Carbon Nanotubes as Plant Growth Regulators: Prospects

  • Pérez-Hernández Hermes
  • Medina-Pérez Gabriela
  • Vera-Reyes Ileana
  • Carmine Fusaro
  • López-Valdez Fernando
  • Miranda-Arámbula Mariana
  • Citlali Padilla-Rodríguez
  • Fernández-Luqueño Fabián
Part of the Nanotechnology in the Life Sciences book series (NALIS)


Nanotechnology has contributed to agriculture for two decades as an advanced technology with excellent potential in the production systems. Under laboratory, greenhouse, and field conditions, a variety of nanomaterials have been tested with different dosages, size of nanoparticles, exposure time, substrate media, and application methods to evaluate their effects on physiological and biochemical characteristics of different edible or nonedible plants. However, the use of carbon nanotubes (CNTs) is still little studied as plant growth regulators. These nanomaterials have been successfully encapsulated to release fertilizers and herbicides to a secure manner because recent studies have shown positive results on the seed germination, root and stem length, chlorophyll, and length plant, among others. Nevertheless, in the literature, there are contradictions regarding the consequence of the different physical and chemical properties of CNTs that affect the interaction with plants. In this chapter, some benefits and disadvantages related to the adsorption, uptake, transport, accumulation, and transformation or degradation of CNTs and their biochemical and physicochemical interactions between CNTs and plants are shown and discussed. Besides, the effects of spreading CNTs in agricultural soils on human beings, plants, and environmental health are also discussed since a prospect vision.


Crop production Green nanotechnology Innocuous and affordable food Plant metabolites Soil pollution Sustainable development 



This research was funded by “Ciencia Básica SEP-CONACyT” project 287225, by the COAH-2019-C13-C006_FONCYT-COECYT project, by the Sustainability of Natural Resources and Energy Programs (Cinvestav-Saltillo), by Cinvestav Zacatenco, and by Instituto Politécnico Nacional.


  1. Abbasian F, Lockington R, Palanisami T, Megharaj M, Naidu R (2016) Multiwalled carbon nanotubes increase the microbial community in crude oil contaminated fresh water sediments. Sci Total Environ 539:370–380. Scholar
  2. Achari GA, Kowshik M (2018) Recent developments on nanotechnology in agriculture: plant mineral nutrition, health, and interactions with soil microflora. J Agric Food Chem 66(33):8647–8661. Scholar
  3. Andón FT, Kapralov AA, Yanamala N, Feng W, Baygan A, Chambers BJ, Hultenby K, Ye F, Toprak M, Brander BD, Fornara A, Klein-Seetharaman J, Kotchey GP, Star A, Shvedova AA, Fadeel B, Kagan VE (2013) Biodegradation of single-walled carbon nanotubes by eosinophil peroxidase. Small 9(16):2721–2729. Scholar
  4. Anjum NA, Rodrigo MAM, Moulick A, Heger Z, Kopel P, Zítka O, Adam V, Lukatkin AS, Duarte AC, Pereira E, Kizek R (2016) Transport phenomena of nanoparticles in plants and animals/humans. Environ Res 151:233–243. Scholar
  5. Aouada FA, De Moura MR (2015) Nanotechnology applied in agriculture: controlled release of agrochemicals. In: Nanotechnologies in food and agriculture. Springer, pp 103–118.
  6. Aslani F, Bagheri S, Muhd Julkapli N, Juraimi AS, Hashemi FSG, Baghdadi A (2014) Effects of engineered nanomaterials on plants growth: an overview. Sci World J:641759.
  7. Athanassiou CG, Kavallieratos NG, Benelli G, Losic D, Rani PU, Desneux N (2018) Nanoparticles for pest control: current status and future perspectives. J Pest Sci 91:1–15. Scholar
  8. Avanasi R, Jackson WA, Sherwin B, Mudge JF, Anderson TA (2014) C60 fullerene soil sorption, biodegradation, and plant uptake. Environ Sci Technol 48(5):2792–2797. Scholar
  9. Avogadro: an open-source molecular builder and visualization tool. Version 1.2.0.
  10. Bai X, Zhao S, Duo L (2017) Impacts of carbon nanomaterials on the diversity of microarthropods in turfgrass soil. Sci Rep 7(1).
  11. Bakytkarim Y, Tursynbolat S, Zeng Q, Huang J, Wang L (2019) Nanomaterial ink for on-site painted sensor on studies of the electrochemical detection of organophosphorus pesticide residuals of supermarket vegetables. J Electroanal Chem 841:45–50. Scholar
  12. Balasubramanian K, Burghard M (2005) Chemically functionalized carbon nanotubes. Small 1:180–192. Scholar
  13. Bandyopadhyay A, Ghosh D, Pati SK (2017) Trapping and sensing of hazardous insecticides by chemically modified single walled carbon nanotubes. Phys Chem Chem Phys 19(35):24059–24066. Scholar
  14. Baptista FR, Belhout SA, Giordani S, Quinn SJ (2015) Recent developments in carbon nanomaterial sensors. Chem Soc Rev 44:4433–4453. Scholar
  15. Basiuk VA, Terrazas T, Luna-Martínez N, Basiuk EV (2018) Phytotoxicity of carbon nanotubes and nanodiamond in long-term assays with Cactaceae plant seedlings. Fullerenes Nanotubes Carbon Nanostruct:1–9.
