Cellular biological and molecular genetic effects of carbon nanomaterials in plant

Prylutska S.V., Franskevych D.V., Yemets A.I.

Review 

SUMMARY. Current research data on the biological effects of carbon nanoparticles (CNPs) such as С₆₀ fullerene, graphene, graphene oxide, single- and multi-walled nanotubes, in in vitro and in vivo plant systems are summarized. The interaction of CNPs with plant cells/organisms, their intracellular localization, and potential mechanisms of action are analyzed. It was found that CNPs improve seed germination, growth of roots and shoots, increase the biomass of different species of monocotyledonous and dicotyledonous plants. The negative effect of CNPs on plant growth and development is observed only at high concentrations, depending on the type of CNPs and the peculiarities of exposure conditions. Due to nanoscale and hydrophobic properties, CNPs are able to penetrate plant cells in both energy-dependent and energy-independent ways, accumulating mainly in plastids, vacuoles, and nuclei, which determines the protective and target action of CNPs. The protective mechanisms of CNPs are based on the antioxidant properties of carbon molecules and are accompanied by changes in the expression of genes that are responsible, in particular, for cellular processes, metabolic processes, and the response to abiotic factors. The positive effect of CNPs on plant productivity, resistance to oxidative stress, as well as their high efficiency at low concentrations and environmental safety indicate the prospect of their use as regulators of physiological conditions, growth and development of higher plants.

Key words: fullerene, graphene, graphene oxide, single- and multi-walled nanotubes, higher plants, algae, phytotoxicity

Tsitologiya i Genetika 2022, vol. 56, no. 4, pp. 48-59

1. National University of Life and Environmental Science of Ukraine, 03041, Ukraine, Kyiv, 15 Heroiv Oborony Str.
2. Taras Shevchenko National University of Kyiv, 01601 Kyiv, Ukraine, 64 Volodymyrska Str.
3. Institute of Food Biotechnology and Genomics, NAS of Ukraine 04123, Ukraine, Kyiv, 2А Osypovskogo Str.

E-mail: psvit_1977 ukr.net, dashaqq gmail.com, yemets.alla nas.gov.ua

Prylutska S.V., Franskevych D.V., Yemets A.I. Cellular biological and molecular genetic effects of carbon nanomaterials in plant, Tsitol Genet., 2022, vol. 56, no. 4, pp. 48-59.

In "Cytology and Genetics":
S. V. Prylutska, D. V. Franskevych & A. I. Yemets Cellular Biological and Molecular Genetic Effects of Carbon Nanomaterials in Plants, Cytol Genet., 2022, vol. 56, no. 4, pp. 351–360
DOI: 10.3103/S0095452722040077

References

Albanese, A., Tang, P.S., and Chan, W.C., The effect of nanoparticle size, shape, and surface chemistry on biological systems, Ann. Rev. Biomed. Eng., 2012, vol. 14, pp. 1–16. https://doi.org/10.1146/annurev-bioeng-071811-150124

Ali-Boucetta, H., Al-Jamal, K.T., Müller, K.H., et al., Cellular uptake and cytotoxic impact of chemically functionalized and polymer-coated carbon nanotubes, Small, 2011, vol. 7, no. 22, pp. 3230–3238. https://doi.org/10.1002/smll.201101004

Anjum, N.A., Singh, N., Singh, M.K., et al., Single-bilayer graphene oxide sheet impacts and underlying potential mechanism assessment in germinating faba bean (Vicia faba L.), Sci. Total Environ., 2014, vol. 472, pp. 834–841. https://doi.org/10.1016/j.scitotenv.2013.11.018

Avanasi, R., Jackson, W.A., Sherwin, B., et al., C60 fullerene soil sorption, biodegradation, and plant uptake, Environ. Sci. Technol., 2014, vol. 48, pp. 2792–2797. https://doi.org/10.1021/es405306w

Begum, P. and Fugetsu, B., Phytotoxicity of multi-walled carbon nanotubes on red spinach (Amaranthus tricolor L.) and the role of ascorbic acid as an antioxidant, J. Hazard. Mater., 2012, vol. 243, pp. 212–222. https://doi.org/10.1016/j.jhazmat.2012.10.025

