Carbon nanomaterials: production, impact on plant development, agricultural and environmental applications
© The Author(s). 2016
Received: 23 December 2015
Accepted: 26 April 2016
Published: 19 July 2016
KeywordsCarbon-based nanomaterials Carbon nanotubes Fullerenes Graphene Germination Plant development Agricultural application
Some chemical elements are able to compose a range of different molecular structures from the same type of atoms—a unique feature known as “allotropy”. Different chemical and physical properties of those materials are determined by the structural geometry of the atoms and the type of chemical bounds within the molecules. In this context, carbon is one of the most interesting elements, with the ability to form a wide range of structures, frequently with fundamentally different properties. Classical examples of carbon allotropes comprise “hard” diamond and “soft” graphite used in science and technology and in a wide range of products, including consumer goods in various areas of human activity .
The list of known carbon allotropes has expanded during the last decades of the 20th century after the discovery of several new low-dimensional carbon forms. The novel materials comprised carbon nanotubes (CNTs), fullerenes and graphene and attracted high interest from science and industry, since these materials exhibited a wide range of outstanding and novel features as promising materials for numerous application fields. Based on these properties, they were repeatedly termed as “wonder materials” in the scientific literature [2–5].
Natural carbon-based nanoparticles exist only in negligible quantities, and the overwhelming majority are engineered, or artificially synthesized. Therefore, their availability does not depend on natural reserves (such as diamonds), and theoretically production can be performed in unlimited quantities as long as raw materials for synthesis are available. According to latest forecasts, a constant increase of production volumes is expected during the next decade [6, 7]. However, despite the fact that carbon-based nanomaterials promote industrial progress there are concerns about a potential release into the environment and interactions of released nanomaterials with living organisms and incorporation into food chains with yet unknown consequences.
Production and potential applications, with special focus on the environmental and agricultural sectors, and the significance for the improvement and development of novel, efficient products and technologies;
Potential impact on living organisms with a special focus on plants, as a fundamental component of food chains in natural and agricultural ecosystems, where increased input of carbon nanomaterials can be expected as a consequence of intentional use in agricultural and environmental applications or by accidental release as unintended contamination.
Classification of carbon-based nanomaterials
For the reasons specified above, carbon can exist in a range of different molecular forms, composed by the same type of atoms but due to different structures, possessing different properties. These forms are termed as “allotropes” or “allotropic modifications” of a certain chemical element. Until recently, only two natural carbon allotropes were known: diamond and graphite. Meanwhile, various new allotropic forms have been described, including carbon nanomaterials. In general, nanomaterials are defined as materials containing particles with at least one dimension between 1 and 100 nm in size . All nanomaterials composed of carbon atoms are termed as carbon-based or carbon nanomaterials. Classification of carbon-based nanomaterials is most commonly performed according to their geometrical structure. Carbon nanostructures include particles which can be tube-shaped, horn-shaped, spherical or ellipsoidal. Nanoparticles having the shape of tubes are termed as carbon nanotubes; horn-shaped particles are nanohorns and spheres or ellipsoids belong to the group of fullerenes. In the meantime, carbon nanomaterials have numerous technical applications including micro- and nanoelectronics, gas storage, production of conductive plastics, composites, displays, antifouling paints, textiles, batteries with improved durability, gas biosensors and others [9–11].
Fullerenes are an allotropic modification of carbon, often termed as a molecular form of carbon, or carbon molecules. Fullerenes were discovered in 1985 by H.W. Kroto, R.F. Curl and R.E. Smalley  who were later awarded with the nobel prize for chemistry in 1996. The fullerene family includes a number of atomic C n clusters (n > 20), composed of carbon atoms on a spherical surface. Carbon atoms are usually located on the surface of the sphere at the vertices of pentagons and hexagons. In fullerenes, carbon atoms are usually present in the sp2-hybrid form and linked together by covalent bonds. Fullerene C60 is the most common and best-investigated fullerene. The spherical molecule is highly symmetric and consists of 60 carbon atoms, located at the vertices of twenty hexagons and twelve pentagons (Fig. 1c). The diameter of fullerene C60 is 0.7 nm .