  16. Begum P, Ikhtiari R, Fugetsu B, Matsuoka M, Akasaka T, Watari F (2012) Phytotoxicity of multi-walled carbon nanotubes assessed by selected plant species in the seedling stage. Appl Surf Sci 262:120–124. Scholar
  17. Begum P, Ikhtiari R, Fugetsu B (2014) Potential impact of multi-walled carbon nanotubes exposure to the seedling stage of selected plant species. Nanomaterials 4(2):203–221. Scholar
  18. Benelli G, Pavela R, Maggi F, Petrelli R, Nicoletti M (2017) Commentary: making green pesticides greener? The potential of plant products for nanosynthesis and pest control. J Clust Sci 28:3–10. Scholar
  19. Bennett SW, Adeleye A, Ji Z, Keller AA (2013) Stability, metal leaching, photoactivity and toxicity in freshwater systems of commercial single wall carbon nanotubes. Water Res 47(12):4074–4085. Scholar
  20. Bhushan B (2016) Introduction to nanotechnology: history, status, and importance of nanoscience and nanotechnology education. In: Global perspectives of nanoscience and engineering education. Springer International Publishing, pp 1–31.
  21. Birbaum K, Brogioli R, Schellenberg M, Martinoia E, Stark WJ, Günther D, Limbach LK (2010) No evidence for cerium dioxide nanoparticle translocation in maize plants. Environ Sci Technol 44:8718–8723. Scholar
  22. Borgatta J, Ma C, Hudson-Smith N, Elmer W, Plaza-Pérez CD, De La Torre-Roche R, Hamers RJ (2018) Copper based nanomaterials suppress root fungal disease in watermelon (Citrullus lanatus): role of particle morphology, composition and dissolution behavior. ACS Sustain Chem Eng 6(11):14847–14856. Scholar
  23. Bourdiol F, Mouchet F, Perrault A, Fourquaux I, Datas L, Gancet C, Boutonnet JC, Pinelli E, Gauthier L, Flahaut E (2013) Biocompatible polymer- assisted dispersion of multi walled carbon nanotubes in water, application to the investigation of their ecotoxicity using Xenopus laevis amphibian larvae. Carbon 54:175–191. Scholar
  24. Brandelli A (2015) Nanobiotechnology strategies for delivery of antimicrobials in agriculture and food. In: Nanotechnologies in food and agriculture. Springer, pp 119–139.
  25. Burlaka OM, Pirko YV, Yemets AI, Blume YB (2015) Plant genetic transformation using carbon nanotubes for DNA delivery. Cytol Genet 49:349–357. Scholar
  26. Cai Z, Wang J, Ma J, Zhu X, Cai J, Yang G (2015) Anaerobic degradation pathway of the novel chiral insecticide paichongding and its impact on bacterial communities in soils. J Agric Food Chem 63:7151–7160. Scholar
  27. Calkins JO, Umasankar Y, O’Neill H, Ramasamy RP (2013) High photo-electrochemical activity of thylakoid–carbon nanotube composites for photosynthetic energy conversion. Energy Environ Sci 6(6):1891–1900. Scholar
  28. 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. Scholar
  29. Cecchin I, Reddy KR, Thom A, Tessaro EF, Schnaid F (2017) Nanobioremediation: integration of nanoparticles and bioremediation for sustainable remediation of chlorinated organic contaminants in soils. Int Biodeterior Biodegrad 119:419–428. Scholar
  30. Chang X, Bouchard D (2015) Exchange of surfactant by natural organic matter on the surfaces of multi-walled carbon nanotubes. 250th American Chemical Society National Meeting & Exposition, Boston, MA, August 15–21Google Scholar
  31. Chen R, Ratnikova TA, Stone MB, Lin S, Lard M, Huang G, Hudson JS, Ke PC (2010) Differential uptake of carbon nanoparticles by plant and mammalian cells. Small 6(5):612–617. Scholar
  32. Chen G, Qiu J, Liu Y, Jiang R, Cai S, Liu Y, Zhu F, Zhen F, Luan T, Ouyang G (2015) Carbon nanotubes act as contaminant carriers and translocate within plants. Sci Rep 5:15682. Scholar
  33. Chen M, Qin X, Zeng G (2017a) Biodegradation of carbon nanotubes, graphene, and their derivatives. Trends Biotechnol 35(9):836–846. Scholar
  34. Chen M, Qin X, Zeng G (2017b) Biodiversity change behind wide applications of nanomaterials? Nano Today 17:11–13. Scholar
  35. Chen M, Sun Y, Liang J, Zeng G, Li Z, Tang L, Chen M, Zhub Y, Jiang D, Song B (2019) Understanding the influence of carbon nanomaterials on microbial communities. Environ Int 126:690–698. Scholar
