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Tracking multi-walled carbon nanotubes inside oat (Avena sativa L.) plants and assessing their effect on growth, yield, and mammalian (human) cell viability

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Abstract

Our findings show that oxidized multi-walled carbon nanotubes (MWCNT) having serpent-like morphology and smaller sizes (diameter of 35 nm and lengths of 200–300 nm) are compatible with oat plant tissues. Applied by seed-priming method as 90 µg/ml concentration, these serpentine MWCNT (having open-end caps) enter the oat plant and traverse the cells. Tracking of MWCNT inside sections and tissues during growth of oat plant has been done using special sample preparation. We present clear images of MWCNT inside the primed seeds and vascular bundles, the conducting tissues of root and shoot of oat. A dye fluorescein isothiocyanate non-covalently bonded to MWCNT also helped in detecting the path through circumferential perimeters of the oat channels, using fluorescence and confocal microscopy. The presence of MWCNT inside oat enhanced the growth of xylem cells by about 1.85-fold in vasculature of shoots. Compared to controls, the chlorophyll content increased by 57%, while photosynthetic activity enhanced by 15% for the same sample in MWCNT-primed plants. Overall, the growth factors were also augmented leading to significant increase in yield components. No toxic effects of MWCNT were observed in the DNA of the primed plants, and in the human cell lines treated with grains harvested from the MWCNT-primed plants. Our study provides some new insights about the role of MWCNT in plants and their potential benefits in agriculture.

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References

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  Google Scholar 

  • Awasthi R, Kaushal N, Vadez V, Turner NC, Berger J, Siddique KH, Nayyar H (2014) Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea. Funct Plant Biol 41:1148–1167

    Article  Google Scholar 

  • Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428

    Article  Google Scholar 

  • Cañas JE, Long M, Nations S, Vadan R, Dai L, Luo M, Ambikapathi R, Lee EH, Olszyk D (2008) Effects of functionalized and nonfunctionalized single-walled carbon nanotubes on root elongation of select crop species. Environ Toxicol Chem 27:1922–1931

    Article  Google Scholar 

  • Chung H, Son Y, Yoon TK, Kim S, Kim W (2011) The effect of multi-walled carbon nanotubes on soil microbial activity. Ecotoxicol Environ Saf 74:569–575

    Article  Google Scholar 

  • Giraldo JP, Landry MP, Faltermeier SM, McNicholas TP, Iverson NM, Boghossian AA, Strano MS (2014) Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat Mater 13:400–408

    Article  Google Scholar 

  • Husen A, Siddiqi KS (2014) Carbon and fullerene nanomaterials in plant system. J Nanobiotechnol 12:16–27

    Article  Google Scholar 

  • Joshi A, Dharamvir K, Verma G (2014) Utility of carbon nanotubes for enhancement of crop (wheat) in agriculture, nanotechnology novel perspectives and prospects. Tata-McGraw Hill, India

    Google Scholar 

  • Joshi A, Sharma A, Nayyar H, Verma G, Dharamvir K (2015) Carbon nanofibers suppress fungal inhibition of seed germination of maize (Zea mays) and barley (Hordeum vulgare L.) crop. AIP Conf Proc 1675:030034–030038

    Article  Google Scholar 

  • Joshi A, Kaur S, Dharamvir K, Nayyar H, Verma G (2018a) Multi-walled carbon nanotubes applied through seed-priming influence early germination, root hair, growth and yield of bread wheat (Triticum aestivum L.). J Sci Food Agric 98:3148–3160​; https://doi.org/10.1002/jsfa.8818

    Google Scholar 

  • Joshi A, Nayyar H, Dharamvir K, Verma G (2018b) Detection of gold nanoparticles signal inside wheat (Triticum aestivum L.) and Oats (Avena sativa) seedlings. AIP Conf Proc 1953:030058. https://doi.org/10.1063/1.5032393

  • Karlsson HL, Cronholm P, Gustafsson J, Moller L (2008) Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21:1726–1732

    Article  Google Scholar 

  • Khodakovskaya MV, Dervishi E, Mahmood M, Xu Y, Li Z, Watanabe F, Biris AS (2009) Carbon nanotubes are able to penetrate plant seed coat and dramatically affect seed germination and plant growth. ACS Nano 3:3221–3227