Carbon nanotubes (CNTs)
Among other carbon-based nanomaterials, CNTs are one of the carbon allotropes with exceptional properties suitable for technical applications. They were discovered in 1991 by the Japanese researcher S. Iijima. Carbon nanotubes are characterized by cylindrical structures with a diameter of several nanometers, consisting of rolled graphene sheets (Fig. 1d). Carbon nanotubes may vary in length, diameter, chirality (symmetry of the rolled graphite sheet) and the number of layers. According to their structure, CNTs may be classified into two main groups: single-walled nanotubes (SWCNTs) and multi-walled nanotubes (MWCNTs). Some researchers additionally isolate double-walled carbon nanotubes (DWCNTs) as a separate class of CNTs. Generally SWCNTs have a diameter around 1–3 nm and a length of a few micrometers. Multi-walled CNTs have a diameter of 5–40 nm and a length around 10 μm. However, recently synthesis of CNTs with a length of even 550 mm has been reported . The structure of CNTs leads to exceptional properties with a unique combination of rigidity, strength and elasticity compared with other fibrous materials. For instance, CNTs exhibit considerably higher aspect ratios (length to diameter ratios) than other materials, and larger aspect ratios for SWCNTs as compared with MWCNTs due to their smaller diameter. Additionally, CNTs show high thermal and electrical conductivity compared to other conductive materials. Electrical properties of SWCNTs depend on their chirality or hexagon orientation with respect to the tube axis. Accordingly, SWCNTs are classified into three sub-classes: (i) armchair (electrical conductivity > copper), (ii) zigzag (semi-conductive properties) and (iii) chiral (semi-conductive properties) (Fig. 1e). By contrast, MWCNTs consisting of multiple carbon layers, frequently with variable chirality, can exhibit extraordinary mechanical properties instead of outstanding electrical characteristics.
Graphene is a two-dimensional allotropic form of carbon, formed by single layers of carbon atoms (Fig. 1f). In graphene, carbon atoms exhibit sp2-hybridization connected by σ- and π-bonds in a two-dimensional hexagonal crystal lattice with a distance of 0.142 nm between neighboring atoms of carbon hexagons. Graphene also represents a structural element of some other carbon allotropes, such as graphite, carbon nanotubes and fullerenes.
Theoretical studies on graphene began a long time before the real material samples were obtained. The Canadian theoretical physicist P. R. Wallace first explored the theory of graphene in 1947, while the first graphene samples were described 57 years later (in 2004) by A. Geim (Dutch-British physicist) and K. Novoselov (Russian-British physicist), awarded with a nobel prize in 2010.
Despite the long history of theoretical investigation, the fact that the real material has been obtained only recently, implies that comprehensive studies on the properties of graphene are still ongoing. Graphene has many unique physical properties, such as extremely high mechanical rigidity and a high thermal stability. Also the electric properties of this carbon allotrope are fundamentally different from the properties of three-dimensional materials.
Synthesis of carbon-based nanomaterials
Industrial synthesis of carbon-based nanomaterials
Fullerenes Since the discovery of carbon-based nanomaterials, their outstanding properties have been intensively studied and different methods for synthesis have been developed. The basic components for carbon nanomaterial production are carbon vapors. Fullerenes were produced for the first time by W. Krätschmer and D.R. Huffman in 1990 by evaporation of graphite electrodes in a helium atmosphere [15, 16]. Later, a reactor was modified by establishing an electric arc between two graphite electrodes. The resulting soot condenses on the cold surface of the reactor, and is collected and processed in boiling toluene, benzene, xylene, or other organic solvents. After evaporation of the solvents a black condensate is formed, containing about 10–15 % of C60 and C70 fullerenes, as well as small amounts of higher fullerenes. Depending on the synthesis parameters, the ratio between the C60 and C70 fullerenes varies, but typically C60 represents the dominant fraction. The described arc-discharge method belongs to the large family of plasma methods which are most popular and commonly used compared to other techniques . However, the practical use of fullerenes is limited due to high costs and the low productivity of the methods currently available for their synthesis.
