- Email: [email protected]
Application of carbon nanomaterials in plant biotechnology
Materials Today: Proceedings xxx (xxxx) xxx
Contents lists available at ScienceDirect
Materials Today: Proceedings journal homepage: www.elsevier.com/locate/matpr
Application of carbon nanomaterials in plant biotechnology Neelofar Majeed b, Kishore C.S. Panigrahi c, Lala Behari Sukla a, Riffat John b, Madhusmita Panigrahy a,⇑ a
Siksha ‘O’ Anusandhan deemed to be University, Odisha, 751002, India University of Kashmir, Srinagar, Jammu & Kashmir, 190006, India c National Institute of Science Education and Research, Odisha, 752050, India b
a r t i c l e
i n f o
Article history: Received 12 December 2019 Received in revised form 19 January 2020 Accepted 22 January 2020 Available online xxxx Keywords: Carbon nanotubes Single walled nanotubes Multi walled nanotubes Nanoparticle Plant Biotechnology
a b s t r a c t Carbon nanomaterials are increasingly used in biomedical engineering and medicinal chemistry in recent years due to their unique structural and mechanical properties. Because of their highly tuneable physical properties, carbon nanotubes are most produced for their applicability in electronics, optics, nanomedicine, solar cells, high energy efficient renewable energy production, remediation, biosensors for pollutants and degradation of contaminants. Application of carbon nanotubes in agriculture and plant research is still a recent development in nanobiotechnology. Despite the potential application of carbon nanotubes for delivering cargo such as proteins, nucleic acids, and drugs for their targeted delivery to cells and organs, inhibition of cell proliferation, induced plasma membrane hyper polarization, oxidative stress in various in vitro mammalian cell studies have raised special concern about their toxicity in animals. This review aims not only to have a brief introduction of types and structures of nanotubes, but also through the detailed descriptions of its applications as biosensors, molecular carriers, in environmental applications, agricultural applications and toxicity issues it will deliver the update knowledge and future perspectives of carbon nano research. Ó 2020 Elsevier Ltd. All rights reserved. Selection and Peer-review under responsibility of the scientific committee of the National Conference on Trends in Minerals & Materials Technology.
Carbon based nanomaterials have been used to understand development and productivity in plants [1–5]. There are of several different types like nanoparticles, nanotubes, nanobeads, nanohorns, fullerenes, nanodiamonds, dots and nanofibres [6–11]. Various carbon nanomaterials that have been used and studied in plants such as carbon nanoparticles (CNPs), single walled carbon nanotubes (SWNT) and multi-walled carbon nanotubes (MWNT) [10,12]. They can affect plant development both positively as well as negatively [10]. 1. Carbon nanotubes – Types and structure Carbon nanotubes (CNT) are particular class of nanomaterials represented by unique physicochemical and structural properties, such as high electrical and thermal conductivity, presence of a hollow cavity and mechanical strength [13]. Due to such properties CNTs appear as useful agents for biomedical engineering [14], ⇑ Corresponding author at: Biofuel & Bioprocessing Research Centre, Siksha ‘O’ Anusandhan deemed to be University, Odisha, 751002, India. E-mail addresses: [email protected], [email protected] (M. Panigrahy).
drug-delivery and stimuli responsive cancer theragnostic [15]. CNTs are of two types: multiwalled carbon nanotubes (MWNTs) and single-walled carbon nanotubes (SWNTs) [16]. Structurally, MWNTs are made of many coaxially placed cylinders. Each cylinder is made up of a single graphene sheet that surrounds a hollow core. MWNTs are having outer diameter in the range of 2–100 nm and inner diameter of 1–3 nm. The length of MWNTs varies up to 1 to several lm [17]. SWNTs are made up of a single graphene cylinder and their diameter ranges from 0.4 to 2 nm [16,18,19]. On the basis of their helicity and diameter SWNTs can be either metallic or semiconducting [20–22]. In SWNTs, van der Walls forces held together nanotubes which usually occur as hexagonal closepacked bundles.
2. Modification of carbon nanotubes with biological molecules Various biological molecules are engineered both covalently as well as non-covalently to get attached to SWNTs while preserving the functional properties of the biological molecules. One such example of biological molecule is 1-pyrenebutanoic acid succinimidyl ester, which is non-covalently and irreversibly adsorbed
https://doi.org/10.1016/j.matpr.2020.01.618 2214-7853/Ó 2020 Elsevier Ltd. All rights reserved. Selection and Peer-review under responsibility of the scientific committee of the National Conference on Trends in Minerals & Materials Technology.
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
2
N. Majeed et al. / Materials Today: Proceedings xxx (xxxx) xxx
on hydrophobic surface of SWNTs [23]. The protein can then be attached to this moiety via nucleophilic substitution reaction where succinimidyl is substituted by amine group of protein. This also adds to the specificity in biological recognition of SWNTs. Carbodiimide chemistry is involved in covalently attaching CNTs to proteins [24] and DNA [25,26]. Carbon nanotubes are functionalized with carboxylic acid and the moiety then undergoes amidation, activated by diimide, to covalently bind proteins, enzymes and antibodies [24–27]. An example in this context is functionalization of SWNT fiber with bovine serum albumin (BSA). Indirect immunochemistry is used to confirm this functionalization in which first a primary antibody is raised against BSA and then a secondary, fluorescently (Fluorescent isothiocyanate FITC)conjugated, antibody is raised against the primary antibody. The complex can then be visualized by fluorescent microscopy. In the same way, amidation reactions can be used to connect amineterminated DNA with the carboxylic acid functional groups of CNTs. In addition, the high specificity of the biotin-avidin/ streptavidin interaction is also employed in designing such modified CNTs. There are many evidences of immobilization of SWNTs by both biotin and streptavidin [28–30]. 3. Effect of carbon nanoparticles on plant growth and development As nanotechnology is expanding rapidly it is necessary to study the interaction of nanomaterials with living organisms. Many studies conducted in this regard have shown that nanoparticles affect various physiological processes such as DNA damage [31,32], alterations of gene expression [33,34] and increase in ROS formation [35,36]. Such responses differ among different plant species [37,38], different varieties [39,40] and different stages of plant development [41]. Interaction of SWCNTs with young seedlings were mainly studied in hydroponics or in SWCNT supplied various culture media. It has been reported that the application of SWCNTs enhance seedling growth in many plant species such as maize (Zea mays) [33], Fig plants (Ficus carica) [42] and tomato (S. lycopersicum) seedlings [43]. A dose dependent response of SWCNTs has been described for pepper (C. annuum), salvia (S. macrosiphon), and tall fescue (F. arundinacea) [44]. The application of SWNTs was done by directly germinating the seeds on media containing SWNT [33]. In other cases, seeds after germination were transferred to hydroponic medium containing MWNTs [37]. Generally, the SWNTs or MWNTs exposure at varied concentrations up to 2000 mg/L was given for 15 days. These studies reported an increase in seedling biomass at 10–30 mg L 1 of SWCNTs, while seedling development was negatively affected at 40 mg L 1 of SWCNTs. MWCNTs affect positively on root and shoot elongation during early growth and seedling development. Such effects have been reported in many plant species such as soybean (G. max), maize (Z. mays) [40], wheat (Triticum aestivum) [45], tomato (S. lycopersicum) [43,46,47], mustard (B. juncea), and black lentil (P. mungo) [48]. The effects of MWCNTs reaches beyond germination and early growth and includes effects on reproductive stage of plant development. It has been reported that there is a doubling of flower setting and yield in tomato after the application of MWCNTs in soil [49]. Such effects were not seen in case of charcoal treated control soils. 4. Modified carbon nanotubes for biosensors Unique structural properties and extremely small size of carbon nanotubes make them the suitable candidate for biosensing. SWNTs are characterized with large surface / volume ratio which
helps them in interaction with several biological molecules. We can also opt for electrical detection as SWNTs are having characteristic electronic structure and good conductance. There occurs a large change in conductance of SWNTs in presence of various small biomolecules [50–53]. SWNT is used as a redox catalyst in the detection of adsorbed cytochrome c, present in mitochondria [53]. The binding of biotin and streptavidin also has been detected electronically by using biotin functionalized SWNTs [50]. This binding reduces the conductance of SWNTs. Such changes in SWNTs upon electronic detection probably originate due to the charge transfer processes at the time of interaction between SWNTs and the analyte. Very minute concentration (1pg/L) of DNA has been detected electronically by using alkaline phosphatase (ALP) enzyme functionalized CNTs [54]. Optical detection of molecules is also possible by using optically transparent conductive SWNT films [55]. Glucose is also selectively and sensitively detected by using CNT nanoelectrode assemblies [56]. The interaction of SWNTs with biological molecules has been used to interpret electrochemical properties of several molecules such as reduced bnicotinamide adenine dinucleotide (NADH) [57], hydrogen peroxide [57,58] and dopamine [59]. In such experiments SWNTs were at par with that of conventional carbon electrodes. Further modifications and fabrications of CNTs were proposed for their more widespread usage. 5. Carbon nanotubes as molecular carriers The structural properties of CNTs [60,61] makes them preferred vectors for targeting molecular probes, such as proteins and DNA, into mammalian cells. Binding of CNTs with several biological molecules such as proteins and DNA helps them in this context. Several proteins such as streptavidin interact with MWNTs [62] and DNA molecules can also get adsorbed on the surface of MWNTs [62–64]. Similarly, cytochrome c, b-Lactase I, and other small protein molecules can be introduced within the cavity of CNTs [65]. Nano-pills are designed in this manner, in which a small molecule is inserted into the interior cavity of CNTs with one end sealed and the other one open, which is then resealed. It appears a convenient way to deliver a drug placed in the interior cavity of nano-pill compared to bound on the outside surface of CNTs. A demonstration was made recently to show the possibility of using SWNTs for intracellular drug delivery [60,61]. A fluorescent probe, FITC was attached with SWNT to allow its tracking [60]. Such SWNTs were then exposed with murine and human fibroblast cell lines and SWNT-FITC start accumulating within the cells. In similar fashion, SWNTs-streptavidin accumulate inside human T cells, 3T3 fibroblast cell lines, leukemia (H60) cells and Chinese hamster ovary (CHO) [61]. 6. Carbon nanoparticles effects on photosynthesis Effect of nanoparticles on plants and their photosynthesis has been studied by several authors. Chronic and acute effects of NPs on photosynthetic apparatus and its productivity have been reported [66,67]. However, many reports are suggesting positive effects of NPs on photosynthesis, growth and development of various plants [68–72]. CuO nanoparticles are abundantly present in the environment and must be affecting the photosynthesis in plants. In this context, many authors have studied the effects of CuO NPs on photosynthesis [73–75]. In Lactuca sativa, Oryza sativa and Brassica oleracea var capitata, Cu accumulated inside leaves and cause structural damage to chloroplast and stomata, also resulting in lesser number of thylakoids per grana [67,76]. Also, it was observed that the content of chlorophyll and carotenoids decreased in both aquatic (Elodea densa, Lemna gibba, Landoltia
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
N. Majeed et al. / Materials Today: Proceedings xxx (xxxx) xxx