    Article  Google Scholar 

  • Khodakovskaya MV, de Silva K, Biris AS, Dervishi E, Villagarcia H (2012) Carbon nanotubes induce growth enhancement of tobacco cells. ACS Nano 6:2128–2135

    Article  Google Scholar 

  • Khodakovskaya MV, Kim BS, Kim JN, Alimohammadi M, Dervishi E, Mustafa T, Cernigla CE (2013) Carbon nanotubes as plant growth regulators: effects on tomato growth, reproductive system, and soil microbial community. Small 9:115–123

    Article  Google Scholar 

  • Kumar B, Balgir PP, Kaur B, Mittu B, Chauhan A (2012) In vitro cytotoxicity of native and rec-pediocin CP2 against cancer cell lines: a comparative study. Pharma Anal Acta 1:183–187

    Google Scholar 

  • Kwak SY, Giraldo JP, Wong MH, Koman VB, Lew TT, Ell J, Weidman MC, Sinclair RM, Landry MP, Tisdale WA, Strano MS (2017) A nanobionic light-emitting plant. Nano Lett 17:7951–7961

    Article  Google Scholar 

  • Lahiani MH, Dervishi E, Chen J, Nima Z, Gaume A, Biris AS, Khodakovskaya MV (2013) Impact of carbon nanotube exposure to seeds of valuable crops. ACS Appl Mater Interfaces 5:7965–7973

    Article  Google Scholar 

  • Lal M, Verma G, Dharamvir K (2012) Better dispersability of un-functionalized multiwalled carbon nanotubes through sonication techniques. Asian J Chem 24:3537–3540

    Google Scholar 

  • Lin S, Reppert J, Hu Q, Hudson JS, Reid ML, Ratnikova TA, Rao AM, Luo H, Ke PC (2009) Uptake, translocation, and transmission of carbon nanomaterials in rice plants. Small 5:1128–1132

    Article  Google Scholar 

  • Liu Q, Chen B, Wang Q, Shi X, Xiao Z, Lin J, Fang X (2009) Carbon nanotubes as molecular transporters for walled plant cells. Nano Lett 9:1007–1010

    Article  Google Scholar 

  • Liu Y, Zhao Y, Sun B, Chen C (2012) Understanding the toxicity of carbon nanotubes. Acc Chem Res 46:702–713

    Article  Google Scholar 

  • Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408:3053–3061

    Article  Google Scholar 

  • Magrez A, Kasas S, Salicio V, Pasquier N, Seo JW, Celio M, Forró L (2006) Cellular toxicity of carbon-based nanomaterials. Nano Lett 6:1121–1125

    Article  Google Scholar 

  • Nair R, Varghese SH, Nair BG, Maekawa T, Yoshida Y, Kumar DS (2010) Nanoparticulate material delivery to plants. Plant Sci 179:154–163

    Article  Google Scholar 

  • Priyadharshini RI, Prasannaraj G, Geetha N, Venkatachalam P (2014) Microwave-mediated extracellular synthesis of metallic silver and zinc oxide nanoparticles using macro-algae (Gracilaria edulis) extracts and its anticancer activity against human PC3 cell lines. Appl Biochem Biotechnol 174:2777–2790

    Article  Google Scholar 

  • Rao DP, Srivastava A (2014) Enhancement of seed germination and plant growth of wheat, maize, peanut and garlic using multiwalled carbon nanotubes. Eur Chem Bull 3:502–504

    Google Scholar 

  • Rico CM, Majumdar S, Duarte-Gardea M, Peralta-Videa JR, Gardea-Torresdey JL (2011) Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric Food Chem 59:3485–3498

    Article  Google Scholar 

  • Robinson DG, Ehlers U, Herken R, Herrmann B, Mayer F, Schürmann FW (2012) Methods of preparation for electron microscopy: an introduction for the biomedical sciences. Springer Science & Business Media, Basel

    Google Scholar 

  • Scholes GD, Sargent EH (2014) Bioinspired materials: boosting plant biology. Nat Mater 13:329–331

    Article  Google Scholar 

  • Shankar SS, Ahmad A, Sastry M (2003) Geranium leaf assisted biosynthesis of silver nanoparticles. Biotechnol Prog 19:1627–1631