Carbon nanotubes Arc discharge, laser ablation and chemical vapor deposition (CVD) are basic methods for CNT synthesis . Currently, one of the most investigated and commonly used techniques for CNT production is CVD . In contrast to two other methods (arc discharge and laser ablation), CVD synthesis requires simpler equipment and milder conditions in terms of temperature and pressure, making it more suitable for the large-scale production of CNTs . CVD synthesis is based on decomposition of hydrocarbons to carbon, and subsequent synthesis of carbon nanostructures on various substrates containing catalysts on which the nanotubes are growing. Metal-based nanoparticles are frequently used as catalysts and their size strongly correlates with the diameter of nanotubes synthesized on it (0.5–5 nm—for SWCNTs, 8–100 nm—for MWCNTs synthesis). Nickel, cobalt or iron nanoparticles are usually acting as catalysts for the synthesis of SWCNTs and MWCNTs.
Industrial applications of CNTs and especially of SWCNTs require homogeneous materials with specific properties. However, shifting from well-controlled laboratory conditions to large-scale production frequently results in heterogeneous products, containing impurities of amorphous carbon, carbon fiber, catalyst residuals and other nanoparticles. Therefore, CNT production frequently requires further purification and separation steps, substantially increasing the production costs. One of the major challenges regarding controlled synthesis of SWCNTs is related to difficulties in obtaining small metal-catalyst particles, their equal dispersion on the substrate and prevention of aggregation. For instance, sintering of fine catalysts into larger particles, leads to an increased diameter of SWCNTs or to formation of DWCNTs and MWCNTs.
Chirality, as another structural feature of SWCNTs, also depends on synthesis conditions and the growth mechanism of the nanotubes. Very often, the yielded products represent a mixture of conductive and semi-conductive SWCNTs, requiring further extraction steps to obtain SWCNTs with defined chirality for specific applications. Establishing convenient methods for sorting nanotubes according to their characteristics (diameter, chirality) and eliminating various undesired impurities will significantly contribute to the developmental progress towards improved applications. Another important area of research is synthesis of vertically or horizontally aligned CNTs, which have numerous structural advantages as compared to bundles of agglomerated CNTs. Production of MWCNTs seems to be less complicated and expensive. However, the controlled formation of inner and outer diameters or defined numbers of walls are still major challenges.
Graphene Since graphene sheets were first obtained by Gheim and Novoselov, using mechanical splitting of graphite with adhesive tape , great progress in graphene research has been made, and meanwhile various methods for graphene production are available . These techniques are based on obtaining nanoscale graphene sheets by splitting or cutting materials, such as graphite or nanotubes , using a range of physical or chemical methods. Production of graphene sheets by CVD synthesis or laser ablation methods is also possible. The different methods are able to provide graphene or reduced graphene oxide sheets of different qualities, depending on the requirements of the corresponding applications. Graphene of moderate quality for structural applications can be obtained in large quantities with relatively low production costs. High quality graphene for electronic devices produced in smaller quantities, are usually more expensive. Liquid phase and thermal exfoliation of graphite, CVD synthesis (potentially most cost effective) and synthesis on silicon carbide—are the major methods suitable for mass production of graphene .
Chemical functionalization of carbon-based nanoparticles
A wide variety of carbon-based nanomaterials can be further expanded by so-called chemical functionalization. Very often, nanoparticles are functionalized by linking certain molecules to the nanoparticle surface, in order to modify the physical and chemical properties of the particles , which in turn greatly expands the field of applications [26, 27]. One example for functionalization of carbon-based nanoparticles is an oxidation of CNTs. This process comprises an ultrasonic treatment of nanotubes in a mixture of acids, leading to attachment of carboxylic functional groups (–COOH) on the sidewalls of the nanotubes (Fig. 1g). Oxidized CNTs acquire solubility in aqueous solutions, but retain their mechanical and electrical properties. Moreover, carboxylic groups attached to the nanotube surface can serve as sites for further functionalization. There are also examples of functionalized fullerenes and graphene.
