Framework for the interpretation of measurements of SOCs in plants. Environ. Sci. Technol. 33, 1799–1804 (1999).
Su, Y. & Zhu, Y. Transport mechanisms for the uptake of organic compounds by rice (Oryza sativa) roots. Environ. Pollut. 148, 94–100 (2007).
McCrady, J., McFarlane, C. & Lindstrom, F. The transport and affinity of substituted benzenes in soybean stems. J. Exp. Bot. 38, 1875–1890 (1987).
Gorge, E., Brandt, S. & Werner, D. Uptake and metabolism of 2,4,6-trinitrotoluene in higher plants. Environ. Sci. Pollut. Res. 1, 229–233 (1994).
Pennington, J. C. Soil Sorption and Plant Uptake of 2,4,6-Trinitrotoluene (1988).
Schneider, K., Oltmanns, J., Radenberg, T., Schneider, T. & Mundegar, D. Uptake of nitroaromatic compounds in plants. Environ. Sci. Pollut. Res. 3, 135–138 (1996).
Nagata, T., Nakumura, A., Akizawa, T. & Panhou, H. Genetic engineering of transgenic tobacco for enhanced uptake and bioaccumulation of mercury. Biol. Pharm. Bull. 32, 1491–1495 (2009).
Antunes, M. et al. Programmable ligand detection system in plants through a synthetic signal transduction pathway. PLoS ONE 6, e16292 (2011).
Heller, D. A. et al. Peptide secondary structure modulates single-walled carbon nanotube fluorescence as a chaperone sensor for nitroaromatics. Proc. Natl Acad. Sci. USA 108, 8544–8549 (2011).
Zhang, J. et al. Molecular recognition using corona phase complexes made of synthetic polymers adsorbed on carbon nanotubes. Nat. Nanotech. 8, 959–968 (2013).
Landry, M. et al. Experimental tools to study molecular recognition within the nanoparticle corona. Sensors 14, 16196–16211 (2014).
Bisker, G. et al. Protein-targeted corona phase molecular recognition. Nat. Commun. 7, 10241 (2016).
Kruss, S. et al. Neurotransmitter detection using corona phase molecular recognition on fluorescent single-walled carbon nanotube sensors. J. Am. Chem. Soc. 136, 713–724 (2014).
Salem, D. P. et al. Chirality dependent corona phase molecular recognition of DNA-wrapped carbon nanotubes. Carbon 97, 147–153 (2016).
Oliveira, S. F. et al. Protein functionalized carbon nanomaterials for biomedical applications. Carbon 95, 767–779 (2015).
Iverson, N. M. et al. Quantitative tissue spectroscopy of near infrared fluorescent nanosensor implants. J. Biomed. Nanotech. 12, 1035–1047 (2016).
Bisker, G., Iverson, N. M., Ahn, J. & Strano, M. S. A pharmacokinetic model of a tissue implantable insulin sensor. Adv. Healthc. Mater. 4, 87–97 (2015).
Giraldo, J. P. et al. Plant nanobionics approach to augment photosythesis and biochemical sensing. Nat. Mater. 13, 400–408 (2014).
Johansson, I., Wallin, S., Nordberg, M., Östmark, H. & Pettersson, A. Near real-time standoff detection of explosives in a realistic outdoor environment at 55 m distance. Propellants Explos. Pyrotech 34, 297–306 (2009).
Liu, Q. et al. Carbon nanotubes as molecular transporters for walled plant cells. Nano Lett. 9, 1007–1010 (2009).
Wong, M. H. et al. Lipid exchange envelope penetration (LEEP) of nanoparticles for plant engineering: a universal localization mechanism. Nano Lett. 16, 1161–1172 (2016).
Chen, P., Zhang, L., Zhu, S. & Cheng, G. A comparative theoretical study of picric acid and its cocrystals. Crystals 5, 346–354 (2015).
Kotidis, P., Deutsch, E. & Goyal, A. Standoff Detection of Chemical and Biological Threats using Miniature Widely Tunable QCLs Vol. 9467 (SPIE, 2015).
Feng, Y., Cheng, J., Zhou, X. & Xiang, H. Ratiometric optical oxygen sensing: a review in respect of material design. Analyst 137, 4885–4901 (2012).
Gryczynski, Z., Gryczynski, I. & Lakowicz, J. Fluorescence sensing methods. Methods Enzymol. 360, 44–75 (2002).
Badugu, R., Lakowicz, J. & Geddes, C. Excitation and emission wavelength ratiometric cyanide-sensitive probes for physiological sensing. Anal. Biochem. 327, 82–90 (2004).
Guidotti, B., Gomes, B., Siqueira-Soares, R. C., Soares, A. C. & Ferrarese-Filho, O. The effects of dopamine on root growth and enzyme activity in soybean seedlings. Plant Signal Behav. 8, e25477 (2013).