  36. Chung H, Son Y, Yoon TK, Kim S, Kim W (2011) The effect of multi-walled carbon nanotubes on soil microbial activity. Ecotoxicol Environ Safe 74(4):569–575. Scholar
  37. Cunningham FJ, Goh NS, Demirer GS, Matos JL, Landry MP (2018) Nanoparticle-mediated delivery towards advancing plant genetic engineering. Trends Biotechnol 36(9):882–897. Scholar
  38. Das KK, You Y, Torres M, Barrios-Masias F, Wang X, Tao S, Xing B, Yang Y (2018) Development and application of a digestion-Raman analysis approach for studying multiwall carbon nanotube uptake in lettuce. Environ Sci Nano 5(3):659–668. Scholar
  39. Dasgupta N, Ranjan S, Ramalingam C (2017) Applications of nanotechnology in agriculture and water quality management. Environ Chem Lett 15(4):591–605. Scholar
  40. De La Torre-Roche R, Hawthorne J, Deng Y, Xing B, Cai W, Newman LA, Wang Q, Ma X, Hamdi H, White JC (2013) Multiwalled carbon nanotubes and C60 fullerenes differentially impact the accumulation of weathered pesticides in four agricultural plants. Environ Sci Technol 47(21):12539–12547. Scholar
  41. Duhan JS, Kumar R, Kumar N, Kaur P, Nehra K, Duhan S (2017) Nanotechnology: the new perspective in precision agriculture. Biotechnol Rep 15:11–23. Scholar
  42. EL-Sayed R, Waraky A, Ezzat K, Albabtain R, ElGammal K, Shityakov S, Hassan M (2019) Degradation of pristine and oxidized single wall carbon nanotubes by CYP3A4. Biochem Biophys Res Commun 515(3):487–492. Scholar
  43. Erady V, Mascarenhas RJ, Satpati AK, Bhakta AK, Mekhalif Z, Delhalle J, Dhason A (2019) Carbon paste modified with Bi decorated multi-walled carbon nanotubes and CTAB as a sensitive voltammetric sensor for the detection of Caffeic acid. Microchem J 146:73–82. Scholar
  44. Etxeberria E, Pozueta-Romero J, Fernández EB (2012) Fluid-phase endocytosis in plant cells. In: Šamaj J (ed) Endocytosis in plants. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 107–122. Scholar
  45. Fan X, Xu J, Lavoie M, Peijnenburg W, Zhu Y, Lu T, Fu Z, Zhu T, Qian H (2018) Multiwall carbon nanotubes modulate paraquat toxicity in Arabidopsis thaliana. Environ Pollut 233:633–641. Scholar
  46. Feizi M, Jalali M, Renella G (2018) Nanoparticles and modified clays influenced distribution of heavy metals fractions in a light-textured soil amended with sewage sludges. J Hazard Mater 343:208–219. Scholar
  47. Fernández-Luqueño F, López-Valdez F, Sarabia-Castillo CR, García-Mayagoitia S, Pérez-Ríos SR (2017) Bioremediation of polycyclic aromatic hydrocarbons-polluted soils at laboratory and field scale: a review of the literature on plants and microorganisms. In: Anjum NA, Gill SS, Tuteja N (eds) Enhancing cleanup of environmental pollutants Vol. 1: Biological approaches. Springer, Cham, pp 43–64. Scholar
  48. Flores D, Chacón R, Alvarado L, Schmidt A, Alvarado C, Chaves J (2014) Effect of using two different types of carbon nanotubes for blackberry (Rubus adenotrichos) in vitro plant rooting, growth and histology. Am J Plant Sci 5:3510–3518. Scholar
  49. Ge Y, Shen C, Wang Y, Sun YQ, Schimel JP, Gardea-Torresdey J, Holden PA (2018) Carbonaceous nanomaterials have higher effects on soybean rhizosphere prokaryotic communities during the reproductive growth phase than during vegetative growth. Environ Sci Technol 52(11):6636–6646. Scholar
  50. Ghosh M, Bhadra S, Adegoke A, Bandyopadhyay M, Mukherjee A (2015) MWCNT uptake in Allium cepa root cells induces cytotoxic and genotoxic responses and results in DNA hyper-methylation. Mutat Res Fundam Mol Mech Mutagen 774:49–58. Scholar
  51. Giraldo JP, Landry MP, Faltermeier SM, McNicholas TP, Iverson NM, Boghossian AA, Reuel NF, Hilmer AJ, Sen F, Brew JA, Strano MS (2014) Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat Mater 13(4):400. Scholar
  52. Goh PS, Ismail AF, Ng BC (2013) Carbon nanotubes for desalination: performance evaluation and current hurdles. Desalination 308:2–14. Scholar
  53. Gong X, Huang D, Liu Y, Zeng G, Wang R, Xu P, Zhang C, Cheng M, Xue W, Chen S (2019) Roles of multiwall carbon nanotubes in phytoremediation: cadmium uptake and oxidative burst in Boehmeria nivea (L.) Gaudich. Environ Sci Nano 6:851–862. Scholar