    Article  Google Scholar 

  • Shi Z, Lian Y, Zhou X, Gu Z, Zhang Y, Iijima S, Zhou L, Yue KT, Zhang S (1999) Mass-production of single-wall carbon nanotubes by arc discharge method. Carbon 37:1449–1453

    Article  Google Scholar 

  • Shrestha B, Acosta-Martinez V, Cox SB, Green MJ, Li S, Canas-Carrell JE (2013) An evaluation of the impact of multiwalled carbon nanotubes on soil microbial community structure and functioning. J Hazard Mater 261:188–197

    Article  Google Scholar 

  • Shukla PK, Misra P, Kole C (2016) Uptake, translocation, accumulation, transformation, and generational transmission of nanoparticles in plants. Plant nanotechnology. Springer International Publishing, Basel, pp 183–218

    Google Scholar 

  • Singh N, Joshi A, Toor AP, Verma G (2017) Drug delivery: advancements and challenges. In Andronescu E, Grumezescu AM (eds) Nanostructures for drug delivery, 1st edn. Elsevier, Amsterdam, pp 865–886

    Chapter  Google Scholar 

  • Stampoulis D, Sinha SK, White JC (2009) Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol 43:9473–9479

    Article  Google Scholar 

  • Tiwari KL, Jadhav SK, Gupta S (2012) Modified CTAB technique for isolation of DNA from some medicinal plants. J Med Plant Res 6:65–73

    Article  Google Scholar 

  • Tiwari DK, Dasgupta-Schubert N, Cendejas LV, Villegas J, Montoya LC, Garcia SB (2014) Interfacing carbon nanotubes (CNT) with plants: enhancement of growth, water and ionic nutrient uptake in maize (Zea mays) and implications for nanoagriculture. Appl Nanosci 4:577–591

    Article  Google Scholar 

  • Tripathi S, Sarkar S (2015) Influence of water soluble carbon dots on the growth of wheat plant. Appl Nanosci 5:609–616

    Article  Google Scholar 

  • Wang X, Han H, Liu X, Gu X, Chen K, Lu D (2012) Multi-walled carbon nanotubes can enhance root elongation of wheat (Triticum aestivum) plants. J Nanopart Res 14:1–10

    Google Scholar 

  • Wild E, Jones KC (2009) Novel method for the direct visualization of in vivo nanomaterials and chemical interactions in plants. Environ Sci Technol 43:5290–5294

    Article  Google Scholar 

  • Wong MH, Giraldo JP, Kwak SY, Koman VB, Sinclair R, Lew TT, Bisker G, Liu P, Strano MS (2017) Nitroaromatic detection and infrared communication from wild-type plants using plant nanobionics. Nat Mater 16:264–272

    Article  Google Scholar 

  • Yuan Z, Zhang Z, Wang X, Li L, Cai K, Han H (2017) Novel impacts of functionalized multi-walled carbon nanotubes in plants: promotion of nodulation and nitrogenase activity in the rhizobium-legume system. Nanoscale 9:9921–9937

    Article  Google Scholar 

Download references

Acknowledgements

A. Joshi is thankful to DST, New Delhi, for financial support in the form of an INSPIRE fellowship. G.Verma acknowledges the contribution of SAP (UGC, New Delhi), PURSE (DST, New Delhi), and TEQIP-II Grants to carry out the experimentation at the Institute. The authors express their sincere gratitude to Dr. Nidarshana Chaturvedi, Department of Biochemistry, Panjab University, Chandigarh, India, for providing technical support in DNA isolation and Dr. Dhirendra Pratap Singh, Scientist, National Institute of Occupational Health, Occupational Medicine Division, Ahmedabad for cell line studies performed in National Agri-Food Biotechnology Institute, Nutrition Science & Technology, Mohali, India. The authors also thank the DST, India for providing funding for instruments and consumables. Funding was provided by the Department of Science and Technology, Ministry of Science and Technology (Grant no. IF130393 INSPIRE FELLOWSHIP).

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Joshi, A., Kaur, S., Singh, P. et al. Tracking multi-walled carbon nanotubes inside oat (Avena sativa L.) plants and assessing their effect on growth, yield, and mammalian (human) cell viability. Appl Nanosci 8, 1399–1414 (2018). https://doi.org/10.1007/s13204-018-0801-1

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