Nitroaromatic detection and infrared communication from wild-type plants using plant nanobionics


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.

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Figure 1: Nitroaromatic detection and infrared communication in wild-type plants via plant nanobionics.
Figure 2: Standoff detection of picric acid using a nanobionic spinach plant.
Figure 3: Monitoring of B-SWCNT/P-SWCNT nIR intensity ratio (B-SWCNT/P-SWCNT) enables detection of picric acid by nanobionic plants.
Figure 4: nIR response of B-SWCNTs and P-SWCNTs to picric acid deposited on the lamina of a spinach leaf.


  1. 1

    Wheeler, T. D. & Stroock, A. D. The transpiration of water at negative pressures in a synthetic tree. Nature 455, 208–212 (2008).

    CAS  Article  Google Scholar 

  2. 2

    Reischl, A., Reissinger, M., Thoma, H. & Hutzinger, O. Uptake and accumulation of PCDD/F in terrestrial plants: basic considerations. Chemosphere 19, 467–474 (1989).

    Article  Google Scholar 

  3. 3

    Buckley, E. H. Accumulation of airbourne polychlorinated biphenyls in foliage. Science 216, 520–522 (1982).

    CAS  Article  Google Scholar 

  4. 4

    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).

    CAS  Article  Google Scholar 

  5. 5

    McLachlan, M. S. Framework for the interpretation of measurements of SOCs in plants. Environ. Sci. Technol. 33, 1799–1804 (1999).

    CAS  Article  Google Scholar 

  6. 6

    Su, Y. & Zhu, Y. Transport mechanisms for the uptake of organic compounds by rice (Oryza sativa) roots. Environ. Pollut. 148, 94–100 (2007).

    CAS  Article  Google Scholar 

  7. 7

    McCrady, J., McFarlane, C. & Lindstrom, F. The transport and affinity of substituted benzenes in soybean stems. J. Exp. Bot. 38, 1875–1890 (1987).

    CAS  Article  Google Scholar 

  8. 8

    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).

    CAS  Article  Google Scholar 

  9. 9

    Pennington, J. C. Soil Sorption and Plant Uptake of 2,4,6-Trinitrotoluene (1988).

    Google Scholar 

  10. 10

    Schneider, K., Oltmanns, J., Radenberg, T., Schneider, T. & Mundegar, D. Uptake of nitroaromatic compounds in plants. Environ. Sci. Pollut. Res. 3, 135–138 (1996).

    CAS  Article  Google Scholar 

  11. 11

    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).

    CAS  Article  Google Scholar 

  12. 12

    Antunes, M. et al. Programmable ligand detection system in plants through a synthetic signal transduction pathway. PLoS ONE 6, e16292 (2011).

    CAS  Article  Google Scholar 

  13. 13

    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).

    CAS  Article  Google Scholar 

  14. 14

    Zhang, J. et al. Molecular recognition using corona phase complexes made of synthetic polymers adsorbed on carbon nanotubes. Nat. Nanotech. 8, 959–968 (2013).

    CAS  Article  Google Scholar 

  15. 15

    Landry, M. et al. Experimental tools to study molecular recognition within the nanoparticle corona. Sensors 14, 16196–16211 (2014).

    Article  CAS  Google Scholar 

  16. 16

    Bisker, G. et al. Protein-targeted corona phase molecular recognition. Nat. Commun. 7, 10241 (2016).

    CAS  Article  Google Scholar 

  17. 17

    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).

    CAS  Article  Google Scholar 

  18. 18

    Salem, D. P. et al. Chirality dependent corona phase molecular recognition of DNA-wrapped carbon nanotubes. Carbon 97, 147–153 (2016).

    CAS  Article  Google Scholar 

  19. 19

    Oliveira, S. F. et al. Protein functionalized carbon nanomaterials for biomedical applications. Carbon 95, 767–779 (2015).

    CAS  Article  Google Scholar 

  20. 20

    Iverson, N. M. et al. Quantitative tissue spectroscopy of near infrared fluorescent nanosensor implants. J. Biomed. Nanotech. 12, 1035–1047 (2016).

    CAS  Article  Google Scholar 

  21. 21

    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).

    CAS  Article  Google Scholar 

  22. 22

    Giraldo, J. P. et al. Plant nanobionics approach to augment photosythesis and biochemical sensing. Nat. Mater. 13, 400–408 (2014).

    CAS  Article  Google Scholar 

  23. 23

    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).

    Article  CAS  Google Scholar 

  24. 24

    Liu, Q. et al. Carbon nanotubes as molecular transporters for walled plant cells. Nano Lett. 9, 1007–1010 (2009).

    CAS  Article  Google Scholar 

  25. 25

    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).

    CAS  Article  Google Scholar 

  26. 26

    Chen, P., Zhang, L., Zhu, S. & Cheng, G. A comparative theoretical study of picric acid and its cocrystals. Crystals 5, 346–354 (2015).

    CAS  Article  Google Scholar 

  27. 27

    Kotidis, P., Deutsch, E. & Goyal, A. Standoff Detection of Chemical and Biological Threats using Miniature Widely Tunable QCLs Vol. 9467 (SPIE, 2015).

    Google Scholar 

  28. 28

    Feng, Y., Cheng, J., Zhou, X. & Xiang, H. Ratiometric optical oxygen sensing: a review in respect of material design. Analyst 137, 4885–4901 (2012).

    CAS  Article  Google Scholar 

  29. 29

    Gryczynski, Z., Gryczynski, I. & Lakowicz, J. Fluorescence sensing methods. Methods Enzymol. 360, 44–75 (2002).

    Article  Google Scholar 

  30. 30

    Badugu, R., Lakowicz, J. & Geddes, C. Excitation and emission wavelength ratiometric cyanide-sensitive probes for physiological sensing. Anal. Biochem. 327, 82–90 (2004).

    CAS  Article  Google Scholar 

  31. 31

    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).

    Article  Google Scholar 

  32. 32

    Fogler, S. Elements of Chemical Reaction Engineering 4th edn (Person Education, 2006).

  33. 33

    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).

    CAS  Article  Google Scholar 

  34. 34

    Sack, L. & Holbrook, N. M. Leaf hydraulics. Annu. Rev. Plant Biol. 57, 361–381 (2006).

    CAS  Article  Google Scholar 

  35. 35

    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).

    Article  Google Scholar 

  36. 36

    Held, G. Introduction to Light Emitting diode Technology and Applications 116 (CRC Press, 2008).

    Google Scholar 

  37. 37

    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).

    Article  Google Scholar 

  38. 38

    Zimmermann, M. H. & Tyree, M. T. Xylem Structure and the Ascent of Sap (Springer-Verlag, 2002).

    Google Scholar 

  39. 39

    Holbrook, N. M. & Zwieniecki, M. A. Vascular Transport in Plants (Elsevier Academic Press, 2005).

    Google Scholar 

  40. 40

    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).

    Article  CAS  Google Scholar 

  41. 41

    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).

    CAS  Article  Google Scholar 

  42. 42

    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).

    CAS  Article  Google Scholar 

  43. 43

    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).

    CAS  Article  Google Scholar 

  44. 44

    Pennington, J. C. & Brannon, J. M. Environmental fate of explosives. Themochim. Acta 384, 163–172 (2002).

    CAS  Article  Google Scholar 

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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.

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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.

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Correspondence to Michael S. Strano.

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The authors declare no competing financial interests.

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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).

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