  54. Gwenzi W, Chaukura N (2018) Organic contaminants in African aquatic systems: current knowledge, health risks, and future research directions. Sci Total Environ 619:1493–1514. Scholar
  55. Haghighi M, da Silva JAT (2014) The effect of carbon nanotubes on the seed germination and seedling growth of four vegetable species. J Crop Sci Biotechnol 17(4):201–208. Scholar
  56. Hao Y, Yu F, Lv R, Ma C, Zhang Z, Rui Y, Liu L, Cao C, Xing B (2016) 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 11(6):0157264. Scholar
  57. Hao Y, Ma C, Zhang Z, Song Y, Cao W, Guo J, Zhou G, Rui Y, Liu L, Xing B (2018) Carbon nanomaterials alter plant physiology and soil bacterial community composition in a rice-soil-bacterial ecosystem. Environ Pollut 232:123–136. Scholar
  58. Hao Y, Xu B, Ma C, Shang J, Gu W, Li W, Hou T, Xiang Y, Cao W, Xing B, Rui Y (2019) Synthesis of novel mesoporous carbon nanoparticles and their phytotoxicity to rice (Oryza sativa L.). J Saudi Chem Soc 23:75–82. Scholar
  59. Hatami M, Hadian J, Ghorbanpour M (2017) Mechanisms underlying toxicity and stimulatory role of single-walled carbon nanotubes in Hyoscyamus niger during drought stress simulated by polyethylene glycol. J Hazard Mater 324:306–320. Scholar
  60. Hu X, Ouyang S, Mu L, An J, Zhou Q (2015) Effects of graphene oxide and oxidized carbon nanotubes on the cellular division, microstructure, uptake, oxidative stress, and metabolic profiles. Environ Sci Technol 49(18):10825–10833. Scholar
  61. Hussain HI, Yi Z, Rookes JE, Kong LX, Cahill DM (2013) Mesoporous silica nanoparticles as a biomolecule delivery vehicle in plants. J Nanopart Res 15:1676. Scholar
  62. Hyung H, Fortner JD, Hughes JB, Kim JH (2007) Natural organic matter stabilizes carbon nanotubes in the aqueous phase. Environ Sci Technol 41(1):179–184. Scholar
  63. Ibrahim RK, Hayyan M, AlSaadi MA, Hayyan A, Ibrahim S (2016) Environmental application of nanotechnology: air, soil, and water. Environ Sci Pollut Res Int 23:13754–13788. Scholar
  64. Jackson P, Jacobsen NR, Baun A, Birkedal R, Kühnel D, Jensen KA, Vogel U, Wallin H (2013) Bioaccumulation and ecotoxicity of carbon nanotubes. Chem Cent J 7:154. Scholar
  65. Jakubus A, Paszkiewicz M, Stepnowski P (2017) Carbon nanotubes application in the extraction techniques of pesticides: a review. Crit Rev Anal Chem 47(1):76–91. Scholar
  66. Jia X, Wei F (2019) Advances in production and applications of carbon nanotubes. In: Single-walled carbon nanotubes. Springer, Cham, pp 299–333. Scholar
  67. Jiang Y, Hua Z, Zhao Y, Liu Q, Wang F, Zhang Q (2014) The effect of carbon nanotubes on rice seed germination and root growth. In: Zhang TC, Ouyang P, Kaplan S, Skarnes B (eds) Proceedings of the 2012 international conference on applied biotechnology (ICAB 2012). Lecture notes in electrical engineering, vol 250. Springer, Berlin, HeidelbergGoogle Scholar
  68. Joseph S, Aluru NR (2008) Why are carbon nanotubes fast transporters of water? Nano Lett 8:452–458. Scholar
  69. 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(8):3148–3160. Scholar
  70. Joshi A, Kaur S, Singh P, Dharamvir K, Nayyar H, Verma G (2018b) 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(6):1399–1414. Scholar
  71. Judy JD, Unrine JM, Rao W, Bertsch PM (2012) Bioaccumulation of gold nanomaterials by Manduca sexta through dietary uptake of surface contaminated plant tissue. Environ Sci Technol 46:12672–12678. Scholar
  72. Kagan VE, Konduru NV, Feng W, Allen BL, Conroy J, Volkov Y, Vlasova II, Belikova NA, Yanamala N, Kapralov A, Tyurina YY, Shi J, Kisin ER, Murray AR, Franks J, Stolz D, Gou P, Klein-Seetharaman J, Fadeel B, Star A, Shvedova AA (2010) Carbon nanotubes degraded by neutrophil myeloperoxidase induce less pulmonary inflammation. Nat Nanotechnol 5(5):354–359. Scholar
  73. Kaminskyj SGW (2008) Effective and flexible methods for visualizing and quantifying endorhizal fungi. In: Siddiqui ZA, Akhtar MS, Futai K (eds) Mycorrhizae: sustainable agriculture and forestry. Springer Netherlands, pp 337–349.
  74. Karimi M, Ghasemi A, Mirkiani S, Moosavi Basri SM, Hamblin MR (2017) Carbon nanotubes: properties and classification. In: Carbon nanotubes in drug and gene delivery. Morgan & Claypool Publishers, pp 2-1–2-9.