punctata) and terrestrial plants (Oryza sativa, Elsholtzia splendens) [67,73,77–80]. It has also been reported that the concentration of chlorophyll A decrease with applied NPs in a dose dependent manner [67,73,78–80]. Rawat et al. [80] reported a decrease in photosynthesis by 59% and that of stomatal conductance by 38% in Capsicum annuum by Cu ion treatment, but he didn’t observe any change in chlorophyll content after CuO treatment. Huang et al. [81] reported a decrease in chlorophyll content as well as in functionality of PSII upon Ag NPs treatment in aquatic plant Skeletonema costatum. ZnO NPs also decreased stomatal conductance, net photosynthesis and intercellular CO2 concentration in Arabidopsis [83]. 7. Environmental applications of carbon nanoparticle Environmental pollution has been a major global problem. A lot of different types of pollutants are entering the environment every day, so, efficient techniques should be there to get rid of them. But the conventional methods are with low efficiency and the environmental sustainability is at risk if we will rely only on them. Hence, need of the hour is to increase the efficiency of conventional methods and also to introduce new innovative approaches. Because of their great absorption potential due to increased surface area, nanomaterials especially those based on carbon can be a promising approach in this context. Many conventional wastewater managements have used activated charcoal as an adsorbent because of its high surface area. It can adsorb a great variety of different organic and inorganic pollutants, but its rate of adsorption is very low and it is nonspecific and ineffective towards microorganisms. However, these wastewater management strategies can be improved by using carbon-based nanomaterials in place of activated charcoal. Available literature has provided us great many examples where carbon nanomaterials have been used for improving wastewater management systems [84–87]. Literatures also suggest that adsorption capacity of CNTs towards lead [88], copper (III) [89] and microcystins (cyanobacterial toxins) [90] is far higher than that of activated charcoal. Using multiwalled nanotubes phosphorus, nitrogen, herbicides and antibiotics have been sorpted from wastewater [91]. Also, various organic pollutants [92], such as lindane (agricultural insecticide) [93] and persistent polychlorinated biphenyls [94] can be mobilized by using CNTs and fullerenes. Such great advantages of CNMs are due to their mechanical and thermal stability, enormous surface area, high chemical affinity for aromatic compounds [95], and potential antibacterial properties. CNM based filters can also be recycled because contaminants after sorption can then be desorbed from them [96,97]. Some hybrid nanoparticles such as silver-(Ag)-coated CNTs possess antimicrobial activity and can thus be used for disinfection purposes [98]. Carbon based nanomaterials can also be used to asses contamination levels in different environments. Potential and efficient sensors can be developed by using carbon nanomaterials which can detect very minute concentrations of various chemical compounds that are present in different environments. 8. Agricultural applications of carbon-based nanomaterials With increasing world population, the major challenge is to increase the agricultural production using minimum available agricultural land. Nanotechnology can be used as an efficient tool in this context. Fertilizers and growth promoters based on nanomaterials can be used to increase the crop production. [99–101]. Nanofertilizer facilitate higher nutrient use efficiency due to their higher surface area, high solubility in different solvents and small particle size [126]. Several plant protectors [102] are also based on nanomaterials such as herbicides [103] and pesticides [104,105]. Sev-
3
eral nano-encapsulated slow release fertilizers can also be used that can reduce the amount of applied agrochemicals. Plants grown in vitro were treated with carbon coated Fe nanoparticles [106]. Nanotechnology is also delivering precision farming to optimize agricultural practices [106]. A positive impact of carbon nanomaterials on plant growth have been reported in several studies which lead to formation of fertilizers containing carbon nanoparticles. Such fertilizers are more promising in reducing nutrient losses, improving plant nutrient availability and stimulating plant growth. CNM showed definite potential to improve plant health and grain quality [10]. However, effect on grain quality due to CNM application has not been shown yet. Lot of advantages are also associated with smart delivery systems, a technique for delivering agrochemicals. Encapsulated agrochemicals have increased use efficiency as they are more stable and are not degraded easily, lowering the use of applied agrochemicals [107]. Functionalized MWNTs were used to encapsulate fungicides that showed increased toxicity against Alternaria alternate fungi in comparison with non-encapsulated pesticide [104]. Conventionally, fertilizers were applied by broadcasting or by spraying. Such practices are associated with increased nutrient losses because of evaporation and leaching. The solution to this problem is the use of slow release or controlled release fertilizers that can be encapsulated by graphene oxide films [108]. 9. Toxicity Apart from many advantages of CNTs, a lot of questions are rising regarding their use in biology and medicine. One of the important concerns of these questions is regarding their toxicity [109,110]. The effect of CNTs should be tested prior to its commercial use. Many laboratories are already working in this regard and are investigating the toxicological effects of CNTs. There are many evidences suggesting harmful effects of CNTs on human health. Skin exposure can lead to several dermal problems such as oxidative stress and loss of cell viability as in case of cultured human skin cells exposed to SWNTs [111]. There is a good correlation of graphite and carbon materials with increased kerarosis and dermatitis, so such effects of CNTs are quite obvious. Pulmonary toxicity is also associated with SWNTs [112,113] and it is shown in case of rodents where there occurs development of granulomas after exposure to SWNTs. All of these toxicological effects appeared after using high concentrations of CNTs, further investigation is required for appropriate measurements. 10. Carbon nanoparticles in abiotic and biotic stress tolerance Because of the changing environmental conditions, plants are constantly being stressed by several biotic and abiotic factors. Crop growth, development and yield is limited by many abiotic stresses, particularly drought stress [114]. Limitation in water content changes many physiological and molecular aspects in plants such as reduction in photosynthesis and biomass and overproduction of reactive oxygen species (ROS). DNA, proteins and cellular membranes get damaged because of the excessive ROS production [114]. So, it is important and equally necessary to control ROS production and maintain the ROS levels at equilibrium. Many carbon nanoparticles such as fullerene and its derivatives are known to play a key role in abiotic stress tolerance of plants [115,116]. Certain studies have also shown that optimum concentrations of fullerol help plants in combating the harmful effects of osmotic stress [117,118]. Liu et al. (2016) also concluded that in presence of fullerol the concentrations of H2O2 and malondialdehyde (MDA) in maize decreased under PEG treatment. Likewise, in sugar beet, fullerol also helps in combating osmotic stress at concentrations of
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
4
N. Majeed et al. / Materials Today: Proceedings xxx (xxxx) xxx
0.01 and 0.001 nmol mm 2 leaf area by decreasing MDA level [117]. Because of the structural properties of fullerene, spherical cage-like, it can scavenge ROS, which plays a pivotal role in plant abiotic stress tolerance, particularly drought [119]. Several studies have illuminated the role of fullerene and its derivatives as powerful ROS detoxification agents [120,121]. Fullerol has also been noted for antioxidant enzyme activation to prevent oxidative damage to the plants [117]. Some antifungal and antibacterial activities of silver nanoparticles have been reported under greenhouse and field conditions, but the interaction of nanoparticles with plants and soil microflora is unknown [122,123]. Tomato (Solanum lycopersicum Mill.) is an important vegetable crop and contribute largely to economic benefits [124]. But its productivity is decreased by 80% because of early blight, caused by Alternaria solani [124]. Some traditional methods were followed to combat this deadly disease but resistant pathogens are continuously evolving [124,123]. However, use of silver nanoparticles can overcome such problem as it possesses multiple modes of actions by which it is hard for pathogen to acquire resistance [82,123]. External application of carbon nanoparticle resulted in increased chlorophyll content and influenced flowering time without any harmful effects [125]
[3] [4] [5] [6]
[7] [8]
[9] [10]
[11]
[12]
[13]
11. Conclusion [14]
Nanobiotechnology and nano agriculture with the researches including carbon nanomaterials have great perspectives in the advances of animal, plant sciences and agriculture. As the size of carbon nanomaterials is of great significance, they also penetrate the seed coat, plant cell wall and may lead to changes in metabolic functions and ultimately increase biomass and grain or fruit yield. The issues need to be carefully addressed in this field is their phytotoxicity, which appeared in some cases. This can be dealt by managing the concentrations and doses to prevent damage. Despite all these concerns, the future prospects of carbon nanomaterials are promising as a low-cost strategy for increased crop production and abiotic stress tolerance. Credit authorship contribution statement Neelofar Majeed: writing. Kishore C.S. Panigrahi: Supervision. Lala Behari Sukla: Supervision. Riffat John: Supervision. Madhusmita Panigrahy: Conceptualization, Visualization, Funding acquisition, Writing - review & editing.
[15] [16] [17] [18] [19] [20] [21] [22] [23]
[24]
[25]
[26]
Declaration of Competing Interest [27]
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements This work is supported by Department of Science and Technology (DST), Science and Engineering Research Board (SERB), India, Young Scientist Start-up Research Grant, No: YSS/2015/000659 and DST, India, WOS-A Women Scientist Grant No: SR/WOS-A/LS369/2018 awarded to MP. References [1] O. Zaytseva, G. Neumann, Carbon nanomaterials: Production, impact on plant development, agricultural and environmental applications, Chem. Biol. Technol. Agric. 3 (2016) 1–26. [2] M.F. Serag, N. Kaji, M. Tokeshi, Y. Baba, Carbon nanotubes and modern nanoagriculture, in: H. Manzer, H. Mohamed, M. Firoz (Eds.), Nanotechnology
[28]
[29]
[30] [31]
[32] [33]
[34]
and plant sciences, Springer International Publishing, Berlin, 2015, pp. 183– 201. B.S. Sekhon, Nanotechnology in agri-food production: An overview, Nanotechnol. Sci. Appl. 7 (2014) 31–53. A. Husen, K.S. Siddiqi, Carbon and fullerene nanomaterials in plant system, J. Nanobiotechnol. 16 (2014) 1–10. A. Ditta, How helpful is nanotechnology in agriculture?, Adv Nat. Sci. Nanosci. Nanotechnol. 3 (2012) 1–10. S. Mishra, D. Beyer, K. Eimre, et al., Topological frustration induces unconventional magnetism in a nanographene, Nat. Nanotechnol. (2019;) 1748–3395, https://doi.org/10.1038/s41565-019-0577-9. B. Nowack, T.D. Bucheli, Occurrence, behaviour and effects of nanoparticles in the environment, Environ. Pollut. 150 (2007) 5–22. Beatriz Rossi Canuto de Menezes, Karla Faquine Rodrigues, Beatriz Carvalho da Silva Fonseca, Renata Ribas, Thais Larissa do Amaral Montanheiro, Gilmar Thim, Recent advances in the use of carbon nanotubes as smart biomaterials, J. Mater. Chem. B 7 (2019) 1343–1360. Z. Hossain, G. Mustafa, S. Komatsu, Plant responses to nanoparticles stress, Int. J. Mol. Sci. 16 (2015) 26644–26653. A. Mukherjee, S. Majumdar, A.D. Servin, L. Pagano, O.P. Dhankher, J.C. White, Carbon nanomaterials in agriculture: A critical review, Front. Plant. Sci. 7 (2016) 1–16. X. Wang, X. Yang, S. Chen, Q. Li, W. Wang, G.X. Hou Chunjiang, L. Wang, S. Wang, Zinc oxide nanoparticles affect biomass accumulation and photosynthesis in Arabidopsis, Front. Plant Sci. 6 (2016) 1–9. S. García-Sánchez, I. Bernales, S. Cristobal, Early response to nanoparticles in the Arabidopsis transcriptome compromises plant defense and root-hair development through salicylic acid signalling, BMC Genom. 16 (2015) 341– 356. M.S. Dresselhaus, G. Dresselhaus, P. Avouris (Eds.), Carbon Nanotubes: Synthesis, Structures, Properties and Applications. Springer-Verlag Berlin, Heidelberg, 2001. C. Cha, S.R. Shin, N. Annabi, M.R. Dokmeci, A. Khademhosseini, ACS Nano. 7 (2013) 2891–2897. E. Heister, E.W. Brunner, G.R. Dieckmann, I. Jurewicz, B. Dalton, ACS Appl. Mater. Interfaces 5 (2013) 1870–1891. S. Iijima, T. Ichihashi, Single-shell carbon nanotubes of 1-nm diameter, Nature 363 (1993) 603. M.S. Dresselhaus, G. Dresselhaus, P.C. Eklund, Science of Fullerenes and Carbon Nanotubes, Academic, San Diego, 1996. L.C. Qin, X. Zhao, K. Hirahara, Y. Miyamoto, Y. Ando, S. Iijima, The smallest carbon nanotube, Nature 408 (2000) 50. N. Wang, Z.K. Tang, G.D. Li, J.S. Chen, Single-walled 4 A carbon nanotube arrays, Nature 408 (2000) 50. J.W. Mintmire, B.I. Dunlap, C.T. White, Are fullerene tubules metallic?, Phys Rev. Lett. 68 (1992) 631. N. Hamada, S.I. Sawada, A. Oshiyama, New one-dimensional conductors: Graphitic microtubules, Phys. Rev. Lett. 68 (1992) 1579. R. Saito, M. Fujita, G. Dresselhaus, M.S. Dresselhaus, Electronic structure of chiral graphene tubules, Appl. Phys. Lett. 60 (1992) 2204. R.J. Chen, Y. Zhang, D. Wang, H. Dai, Noncovalent sidewall functionalization of single-walled carbon nanotubes for protein immobilization, J. Am. Chem. Soc. 123 (2001) 3838. W. Huang, S. Taylor, K. Fu, Y. Lin, D. Zhang, T.W. Hanks, A.M. Rao, Y.-P. Sun, Attaching proteins to carbon nanotubes via diimide-activated amidation, Nano. Lett. 2 (2002) 311. C. Dwyer, M. Guthold, M. Falvo, S. Washburn, R. Superfine, D. Erie, DNAfunctionalized single-walled carbon nanotubes, Nanotechnology 13 (2002) 601. K.A. Williams, P.T.M. Veenhuizen, B.G. de la Torre, R. Eritja, C. Dekker, Nanotechnology: Carbon nanotubes with DNA recognition, Nature 420 (2002) 761. B.R. Azamian, J.J. Davis, K.S. Coleman, C.B. Bagshaw, M.L.H. Green, Bioelectrochemical single-walled carbon nanotubes, J. Am. Chem. Soc. 124 (2002) 12664. M. Zheng, A. Jagota, E.D. Semke, B.A. Diner, R.S. McLean, S.R. Lustig, R.E. Richardson, N.G. Tassi, DNA assisted dispersion and separation of carbon nanotubes, Nature Mater. 2 (2003) 338. J.N. Wohlstadter, J.L. Wilbur, G.B. Sigal, H.A. Biebuyck, M.A. Billadeau, L. Dong, A.B. Fischer, S.R. Gudibande, S.H. Jameison, J.H. Kenten, J. Leginus, J.K. Leland, R.J. Massey, S.J. Wohlstadter, Carbon nanotube-based biosensor, Adv. Mater. 15 (2003) 1184. K. Keren, R.S. Berman, E. Buchstab, U. Sivan, E. Braun, DNA-templated carbon nanotube field-effect transistor, Science 302 (2003) 1380. M. Ghosh, A. Chakraborty, M. Bandyopadhyay, A. Mukherjee, Multi-walled carbon nanotubes (MWCNT): Induction of DNA damage in plant and mammalian cells, J. Hazard. Mater. 197 (2011) 327–336. D.R. Katti, A. Sharma, S.M. Pradhan, K.S. Katti, Carbon nanotube proximity influences rice DNA, Chem. Phys. 455 (2015) 17–22. S. Yan, L. Zhao, H. Li, Q. Zhang, J. Tan, M. Huang, S. He, L. Li, Single-walled carbon nanotubes selectively influence maize root tissue development accompanied by the change in the related gene expression, J. Hazard Mater. 246–247 (2013) 110–118. M. Ghosh, S. Bhadra, A. Adegoke, M. Bandyopadhyay, A. Mukherjee, MWCNT uptake in Allium cepa root cells induces cytotoxic and genotoxic responses and results in DNA hyper-methylation, Mutat. Res. 774 (2015) 49–58.