Begum, P., Ikhtiari, R., Fugetsu, B., et al., Phytotoxicity of multi-walled carbon nanotubes assessed by selected plant species in the seedling stage, Appl. Surf. Sci., 2012, vol. 262, pp. 120–124. https://doi.org/10.1016/j.apsusc.2012.03.028

Bianco, A., Kostarelos, K., and Prato, M., Applications of carbon nanotubes in drug delivery, Curr. Opin. Chem. Biol., 2005, vol. 9, no. 6, pp. 674–679. https://doi.org/10.1016/j.cbpa.2005.10.005

Blume, Y.B., Krasylenko, Y.A., and Yemets, A.I., Effects of phytohormones on the cytoskeleton of the plant cell, Rus. J., Plant Physiol., 2012, vol. 59, no. 4, 515–529. https://doi.org/10.1134/S1021443712040036

Burlaka, O.M., Pirko, Ya.V., Yemets, A.I., et al., Application of carbon nanotubes for plant genetic transformation, in Nanocomposites, Nanophotonics, Nanobiotechnology, and Applications, vol. 156: Springer Proceedings in Physics, Fesenko, O. and Yatsenko L., Eds., Springer-Verlag, 2015, Chapter 20, p. 233–255. https://doi.org/10.1007/978-3-319-06611-0_20

Burlaka, O.M., Yemets, A.I., Pirko, Ya.V., et al., Non-covalent functionalization of carbon nanotubes for efficient gene delivery, in Nanophysics, Nanophotonics, Surface Studies, and Applications vol. 183: Springer Proceedings in Physics, Fesenko, O. and Yatsenko L., Eds., Springer-Verlag, 2016, Chapter 30, p. 355–370. https://doi.org/10.1007/978-3-319-30737-4_30

Burlaka, O.M., Pirko, Ya.V., Yemets, A.I., and Blume, Ya.B., Carbon nanotubes and their application for plant genetic engineering, Nanostruct. Mater. Sci., 2011, vol. 2, pp. 84–101. http://dspace.nbuv.gov.ua/handle/123456789/62783.

Burlaka, O.M., Pirko, Ya.V., Yemets, A.I., and Blume, Ya.B., Gene material delivering into plant cells using carbon nanotubes, Dopov. Nac. Akad. Nauk Ukr., 2015a, vol. 8, pp. 122–130. https://doi.org/10.15407/dopovidi2015.08.122

Burlaka, O.M., Pirko, Ya.V., Yemets, A.I., and Blume, Ya.B., Investigation of the effect of carbon nanotubes on tobacco protoplasts for the development of novel approaches in plant biotechnology, Factory Exp. Evol. Org., 2015b, vol. 17, pp. 121–125. http://utgis.org.ua/journals/index.php/ Faktory/article/view/486.

Buzaneva, E., Karlash, A., Yakovkin, K., et al., DNA nanotechnology of carbon nanotube cells: physico-chemical models of self-organization and properties, Mater. Sci. Engineer., 2002, vol. 19, nos. 1–2, pp. 41–45. https://doi.org/10.1016/S0928-4931(01)00425-8

Byon, H.R., and Choi, H.C., Network single-walled carbon nanotube-field effect transistors (SWNT FETs) with increased Schottky contact area for highly sensitive biosensor applications, J. Am. Chem. Soc., 2006, vol. 128, pp. 2188–2189. https://doi.org/10.1021/ja056897n

Cañas, J.E., Long, M., Nations, S., et al., Effects of functionalized and nonfunctionalized single-walled carbon nanotubes on root elongation of select crop species, Environ. Toxicol. Chem., 2008, vol. 27, no. 9, pp. 1922–1931. https://doi.org/10.1897/08-117.1

Cecchini, N.M., Monteoliva, M.I., and Alvarez, M.E., Proline dehydrogenase contributes to pathogen defense in Arabidopsis, Plant. Physiol., 2011, vol. 155, no. 4, pp. 1947–1959. https://doi.org/10.1104/pp.110.167163