  75. Kerfahi D, Tripathi BM, Singh D, Kim H, Lee S, Lee J, Adams JM (2015) Effects of functionalized and raw multi-walled carbon nanotubes on soil bacterial community composition. PLoS One 10(3):0123042. Scholar
  76. Khalifa NS (2018) The effect of multi-walled carbon nanotubes on pennycress (Thlaspi arvense L.) plant. Egypt J Bot 58(3):529–537Google Scholar
  77. Khodakovskaya M, 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(10):3221–3227. Scholar
  78. 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(1):115–123. Scholar
  79. Khosravi-Katuli K, Prato E, Lofrano G, Guida M, Vale G, Libralato G (2017) Effects of nanoparticles in species of aquaculture interest. Environ Sci Pollut Res 24(21):17326–17346. Scholar
  80. Kostarelos K, Lacerda L, Pastorin G, Wu W, Wieckowski S, Luangsivilay J, Godefroy S, Pantarotto D, Briand J, Muller S, Prato M, Bianco A (2007) Cellular uptake of functionalized carbon nanotubes is independent of functional group and cell type. Nat Nanotechnol 2(2):108–113. Scholar
  81. Kotchey GP, Hasan SA, Kapralov AA, Ha SH, Kim K, Shvedova AA, Kagan VE, Star A (2012) A natural vanishing act: the enzyme-catalyzed degradation of carbon nanomaterials. Acc Chem Res 45(10):1770–1781. Scholar
  82. Kotchey GP, Zhao Y, Kagan VE, Star A (2013) Peroxidase-mediated biodegradation of carbon nanotubes in vitro and in vivo. Adv Drug Deliv Rev 65(15):1921–1932. Scholar
  83. Kumar V, Sachdev D, Pasricha R, Maheshwari PH, Taneja NK (2018) Zinc supported multiwalled carbon nanotube nanocomposite; a synergism to micronutrient release and a smart distributor to promote the growth of onion seeds in arid conditions. ACS Appl Mater Interfaces 10(43):36733–36745. Scholar
  84. Kwak SY, Lew TTS, Sweeney CJ, Koman VB, Wong MH, Bohmert-Tatarev K, Snell KD, Seo JS, Chua N, Strano MS (2019) Chloroplast-selective gene delivery and expression in planta using chitosan-complexed single-walled carbon nanotube carriers. Nat Nanotechnol 14:447–455. Scholar
  85. Lahiani MH, Chen J, Irin F, Puretzky AA, Green MJ, Khodakovskaya MV (2015) Interaction of carbon nanohorns with plants: uptake and biological effects. Carbon 81:607–619. Scholar
  86. Lahiani MH, Khare S, Cerniglia C, Boy R, Ivanov IN, Khodakovskaya M (2019) The impact of tomato fruits containing multi-walled carbon nanotube residues on human intestinal epithelial cell barrier function and intestinal microbiome composition. Nanoscale 11:3639–3655. Scholar
  87. Lara-Romero J, Campos-García J, Dasgupta-Schubert N, Borjas-García S, Tiwari D, Paraguay-Delgado F, Jiménez-Sandoval S, Alonso-Nuñez G, Gómez-Romero M, Lindig-Cisneros R, Reyes De la Cruz H, Villegas JA (2017) Biological effects of carbon nanotubes generated in forest wildfire ecosystems rich in resinous trees on native plants. PeerJ 5:3658. Scholar
  88. Larue C, Pinault M, Czarny B, Georgin D, Jaillard D, Bendiab N, Mayne-L’Hermite M, Taran F, Dive V, Carrière M (2012a) Quantitative evaluation of multi-walled carbon nanotube uptake in wheat and rapeseed. J Hazard Mater 227:155–163. Scholar
  89. Larue C, Laurette J, Herlin-Boime N, Khodja H, Fayard B, Flank AM, Brisset F, Carriere M (2012b) Accumulation, translocation and impact of TiO2 nanoparticles in wheat (Triticum aestivum spp.): influence of diameter and crystal phase. Sci Total Environ 431:197–208. Scholar
  90. Lee WM, An YJ, Yoon H, Kweon HS (2008) Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles. Environ Toxicol Chem 27:1915–1921. Scholar
  91. Li Z, de Barros ALB, Soares DCF, Moss SN, Alisaraie L (2017) Functionalized single-walled carbon nanotubes: cellular uptake, biodistribution and applications in drug delivery. Int J Pharm 524(1–2):41–54. Scholar
  92. Liang T, Yin Q, Zhang Y, Wang B, Guo W, Wang J, Xie J (2013) Effects of carbon nanoparticles application on the growth, physiological characteristics and nutrient accumulation in tobacco plants. J Food Agric Environ 11(3/4):954–958Google Scholar
  93. Lin D, Xing B (2008) Root uptake and phytotoxicity of ZnO nanoparticles. Environ Sci Technol 42:5580–5585. Scholar
  94. 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. Scholar
  95. Liné C, Larue C, Flahaut E (2017) Carbon nanotubes: impacts and behaviour in the terrestrial ecosystem-a review. Carbon 123:767–785. Scholar
  96. Liu R, Lal R (2015) Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Sci Total Environ 514:131–139. Scholar
  97. 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(3):1007–1010. Scholar
  98. Liu Y, Wang S, Lan W, Qin W (2019) Fabrication of polylactic acid/carbon nanotubes/chitosan composite fibers by electrospinning for strawberry preservation. Int J Biol Macromol 121:1329–1336. Scholar
  99. Lu Y, Yang K, Lin D (2014) Transport of surfactant-facilitated multiwalled carbon nanotube suspensions in columns packed with sized soil particles. Environ Pollut 192:36–43. Scholar
  100. 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(16):3053–3061. Scholar
  101. Maksimova YG (2019) Microorganisms and carbon nanotubes: interaction and applications (review). Appl Biochem Microbiol 55(1):1–12. Scholar
  102. Martín C, Kostarelos K, Prato M, Bianco A (2019) Biocompatibility and biodegradability of 2D materials: graphene and beyond. Chem Commun 55(39):5540–5546. Scholar
  103. Martínez-Ballesta MC, Zapata L, Chalbi N, Carvajal M (2016) Multiwalled carbon nanotubes enter broccoli cells enhancing growth and water uptake of plants exposed to salinity. J Nanobiotechnol 14(1):42. Scholar
  104. Mastronardi E, Tsae P, Zhang X, Monreal C, DeRosa MC (2015) Strategic role of nanotechnology in fertilizers: potential and limitations. In: Nanotechnologies in food and agriculture. Springer, pp 25–67.