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
N. Majeed et al. / Materials Today: Proceedings xxx (xxxx) xxx [35] P. Begum, B. Fugetsu, Phytotoxicity of multi-walled carbon nanotubes on red spinach (Amaranthus tricolor L) and the role of ascorbic acid as an antioxidant, J. Hazard Mater. 243 (2012) 212–222. [36] Q. Liu, X. Zhang, Y. Zhao, J. Lin, C. Shu, C. Wang, X. Fang, Fullerene-induced increase of glycosyl residue on living plant cell wall, Environ. Sci. Technol. 47 (2013) 7490–7498. [37] P. Begum, R. Ikhtiari, B. Fugetsu, M. Matsuoka, T. Akasaka, F. Watari, Phytotoxicity of multi-walled carbon nanotubes assessed by selected plant species in the seedling stage, Appl. Surf. Sci. 262 (2012) 120–124. [38] Cañas JE, Long M, Nations S, Vadan R, Dai L, Luo M, Ambikapathi R, Lee EH, Olszyk D, Effects of functionalized and nonfunctionalized single walled carbon nanotubes on root elongation of select crop species, Environ. Toxicol. Chem. 27 (2008) 1922–1931. [39] D.K. Tiwari, N. Dasgupta-Schubert, L.M. Cendejas, J. Villegas, L. Carreto Montoya, S.E. García, Interfacing carbon nanotubes (CNT) with plants: Enhancement of growth, water and ionic nutrient uptake in maize (Zea mays) and implications for nano agriculture, Appl. Nanosci. 4 (2014) 577– 591. [40] M.H. Lahiani, E. Dervishi, J. Chen, Z. Nima, A. Gaume, A.S. Biris, M.V. Khodakovskaya, Impact of carbon nanotube exposure to seeds of valuable crops, ACS Appl. Mater. Interfaces 5 (2013) 7965–7973. [41] D. Stampoulis, S.K. Sinha, J.C. White, Assay-dependent phytotoxicity of nanoparticles to plants, Environ. Sci. Technol. 43 (2009) 9473–9479. [42] D. Flores, J.S. Chaves, R. Chacón, A. Schmidt, A novel technique using SWCNTs to enhanced development and root growth of fig plants (Ficus carica), in: Nanotechnology 2013. Bio sensors, instruments, medical, environment and energy technical proceedings of the 2013 NSTI Nanotechnology Conference and Expo. Boston: Nano Science and Technology Institute, 2013, pp. 167–170. [43] M.V. Khodakovskaya, K. de Silva, D.A. Nedosekin, E. Dervishi, A.S. Biris, E.V. Shashkov, E.I. Galanzha, V.P. Zharov, Complex genetic, photothermal and photoacoustic analysis of nanoparticle-plant interactions, Proc. Natl. Acad. Sci. 108 (2011) 1028–1033. [44] A. Pourkhaloee, M. Haghighi, M.J. Saharkhiz, H. Jouzi, M.M. Doroodmand, Carbon nanotubes can promote seed germination via seed coat penetration, Seed Technol. 33 (2011) 155–169. [45] X. Wang, H. Han, X. Liu, X. Gu, K. Chen, D. Lu, Multi-walled carbon nanotubes can enhance root elongation of wheat (Triticum aestivum) plants, J. Nanopart. Res. 14 (2012) 841. [46] M. Khodakovskaya, E. Dervishi, M. Mahmood, Y. Xu, Z. Li, F. Watanabe, A.S. Biris, Carbon nanotubes are able to penetrate plant seed coat and dramatically affect seed germination and plant growth, ACS Nano. 3 (2009) 3221–3227. [47] H. Villagarcia, E. Dervishi, K. de Silva, A.S. Biris, M.V. Khodakovskaya, Surface chemistry of carbon nanotubes impacts the growth and expression of water channel protein in tomato plants, Small 8 (2012) 2328–2334. [48] G. Ghodake, Y.D. Seo, D. Park, D.S. Lee, Phytotoxicity of carbon nanotubes assessed by Brassica juncea and Phaseolus mungo, J. Nanoelectron. Optoelectron. 5 (2010) 157–160. [49] M.V. Khodakovskaya, B. Kim, J.N. Kim, M. Alimohammadi, E. Dervishi, T. Mustafa, C.E. Cernigla, Carbon nanotubes as plant growth regulators: Effects on tomato growth, reproductive system, and soil microbial community, Small 9 (2013) 115–123. [50] A. Star, J.C.P. Gabriel, K. Bradley, G. Gruner, Electronic detection of specific protein binding using nanotube FET devices, Nano. Lett. 3 (2003) 459. [51] K. Besteman, J.O. Lee, F.G. Wiertz, H.A. Heering, C. Dekker, Enzyme-coated carbon nanotubes as singlemolecule biosensors, Nano. Lett. 3 (2003) 727. [52] R.J. Chen, S. Bangsaruntip, K.A. Drouvalakis, N.W.S. Kam, M. Shim, Y. Li, W. Kim, P.J. Utz, H. Dai, Noncovalent functionalization of carbon nanotubes for highly specific electronic biosensors, Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 4984. [53] S. Boussaad, N.J. Tao, R. Zhang, T. Hopson, L.A. Nagahara, In situ detection of cytochrome c adsorption with single walled carbon nanotube device, Chem. Commun. (2003) 1502. [54] J. Wang, G. Liu, M.R. Jan, Ultrasensitive electrical biosensing of proteins and DNA: Carbon-nanotube derived amplification of the recognition and transduction events, J. Am. Chem. Soc. 126 (2004) 3010. [55] Z. Wu, Z. Chen, X. Du, J.M. Logan, J. Sippel, M. Nikolou, K. Kamaras, J.R. Reynolds, D.B. Tanner, A.F. Hebard, A.G. Rinzler, Transparent, conductive carbon nanotube films, Science 305 (2004) 1273. [56] Y. Lin, F. Lu, Y. Tu, Z. Ren, Glucose biosensors based on carbon nanotube nanoelectrode ensembles, Nano. Lett. 4 (2004) 191. [57] J. Wang, M. Musameh, Carbon nanotube/Teflon composite electrochemical sensors and biosensors, Anal. Chem. 75 (2003) 2075. [58] J. Wang, M. Musameh, Y. Lin, Solubilization of carbon nanotubes by Nafion toward the preparation of amperometric biosensors, J. Am. Chem. Soc. 125 (2003) 2408. [59] P.J. Britto, S.K.V. Santhaman, P.M. Ajayan, Carbon nanotube electrode for oxidation of dopamine, Bioelectrochem. Bioelectronics 41 (1996) 121. [60] D. Pantarotto, J.-P. Briand, M. Prato, A. Bianco, Translocation of bioactive peptides across cell membranes by carbon nanotubes, Chem. Commun. (2004) 16. [61] N.W.S. Kam, T.C. Jessop, P.A. Wender, H. Dai, Nanotube molecular transporters: Internalization of carbon nanotube-protein conjugates into mammalian cells, J. Am. Chem. Soc. 126 (2004) 6850. [62] F. Balavoine, P. Schultz, C. Richard, V. Mallouh, T.W. Ebbesen, C. Mioskowski, Helical crystallization of proteins on carbon nanotubes: A first step towards the development of new biosensors, Angew. Chem. Int. Ed. 38 (1999) 1912.