Naturally occurring carbon nanomaterials
Apart from engineered nanomaterials, naturally occurring carbon-based nanoparticles have also been identified [28, 29]. Velasco-Santos et al.  reported the presence of carbon nanotubes in a coal-petroleum mix. For SWCNT synthesis using the CVD method, Su and Chen  and Mracek et al.  used volcanic lava as a substrate and catalyst, containing particles of metal oxides. The authors speculated that this process may provide evidence for a possible formation of nanotubes under natural conditions when the temperature rises extremely high e.g. during volcano eruptions. Beside carbon nanotubes, there is also evidence for the occurrence of fullerenes in geological materials. Fullerenes have been detected in the natural mineral shungit from Karelia in low concentrations (2 % w/w) [32–35] and also in meteorite samples of cosmic origin .
Interestingly, the spherical structure of fullerenes seems to be not only restricted to carbon nanomaterials. Recently, fullerene-like structures have been described in pollen grains of Chinese hibiscus (Hibiscus rosa-sinensis), with putative functions for mechanical stability and adaptive properties important for the pollination process .
Potential applications of carbon-based nanomaterials
Environmental applications of carbon-based nanomaterials
Environmental pollution is one of the major global challenges since pollutants of different nature contaminate urban and agricultural areas. In order to improve pollutant remediation strategies for environmental sustainability, there is a need to increase the efficiency of conventional methods or to introduce innovative approaches. In this context, nanotechnology, and especially carbon-based nanomaterials can greatly contribute because they possess an enormous absorption potential due to their high surface area.
Activated carbon (AC) has been widely used as a sorbent for conventional wastewater treatment due to its large surface area and ability to adsorb a broad spectrum of organic and inorganic contaminants. However, AC has slow adsorption kinetics; it is a nonspecific adsorbent and its effectiveness against microorganisms is low. The presence of solids, oil and grease in wastewater often causes pore blockage in AC. Moreover, AC is frequently removed together with the adsorbed pollutants and therefore, needs to be replaced in regular intervals. In this context, utilization of carbon-based nanomaterials has a promising potential to improve wastewater filtration systems with numerous examples in the available literature [52–55]. It has been reported that the adsorption capacity of CNTs towards microcystins (cyanobacterial toxins) , lead  and copper (III)  was even stronger than that of AC. Multi-walled nanotubes have been also used for sorption of antibiotics , herbicides  or nitrogen and phosphorus in wastewater . On the other hand, fullerenes as well as CNTs exhibit a mobilization potential for various organic pollutants , such as lindane (agricultural insecticide)  and persistent polychlorinated biphenyls . The significant advantages of CNMs comprise their enormous surface area, mechanical and thermal stability, high chemical affinity for aromatic compounds , and potential antibacterial properties (described below). Moreover, contaminants can be desorbed from CNMs, and therefore, filters based on CNMs can be recycled [66, 67]. However, challenges related with high costs of CNM production, difficulties in obtaining of CNTs with uniform size and diameter distribution, uncertainties regarding the leaching potential of CNTs, as well as ecological safety and human health issues are still limitations for commercial applications in wastewater clean-up technologies.
Carbon-based nanomaterials also possess antimicrobial properties, although the mode of action is still under investigation. Some studies suggest possible applications of CNTs for disinfection purposes or antimicrobial surface coatings. Particularly silver-(Ag)-coated CNTs hybrid nanoparticles have shown antimicrobial activity  and the authors suggest that such materials could find their applications in biomedical devices and antibacterial control systems. Al-Hakami et al.  described a method of water disinfection based on interactions of functionalized CNTs with microwaves. According to the authors, CNTs, functionalized with the aliphatic alcohol 1-octadecanol (C18H38O) had outstanding antimicrobial properties since the long carbon chains contributed to a better absorption of the microwaves by CNTs. Water purification technologies employing CNTs, including water disinfection have been described in the comprehensive reviews of Upadhyayula et al.  and Das et al. . Studies on antibacterial and antifungal properties of graphene, CNTs and fullerenes, and their applications in agriculture are summarized in “Antifungal and antibacterial agents” section below.