Cherukuri, P., Bachilo, S.M., Litovsky, S.H., et al., Near-infrared fluorescence microscopy of single-walled carbon nanotubes in phagocytic cells, J. Am. Chem. Soc., 2004, vol. 126, no. 48, pp. 15638–15639. https://doi.org/10.1021/ja0466311

Cherukuri, P., Gannon, C.J., Leeuw, T.K., et al., Mammalian pharmacokinetics of carbon nanotubes using intrinsic near-infrared fluorescence, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 18882–18886. https://doi.org/10.1073/pnas.0609265103

Chithrani, B.D., Ghazani, A.A., and Chan, W.C.W., Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells, Nano Lett., 2006, vol. 6, no. 4, pp. 662–668.https://doi.org/10.1021/nl052396o

Cui, D., Zhang, H., Sheng, J., et al., Effects of CdSe/ZnS quantum dots covered multi-walled carbon nanotubes on murine embryonic stem cells, Nano Biomed. Eng., 2010, vol. 2, pp. 236–244. https://doi.org/10.5101/NBE.V214.P236-244

De La Torre-Roche, R., Hawthorne, J., Deng, Y., et al., Fullerene-enhanced accumulation of p,p'-DDE in agricultural crop species, Environ. Sci. Technol., 2012, vol. 46, no. 17, pp. 9315–9323. https://doi.org/10.1021/es301982w

Galbraith, D.W., Nanobiotechnology: silica breaks through in plants, Nat. Nanotechnol., 2007, vol. 2, pp. 272–273. https://doi.org/10.1038/nnano.2007.118

Gao, J., Wang, Y., Folta, K.M., et al., Polyhydroxy fullerenes (fullerols or fullerenols): beneficial effects on growth and lifespan in diverse biological models, PLoS One, 2011, vol. 6, no. 5, art. ID e19976. https://doi.org/10.1371/journal.pone.0019976

Ghorbanpour, M. and Hadian, J., Multi-walled carbon nanotubes stimulate callus induction, secondary metabolites biosynthesis and antioxidant capacity in medicinal plant Satureja khuzestanica grown in vitro, Carbon, 2015, vol. 94, pp. 749–759. https://doi.org/10.1016/j.carbon.2015.07.056

Ghosh, M., Chakraborty, A., Bandyopadhyay, M., et al., Multi-walled carbon nanotubes (MWCNT): induction of DNA damage in plant and mammalian cells, J. Hazard. Mater., 2011, vol. 197, pp. 327–336. https://doi.org/10.1016/j.jhazmat.2011.09.090

Giraldo, J.P., Landry, M.P., Faltermeier, S.M., et al., Plant nanobionics approach to augment photosynthesis and biochemical sensing, Nat. Mater., 2014, vol. 13, pp. 400–408. https://doi.org/10.1038/nmat3890

Gogos, A., Knauer, K., and Bucheli, T.D., Nanomaterials in plant protection and fertilization: current state, foreseen applications, and research priorities, J. Agric. Food Chem., 2012, vol. 60, pp. 9781–9792. https://doi.org/10.1021/jf302154y

Grebinyk, A., Prylutska, S., Buchelnikov, A., et al., C60 fullerene as effective nanoplatform of alkaloid berberine delivery into leukemic cells, Pharmaceutics, 2019, vol. 11, no. 11, art. ID 586. https://doi.org/10.3390/pharmaceutics11110586

Grebinyk, A., Prylutska, S., Grebinyk, S., et al., Antitumor efficiency of the natural alkaloid berberine complexed with C60 fullerene in Lewis lung carcinoma in vitro and in vivo, Cancer Nanotechnol., 2021, vol. 12, art. ID 24. https://doi.org/10.1186/s12645-021-00096-6

Hamdi, H., De La Torre-Roche, R., et al., Impact of non-functionalized and amino-functionalized multiwall carbon nanotubes on pesticide uptake by lettuce (Lactuca sativa L.), Nanotoxicology, 2014, vol. 9, no. 2. https://doi.org/10.3109/17435390.2014.907456