5
[63] S.C. Tsang, Z. Guo, Y.K. Chen, M.L.H. Green, H.A.O. Hill, T.W. Hambley, P.J. Sadler, Immobilization of platinated and iodinated oligonucleotides on carbon nanotubes, Angew. Chem. Int. Ed. 36 (1997) 2198. [64] Z. Guo, P.J. Sadler, S.C. Tsang, Immobilization and visualization of DNA and proteins on carbon nanotubes, Adv. Mater. 10 (1998) 701. [65] J.J. Davis, M.L.H. Green, H.A.O. Hill, Y.C. Leung, P.J. Sadler, J. Sloan, A.V. Xavier, S.C. Tsang, The immobilization of proteins in carbon nanotubes, Inorg. Chem. Acta. 272 (1998) 261. [66] S.C. Arruda, A.L. Silva, R.M. Galazzi, R.A. Azevedo, M.A. Arruda, Nanoparticles applied to plant science: a review, Talanta 131 (2015) 693–705. [67] M.V.J. Da Costa, P.K. Sharma, Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa, Photosynthetica 54 (2016) 110–119. [68] F. Hong, J. Zhou, C. Liu, F. Yang, C. Wu, L. Zheng, P. Yang, Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach, Biol. Trace Elem. Res. 105 (2005) 269–279. [69] S. Mingyu, H. Fashui, L. Chao, W. Xiao, L. Xiaoqing, C. Liang, G. Fengqing, L. Zhongrui, Effects of nano-anatase TiO2 on absorption, distribution of light, and photoreduction activities of chloroplast membrane of spinach, Biol. Trace Elem. Res. 118 (2007) 120–130. [70] M.K. Sarmast, H. Salehi, Silver nanoparticles: An influential element in plant nanobiotechnology, Mol. Biotechnol. 58 (2016) 441–449. [71] G.S. Zarate-Cruz, H.A. Zavaleta-Mancera, A. Alarcón, L.F. Jiménez-García, Fitotoxicidad de nanopartículas de ZnO en el helecho acuático Azolla filiculoides Lam, Agrociencia 50 (2016) 677–691. [72] Z. Cao, L. Rossi, C. Stowers, W. Zhang, L. Lombardini, X. Ma, The impact of cerium oxide nanoparticles on the physiology of soybean (Glycine max (L.) Merr.) under different soil moisture conditions, Environ. Sci. Pollut. Control Ser. 25 (2018) 930–939. [73] C.M. Lalau, R. de Almeida Mohedano, É.C. Schmidt, Z.L. Bouzon, L.C. Ouriques, R.W. dos Santos, C.H. Da Costa, D.S. Vicentini, W.G. Matias, Toxicological effects of copper oxide nanoparticles on the growth rate, photosynthetic pigment content, and cell morphology of the duckweed Landoltia punctata, Protoplasma 252 (2014) 221–229. [74] F. Perreault, M. Samadani, D. Dewez, Effect of soluble copper released from copper oxide nanoparticles solubilisation on growth and photosynthetic processes of Lemna gibba L, Nanotoxicology 8 (2014) 374–382. [75] N. Regier, C. Cosio, N. von Moos, V.I. Slaveykova, Effects of copper-oxide nanoparticles, dissolved copper and ultraviolet radiation on copper bioaccumulation, photosynthesis and oxidative stress in the aquatic macrophyte Elodea nuttallii, Chemosphere 128 (2015) 56–61. [76] T. Xiong, C. Dumat, V. Dappe, H. Vezin, E. Schreck, M. Shahid, A. Pieral, S. Sobanska, Copper oxide nanoparticle foliar uptake, phytotoxicity, and consequences for sustainable urban agriculture, Environ. Sci. Technol. 51 (2017) 5242–5251. [77] F. Perreault, A. Oukarroum, L. Pirastru, L. Sirois, W. Gerson Matias, R. Popovic, Evaluation of copper oxide nanoparticles toxicity using chlorophyll fluorescence imaging in Lemna gibba, J. Bot. 763142 (2010). [78] G.F. Nekrasova, O.S. Ushakova, A.E. Ermakov, M.A. Uimin, I.V. Byzov, Effects of copper (II) ions and copper oxide nanoparticles on Elodea densa Planch, Russ. J. Ecol. 42 (2011) 458–463. [79] J. Shi, C. Peng, Y. Yang, J. Yang, H. Zhang, X. Yuan, Y. Chen, T. Hu, Phytotoxicity and accumulation of copper oxide nanoparticles to the Cu-tolerant plant Elsholtzia splendens, Nanotoxicology 8 (2013) 179–188. [80] S. Rawat, V.L. Pullagurala, M. Hernandez-Molina, Y. Sun, G. Niu, J.A. Hernandez-Viezcas, J. Perata-Videa, J.L. Gardea-Torresdey, Impacts of copper oxide nanoparticles on bell pepper (Capsicum annuum L.) plants: A full life cycle study, Environ. Sci. J. Integr. Environ. Res.: Nano 5 (2018) 83–95. [81] J. Huang, J. Cheng, J. Yi, Impact of silver nanoparticles on marine diatom Skeletonema costatum, J. Appl. Toxicol. 36 (2016) 1343–1354. [82] S. Wang, J. Lv, J. Ma, S. Zhang, Cellular internalization and intracellular biotransformation of silver nanoparticles in Chlamydomonas reinhardtii, Nanotoxicology 10 (2016) 1129–1135. [83] R. Das, M.E. Ali, S.B.A. Hamid, S. Ramakrishna, Z.Z. Chowdhury, Carbon nanotube membranes for water purification: A bright future in water desalination, Desalination 336 (2014) 97–109. [84] X. Qu, P.J.J. Alvarez, Q. Li, Applications of nanotechnology in water and wastewater treatment, Water Res. 47 (2013) 3931–3946. [85] X. Liu, M. Wang, S. Zhang, B. Pan, Application potential of carbon nanotubes in water treatment: A review, J. Environ. Sci. (China) 25 (2013) 1263–1280. [86] S.C. Smith, D.F. Rodrigues, Carbon-based nanomaterials for removal of chemical and biological contaminants from water: A review of mechanisms and applications, Carbon 91 (2015) 122–143. [87] Y. Li, S. Wang, J. Wei, X. Zhang, C. Xu, Z. Luan, D. Wu, B. Wei, Lead adsorption on carbon nanotubes, Chem. Phys. Lett. 357 (2002) 263–266. [88] A.B. Dichiara, M.R. Webber, W.R. Gorman, R.E. Rogers, Removal of copper ions from aqueous solutions via adsorption on carbon nanocomposites, ACS Appl. Mater. Interfaces 7 (2015) 15674–15680. [89] H. Yan, A. Gong, H. He, J. Zhou, Y. Wei, L. Lv, Adsorption of microcystins by carbon nanotubes, Chemosphere 62 (2006) 142–148. [90] X. Zheng, Y. Su, Y. Chen, Y. Wei, M. Li, H. Huang, The effects of carbon nanotubes on nitrogen and phosphorus removal from real wastewater in the activated sludge system, RSC Adv. 4 (2014) 45953–45959. [91] A. Mishra, J.H. Clark, Green materials for sustainable water remediation and treatment, Royal Society of Chemistry, Cambridge, 2013.
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
6
N. Majeed et al. / Materials Today: Proceedings xxx (xxxx) xxx
[92] M. Srivastava, P.C. Abhilash, N. Singh, Remediation of lindane using engineered nanoparticles, J. Biomed. Nanotechnol. 7 (2011) 172–174. [93] L. Wang, J.D. Fortner, L. Hou, C. Zhang, A.T. Kan, M.B. Tomson, W. Chen, Contaminant-mobilizing capability of fullerene nanoparticles (nC60): Effect of solvent-exchange process in nC60 formation, Environ. Toxicol. Chem. 32 (2013) 329–336. [94] J. Yoo, H. Ozawa, T. Fujigaya, N. Nakashima, Evaluation of affinity of molecules for carbon nanotubes, Nanoscale 3 (2011) 2517–2522. [95] W.S. Choi, H.M. Yang, H.Y. Koo, H. Lee, Y.B. Lee, T.S. Bae, I.C. Jeon, Smart microcapsules encapsulating reconfigurable carbon nanotube cores, Adv. Funct. Mater. 20 (2010) 820–825. [96] H. Wang, H. Ma, W. Zheng, D. An, C. Na, Multifunctional and recollectable carbon nanotube ponytails for water purification, ACS Appl. Mater. Interfaces 6 (2014) 9426–9434. [97] J.H. Jung, G.B. Hwang, J.E. Lee, G.N. Bae, Preparation of airborne Ag/CNT hybrid nanoparticles using an aerosol process and their application to antimicrobial air filtration, Langmuir 27 (2011) 10256–10264. [98] C. Parisi, M. Vigani, E. Rodríguez-Cerezo (Eds.), Proceedings of a workshop on ‘‘Nanotechnology for the agricultural sector: From research to the field” (2014) Luxembourg. [99] L.R. Khot, S. Sankaran, J.M. Maja, R. Ehsani, E.W. Schuster, Applications of nanomaterials in agricultural production and crop protection: A review, Crop Prot. 35 (2012) 64–70. [100] J. Hong, J.R. Peralta-Videa, J.L. Gardea-Torresdey, Nanomaterials in agricultural production: Benefits and possible threats?, in: N. Shamim, V.K. Sharma (Eds.), Sustainable nanotechnology and the environment: Advances and achievements, American Chemical Society, Washington, D.C, 2013, pp. 73–90. [101] A. Gogos, K. Knauer, T.D. Bucheli, Nanomaterials in plant protection and fertilization: current state, foreseen applications, and research priorities, J. Agric. Food Chem. 60 (2012) 9781–9792. [102] A. Pereira, R. Grillo, N.F. Mello, A.H. Rosa, L.F. Fraceto, Application of poly (epsilon-caprolactone) nanoparticles containing atrazine herbicide as an alternative technique to control weeds and reduce damage to the environment, J. Hazard. Mater. 268 (2014) 207–215. [103] N. Sarlak, A. Taherifar, F. Salehi, 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 (2014) 4833–4838. [104] R.S. Suresh Kumar, P.J. Shiny, C.H. Anjali, J. Jerobin, K.M. Goshen, S. Magdassi, A. Mukherjee, N. Chandrasekaran, Distinctive effects of nanosized permethrin in the environment, Environ. Sci. Pollut. Res. Int. 20 (2013) 2593–2602. [105] H. Auernhammer, Precision farming—the environmental challenge, Comput. Electron. Agric. 30 (2001) 31–43. [106] P. González-Melendi, R. Fernández-Pacheco, M.J. Coronado, E. Corredor, P.S. Testillano, M.C. Risueño, C. Marquina, M.R. Ibarra, D. Rubiales, Luque A. Pérez-de-, Nanoparticles as smart treatment-delivery systems in plants: Assessment of different techniques of microscopy for their visualization in plant tissues, Ann. Bot. 101 (2008) 187–195. [107] M. Zhang, B. Gao, J. Chen, Y. Li, A.E. Creamer, H. Chen, Slow-release fertilizer encapsulated by graphene oxide films, Chem. Eng. J. 255 (2014) 107–113. [108] Service RF, Nanomaterials show signs of toxicity, Science 300 (2003) 243. [109] Service RF, Nanotoxicology. Nanotechnology grows up, Science 304 (2004) 1732. [110] A.A. Shvedova, V. Castranova, E.R. Kisin, D. Schwegler-Berry, A.R. Murray, V.Z. Gandelsman, A. Maynard, P. Baron, Exposure to carbon nanotube material:
[111]
[112]
[113]
[114]
[115]
[116]
[117]
[118]
[119]
[120]
[121]
[122]
[123]
[124]
[125]
[126]
Assessment of nanotube cytotoxicity using human keratinocyte cells, J. Toxicol. Environ. Health A 66 (2003) 1909. C.W. Lam, J.T. James, R. McCluskey, R.L. Hunter, Pulmonary toxicity of singlewall carbon nanotubes in mice 7 and 90 days after intratracheal instillation, Toxicol. Sci. 77 (2004) 126. D.B. Warheit, B.R. Laurence, K.L. Reed, D.H. Roach, G.A. Reynolds, T.R. Webb, Comparative pulmonary toxicity assessment of single-wall carbon nanotubes in rats, Toxicol. Sci. 77 (2004) 117. S.M. Impa, S. Nadaradjan, S.V.K. Jagadish, Drought stress induced reactive oxygen species and anti-oxidants in plants, in: P. Ahmad, M.N.V. Prasad (Eds.), Abiotic Stress Responses in Plants, Springer, New York, 2011, pp. 131– 147. J.S. Duhan, R. Kumar, N. Kumar, P. Kaur, K. Nehra, S. Duhan, Nanotechnology: the new perspective in precision agriculture, Biotechnol. Rep. 15 (2017) 11– 23. M.N. Khan, M. Mobin, Z.K. Abbas, K.A. AlMutairi, Z.H. Siddiqui, Role of nanomaterials in plants under challenging environments, Plant Physiol. Biochem. 110 (2017) 194–209. M. Borišev, I. Borišev, M. Zˇupunski, D. Arsenov, S. Pajevic´, Zˇ. C´urcˇic´, J. Vasin, A. Djordjevic, Drought impact is alleviated in sugar beets (Beta vulgaris L.) by foliar application of fullerenol nanoparticles, PLoS One 11 (2016) e0166248. G.G. Panova, I.N. Ktitorova, O.V. Skobeleva, N.G. Sinjavina, N.A. Charykov, K.N. Semenov, Impact of polyhydroxy fullerene (fullerol or fullerenol) on growth and biophysical characteristics of barley seedlings in favourable and stressful conditions, Plant Growth Regul. 79 (2016) 309–317. A. Trpkovic, B. Todororic-Markovic, V. Trajkovic, Toxicity of pristine versus functionalized fullerenes: mechanisms of cell damage and the role of oxidative stress, Arch. Toxicol. 86 (2012) 1809–1827. H. Wei, E. Wang, Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes, Chem. Soc. Rev. 42 (2011) 6060–6093. M.J. Akhtar, M. Ahamed, H.A. Alhadlaq, A. Alshamsan, Mechanism of ROS scavenging and antioxidant signalling by redox metallic and fullerene nanomaterials: Potential implications in ROS associated degenerative disorders, Biochim. Biophys. Acta 1851 (2017) 802–813. A. Mishra, M. Kumari, S. Pandey, V. Chaudhry, K.C. Gupta, C.S. Nautiyal, Biocatalytic and antimicrobial activities of gold nanoparticles synthesized by Trichoderma sp, Bioresour. Technol. 166 (2014) 235–242. I. Ocsoy, M.L. Paret, M.A. Ocsoy, S. Kunwar, T. Chen, M. You, W. Tan, Nanotechnology in plant disease management: DNA-directed silver nanoparticles on graphene oxide as an antibacterial against Xanthomonas perforans, ACS Nano. 7 (10) (2013) 8972–8980. N. Khan, A. Mishra, C.S. Nautiyal, Paenibacillus lentimorbus B-30488r controls early blight disease in tomato by inducing host resistance associated gene expression and inhibiting Alternaria solani, Biol. Control 62 (2012) 65–74. R. Dixit, L. Agarwal, S. Gupta, M. Kumar, S. Yadav, P.S. Chauhan, C.S. Nautiyal, Southern blight disease of tomato control by 1-aminocyclopropane-1carboxylate (ACC) deaminase producing Paenibacillus lentimorbus B-30488, Plant Signal. Behav. 11 (2) (2016) e1113363. A. Kumar, A. Singh, M. Panigrahy, P.K. Sahoo, K.C. Panigrahi, Carbon nanoparticle influences photomorphogenesis and flowering time in Arabidopsis thaliana, Plant Cell Rep. 37 (6) (2018) 901–912. N. Mahanta, A. Dambale, M. Rajkhowa, Nutrient use efficiency through Nano fertilizers, Int. J. Chem. Studies 7 (3) (2019) 2839–2842.