Additionally, not only removal of pollutants from different environmental compartments, but also monitoring of contamination levels has considerable importance. Carbon-based nanomaterials can be employed for the development of novel, very efficient biochemical sensors for detecting of very low concentrations of chemical compounds in different environments. These sensors also exhibit application potential in agriculture and are discussed in more detail in “Sensing systems and precision agriculture” section.
Agricultural applications of carbon-based nanomaterials
Increase of crop productivity by use of plant growth promoters and new fertilizers based on nanomaterials;
A general reduction of applied agrochemicals using nanoencapsulated plant protection products and slow-release fertilizers;
Nanotechnologies for optimization of agricultural practices by introducing precision farming .
According to Gogos et al. , 40 % of all contributions of nanotechnology to agriculture will be provided by carbon-based nanomaterials acting as additives as well as active components. The majority of such applications are still in the developmental stage and a selection of promising approaches will be presented in this section.
Plant growth stimulators and fertilizers
Influence of carbon-based nanomaterials on seed germination
Type of NPs
Size of NPs
Concentration (mg L−1)
Ø 1–2 nm
L 30 µm
No effect on seed germination
Radish, rape, ryegrass, lettuce, maize, cucumber
Ø 10–20 nm
L 1–2 µm
No effect on seed germination
Ø 3 ± 4 nm
No effect on seed germination
Ø 13–16 nm
L 1–10 µm
No effect on seed germination
Mustard, black lentil
Ø 110–170 nm
L 5–9 µm
10, 20, 40
No effect on seed germination
Ø 6–13 nm
L 2.5–0 µm
10, 20, 40, 80, 160
No effect on seed germination
Wheat, maize, peanut, garlic bulb
Ø 10–20 nmL 10–30 µm
Barley, maize, soybean
50, 100, 200
Barley, maize, soybean,
25, 50, 100 (spray)
At 25 mg L−1 no effect, at 100 mg L−1 increased germination rate
10, 20, 40
Increased seed moisture content, accelerated germination, improved germination rate
Ø 8 nm
L 30 µm
50, 100, 150
Enhanced germination speed and rate
Basal growth medium
Increased seed water content, germination rate
Tomato, onion, turnip, radish
Ø 8– 15 nm
L > 10 μm
10, 20 and 40
Improved germination of tomato and onion
5, 50, 100, 200
Delayed germination with the increasing of graphene concentration
Graphene, GO, graphene ribbon
Graphene and GO: inhibited germination, graphene ribbon: enhanced germination
Nanoencapsulation and smart delivery systems
Development of smart delivery systems—a promising technique for target delivery of agrochemicals—has numerous potential advantages. Encapsulated agrochemicals exhibit improved stability, and protection from degradation as a perspective to reduce the amount of applied agrochemicals and increase their use efficiency . In this context Sarlak et al.  demonstrated that fungicides, encapsulated in MWCNTs functionalized with citric acid, had a higher toxicity against Alternaria alternata fungi compared to the not encapsulated bulk pesticide.
A still common practice of fertilizer application in conventional agriculture is broadcasting or foliar application by spraying. These techniques are often associated with considerable losses of nutrients by leaching or evaporation. So-called slow release or controlled release fertilizers are employed for adaptation of the nutrient supply to the current demand of the plant, avoiding temporal overdoses, extending the time of function, and counteracting losses by leaching. Slow release fertilizers can be encapsulated by graphene oxide films . Even for very soil-mobile nutrients, such as potassium nitrate, encapsulation by graphene oxide considerably prolongs the process of fertilizer release and large-scale production of encapsulates seems to be possible at a relatively low cost .
Smart delivery systems of agrochemicals and organic molecules including transport of DNA molecules or oligonucleotides into plant cells are potential applications of nano-biotechnology, based on the ability of carbon nanomaterials to penetrate through cell walls and membranes of plant cells . A recently published study reported a possibility to deliver SWCNTs and ceria nanoparticles into isolated chloroplasts. These nanoparticles, passively penetrating through the chloroplast membrane via diffusion were able to influence photosynthetic activity by supplying electrons into the photosynthetic electron transport chain . Apart from agricultural applications, CNTs are also being investigated as molecular transporters also in animal cells for medical purpose [84–90]. In parallel, much attention is paid to research and development of techniques for directed modifications of CNTs to prevent cytotoxicity. Some of these approaches are summarized in the review by Jain et al. .