Hao, Y., Yu, F., Lv, R., et al., Carbon nanotubes filled with different ferromagnetic alloys affect the growth and development of rice seedlings by changing the C:N ratio and plant hormones concentrations, PloS One, 2016, vol. 11. https://doi.org/10.1371/journal.pone.0157264

Heller, D.A., Baik, S., Eurell, T.E., et al., Single-walled carbon nanotube spectroscopy in live cells: towards long-term labels and optical sensors, Adv. Mater., 2005, vol. 17, no. 23, pp. 2793–2799. https://doi.org/10.1002/ADMA.200500477

Imlay, J.A., and Linn, S., DNA damage and oxygen radical toxicity, Science (Washington), 1988, vol. 240, pp. 1302–1309. https://doi.org/10.1126/science.3287616

Jiang, Y., Hua, Z., Zhao., Y., et al., The effect of carbon nanotubes on rice seed germination and root growth, Proc. Int. Conf. Appl. Biotechnol., 2014.

Jin, H., Heller, D.A., Sharma, R., et al., Size dependent cellular uptake and expulsion of single-walled carbon nanotubes: single particle tracking and a generic uptake model for nanoparticles, ACS Nano, 2009, vol. 3, no. 1, pp. 149–158. https://doi.org/10.1021/nn800532m

Jin, H., Heller, D.A., and Strano, M.S., Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells, Nano Lett., 2008, vol. 8, no. 6, pp. 1577–1585. https://doi.org/10.1021/nl072969s

Kelsey, J.W. and White, J.C., Effect of C60 fullerenes on the accumulation of weathered p,p’-DDE by plant and earthworm species under single and multispecies conditions, Environ. Toxicol. Chem., 2013, vol. 32, pp. 1117–1123. https://doi.org/10.1002/etc.2158

Khodakovskaya, M.V., de Silva, K., Biris, A.S., et al., Carbon nanotubes induce growth enhancement of tobacco cells, ACS Nano, 2012, vol. 6, no. 3, pp. 2128–2135. https://doi.org/10.1021/nn204643g

Khodakovskaya, M., de Silva, K., Nedosekin, D., et al., Complex genetic, photothermal, and photoacoustic analysis of nanoparticle-plant interactions, Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, pp. 1028–1033. https://doi.org/10.1073/pnas.1008856108

Khodakovskaya, M., Dervishi, E., Mahmood, M., et al., Carbon nanotubes are able to penetrate plant seed coat and dramatically affect seed germination and plant growth, ACS Nano, 2009, vol. 3, no. 10, pp. 3221–3227. https://doi.org/10.1021/nn900887m

Khodakovskaya, M.V., Kim, B.S., Kim, J.N., et al., Carbon nanotubes as plant growth regulators: effects on tomato growth, reproductive system, and soil microbial community, Small, 2013, vol. 9, no, 1, pp. 115–123. https://doi.org/10.1002/smll.201201225

Kim, S.N., Rusling, J.F., and Papadimitrakopoulos, F., Carbon nanotubes for electronic and electrochemical detection of biomolecules, Adv. Mater., 2007, vol. 19, no. 20, pp. 3214–3228. https://doi.org/10.1002/adma.200700665

Kole, C., Kole, P., Randunu, K.M., et al., Nanobiotechnology can boost crop production and quality: first evidence from increased plant biomass, fruit yield and phytomedicine content in bitter melon (Momordica charantia), BMC Biotechnol., 2013, vol. 13, no. 1, art. ID 37. https://doi.org/10.1186/1472-6750-13-37

Kostarelos, K., Lacerda, L., Pastorin, G., et al., Cellular uptake of functionalized carbon nanotubes is independent of functional group and cell type, Nat. Nanotechnol., 2007, vol. 2, pp. 108–113. https://doi.org/10.1038/nnano.2006.209

Lacerda, L., Russier, J., Pastorin, G., et al., (2012) Translocation mechanisms of chemically functionalized carbon nanotubes across plasma membranes Biomaterials 33: 3334–3343. https://doi.org/10.1016/j.biomaterials.2012.01.024