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
Contents lists available at ScienceDirect
Materials Today: Proceedings journal homepage: www.elsevier.com/locate/matpr
Application of carbon nanomaterials in plant biotechnology Neelofar Majeed b, Kishore C.S. Panigrahi c, Lala Behari Sukla a, Riffat John b, Madhusmita Panigrahy a,⇑ a
Siksha ‘O’ Anusandhan deemed to be University, Odisha, 751002, India University of Kashmir, Srinagar, Jammu & Kashmir, 190006, India c National Institute of Science Education and Research, Odisha, 752050, India b
a r t i c l e
i n f o
Article history: Received 12 December 2019 Received in revised form 19 January 2020 Accepted 22 January 2020 Available online xxxx Keywords: Carbon nanotubes Single walled nanotubes Multi walled nanotubes Nanoparticle Plant Biotechnology
a b s t r a c t Carbon nanomaterials are increasingly used in biomedical engineering and medicinal chemistry in recent years due to their unique structural and mechanical properties. Because of their highly tuneable physical properties, carbon nanotubes are most produced for their applicability in electronics, optics, nanomedicine, solar cells, high energy efficient renewable energy production, remediation, biosensors for pollutants and degradation of contaminants. Application of carbon nanotubes in agriculture and plant research is still a recent development in nanobiotechnology. Despite the potential application of carbon nanotubes for delivering cargo such as proteins, nucleic acids, and drugs for their targeted delivery to cells and organs, inhibition of cell proliferation, induced plasma membrane hyper polarization, oxidative stress in various in vitro mammalian cell studies have raised special concern about their toxicity in animals. This review aims not only to have a brief introduction of types and structures of nanotubes, but also through the detailed descriptions of its applications as biosensors, molecular carriers, in environmental applications, agricultural applications and toxicity issues it will deliver the update knowledge and future perspectives of carbon nano research. Ó 2020 Elsevier Ltd. All rights reserved. Selection and Peer-review under responsibility of the scientific committee of the National Conference on Trends in Minerals & Materials Technology.
Carbon based nanomaterials have been used to understand development and productivity in plants [1–5]. There are of several different types like nanoparticles, nanotubes, nanobeads, nanohorns, fullerenes, nanodiamonds, dots and nanofibres [6–11]. Various carbon nanomaterials that have been used and studied in plants such as carbon nanoparticles (CNPs), single walled carbon nanotubes (SWNT) and multi-walled carbon nanotubes (MWNT) [10,12]. They can affect plant development both positively as well as negatively [10]. 1. Carbon nanotubes – Types and structure Carbon nanotubes (CNT) are particular class of nanomaterials represented by unique physicochemical and structural properties, such as high electrical and thermal conductivity, presence of a hollow cavity and mechanical strength [13]. Due to such properties CNTs appear as useful agents for biomedical engineering [14], ⇑ Corresponding author at: Biofuel & Bioprocessing Research Centre, Siksha ‘O’ Anusandhan deemed to be University, Odisha, 751002, India. E-mail addresses: [email protected], [email protected] (M. Panigrahy).
drug-delivery and stimuli responsive cancer theragnostic [15]. CNTs are of two types: multiwalled carbon nanotubes (MWNTs) and single-walled carbon nanotubes (SWNTs) [16]. Structurally, MWNTs are made of many coaxially placed cylinders. Each cylinder is made up of a single graphene sheet that surrounds a hollow core. MWNTs are having outer diameter in the range of 2–100 nm and inner diameter of 1–3 nm. The length of MWNTs varies up to 1 to several lm [17]. SWNTs are made up of a single graphene cylinder and their diameter ranges from 0.4 to 2 nm [16,18,19]. On the basis of their helicity and diameter SWNTs can be either metallic or semiconducting [20–22]. In SWNTs, van der Walls forces held together nanotubes which usually occur as hexagonal closepacked bundles.
2. Modification of carbon nanotubes with biological molecules Various biological molecules are engineered both covalently as well as non-covalently to get attached to SWNTs while preserving the functional properties of the biological molecules. One such example of biological molecule is 1-pyrenebutanoic acid succinimidyl ester, which is non-covalently and irreversibly adsorbed
https://doi.org/10.1016/j.matpr.2020.01.618 2214-7853/Ó 2020 Elsevier Ltd. All rights reserved. Selection and Peer-review under responsibility of the scientific committee of the National Conference on Trends in Minerals & Materials Technology.
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
2
N. Majeed et al. / Materials Today: Proceedings xxx (xxxx) xxx
on hydrophobic surface of SWNTs [23]. The protein can then be attached to this moiety via nucleophilic substitution reaction where succinimidyl is substituted by amine group of protein. This also adds to the specificity in biological recognition of SWNTs. Carbodiimide chemistry is involved in covalently attaching CNTs to proteins [24] and DNA [25,26]. Carbon nanotubes are functionalized with carboxylic acid and the moiety then undergoes amidation, activated by diimide, to covalently bind proteins, enzymes and antibodies [24–27]. An example in this context is functionalization of SWNT fiber with bovine serum albumin (BSA). Indirect immunochemistry is used to confirm this functionalization in which first a primary antibody is raised against BSA and then a secondary, fluorescently (Fluorescent isothiocyanate FITC)conjugated, antibody is raised against the primary antibody. The complex can then be visualized by fluorescent microscopy. In the same way, amidation reactions can be used to connect amineterminated DNA with the carboxylic acid functional groups of CNTs. In addition, the high specificity of the biotin-avidin/ streptavidin interaction is also employed in designing such modified CNTs. There are many evidences of immobilization of SWNTs by both biotin and streptavidin [28–30]. 3. Effect of carbon nanoparticles on plant growth and development As nanotechnology is expanding rapidly it is necessary to study the interaction of nanomaterials with living organisms. Many studies conducted in this regard have shown that nanoparticles affect various physiological processes such as DNA damage [31,32], alterations of gene expression [33,34] and increase in ROS formation [35,36]. Such responses differ among different plant species [37,38], different varieties [39,40] and different stages of plant development [41]. Interaction of SWCNTs with young seedlings were mainly studied in hydroponics or in SWCNT supplied various culture media. It has been reported that the application of SWCNTs enhance seedling growth in many plant species such as maize (Zea mays) [33], Fig plants (Ficus carica) [42] and tomato (S. lycopersicum) seedlings [43]. A dose dependent response of SWCNTs has been described for pepper (C. annuum), salvia (S. macrosiphon), and tall fescue (F. arundinacea) [44]. The application of SWNTs was done by directly germinating the seeds on media containing SWNT [33]. In other cases, seeds after germination were transferred to hydroponic medium containing MWNTs [37]. Generally, the SWNTs or MWNTs exposure at varied concentrations up to 2000 mg/L was given for 15 days. These studies reported an increase in seedling biomass at 10–30 mg L 1 of SWCNTs, while seedling development was negatively affected at 40 mg L 1 of SWCNTs. MWCNTs affect positively on root and shoot elongation during early growth and seedling development. Such effects have been reported in many plant species such as soybean (G. max), maize (Z. mays) [40], wheat (Triticum aestivum) [45], tomato (S. lycopersicum) [43,46,47], mustard (B. juncea), and black lentil (P. mungo) [48]. The effects of MWCNTs reaches beyond germination and early growth and includes effects on reproductive stage of plant development. It has been reported that there is a doubling of flower setting and yield in tomato after the application of MWCNTs in soil [49]. Such effects were not seen in case of charcoal treated control soils. 4. Modified carbon nanotubes for biosensors Unique structural properties and extremely small size of carbon nanotubes make them the suitable candidate for biosensing. SWNTs are characterized with large surface / volume ratio which
helps them in interaction with several biological molecules. We can also opt for electrical detection as SWNTs are having characteristic electronic structure and good conductance. There occurs a large change in conductance of SWNTs in presence of various small biomolecules [50–53]. SWNT is used as a redox catalyst in the detection of adsorbed cytochrome c, present in mitochondria [53]. The binding of biotin and streptavidin also has been detected electronically by using biotin functionalized SWNTs [50]. This binding reduces the conductance of SWNTs. Such changes in SWNTs upon electronic detection probably originate due to the charge transfer processes at the time of interaction between SWNTs and the analyte. Very minute concentration (1pg/L) of DNA has been detected electronically by using alkaline phosphatase (ALP) enzyme functionalized CNTs [54]. Optical detection of molecules is also possible by using optically transparent conductive SWNT films [55]. Glucose is also selectively and sensitively detected by using CNT nanoelectrode assemblies [56]. The interaction of SWNTs with biological molecules has been used to interpret electrochemical properties of several molecules such as reduced bnicotinamide adenine dinucleotide (NADH) [57], hydrogen peroxide [57,58] and dopamine [59]. In such experiments SWNTs were at par with that of conventional carbon electrodes. Further modifications and fabrications of CNTs were proposed for their more widespread usage. 5. Carbon nanotubes as molecular carriers The structural properties of CNTs [60,61] makes them preferred vectors for targeting molecular probes, such as proteins and DNA, into mammalian cells. Binding of CNTs with several biological molecules such as proteins and DNA helps them in this context. Several proteins such as streptavidin interact with MWNTs [62] and DNA molecules can also get adsorbed on the surface of MWNTs [62–64]. Similarly, cytochrome c, b-Lactase I, and other small protein molecules can be introduced within the cavity of CNTs [65]. Nano-pills are designed in this manner, in which a small molecule is inserted into the interior cavity of CNTs with one end sealed and the other one open, which is then resealed. It appears a convenient way to deliver a drug placed in the interior cavity of nano-pill compared to bound on the outside surface of CNTs. A demonstration was made recently to show the possibility of using SWNTs for intracellular drug delivery [60,61]. A fluorescent probe, FITC was attached with SWNT to allow its tracking [60]. Such SWNTs were then exposed with murine and human fibroblast cell lines and SWNT-FITC start accumulating within the cells. In similar fashion, SWNTs-streptavidin accumulate inside human T cells, 3T3 fibroblast cell lines, leukemia (H60) cells and Chinese hamster ovary (CHO) [61]. 6. Carbon nanoparticles effects on photosynthesis Effect of nanoparticles on plants and their photosynthesis has been studied by several authors. Chronic and acute effects of NPs on photosynthetic apparatus and its productivity have been reported [66,67]. However, many reports are suggesting positive effects of NPs on photosynthesis, growth and development of various plants [68–72]. CuO nanoparticles are abundantly present in the environment and must be affecting the photosynthesis in plants. In this context, many authors have studied the effects of CuO NPs on photosynthesis [73–75]. In Lactuca sativa, Oryza sativa and Brassica oleracea var capitata, Cu accumulated inside leaves and cause structural damage to chloroplast and stomata, also resulting in lesser number of thylakoids per grana [67,76]. Also, it was observed that the content of chlorophyll and carotenoids decreased in both aquatic (Elodea densa, Lemna gibba, Landoltia
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
N. Majeed et al. / Materials Today: Proceedings xxx (xxxx) xxx