Antifungal and antibacterial agents
Due to antifungal properties, carbon-based nanomaterials are promising materials for the development of novel fungicides . Among the various carbon nanomaterials including nanotubes, fullerenes and graphene oxide, tested against two plant pathogenic fungi Fusarium graminearum and F. poae, SWCNTs showed the strongest antifungal activity. By contrast, fullerenes and activated carbon used in the assay were largely ineffective. According to Wang et al. , an important prerequisite determining the antifungal activity seems to be a tight contact of the nanoparticles with the fungal spores, which induces plasmolysis, associated with reduced water content and growth arrest.
In other studies, anti-microbial activity of graphene oxide (GO) has been attributed to induction of microbial membrane damage, disturbance of the membrane potential  and electron transport , as well as oxidative stress by increased production of reactive oxygen species (ROS) [95, 96]. Antibacterial properties of graphene oxide were also found to be dependent on the size of the GO sheets: larger GO sheets, wrapping bacterial cells, can effectively isolate bacteria from their environment, and show stronger antibacterial activity as compared to small GO sheets . Also the basal plane of GO sheets seems to play a key role in this mechanism  since masking of the basal plane by non-covalent protein adsorption with bovine serum albumin resulted in loss of antibacterial activity . Accordingly, sticking the layers of GO sheets closely together  to avoid the interactions of bacteria with the sharp edges of single GO sheets, while keeping contact of the bacteria with the basal plane, retained the antimicrobial activity. These findings underline the importance of the basal plane as a central structural element mediating antibacterial properties of GO.
The CNMs with antifungal and antimicrobial properties described above received considerable attention due to potential applications as novel fungicides and disinfection agents suitable for agricultural purposes (e.g. in plant protection). However, due to the largely unknown behavior of CNMs in complex environmental matrices, it is quite difficult to predict to what extent the described in vitro properties will be manifested when the CNMs or CNM-containing products are released into the environment. This requires much more detailed investigations of the antifungal and antibacterial properties of CNMs, considering a wider range of crops and pathogens to be investigated under real field conditions . On the other hand, for environmental risk assessment, the potential impact of CNMs on non-target organisms also requires comprehensive evaluation before commercialization of novel agrochemicals.
Sensing systems and precision agriculture
Carbon-based nanomaterials with novel chemical, physical and mechanical properties are employed to develop highly sensitive sensors and diagnostic devices for numerous agricultural and environmental applications. Nanosensors exhibit numerous operating principles  but a common mode of action is conversion of physicochemical properties into signals. The high sensitivity of these devices is determined by the nanoscale size of the sensing elements, such as carbon nanotubes. Therefore, a few molecules are frequently sufficient to influence the electrical properties (chemical to electrical transduction) of the nanoparticles. Moreover, the great surface area of carbon-based nanomaterials provides large spaces for interactions with the sensed molecules.
Development of novel technologies based on nanomaterials which can be successfully used for easy, rapid and highly sensitive chemical analysis, is documented in numerous studies. A graphene-based sensor for the detection of cadmium contaminations in water, which works effectively at concentration levels of 0.25 μg L−1 has been described by Wu et al. . A highly sensitive sensor for the determination of nickel, not only in environmental samples but also in food, is based on modified nanotubes and has a detection limit of 4.9 ng L−1 . CNT-based gas sensors for ammonia detection can be used for trace gas measurements . Sensors to detect pesticides, herbicides and their metabolites in environmental samples have been developed based on modified MWCNTs [104, 105] or on GO . Moreover, nanosensors have been employed for monitoring soil moisture .