  105. McGehee DL, Lahiani MH, Irin F, Green MJ, Khodakovskaya MV (2017) Multiwalled carbon nanotubes dramatically affect the fruit metabolome of exposed tomato plants. ACS Appl Mater Interfaces 9(38):32430–32435. Scholar
  106. Moll J, Gogos A, Bucheli TD, Widmer F, van der Heijden MGA (2016) Effect of nanoparticles on red clover and its symbiotic microorganisms. J Nanobiotechnol 14:36. Scholar
  107. Mondal A, Basu R, Das S, Nandy P (2011) Beneficial role of carbon nanotubes on mustard plant growth: an agricultural prospect. J Nanopart Res 13:4519–4528. Scholar
  108. Morla S, Rao CR, Chakrapani R (2011) Factors affecting seed germination and seedling growth of tomato plants cultured in vitro conditions. J Chem Biol Phys Sci 1(2):328–334Google Scholar
  109. Mukesh T, Jha AK (2017) A review on: carbon nanotubes are vital for plant growth. Am J Agric For 5(5–1):1–9. Scholar
  110. Mukherjee A, Majumdar S, Servin AD, Pagano L, Dhankher OP, White JC (2016) Carbon nanomaterials in agriculture: a critical review. Front Plant Sci 7(172).
  111. Okuyama R, Izumida W, Eto M (2019) Topological classification of the single-wall carbon nanotube. Phys Rev B 99(11):115409-1–115409-10. Scholar
  112. Oloumi H, Mousavi EA, Nejad RM (2018) Multi-Wall carbon nanotubes effects on plant seedlings growth and cadmium/lead uptake in vitro. Russ J Plant Physiol 65(2):260–268. Scholar
  113. Pachapur VL, Larios AD, Cledón M, Brar SK, Verma M, Surampalli RY (2016) Behavior and characterization of titanium dioxide and silver nanoparticles in soils. Sci Total Environ 563–564:933–943. Scholar
  114. Pandey K, Lahiani MH, Hicks VK, Hudson MK, Green MJ, Khodakovskaya M (2018) Effects of carbon-based nanomaterials on seed germination, biomass accumulation and salt stress response of bioenergy crops. PLoS One 13(8):e0202274. Scholar
  115. Petersen EJ, Flores-Cervantes DX, Bucheli TD, Elliott LCC, Fagan JA, Gogos A, Hanna S, Kägi R, Mansfield E, Bustos ARM, Plata DL, Reipa V, Westerhoff P, Winchester MR (2016) Quantification of carbon nanotubes in environmental matrices: current capabilities, case studies, and future prospects. Environ Sci Technol 50(9):4587–4605. Scholar
  116. Qian H, Ke M, Qu Q, Li X, Du B, Lu T, Sun L, Pan X (2018) Ecological effects of single-walled carbon nanotubes on soil microbial communities and soil fertility. Bull Environ Contam Toxicol 101(4):536–542. Scholar
  117. Rai M, Ribeiro C, Mattoso L, Duran N (2015) Nanotechnologies in food and agriculture. Springer, Cham/Heidelberg/New York/Dordrecht/London, p 347. ISBN 978-3-319-14023-0. ISBN 978-3-319-14024-7 (eBook). Scholar
  118. Raliya R, Franke C, Chavalmane S, Nair R, Reed N, Biswas P (2016) Quantitative understanding of nanoparticle uptake in watermelon plants. Front Plant Sci 7:1288. Scholar
  119. Ratnikova TA, Podila R, Rao AM, Taylor AG (2015) Tomato seed coat permeability to selected carbon nanomaterials and enhancement of germination and seedling growth. Sci World J:1–9.
  120. Reipa V, Hanna SK, Urbas A, Sander L, Elliott J, Conny J, Petersen EJ (2018) Efficient electrochemical degradation of multiwall carbon nanotubes. J Hazard Mater 354:275–282. Scholar
  121. 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. Scholar
  122. Russier J, Ménard-Moyon C, Venturelli E, Gravel E, Marcolongo G, Meneghetti M, Doris E, Bianco A (2011) Oxidative biodegradation of single-and multi-walled carbon nanotubes. Nanoscale 3(3):893–896. Scholar
  123. Sarlak N, Taherifar A, Salehi F (2014) Synthesis of nanopesticides by encapsulating pesticide nanoparticles using functionalized carbon nanotubes and application of new nanocomposite for plant disease treatment. J Agric Food Chem 62(21):4833–4838. Scholar
  124. Serag MF, Kaji N, Gaillard C, Okamoto Y, Terasaka K, Jabasini M, Tokeshi M, Mizukami H, Bianco A, Baba Y (2011) Trafficking and subcellular localization of multiwalled carbon nanotubes in plant cells. ACS Nano 5:493–499. Scholar
  125. Serag MF, Kaji N, Habuchi S, Bianco A, Baba Y (2013) Nanobiotechnology meets plant cell biology: carbon nanotubes as organelle targeting nanocarriers. RSC Adv 3(15):4856–4862. Scholar
  126. Shan J, Ji R, Yu Y, Xie Z, Yan X (2015) Biochar, activated carbon, and carbon nanotubes have different effects on fate of 14C-catechol and microbial community in soil. Sci Rep 5(1).