punctata) and terrestrial plants (Oryza sativa, Elsholtzia splendens) [67,73,77–80]. It has also been reported that the concentration of chlorophyll A decrease with applied NPs in a dose dependent manner [67,73,78–80]. Rawat et al. [80] reported a decrease in photosynthesis by 59% and that of stomatal conductance by 38% in Capsicum annuum by Cu ion treatment, but he didn’t observe any change in chlorophyll content after CuO treatment. Huang et al. [81] reported a decrease in chlorophyll content as well as in functionality of PSII upon Ag NPs treatment in aquatic plant Skeletonema costatum. ZnO NPs also decreased stomatal conductance, net photosynthesis and intercellular CO2 concentration in Arabidopsis [83]. 7. Environmental applications of carbon nanoparticle Environmental pollution has been a major global problem. A lot of different types of pollutants are entering the environment every day, so, efficient techniques should be there to get rid of them. But the conventional methods are with low efficiency and the environmental sustainability is at risk if we will rely only on them. Hence, need of the hour is to increase the efficiency of conventional methods and also to introduce new innovative approaches. Because of their great absorption potential due to increased surface area, nanomaterials especially those based on carbon can be a promising approach in this context. Many conventional wastewater managements have used activated charcoal as an adsorbent because of its high surface area. It can adsorb a great variety of different organic and inorganic pollutants, but its rate of adsorption is very low and it is nonspecific and ineffective towards microorganisms. However, these wastewater management strategies can be improved by using carbon-based nanomaterials in place of activated charcoal. Available literature has provided us great many examples where carbon nanomaterials have been used for improving wastewater management systems [84–87]. Literatures also suggest that adsorption capacity of CNTs towards lead [88], copper (III) [89] and microcystins (cyanobacterial toxins) [90] is far higher than that of activated charcoal. Using multiwalled nanotubes phosphorus, nitrogen, herbicides and antibiotics have been sorpted from wastewater [91]. Also, various organic pollutants [92], such as lindane (agricultural insecticide) [93] and persistent polychlorinated biphenyls [94] can be mobilized by using CNTs and fullerenes. Such great advantages of CNMs are due to their mechanical and thermal stability, enormous surface area, high chemical affinity for aromatic compounds [95], and potential antibacterial properties. CNM based filters can also be recycled because contaminants after sorption can then be desorbed from them [96,97]. Some hybrid nanoparticles such as silver-(Ag)-coated CNTs possess antimicrobial activity and can thus be used for disinfection purposes [98]. Carbon based nanomaterials can also be used to asses contamination levels in different environments. Potential and efficient sensors can be developed by using carbon nanomaterials which can detect very minute concentrations of various chemical compounds that are present in different environments. 8. Agricultural applications of carbon-based nanomaterials With increasing world population, the major challenge is to increase the agricultural production using minimum available agricultural land. Nanotechnology can be used as an efficient tool in this context. Fertilizers and growth promoters based on nanomaterials can be used to increase the crop production. [99–101]. Nanofertilizer facilitate higher nutrient use efficiency due to their higher surface area, high solubility in different solvents and small particle size [126]. Several plant protectors [102] are also based on nanomaterials such as herbicides [103] and pesticides [104,105]. Sev-
3
eral nano-encapsulated slow release fertilizers can also be used that can reduce the amount of applied agrochemicals. Plants grown in vitro were treated with carbon coated Fe nanoparticles [106]. Nanotechnology is also delivering precision farming to optimize agricultural practices [106]. A positive impact of carbon nanomaterials on plant growth have been reported in several studies which lead to formation of fertilizers containing carbon nanoparticles. Such fertilizers are more promising in reducing nutrient losses, improving plant nutrient availability and stimulating plant growth. CNM showed definite potential to improve plant health and grain quality [10]. However, effect on grain quality due to CNM application has not been shown yet. Lot of advantages are also associated with smart delivery systems, a technique for delivering agrochemicals. Encapsulated agrochemicals have increased use efficiency as they are more stable and are not degraded easily, lowering the use of applied agrochemicals [107]. Functionalized MWNTs were used to encapsulate fungicides that showed increased toxicity against Alternaria alternate fungi in comparison with non-encapsulated pesticide [104]. Conventionally, fertilizers were applied by broadcasting or by spraying. Such practices are associated with increased nutrient losses because of evaporation and leaching. The solution to this problem is the use of slow release or controlled release fertilizers that can be encapsulated by graphene oxide films [108]. 9. Toxicity Apart from many advantages of CNTs, a lot of questions are rising regarding their use in biology and medicine. One of the important concerns of these questions is regarding their toxicity [109,110]. The effect of CNTs should be tested prior to its commercial use. Many laboratories are already working in this regard and are investigating the toxicological effects of CNTs. There are many evidences suggesting harmful effects of CNTs on human health. Skin exposure can lead to several dermal problems such as oxidative stress and loss of cell viability as in case of cultured human skin cells exposed to SWNTs [111]. There is a good correlation of graphite and carbon materials with increased kerarosis and dermatitis, so such effects of CNTs are quite obvious. Pulmonary toxicity is also associated with SWNTs [112,113] and it is shown in case of rodents where there occurs development of granulomas after exposure to SWNTs. All of these toxicological effects appeared after using high concentrations of CNTs, further investigation is required for appropriate measurements. 10. Carbon nanoparticles in abiotic and biotic stress tolerance Because of the changing environmental conditions, plants are constantly being stressed by several biotic and abiotic factors. Crop growth, development and yield is limited by many abiotic stresses, particularly drought stress [114]. Limitation in water content changes many physiological and molecular aspects in plants such as reduction in photosynthesis and biomass and overproduction of reactive oxygen species (ROS). DNA, proteins and cellular membranes get damaged because of the excessive ROS production [114]. So, it is important and equally necessary to control ROS production and maintain the ROS levels at equilibrium. Many carbon nanoparticles such as fullerene and its derivatives are known to play a key role in abiotic stress tolerance of plants [115,116]. Certain studies have also shown that optimum concentrations of fullerol help plants in combating the harmful effects of osmotic stress [117,118]. Liu et al. (2016) also concluded that in presence of fullerol the concentrations of H2O2 and malondialdehyde (MDA) in maize decreased under PEG treatment. Likewise, in sugar beet, fullerol also helps in combating osmotic stress at concentrations of
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
4
N. Majeed et al. / Materials Today: Proceedings xxx (xxxx) xxx
0.01 and 0.001 nmol mm 2 leaf area by decreasing MDA level [117]. Because of the structural properties of fullerene, spherical cage-like, it can scavenge ROS, which plays a pivotal role in plant abiotic stress tolerance, particularly drought [119]. Several studies have illuminated the role of fullerene and its derivatives as powerful ROS detoxification agents [120,121]. Fullerol has also been noted for antioxidant enzyme activation to prevent oxidative damage to the plants [117]. Some antifungal and antibacterial activities of silver nanoparticles have been reported under greenhouse and field conditions, but the interaction of nanoparticles with plants and soil microflora is unknown [122,123]. Tomato (Solanum lycopersicum Mill.) is an important vegetable crop and contribute largely to economic benefits [124]. But its productivity is decreased by 80% because of early blight, caused by Alternaria solani [124]. Some traditional methods were followed to combat this deadly disease but resistant pathogens are continuously evolving [124,123]. However, use of silver nanoparticles can overcome such problem as it possesses multiple modes of actions by which it is hard for pathogen to acquire resistance [82,123]. External application of carbon nanoparticle resulted in increased chlorophyll content and influenced flowering time without any harmful effects [125]
[3] [4] [5] [6]
[7] [8]
[9] [10]
[11]
[12]
[13]
11. Conclusion [14]
Nanobiotechnology and nano agriculture with the researches including carbon nanomaterials have great perspectives in the advances of animal, plant sciences and agriculture. As the size of carbon nanomaterials is of great significance, they also penetrate the seed coat, plant cell wall and may lead to changes in metabolic functions and ultimately increase biomass and grain or fruit yield. The issues need to be carefully addressed in this field is their phytotoxicity, which appeared in some cases. This can be dealt by managing the concentrations and doses to prevent damage. Despite all these concerns, the future prospects of carbon nanomaterials are promising as a low-cost strategy for increased crop production and abiotic stress tolerance. Credit authorship contribution statement Neelofar Majeed: writing. Kishore C.S. Panigrahi: Supervision. Lala Behari Sukla: Supervision. Riffat John: Supervision. Madhusmita Panigrahy: Conceptualization, Visualization, Funding acquisition, Writing - review & editing.
[15] [16] [17] [18] [19] [20] [21] [22] [23]
[24]
[25]
[26]
Declaration of Competing Interest [27]
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements This work is supported by Department of Science and Technology (DST), Science and Engineering Research Board (SERB), India, Young Scientist Start-up Research Grant, No: YSS/2015/000659 and DST, India, WOS-A Women Scientist Grant No: SR/WOS-A/LS369/2018 awarded to MP. References [1] O. Zaytseva, G. Neumann, Carbon nanomaterials: Production, impact on plant development, agricultural and environmental applications, Chem. Biol. Technol. Agric. 3 (2016) 1–26. [2] M.F. Serag, N. Kaji, M. Tokeshi, Y. Baba, Carbon nanotubes and modern nanoagriculture, in: H. Manzer, H. Mohamed, M. Firoz (Eds.), Nanotechnology
[28]
[29]
[30] [31]
[32] [33]
[34]
and plant sciences, Springer International Publishing, Berlin, 2015, pp. 183– 201. B.S. Sekhon, Nanotechnology in agri-food production: An overview, Nanotechnol. Sci. Appl. 7 (2014) 31–53. A. Husen, K.S. Siddiqi, Carbon and fullerene nanomaterials in plant system, J. Nanobiotechnol. 16 (2014) 1–10. A. Ditta, How helpful is nanotechnology in agriculture?, Adv Nat. Sci. Nanosci. Nanotechnol. 3 (2012) 1–10. S. Mishra, D. Beyer, K. Eimre, et al., Topological frustration induces unconventional magnetism in a nanographene, Nat. Nanotechnol. (2019;) 1748–3395, https://doi.org/10.1038/s41565-019-0577-9. B. Nowack, T.D. Bucheli, Occurrence, behaviour and effects of nanoparticles in the environment, Environ. Pollut. 150 (2007) 5–22. Beatriz Rossi Canuto de Menezes, Karla Faquine Rodrigues, Beatriz Carvalho da Silva Fonseca, Renata Ribas, Thais Larissa do Amaral Montanheiro, Gilmar Thim, Recent advances in the use of carbon nanotubes as smart biomaterials, J. Mater. Chem. B 7 (2019) 1343–1360. Z. Hossain, G. Mustafa, S. Komatsu, Plant responses to nanoparticles stress, Int. J. Mol. Sci. 16 (2015) 26644–26653. A. Mukherjee, S. Majumdar, A.D. Servin, L. Pagano, O.P. Dhankher, J.C. White, Carbon nanomaterials in agriculture: A critical review, Front. Plant. Sci. 7 (2016) 1–16. X. Wang, X. Yang, S. Chen, Q. Li, W. Wang, G.X. Hou Chunjiang, L. Wang, S. Wang, Zinc oxide nanoparticles affect biomass accumulation and photosynthesis in Arabidopsis, Front. Plant Sci. 6 (2016) 1–9. S. García-Sánchez, I. Bernales, S. Cristobal, Early response to nanoparticles in the Arabidopsis transcriptome compromises plant defense and root-hair development through salicylic acid signalling, BMC Genom. 16 (2015) 341– 356. M.S. Dresselhaus, G. Dresselhaus, P. Avouris (Eds.), Carbon Nanotubes: Synthesis, Structures, Properties and Applications. Springer-Verlag Berlin, Heidelberg, 2001. C. Cha, S.R. Shin, N. Annabi, M.R. Dokmeci, A. Khademhosseini, ACS Nano. 7 (2013) 2891–2897. E. Heister, E.W. Brunner, G.R. Dieckmann, I. Jurewicz, B. Dalton, ACS Appl. Mater. Interfaces 5 (2013) 1870–1891. S. Iijima, T. Ichihashi, Single-shell carbon nanotubes of 1-nm diameter, Nature 363 (1993) 603. M.S. Dresselhaus, G. Dresselhaus, P.C. Eklund, Science of Fullerenes and Carbon Nanotubes, Academic, San Diego, 1996. L.C. Qin, X. Zhao, K. Hirahara, Y. Miyamoto, Y. Ando, S. Iijima, The smallest carbon nanotube, Nature 408 (2000) 50. N. Wang, Z.K. Tang, G.D. Li, J.S. Chen, Single-walled 4 A carbon nanotube arrays, Nature 408 (2000) 50. J.W. Mintmire, B.I. Dunlap, C.T. White, Are fullerene tubules metallic?, Phys Rev. Lett. 68 (1992) 631. N. Hamada, S.I. Sawada, A. Oshiyama, New one-dimensional conductors: Graphitic microtubules, Phys. Rev. Lett. 68 (1992) 1579. R. Saito, M. Fujita, G. Dresselhaus, M.S. Dresselhaus, Electronic structure of chiral graphene tubules, Appl. Phys. Lett. 60 (1992) 2204. R.J. Chen, Y. Zhang, D. Wang, H. Dai, Noncovalent sidewall functionalization of single-walled carbon nanotubes for protein immobilization, J. Am. Chem. Soc. 123 (2001) 3838. W. Huang, S. Taylor, K. Fu, Y. Lin, D. Zhang, T.W. Hanks, A.M. Rao, Y.-P. Sun, Attaching proteins to carbon nanotubes via diimide-activated amidation, Nano. Lett. 2 (2002) 311. C. Dwyer, M. Guthold, M. Falvo, S. Washburn, R. Superfine, D. Erie, DNAfunctionalized single-walled carbon nanotubes, Nanotechnology 13 (2002) 601. K.A. Williams, P.T.M. Veenhuizen, B.G. de la Torre, R. Eritja, C. Dekker, Nanotechnology: Carbon nanotubes with DNA recognition, Nature 420 (2002) 761. B.R. Azamian, J.J. Davis, K.S. Coleman, C.B. Bagshaw, M.L.H. Green, Bioelectrochemical single-walled carbon nanotubes, J. Am. Chem. Soc. 124 (2002) 12664. M. Zheng, A. Jagota, E.D. Semke, B.A. Diner, R.S. McLean, S.R. Lustig, R.E. Richardson, N.G. Tassi, DNA assisted dispersion and separation of carbon nanotubes, Nature Mater. 2 (2003) 338. J.N. Wohlstadter, J.L. Wilbur, G.B. Sigal, H.A. Biebuyck, M.A. Billadeau, L. Dong, A.B. Fischer, S.R. Gudibande, S.H. Jameison, J.H. Kenten, J. Leginus, J.K. Leland, R.J. Massey, S.J. Wohlstadter, Carbon nanotube-based biosensor, Adv. Mater. 15 (2003) 1184. K. Keren, R.S. Berman, E. Buchstab, U. Sivan, E. Braun, DNA-templated carbon nanotube field-effect transistor, Science 302 (2003) 1380. M. Ghosh, A. Chakraborty, M. Bandyopadhyay, A. Mukherjee, Multi-walled carbon nanotubes (MWCNT): Induction of DNA damage in plant and mammalian cells, J. Hazard. Mater. 197 (2011) 327–336. D.R. Katti, A. Sharma, S.M. Pradhan, K.S. Katti, Carbon nanotube proximity influences rice DNA, Chem. Phys. 455 (2015) 17–22. S. Yan, L. Zhao, H. Li, Q. Zhang, J. Tan, M. Huang, S. He, L. Li, Single-walled carbon nanotubes selectively influence maize root tissue development accompanied by the change in the related gene expression, J. Hazard Mater. 246–247 (2013) 110–118. M. Ghosh, S. Bhadra, A. Adegoke, M. Bandyopadhyay, A. Mukherjee, MWCNT uptake in Allium cepa root cells induces cytotoxic and genotoxic responses and results in DNA hyper-methylation, Mutat. Res. 774 (2015) 49–58.