Nanosensor-based monitoring systems for crop health have also been described. In this context, CNT sensors were successfully used for in vivo monitoring of ROS formation in plant tissues as stress indicators . An electronic device for real-time sensing of toxic gases based on CNTs, which could be placed onto insects or plants  can be applied in remote sensing systems for plant diseases. Covering a field site with multiple sensors can provide a full picture of the spatial distribution of disease severity at a field scale and allows the detection of hot spots, requiring a special treatment, as a significant contribution to reducing the input of agrochemicals.
However, currently the majority of nanosensors are still in the product development stage and large-scale production has not yet been established due to a number of restrictions. First of all, on the way from the lab to the market scale, long-term testing is required for calibration and validation of the developed devices . Currently, only a limited number of studies reported measurements of real samples under natural conditions . Challenges related with up-scaling production techniques and the high costs of the materials and equipment required for the production of nanosensors have been claimed by various authors [111, 112]. Major challenges still remain around the issues of safety, health aspects and risk assessment, requiring an entire life cycle analysis of a product . However, despite the listed issues, several authors are expecting intensive commercialization of nanosensor technologies  in the near future, also confirmed by recently issued market forecasts [114, 115].
Impact of carbon-based nanomaterials on plants
Influence of carbon-based nanomaterials on plant growth and development
Type of nanomaterial
Size of NPs
Ø 3 nm
28, 160, 900, 5000 mg L−1
Ø 3 nm
28, 160, 900, 5000 mg L−1
Enhanced root elongation
Ø 1–2 nm
L 5–30 µm
5–250 mg L−1
Cell aggregation, chromatin condensation, plasma membrane deposition, H2O2 accumulation.
Ø 3 nm
28, 160, 900, 5000 mg L−1
Inhibited root elongation
Ø 0.86–2.22 nm
50 mg L−1
Increased fresh and dry plant biomass
Ø 6–9 nm
L 5 µm
5, 10, 20, 40, 60 mg L−1
Nutrient agar medium
At 20 mg L−1 increased dry weight and Ca, Fe concentration. At high dose: depressed growth
Barley, maize, soybean
50, 100, 200 mg L−1
Increased leave length and biomass in maize, increased root length in soybean
10, 20, 40 mg L−1
Increased stem length, biomass
Ø 42.2 nm
1000 mg L−1
No impact on development; uptake by roots and translocation to leaves
Ø 10–150 nm
1000 mg L−1
No effect on development
Ø 9.5 nm
L 1.5 µm
10, 60, 100, 600 mg L−1
Decreased cell dry weight, cell viabilities, cell chlorophyll content, and superoxide dismutase activities
Ø < 50 nm
25, 50, 100, 250, 500 mg L−1
Increased callus growth
Wheat, maize, peanut, garlic
Ø 10–20 nm
L 10–30 µm
20, 50 mg L−1
Root and shoot elongation
Ø 25 nm
MS medium,later soil
Enhanced growth, flower and fruit number formation
Ø 10–35 nm
L 6 µm
50, 100, 200 mg L−1
Increased total biomass, up-regulation of stress-related genes; penetration into roots, leaves, and fruits
Ø 11 nm
L > 1 µm
125–1000 mg L−1
Modified Hoagland medium
Inhibited root and shoot elongation, reduced weight, leaf area, enhanced electrolyte damage and ROS
Ø 7−15 nm
L 0.5−200 µm
5, 20, 50 mg L−1
Filter sterilized water
5 and 10 mg L−1
Filter sterilized water
Cucumber, rice, lettuce, red spinach
Ø 13 nm
L > 1 µm
20, 200, 1000, 2000 mg L−1
Modified Hoagland medium (hydroponic)
Decreased shoot length, biomass, increased membrane leakage
Ø 13–16 nm
L 1–10 µm
1000 mg L−1
Decreased cell density
Ø < 10 nm
L 5–15 µm
20 mg L−1
Cell culture MS medium
Decreased cell viability, increased ROS
10–50 mg L−1
Stimulated growth of maize, inhibited growth of soybean; uptake and translocation
Ø 6–13 nm
L 2.5–20 µm
10, 20, 40, 80, 160 mg L−1
Increased cell elongation in roots, root length, biomass