Lahiani, M., Chen, J., Irin, F., et al., Interaction of carbon nanohorns with plants: uptake and biological effects, Carbon, 2015, vol. 81, pp. 607–619. https://doi.org/10.1016/j.carbon.2014.09.095

Lahiani, M.H., Dervishi, E., Chen, J., et al., Impact of carbon nanotube exposure to seeds of valuable crops, ACS Appl. Mater. Interfaces, 2013, vol. 5, pp. 7965–7973. https://doi.org/10.1021/am402052x

Lahiani, M.H., Dervishi, E., Ivanov, I., et al., Comparative study of plant responses to carbon-based nanomaterials with different morphologies, Nanotechnology, 2016, vol. 27, no. 26, art. ID 265102. https://doi.org/10.1088/0957-4484/27/26/265102

Lang, J., Melnykova, M., Catania, M., et al., A water-soluble [60]fullerene-derivative stimulates chlorophyll accumulation and has no toxic effect on Chlamydomonas reinhardtii, Acta Biochim. Pol., 2009, vol. 66, no. 3, pp. 257–262. https://doi.org/10.18388/abp.2019_2835

Larue, C., Pinault, M., Czarny, B., et al., Quantitative evaluation of multi-walled carbon nanotube uptake in wheat and rapeseed, J. Hazard. Mater., 2012, vols. 227–228, pp. 155–163. https://doi.org/10.1016/j.jhazmat.2012.05.033

Leeuw, T.K., Reith, R.M., Simonette, R.A., et al., Single-walled carbon nanotubes in the intact organism: near-IR imaging and biocompatibility studies in Drosophila, Nano Lett., 2007, vol. 7, no. 9, pp. 2650–2654. https://doi.org/10.1021/nl0710452

Lin, C., Fugetsu, B., Su, Y., et al., Studies on toxicity of multi-walled carbon nanotubes on Arabidopsis T87 suspension cells, J. Hazard. Mater., 2009, vol. 170, pp. 578–583. https://doi.org/10.1016/j.jhazmat.2009.05.025

Lin, D. and Xing, B., Phytotoxicity of nanoparticles: inhibition of seed germination and root growth, Environ. Pollut., 2007, vol. 150, no. 2, pp. 243–250. https://doi.org/10.1016/j.envpol.2007.01.016

Lin, S., Reppert, J., Hu, Q., et al., Uptake, translocation, and transmission of carbon nanomaterials in rice plants, Small, 2009, vol. 5, no. 10, pp. 1128–1132. https://doi.org/10.1002/smll.200801556

Liu, Q., Chen, B., Wang, Q., et al., Carbon nanotubes as molecular transporters for walled plant cells, Nano Lett., 2009, vol. 9, no. 3, pp. 1007–1010. https://doi.org/10.1021/nl803083u

Molchan, O.V. and Zubei, E.S., The effect of fullerene on the physiological and biochemical parameters of barley plants in hydroponic culture, Proc. Natl. Acad. Sci. Belarus, Biol. Ser., 2021, vol. 66, no. 1, pp. 74–87. https://doi.org/10.29235/1029-8940-2021-66-1-74-87

Nazarenus, M., Zhang, Q., Soliman, M.G., et al., In vitro interaction of colloidal nanoparticles with mammalian cells: What have we learned thus far?, Beilstein J. Nanotechnol., 2014, vol. 5, pp. 1477–1490. https://doi.org/10.3762/bjnano.5.161

Nima, Z.A., Lahiani, M.H., Watanabe, F., et al., Plasmonically active nanorods for delivery of bioactive agents and highsensitivity SERS detection in planta, RSC Adv., 2014, vol. 4, no. 110, pp. 64985–64993. https://doi.org/10.1039/C4RA10358K

Panova, G.G., Kanash, E.V., Semenov, K.N., et al., Fullerene derivatives influence production process, growth and resistance to oxidative stress in barley and wheat plants, Agric. Biol., 2018, vol. 53, no. 1, pp. 38–49. https://doi.org/10.15389/agrobiology.2018.1.38rus