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
N. Majeed et al. / Materials Today: Proceedings xxx (xxxx) xxx [35] P. Begum, B. Fugetsu, Phytotoxicity of multi-walled carbon nanotubes on red spinach (Amaranthus tricolor L) and the role of ascorbic acid as an antioxidant, J. Hazard Mater. 243 (2012) 212–222. [36] Q. Liu, X. Zhang, Y. Zhao, J. Lin, C. Shu, C. Wang, X. Fang, Fullerene-induced increase of glycosyl residue on living plant cell wall, Environ. Sci. Technol. 47 (2013) 7490–7498. [37] P. Begum, R. Ikhtiari, B. Fugetsu, M. Matsuoka, T. Akasaka, F. Watari, Phytotoxicity of multi-walled carbon nanotubes assessed by selected plant species in the seedling stage, Appl. Surf. Sci. 262 (2012) 120–124. [38] Cañas JE, Long M, Nations S, Vadan R, Dai L, Luo M, Ambikapathi R, Lee EH, Olszyk D, Effects of functionalized and nonfunctionalized single walled carbon nanotubes on root elongation of select crop species, Environ. Toxicol. Chem. 27 (2008) 1922–1931. [39] D.K. Tiwari, N. Dasgupta-Schubert, L.M. Cendejas, J. Villegas, L. Carreto Montoya, S.E. García, Interfacing carbon nanotubes (CNT) with plants: Enhancement of growth, water and ionic nutrient uptake in maize (Zea mays) and implications for nano agriculture, Appl. Nanosci. 4 (2014) 577– 591. [40] M.H. Lahiani, E. Dervishi, J. Chen, Z. Nima, A. Gaume, A.S. Biris, M.V. Khodakovskaya, Impact of carbon nanotube exposure to seeds of valuable crops, ACS Appl. Mater. Interfaces 5 (2013) 7965–7973. [41] D. Stampoulis, S.K. Sinha, J.C. White, Assay-dependent phytotoxicity of nanoparticles to plants, Environ. Sci. Technol. 43 (2009) 9473–9479. [42] D. Flores, J.S. Chaves, R. Chacón, A. Schmidt, A novel technique using SWCNTs to enhanced development and root growth of fig plants (Ficus carica), in: Nanotechnology 2013. Bio sensors, instruments, medical, environment and energy technical proceedings of the 2013 NSTI Nanotechnology Conference and Expo. Boston: Nano Science and Technology Institute, 2013, pp. 167–170. [43] M.V. Khodakovskaya, K. de Silva, D.A. Nedosekin, E. Dervishi, A.S. Biris, E.V. Shashkov, E.I. Galanzha, V.P. Zharov, Complex genetic, photothermal and photoacoustic analysis of nanoparticle-plant interactions, Proc. Natl. Acad. Sci. 108 (2011) 1028–1033. [44] A. Pourkhaloee, M. Haghighi, M.J. Saharkhiz, H. Jouzi, M.M. Doroodmand, Carbon nanotubes can promote seed germination via seed coat penetration, Seed Technol. 33 (2011) 155–169. [45] X. Wang, H. Han, X. Liu, X. Gu, K. Chen, D. Lu, Multi-walled carbon nanotubes can enhance root elongation of wheat (Triticum aestivum) plants, J. Nanopart. Res. 14 (2012) 841. [46] M. Khodakovskaya, E. Dervishi, M. Mahmood, Y. Xu, Z. Li, F. Watanabe, A.S. Biris, Carbon nanotubes are able to penetrate plant seed coat and dramatically affect seed germination and plant growth, ACS Nano. 3 (2009) 3221–3227. [47] H. Villagarcia, E. Dervishi, K. de Silva, A.S. Biris, M.V. Khodakovskaya, Surface chemistry of carbon nanotubes impacts the growth and expression of water channel protein in tomato plants, Small 8 (2012) 2328–2334. [48] G. Ghodake, Y.D. Seo, D. Park, D.S. Lee, Phytotoxicity of carbon nanotubes assessed by Brassica juncea and Phaseolus mungo, J. Nanoelectron. Optoelectron. 5 (2010) 157–160. [49] M.V. Khodakovskaya, B. Kim, J.N. Kim, M. Alimohammadi, E. Dervishi, T. Mustafa, C.E. Cernigla, Carbon nanotubes as plant growth regulators: Effects on tomato growth, reproductive system, and soil microbial community, Small 9 (2013) 115–123. [50] A. Star, J.C.P. Gabriel, K. Bradley, G. Gruner, Electronic detection of specific protein binding using nanotube FET devices, Nano. Lett. 3 (2003) 459. [51] K. Besteman, J.O. Lee, F.G. Wiertz, H.A. Heering, C. Dekker, Enzyme-coated carbon nanotubes as singlemolecule biosensors, Nano. Lett. 3 (2003) 727. [52] R.J. Chen, S. Bangsaruntip, K.A. Drouvalakis, N.W.S. Kam, M. Shim, Y. Li, W. Kim, P.J. Utz, H. Dai, Noncovalent functionalization of carbon nanotubes for highly specific electronic biosensors, Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 4984. [53] S. Boussaad, N.J. Tao, R. Zhang, T. Hopson, L.A. Nagahara, In situ detection of cytochrome c adsorption with single walled carbon nanotube device, Chem. Commun. (2003) 1502. [54] J. Wang, G. Liu, M.R. Jan, Ultrasensitive electrical biosensing of proteins and DNA: Carbon-nanotube derived amplification of the recognition and transduction events, J. Am. Chem. Soc. 126 (2004) 3010. [55] Z. Wu, Z. Chen, X. Du, J.M. Logan, J. Sippel, M. Nikolou, K. Kamaras, J.R. Reynolds, D.B. Tanner, A.F. Hebard, A.G. Rinzler, Transparent, conductive carbon nanotube films, Science 305 (2004) 1273. [56] Y. Lin, F. Lu, Y. Tu, Z. Ren, Glucose biosensors based on carbon nanotube nanoelectrode ensembles, Nano. Lett. 4 (2004) 191. [57] J. Wang, M. Musameh, Carbon nanotube/Teflon composite electrochemical sensors and biosensors, Anal. Chem. 75 (2003) 2075. [58] J. Wang, M. Musameh, Y. Lin, Solubilization of carbon nanotubes by Nafion toward the preparation of amperometric biosensors, J. Am. Chem. Soc. 125 (2003) 2408. [59] P.J. Britto, S.K.V. Santhaman, P.M. Ajayan, Carbon nanotube electrode for oxidation of dopamine, Bioelectrochem. Bioelectronics 41 (1996) 121. [60] D. Pantarotto, J.-P. Briand, M. Prato, A. Bianco, Translocation of bioactive peptides across cell membranes by carbon nanotubes, Chem. Commun. (2004) 16. [61] N.W.S. Kam, T.C. Jessop, P.A. Wender, H. Dai, Nanotube molecular transporters: Internalization of carbon nanotube-protein conjugates into mammalian cells, J. Am. Chem. Soc. 126 (2004) 6850. [62] F. Balavoine, P. Schultz, C. Richard, V. Mallouh, T.W. Ebbesen, C. Mioskowski, Helical crystallization of proteins on carbon nanotubes: A first step towards the development of new biosensors, Angew. Chem. Int. Ed. 38 (1999) 1912.
5
[63] S.C. Tsang, Z. Guo, Y.K. Chen, M.L.H. Green, H.A.O. Hill, T.W. Hambley, P.J. Sadler, Immobilization of platinated and iodinated oligonucleotides on carbon nanotubes, Angew. Chem. Int. Ed. 36 (1997) 2198. [64] Z. Guo, P.J. Sadler, S.C. Tsang, Immobilization and visualization of DNA and proteins on carbon nanotubes, Adv. Mater. 10 (1998) 701. [65] J.J. Davis, M.L.H. Green, H.A.O. Hill, Y.C. Leung, P.J. Sadler, J. Sloan, A.V. Xavier, S.C. Tsang, The immobilization of proteins in carbon nanotubes, Inorg. Chem. Acta. 272 (1998) 261. [66] S.C. Arruda, A.L. Silva, R.M. Galazzi, R.A. Azevedo, M.A. Arruda, Nanoparticles applied to plant science: a review, Talanta 131 (2015) 693–705. [67] M.V.J. Da Costa, P.K. Sharma, Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa, Photosynthetica 54 (2016) 110–119. [68] F. Hong, J. Zhou, C. Liu, F. Yang, C. Wu, L. Zheng, P. Yang, Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach, Biol. Trace Elem. Res. 105 (2005) 269–279. [69] S. Mingyu, H. Fashui, L. Chao, W. Xiao, L. Xiaoqing, C. Liang, G. Fengqing, L. Zhongrui, Effects of nano-anatase TiO2 on absorption, distribution of light, and photoreduction activities of chloroplast membrane of spinach, Biol. Trace Elem. Res. 118 (2007) 120–130. [70] M.K. Sarmast, H. Salehi, Silver nanoparticles: An influential element in plant nanobiotechnology, Mol. Biotechnol. 58 (2016) 441–449. [71] G.S. Zarate-Cruz, H.A. Zavaleta-Mancera, A. Alarcón, L.F. Jiménez-García, Fitotoxicidad de nanopartículas de ZnO en el helecho acuático Azolla filiculoides Lam, Agrociencia 50 (2016) 677–691. [72] Z. Cao, L. Rossi, C. Stowers, W. Zhang, L. Lombardini, X. Ma, The impact of cerium oxide nanoparticles on the physiology of soybean (Glycine max (L.) Merr.) under different soil moisture conditions, Environ. Sci. Pollut. Control Ser. 25 (2018) 930–939. [73] C.M. Lalau, R. de Almeida Mohedano, É.C. Schmidt, Z.L. Bouzon, L.C. Ouriques, R.W. dos Santos, C.H. Da Costa, D.S. Vicentini, W.G. Matias, Toxicological effects of copper oxide nanoparticles on the growth rate, photosynthetic pigment content, and cell morphology of the duckweed Landoltia punctata, Protoplasma 252 (2014) 221–229. [74] F. Perreault, M. Samadani, D. Dewez, Effect of soluble copper released from copper oxide nanoparticles solubilisation on growth and photosynthetic processes of Lemna gibba L, Nanotoxicology 8 (2014) 374–382. [75] N. Regier, C. Cosio, N. von Moos, V.I. Slaveykova, Effects of copper-oxide nanoparticles, dissolved copper and ultraviolet radiation on copper bioaccumulation, photosynthesis and oxidative stress in the aquatic macrophyte Elodea nuttallii, Chemosphere 128 (2015) 56–61. [76] T. Xiong, C. Dumat, V. Dappe, H. Vezin, E. Schreck, M. Shahid, A. Pieral, S. Sobanska, Copper oxide nanoparticle foliar uptake, phytotoxicity, and consequences for sustainable urban agriculture, Environ. Sci. Technol. 51 (2017) 5242–5251. [77] F. Perreault, A. Oukarroum, L. Pirastru, L. Sirois, W. Gerson Matias, R. Popovic, Evaluation of copper oxide nanoparticles toxicity using chlorophyll fluorescence imaging in Lemna gibba, J. Bot. 763142 (2010). [78] G.F. Nekrasova, O.S. Ushakova, A.E. Ermakov, M.A. Uimin, I.V. Byzov, Effects of copper (II) ions and copper oxide nanoparticles on Elodea densa Planch, Russ. J. Ecol. 42 (2011) 458–463. [79] J. Shi, C. Peng, Y. Yang, J. Yang, H. Zhang, X. Yuan, Y. Chen, T. Hu, Phytotoxicity and accumulation of copper oxide nanoparticles to the Cu-tolerant plant Elsholtzia splendens, Nanotoxicology 8 (2013) 179–188. [80] S. Rawat, V.L. Pullagurala, M. Hernandez-Molina, Y. Sun, G. Niu, J.A. Hernandez-Viezcas, J. Perata-Videa, J.L. Gardea-Torresdey, Impacts of copper oxide nanoparticles on bell pepper (Capsicum annuum L.) plants: A full life cycle study, Environ. Sci. J. Integr. Environ. Res.: Nano 5 (2018) 83–95. [81] J. Huang, J. Cheng, J. Yi, Impact of silver nanoparticles on marine diatom Skeletonema costatum, J. Appl. Toxicol. 36 (2016) 1343–1354. [82] S. Wang, J. Lv, J. Ma, S. Zhang, Cellular internalization and intracellular biotransformation of silver nanoparticles in Chlamydomonas reinhardtii, Nanotoxicology 10 (2016) 1129–1135. [83] R. Das, M.E. Ali, S.B.A. Hamid, S. Ramakrishna, Z.Z. Chowdhury, Carbon nanotube membranes for water purification: A bright future in water desalination, Desalination 336 (2014) 97–109. [84] X. Qu, P.J.J. Alvarez, Q. Li, Applications of nanotechnology in water and wastewater treatment, Water Res. 47 (2013) 3931–3946. [85] X. Liu, M. Wang, S. Zhang, B. Pan, Application potential of carbon nanotubes in water treatment: A review, J. Environ. Sci. (China) 25 (2013) 1263–1280. [86] S.C. Smith, D.F. Rodrigues, Carbon-based nanomaterials for removal of chemical and biological contaminants from water: A review of mechanisms and applications, Carbon 91 (2015) 122–143. [87] Y. Li, S. Wang, J. Wei, X. Zhang, C. Xu, Z. Luan, D. Wu, B. Wei, Lead adsorption on carbon nanotubes, Chem. Phys. Lett. 357 (2002) 263–266. [88] A.B. Dichiara, M.R. Webber, W.R. Gorman, R.E. Rogers, Removal of copper ions from aqueous solutions via adsorption on carbon nanocomposites, ACS Appl. Mater. Interfaces 7 (2015) 15674–15680. [89] H. Yan, A. Gong, H. He, J. Zhou, Y. Wei, L. Lv, Adsorption of microcystins by carbon nanotubes, Chemosphere 62 (2006) 142–148. [90] X. Zheng, Y. Su, Y. Chen, Y. Wei, M. Li, H. Huang, The effects of carbon nanotubes on nitrogen and phosphorus removal from real wastewater in the activated sludge system, RSC Adv. 4 (2014) 45953–45959. [91] A. Mishra, J.H. Clark, Green materials for sustainable water remediation and treatment, Royal Society of Chemistry, Cambridge, 2013.