Fogler, S. Elements of Chemical Reaction Engineering 4th edn (Person Education, 2006).
de Swaef, T., Verbist, K., Cornelis, W. & Steppe, K. Tomato sap flow, stem and fruit growth in relation to water availability in rockwool growing medium. Plant Soil 350, 237–252 (2012).
Sack, L. & Holbrook, N. M. Leaf hydraulics. Annu. Rev. Plant Biol. 57, 361–381 (2006).
Giraldo, J. P., Wheeler, J. K., Huggett, B. A. & Holbrook, N. M. The role of leaf hydraulic conductance dynamics on the timing of leaf senescence. Funct. Plant Biol. 41, 37–47 (2014).
Held, G. Introduction to Light Emitting diode Technology and Applications 116 (CRC Press, 2008).
Guan, Y. & Fredlund, D. G. Use of the tensile strength of water for the direct measurement of high soil suction. Can. Geotech. J. 34, 604–614 (1997).
Zimmermann, M. H. & Tyree, M. T. Xylem Structure and the Ascent of Sap (Springer-Verlag, 2002).
Holbrook, N. M. & Zwieniecki, M. A. Vascular Transport in Plants (Elsevier Academic Press, 2005).
Chang, Y. L. & Strano, M. S. Understanding the dynamics of a signal transduction for adsorption of gases and vapors on carbon nanotube sensors. Langmuir 21, 5192–5196 (2005).
Huang, X. et al. Magnetic virus-like nanoparticles in N benthamiana plants: a new paradigm for environmental and agronomic biotechnological research. ACS Nano 5, 4037–4045 (2011).
Pavlostathis, S. G., Comstock, K. K., Jacobson, M. E. & Saunders, F. M. Transformation of 2,4,6-Trinitrotoluene by the aquatic plant Myriphyllum spicatum. Environ. Toxicol. Chem. 17, 2266–2273 (1998).
Thompson, P., Ramer, L. & Schnoor, J. Hexahydro-1,3,5-trinitro-1,3,5-triazine translocation in poplar trees. Environ. Toxicol. 18, 279–284 (1999).
Pennington, J. C. & Brannon, J. M. Environmental fate of explosives. Themochim. Acta 384, 163–172 (2002).
Acknowledgements
The nitroaromatic detection work using B-SWCNTs and P-SWCNTs were supported by the US Army Research Office under contract W911NF-13-D-0001. The graphene work was supported by the US Department of Energy, Office of Science, Basic Energy Sciences under Award grant number DE-FG02-08ER46488 Mod 0008. M.H.W. is supported on a graduate fellowship by the Agency of Science, Research and Technology Singapore. J.P.G. was supported by National Science Foundation Postdoctoral Research Fellowship in Biology under Grant No. 1103600. V.B.K. is supported by The Swiss National Science Foundation (project No. P2ELP3_162149). The authors wish to thank Melanie Gronick (MIT media) for her invaluable assistance in producing the Supplementary Movie 3 and also G. Verma for helpful discussions.
Author information
Authors and Affiliations
Contributions
M.H.W., J.P.G. and M.S.S. conceived experiments and wrote the paper. M.H.W., J.P.G. and M.S.S. performed experiments and data analysis. S.-Y.K. and R.S. assisted in standoff experimental set-up and analysis. M.H.W., V.B.K. and P.L. performed graphene transfer experiments. G.B. and T.T.S.L. assisted in data analysis. All authors have given their approval to the final version of the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
Supplementary Information (PDF 648 kb)
Supplementary Information
Supplementary movie 1 (AVI 717 kb)
Supplementary Information
Supplementary movie 2 (AVI 2816 kb)
Supplementary Information
Supplementary movie 3 (MOV 26671 kb)
Supplementary Information
Supplementary movie 4 (AVI 3135 kb)
Rights and permissions
About this article
Cite this article
Wong, M., Giraldo, J., Kwak, SY. et al. Nitroaromatic detection and infrared communication from wild-type plants using plant nanobionics. Nature Mater 16, 264–272 (2017). https://doi.org/10.1038/nmat4771
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nmat4771
This article is cited by
-
A bioinspired, self-powered, flytrap-based sensor and actuator enabled by voltage triggered hydrogel electrodes
Nano Research (2023)
-
CoCoNet: Coupled Contrastive Learning Network with Multi-level Feature Ensemble for Multi-modality Image Fusion
International Journal of Computer Vision (2023)
-
Engineering plants with carbon nanotubes: a sustainable agriculture approach
Journal of Nanobiotechnology (2022)
-
Site-selective proteolytic cleavage of plant viruses by photoactive chiral nanoparticles
Nature Catalysis (2022)