Panova, G.G., Ktitorova, I.N., Skobeleva, O.V., et al., Impact of polyhydroxy fullerene (fullerol or fullerenol) on growth and biophysical characteristics of barley seedlings in favourable and stressful conditions, Plant Growth Regul., 2015, vol. 79, pp. 309–317. https://doi.org/10.1007/s10725-015-0135-x

Prylutska, S.V., Grynyuk, I.I., Matyshevska, O.P., et al., Estimation of multi-walled carbon nanotubes toxicity in vitro, Physica, 2008, vol. 40, no. 7, pp. 2565–2569. https://doi.org/10.1016/j.physe.2007.07.017

Prylutska, S.V., Grynyuk, I.I., Palyvoda, K.O., et al., Photoinduced cytotoxic effect of fullerenes C60 on transformed T-lymphocytes, Exp. Oncol., 2010, vol. 32, no. 1, pp. 29–32.

Prylutska, S., Grynyuk, I., Skaterna, T., et al., Toxicity of C60 fullerene–cisplatin nanocomplex against Lewis lung carcinoma cells, Arch. Toxicol., 2019, vol. 93, no. 5, pp. 1213–1226. https://doi.org/10.1007/s00204-019-02441-6

Rico, C., Peralta-Videa, J., and Gardea-Torresdey, J., Chemistry, biochemistry of nanoparticles, and their role in antioxidant defense system in plants, Nanotechnol. Plant Sci., 2015, pp. 1–17. https://doi.org/10.1007/978-3-319-14502-0_1

Sakhno, L.O., Yemets, A.I., and Blume, Ya.B., Carbon nanotubes and fullerenes as DNA/RNA carriers for plant genetic transformation, in Research Advances in Plant Biotechnology, Blume, Ya.B., Ed., New York: Nova Sci. Publ., 2020, Chapter 1, pp. 1–31.

Šamaj, J., Baluška, F., Voigt, B., et al., Endocytosis, actin cytoskeleton, and signaling, Plant Physiol., 2004, vol. 135, no. 3, pp. 1150–1161. https://doi.org/10.1104/pp.104.040683

Serag, M.F., Braeckmans, K., Habuchi, S., et al., Spatiotemporal visualization of subcellular dynamics of carbon nanotubes, Nano Lett., 2012, vol. 12, no. 12, pp. 6145–6151. https://doi.org/10.1021/nl3029625

Serag, M.F., Kaji, N., Gaillard, C., et al., Trafficking and subcellular localization of multiwalled carbon nanotubes in plant cells, ACS Nano, 2011, vol. 5, no. 1, pp. 493–499. https://doi.org/10.1021/nn102344t

Serag, M.F., Kaji, N., Habuchi, S., et al., Nanobiotechnology meets plant cell biology: carbon nanotubes as organelle targeting nanocarriers, RSC Adv., 2013, vol. 3, no. 15, pp. 4856–4862. https://doi.org/10.1039/c2ra22766e

Serag, M.F., Kaji, N., Venturelli, E., et al., A functional platform for controlled subcellular distribution of carbon nanotubes, ACS Nano, 2011, vol. 5, no. 1, pp. 9264–9270. https://doi.org/10.1021/nn2035654

Scharff, P., Ritter, U., Matyshevska, O.P., et al., Therapeutic reactive oxygen generation, Tumori, 2008, vol. 94, no. 2, pp. 278–283.

Sharma, P., Jha, A.B., Dubey, R.S., et al., Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions, J. Bot., 2012, vol. 2012, art. ID 217037. https://doi.org/10.1155/2012/217037

Shen, C.X., Zhang, Q.F., Li, J., et al., Induction of programmed cell death in Arabidopsis and rice by single-wall carbon nanotubes, Am. J. Bot., 2010, vol. 97, pp. 1602–1609. https://doi.org/10.3732/ajb.1000073

Smirnova, E., Gusev, A., Zaytseva, O., et al., Uptake and accumulation of multiwalled carbon nanotubes change the morphometric and biochemical characteristics of Onobrychis arenaria seedlings, Front. Chem. Sci. Eng., 2012, vol. 6, pp. 132–138. https://doi.org/10.1007/s11705-012-1290-5