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618
6
N. Majeed et al. / Materials Today: Proceedings xxx (xxxx) xxx
[92] M. Srivastava, P.C. Abhilash, N. Singh, Remediation of lindane using engineered nanoparticles, J. Biomed. Nanotechnol. 7 (2011) 172–174. [93] L. Wang, J.D. Fortner, L. Hou, C. Zhang, A.T. Kan, M.B. Tomson, W. Chen, Contaminant-mobilizing capability of fullerene nanoparticles (nC60): Effect of solvent-exchange process in nC60 formation, Environ. Toxicol. Chem. 32 (2013) 329–336. [94] J. Yoo, H. Ozawa, T. Fujigaya, N. Nakashima, Evaluation of affinity of molecules for carbon nanotubes, Nanoscale 3 (2011) 2517–2522. [95] W.S. Choi, H.M. Yang, H.Y. Koo, H. Lee, Y.B. Lee, T.S. Bae, I.C. Jeon, Smart microcapsules encapsulating reconfigurable carbon nanotube cores, Adv. Funct. Mater. 20 (2010) 820–825. [96] H. Wang, H. Ma, W. Zheng, D. An, C. Na, Multifunctional and recollectable carbon nanotube ponytails for water purification, ACS Appl. Mater. Interfaces 6 (2014) 9426–9434. [97] J.H. Jung, G.B. Hwang, J.E. Lee, G.N. Bae, Preparation of airborne Ag/CNT hybrid nanoparticles using an aerosol process and their application to antimicrobial air filtration, Langmuir 27 (2011) 10256–10264. [98] C. Parisi, M. Vigani, E. Rodríguez-Cerezo (Eds.), Proceedings of a workshop on ‘‘Nanotechnology for the agricultural sector: From research to the field” (2014) Luxembourg. [99] L.R. Khot, S. Sankaran, J.M. Maja, R. Ehsani, E.W. Schuster, Applications of nanomaterials in agricultural production and crop protection: A review, Crop Prot. 35 (2012) 64–70. [100] J. Hong, J.R. Peralta-Videa, J.L. Gardea-Torresdey, Nanomaterials in agricultural production: Benefits and possible threats?, in: N. Shamim, V.K. Sharma (Eds.), Sustainable nanotechnology and the environment: Advances and achievements, American Chemical Society, Washington, D.C, 2013, pp. 73–90. [101] A. Gogos, K. Knauer, T.D. Bucheli, Nanomaterials in plant protection and fertilization: current state, foreseen applications, and research priorities, J. Agric. Food Chem. 60 (2012) 9781–9792. [102] A. Pereira, R. Grillo, N.F. Mello, A.H. Rosa, L.F. Fraceto, Application of poly (epsilon-caprolactone) nanoparticles containing atrazine herbicide as an alternative technique to control weeds and reduce damage to the environment, J. Hazard. Mater. 268 (2014) 207–215. [103] N. Sarlak, A. Taherifar, F. Salehi, 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 (2014) 4833–4838. [104] R.S. Suresh Kumar, P.J. Shiny, C.H. Anjali, J. Jerobin, K.M. Goshen, S. Magdassi, A. Mukherjee, N. Chandrasekaran, Distinctive effects of nanosized permethrin in the environment, Environ. Sci. Pollut. Res. Int. 20 (2013) 2593–2602. [105] H. Auernhammer, Precision farming—the environmental challenge, Comput. Electron. Agric. 30 (2001) 31–43. [106] P. González-Melendi, R. Fernández-Pacheco, M.J. Coronado, E. Corredor, P.S. Testillano, M.C. Risueño, C. Marquina, M.R. Ibarra, D. Rubiales, Luque A. Pérez-de-, Nanoparticles as smart treatment-delivery systems in plants: Assessment of different techniques of microscopy for their visualization in plant tissues, Ann. Bot. 101 (2008) 187–195. [107] M. Zhang, B. Gao, J. Chen, Y. Li, A.E. Creamer, H. Chen, Slow-release fertilizer encapsulated by graphene oxide films, Chem. Eng. J. 255 (2014) 107–113. [108] Service RF, Nanomaterials show signs of toxicity, Science 300 (2003) 243. [109] Service RF, Nanotoxicology. Nanotechnology grows up, Science 304 (2004) 1732. [110] A.A. Shvedova, V. Castranova, E.R. Kisin, D. Schwegler-Berry, A.R. Murray, V.Z. Gandelsman, A. Maynard, P. Baron, Exposure to carbon nanotube material:
[111]
[112]
[113]
[114]
[115]
[116]
[117]
[118]
[119]
[120]
[121]
[122]
[123]
[124]
[125]
[126]
Assessment of nanotube cytotoxicity using human keratinocyte cells, J. Toxicol. Environ. Health A 66 (2003) 1909. C.W. Lam, J.T. James, R. McCluskey, R.L. Hunter, Pulmonary toxicity of singlewall carbon nanotubes in mice 7 and 90 days after intratracheal instillation, Toxicol. Sci. 77 (2004) 126. D.B. Warheit, B.R. Laurence, K.L. Reed, D.H. Roach, G.A. Reynolds, T.R. Webb, Comparative pulmonary toxicity assessment of single-wall carbon nanotubes in rats, Toxicol. Sci. 77 (2004) 117. S.M. Impa, S. Nadaradjan, S.V.K. Jagadish, Drought stress induced reactive oxygen species and anti-oxidants in plants, in: P. Ahmad, M.N.V. Prasad (Eds.), Abiotic Stress Responses in Plants, Springer, New York, 2011, pp. 131– 147. J.S. Duhan, R. Kumar, N. Kumar, P. Kaur, K. Nehra, S. Duhan, Nanotechnology: the new perspective in precision agriculture, Biotechnol. Rep. 15 (2017) 11– 23. M.N. Khan, M. Mobin, Z.K. Abbas, K.A. AlMutairi, Z.H. Siddiqui, Role of nanomaterials in plants under challenging environments, Plant Physiol. Biochem. 110 (2017) 194–209. M. Borišev, I. Borišev, M. Zˇupunski, D. Arsenov, S. Pajevic´, Zˇ. C´urcˇic´, J. Vasin, A. Djordjevic, Drought impact is alleviated in sugar beets (Beta vulgaris L.) by foliar application of fullerenol nanoparticles, PLoS One 11 (2016) e0166248. G.G. Panova, I.N. Ktitorova, O.V. Skobeleva, N.G. Sinjavina, N.A. Charykov, K.N. Semenov, Impact of polyhydroxy fullerene (fullerol or fullerenol) on growth and biophysical characteristics of barley seedlings in favourable and stressful conditions, Plant Growth Regul. 79 (2016) 309–317. A. Trpkovic, B. Todororic-Markovic, V. Trajkovic, Toxicity of pristine versus functionalized fullerenes: mechanisms of cell damage and the role of oxidative stress, Arch. Toxicol. 86 (2012) 1809–1827. H. Wei, E. Wang, Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes, Chem. Soc. Rev. 42 (2011) 6060–6093. M.J. Akhtar, M. Ahamed, H.A. Alhadlaq, A. Alshamsan, Mechanism of ROS scavenging and antioxidant signalling by redox metallic and fullerene nanomaterials: Potential implications in ROS associated degenerative disorders, Biochim. Biophys. Acta 1851 (2017) 802–813. A. Mishra, M. Kumari, S. Pandey, V. Chaudhry, K.C. Gupta, C.S. Nautiyal, Biocatalytic and antimicrobial activities of gold nanoparticles synthesized by Trichoderma sp, Bioresour. Technol. 166 (2014) 235–242. I. Ocsoy, M.L. Paret, M.A. Ocsoy, S. Kunwar, T. Chen, M. You, W. Tan, Nanotechnology in plant disease management: DNA-directed silver nanoparticles on graphene oxide as an antibacterial against Xanthomonas perforans, ACS Nano. 7 (10) (2013) 8972–8980. N. Khan, A. Mishra, C.S. Nautiyal, Paenibacillus lentimorbus B-30488r controls early blight disease in tomato by inducing host resistance associated gene expression and inhibiting Alternaria solani, Biol. Control 62 (2012) 65–74. R. Dixit, L. Agarwal, S. Gupta, M. Kumar, S. Yadav, P.S. Chauhan, C.S. Nautiyal, Southern blight disease of tomato control by 1-aminocyclopropane-1carboxylate (ACC) deaminase producing Paenibacillus lentimorbus B-30488, Plant Signal. Behav. 11 (2) (2016) e1113363. A. Kumar, A. Singh, M. Panigrahy, P.K. Sahoo, K.C. Panigrahi, Carbon nanoparticle influences photomorphogenesis and flowering time in Arabidopsis thaliana, Plant Cell Rep. 37 (6) (2018) 901–912. N. Mahanta, A. Dambale, M. Rajkhowa, Nutrient use efficiency through Nano fertilizers, Int. J. Chem. Studies 7 (3) (2019) 2839–2842.
Please cite this article as: N. Majeed, K. C. S. Panigrahi, L. B. Sukla et al., Application of carbon nanomaterials in plant biotechnology, Materials Today: Proceedings, https://doi.org/10.1016/j.matpr.2020.01.618