  127. Shen C-X, Zhang Q-F, Li J, Bi F-C, Yao N (2010) Induction of programmed cell death in Arabidopsis and rice by single-wall carbon nanotubes. Am J Bot 97(10):1602–1609. Scholar
  128. Shen X, Li S, Zhang H, Chen W, Yang Y, Li J, Tao S, Wang X (2018) Effect of multiwalled carbon nanotubes on uptake of pyrene by cucumber (Cucumis sativus L.): mechanistic perspectives. NanoImpact 10:168–176. Scholar
  129. Simonin M, Richaume A (2015) Impact of engineered nanoparticles on the activity, abundance, and diversity of soil microbial communities: a review. Environ Sci Pollut R 22(18):13710–13723. Scholar
  130. Singh S, Vishwakarma K, Singh S, Sharma S, Dubey NK, Singh VK, Liu S, Tripathi DK, Chauhan DK (2017) Understanding the plant and nanoparticle interface at transcriptomic and proteomic level: a concentric overview. Plant Gene 11:265–272. Scholar
  131. Solanki P, Bhargava A, Chhipa H, Jain N, Panwar J (2015) Nano-fertilizers and their smart delivery system. In: Nanotechnologies in food and agriculture. Springer, pp 81–101.
  132. Song B, Xu P, Zeng G, Gong J, Wang X, Yan J, Wang S, Zang P, Cao W, Ye S (2018) Modeling the transport of sodium dodecyl benzene sulfonate in riverine sediment in the presence of multi-walled carbon nanotubes. Water Res 129:20–28. Scholar
  133. Song B, Chen M, Ye S, Xu P, Zeng G, Gong J, Li L, Zhang P, Cao W (2019) Effects of multi-walled carbon nanotubes on metabolic function of the microbial community in riverine sediment contaminated with phenanthrene. Carbon 144:1–7. Scholar
  134. Stampoulis D, Sinha SK, White JC (2009) Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol 43:9473–9479. Scholar
  135. Subramanian KS, Manikandan A, Thirunavukkarasu M, Rahale CS (2015) Nano-fertilizers for balanced crop nutrition. In: Nanotechnologies in food and agriculture. Springer, pp 69–80.
  136. Taha RA, Hassan MM, Ibrahim EA, Baker NHA, Shaaban EA (2016) Carbon nanotubes impact on date palm in vitro cultures. Plant Cell Tissue Organ Cult 127(2):525–534. Scholar
  137. Tan X, Lin C, Fugetsu B (2009) Studies on toxicity of multi-walled carbon nanotubes on suspension rice cells. Carbon 47(15):3479–3487. Scholar
  138. Tan W, Peralta-Videa JR, Gardea-Torresdey JL (2018) Interaction of titanium dioxide nanoparticles with soil components and plants: current knowledge and future research needs- a critical review. Environ Sci Nano 5:257–278. Scholar
  139. Tang W, Yan T, Wang F, Yang J, Wu J, Wang J, Yue T, Li Z (2019) Rapid fabrication of wearable carbon nanotube/graphite strain sensor for real-time monitoring of plant growth. Carbon 147:295–302. Scholar
  140. Tiwari DK, Dasgupta-Schubert N, Villaseñor Cendejas LM, Villegas J, Carreto Montoya L, Borjas García SE (2013) 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(5):577591. Scholar
  141. Torney F, Trewyn BG, Lin VSY, Wang K (2007) Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nat Nanotechnol 2:295–300. Scholar
  142. Tripathi S, Sonkar SK, Sarkar S (2011) Growth stimulation of gram (Cicer arietinum) plant by water soluble carbon nanotubes. Nanoscale 3(3):1176–1181. Scholar
  143. Tripathi DK, Singh S, Singh VP, Prasad SM, Chauhan DK, Dubey NK (2016) Silicon nanoparticles more efficiently alleviate arsenate toxicity than silicon in maize cultivar and hybrid differing in arsenate tolerance. Front Environ Sci 4:46. Scholar
  144. Verma SK, Das AK, Patel MK, Shah A, Kumar V, Gantait S (2018) Engineered nanomaterials for plant growth and development: a perspective analysis. Sci Total Environ 630:1413–1435. Scholar
  145. Verma SK, Das AK, Gantait S, Kumar V, Gurel E (2019) Applications of carbon nanomaterials in the plant system: a perspective view on the pros and cons. Sci Total Environ 667:485–499. Scholar
  146. Villagarcia H, Dervishi E, de Silva K, Biris AS, Khodakovskaya MV (2012) Surface chemistry of carbon nanotubes impacts the growth and expression of water channel protein in tomato plants. Small 8(15):2328–2334. Scholar
  147. Vithanage M, Seneviratne M, Ahmad M, Sarkar B, Ok YS (2017) Contrasting effects of engineered carbon nanotubes on plants: a review. Environ Geochem Health 39(6):1421–1439. Scholar
  148. Wang X, Han H, Liu X, Gu X, Chen K, Lu D (2012a) Multi-walled carbon nanotubes can enhance root elongation of wheat (Triticum aestivum) plants. J Nanopart Res 14:841. Scholar
  149. Wang M, Chen L, Chen S, Ma Y (2012b) Ecotoxicology and environmental safety alleviation of cadmium-induced root growth inhibition in crop seedlings by nanoparticles. Ecotoxicol Environ Saf 79:48–54. Scholar