Stampoulis, D., Sinha, S.K., and White, J.C., Assay-dependent phytotoxicity of nanoparticles to plants, Environ. Sci. Technol., 2009, vol. 43, no. 24, pp. 9473–9479. https://doi.org/10.1021/es901695c

Sukhodub, L.B., Sukhodub, L.F., Prylutskyy, Yu.I., et al., Composite material based on hydroxyapatite and multi-walled carbon nanotubes filled by iron: Preparation, properties and drug release ability, Mater. Sci. Eng.: C., 2018, vol. 93, pp. 606–614. https://doi.org/10.1016/j.msec.2018.08.019

Tan, X., Lin, C., and Fugetsu, B., Studies on toxicity of multi-walled carbon nanotubes on suspension rice cells, Carbon, 2009, vol. 47, pp. 3479–3487. https://doi.org/10.1016/j.carbon.2009.08.018

Torney, F., Trewyn, B.G., Lin, V., et al., Mesoporous silica nanoparticles deliver DNA and chemicals into plants, Nat. Nanotechnol., 2007, vol. 2, pp. 295–300. https://doi.org/10.1038/nnano.2007.108

Upadhyayula, V.K.K., Deng, S., Mitchell, M.C., et al., Application of carbon nanotube technology for removal of contaminants in drinking water: A review, Sci. Total Environ., 2009, vol. 408, no. 1, pp. 1–13. https://doi.org/10.1016/j.scitotenv.2009.09.027

Villagarcia, H., Dervishi, E., de Silva, K., et al., Surface chemistry of carbon nanotubes impacts the growth and expression of water channel protein in tomato plants, Small, 2012, vol. 8, no. 15, pp. 2328–2334. https://doi.org/10.1002/smll.201102661

Wang, X., Han, H., Liu, X., et al., Multi-walled carbon nanotubes can enhance root elongation of wheat (Triticum aestivum) plants, J. Nanopart. Res., 2012, vol. 14, art. ID 841. https://doi.org/10.1007/s11051-012-0841-5

Warheit, D., Nanoparticles: Health impacts?, Mater. Today, 2004, vol. 7, no. 2, pp. 32–35. https://doi.org/10.1016/S1369-7021(04)00081-1

Welsher, K., Liu, Z., Daranciang, D., and Dai, H., Selective probing and imaging of cells with single walled carbon nanotubes as near-infrared fluorescent molecules, Nano Lett., 2008, vol. 8, no. 2, pp. 586–590. https://doi.org/10.1021/nl072949q

Wild, E. and Jones, K.C., Novel method for the direct visualization of in vivo nanomaterials and chemical interactions in plants, Environ. Sci. Technol., 2009, vol. 43, no. 14, pp. 5290–5294. https://doi.org/10.1021/es900065h

Yoshiba, Y., Kiyosue, T., Nakashima, K., et al., Regulation of levels of proline as an osmolyte in plants under water stress, Plant Cell Physiol., 1997, vol. 38, no. 10, pp. 1095–1102. https://doi.org/10.1093/oxfordjournals.pcp.a029093

Zaytseva, O. and Neumann, G., Differential impact of multi-walled carbon nanotubes on germination and seedling development of Glycine max, Phaseolusvulgaris and Zea mays, Eur. Chem. Bull., 2016, vol. 5, no. 5, pp. 202–210.https://doi.org/10.17628/ECB.2016.5.202

Zaytseva, O., Wang, Z., and Neumann, G., Phytotoxicity of carbon nanotubes in soybean as determined by interactions with micronutrients, J. Nanopart. Res., 2017, vol. 19, art. ID 29. https://doi.org/10.1007/s11051-016-3722-5

Zhang, M., Gao, B., Chen, J., et al., Effects of graphene on seed germination and seedling growth, J. Nanopart. Res., 2015, vol. 17, no. 2, art. ID 78. https://doi.org/10.1007/s11051-015-2885-9

Zhang, W., Zhang, Z., and Zhang, Y., The application of carbon nanotubes in target drug delivery systems for cancer therapies, Nano Res. Lett., 2011, vol. 6, art. ID 555. https://doi.org/10.1186/1556-276X-6-555