  150. Wang P, Lombi E, Zhao FJ, Kopittke PM (2016) Nanotechnology: a new opportunity in plant sciences. Trends Plant Sci 21:699–712. Scholar
  151. Wang H, Liu Z, Liu H, Guan L, Cao X, Zhang Z, Huang Y, Jin C (2019) Probing the degradation of carbon nanotubes in aqueous solution by liquid cell transmission electron microscopy. Carbon 148:481–486. Scholar
  152. Watanabe T, Misawa S, Hiradate S, Osaki M (2008) Root mucilage enhances aluminum accumulation in Melastoma malabathricum, an aluminum accumulator. Plant Signal Behav 3:603–605. Scholar
  153. 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. Scholar
  154. Wong MH, Misra RP, Giraldo JP, Kwak SY, Son Y, Landry MP, Swan JW, Blankschtein D, Strano MS (2016) Lipid exchange envelope penetration (LEEP) of nanoparticles for plant engineering: a universal localization mechanism. Nano Lett 16(2):1161–1172. Scholar
  155. Wu F, You Y, Zhang X, Zhang H, Chen W, Yang Y, Werner D, Tao S, Wang X (2019) Effects of various carbon nanotubes on soil bacterial community composition and structure. Environ Sci Technol 53(10):5707–5716. Scholar
  156. Yan S, Zhao L, Li H, Zhang Q, Tan J, Huang M, He S, Li L (2013) Single-walled carbon nanotubes selectively influence maize root tissue development accompanied by the change in the related gene expression. J Hazard Mater 246–247:110–118. Scholar
  157. Yang YF, Cheng YH, Liao CM (2016) In situ remediation-released zero-valent iron nanoparticles impair soil ecosystems health: a C. elegans biomarker-based risk assessment. J Hazard Mater 317:210–220. Scholar
  158. Yang YF, Cheng YH, Liao CM (2017) Nematode-based biomarkers as critical risk indicators on assessing the impact of silver nanoparticles on soil ecosystems. Ecol Indic 75:340–351. Scholar
  159. Yuan H, Hu S, Huang P, Song H, Wang K, Ruan J, He R, Cui D (2011) Single walled carbon nanotubes exhibit dual-phase regulation to exposed arabidopsis mesophyll cells. Nanoscale Res Lett 6:44. Scholar
  160. 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(28):9921–9937. Scholar
  161. Zhai G, Gutowski SM, Walters KS, Yan B, Schnoor JL (2015) Charge, size, and cellular selectivity for multiwall carbon nanotubes by maize and soybean. Environ Sci Technol 49(12):7380–7390. Scholar
  162. Zhang C, Chen W, Alvarez PJ (2014) Manganese peroxidase degrades pristine but not surface-oxidized (carboxylated) single-walled carbon nanotubes. Environ Sci Technol 48(14):7918–7923. Scholar
  163. Zhang H, Yue M, Zheng X, Xie C, Zhou H, Li L (2017) Physiological effects of single- and multi-walled carbon nanotubes on rice seedlings. IEEE Trans Nanobioscience 16(7):563–570. Scholar
  164. Zhang M, Deng Y, Yang M, Nakajima H, Yudasaka M, Iijima S, Okazaki T (2019) A simple method for removal of carbon nanotubes from wastewater using hypochlorite. Sci Rep 9(1):1284–1290. Scholar
  165. Zhao Y, Allen BL, Star A (2011) Enzymatic degradation of multiwalled carbon nanotubes. J Phys Chem 115(34):9536–9544. Scholar
  166. Zhao Q, Ma C, White JC, Dhankher OP, Zhang X, Zhang S, Xing B (2017) Quantitative evaluation of multi-wall carbon nanotube uptake by terrestrial plants. Carbon 114:661–670. Scholar
  167. Zuverza-Mena N, Martínez-Fernández D, Du W, Hernandez-Viezcas JA, Bonilla-Bird N, Lopez-Moreno ML, Komarek M, Peralta-Videa JR, Gardea-Torresdey JL (2017) Exposure of engineered nanomaterials to plants: insights into the physiological and biochemical responses-a review. Plant Physiol Biochem 110:236–264. Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Pérez-Hernández Hermes
    • 1
  • Medina-Pérez Gabriela
    • 2
  • Vera-Reyes Ileana
    • 3
  • Carmine Fusaro
    • 4
  • López-Valdez Fernando
    • 5
  • Miranda-Arámbula Mariana
    • 5
  • Citlali Padilla-Rodríguez
    • 5
  • Fernández-Luqueño Fabián
    • 6
  1. 1.El Colegio de la Frontera Sur, Agroecología, Unidad CampecheCampecheMexico
  2. 2.Transdisciplinary Doctoral Program in Scientific and Technological Development for the Society, Cinvestav-ZacatencoMexico CityMexico
  3. 3.CONACYT-Centro de Investigación en Química Aplicada, Department of Bioscience and AgrotechnologySaltilloMexico
  4. 4.Laboratory of Soil Ecology, ABACUS, CinvestavMexico CityMexico
  5. 5.Agricultural Biotechnology Group, Research Center for Applied Biotechnology (CIBA) — Instituto Politécnico NacionalTlaxcalaMexico
  6. 6.Sustainability of Natural Resources and Energy Programs, Cinvestav-SaltilloRamos ArizpeMexico

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