Ø 10–50 nm
6.0 mg L−1
Increased growth rate
25,75, 125 mg pot−1
Increased plant height, leaf area, dry matter accumulation, chlorophyll, soluble protein, N and K contents
Basal salt medium
Reduced photosynthesis, transpiration, carbon gain, chlorophyll fluorescence
MWCNTs Fullerene C70
Ø 5–40 nm
L 0.5–2 µm
2.5–800 mg L−1
MWCNTs: insignificant uptake C70: uptake, accumulation and translocation within the plant
Sand substrate and hydroponic
Uptake by plants and transportation
1670 mg kg−1 soil
Sandy loam soil with DDT residues
Increased shoot mass and decreased root mass
Green algae, arabidopsis
0.001–20 mg L−1 1–200 mg L−1
Increased the algal culture density; enhanced growth in Arabidopsis
0.943, 4.72, 9.43, 10.88, 47.2 nM
Increased fruit length, number, weight and phytomedicines content
5–20 mg L−1
Increased biomass, nitrogen, potassium, calcium and magnesium content
5–10, 10–20 mg L−1
Promoted root growth, increased shoot and root biomass and improved potassium content
400, 800 mg L−1
Decreased levels of H2O2, and lipid and protein oxidation, and enhanced H2O2 decomposing enzymes; increased proline and seed-relative water content
400, 800 mg L−1
Increased ratio of the reduced glutathione (GSH)-to oxidized GSH, reduced GSH pool and GSH reductase activity, decreased activities of GSH-metabolizing enzymes
100, 200, 1600 mg L−1
Reduced growth, reduced activity of H2O2-decomposing enzymes; increased levels of electrolyte leakage, H2O2, and lipid and protein oxidation
100, 200, 1600 mg L−1
Decreased (GSH) redox ratio, reduced GSH pool, elevated activities of GSH-regenerating and GSH-metabolizing enzymes
0.1–10 mg L−1
GO amplifies phytotoxicity of arsenic (As)
Cabbage, tomato, red spinach, lettuce
500, 1000, 2000 mg L−1
Modified Hoagland medium
Inhibited plant growth and biomass
40 mg L−1
Longer roots and shoots, but reduced biomass
5, 50, 100, 200 mg L−1
At 5 mg L−1: improved seedling growth, at higher concentration: inhibited growth
The high variability of nanomaterials in terms of chemical composition, size and shape, surface structure, solubility, aggregation and application modes are also factors most likely contributing to the heterogeneity of plant responses reported in the literature [129, 130]. Knowledge of the special structural features of nanomaterials determining the adverse effects on living organisms is a pre-requisite for the so called “safe-by-design” approach for a directed design of nanomaterials without negative environmental side effects [131–133].
Impact of fullerenes on plants
Germination Only a limited number of studies report effects of fullerenes or their derivatives on seed germination. For instance, fullerenes applied in aqueous suspensions (10–500 mg L−1) or by soil incorporation (1000 mg kg−1) did not affect seed germination of wheat (Triticum aestivum), rice (Oryza sativa), cucumber (Cucumis sativus) and green gram (Vigna radiata) . The authors explained the absence of fullerene effects on seed germination as a consequence of selective seed coat permeability. Similarly, Liu et al.  reported that fullerene malonic acid derivative (FMAD, C70(C(COOH)2)4-8) did not affected the germination of Arabidopsis (Arabidopsis thaliana) seeds most likely due to protective effects of seed coat.
Plant growth and development The majority of studies focusing on the effects of fullerenes on terrestrial and aquatic plants, report negative or no effects of fullerene C60 on plant growth and development. Tao et al.  found inhibition of photosynthesis and Mg uptake of phytoplankton exposed to fullerenes C60. Similarly, fullerenes inhibited growth and chlorophyll accumulation in duckweed (Lemna gibba) .
In a study of terrestrial plants with fullerene soil amendments used for immobilization of pesticide residues, reduced biomass accumulation was reported at higher fullerene concentrations (500–5000 mg kg−1 soil): up to 40 % reduction for soybean (Glycine max), 44 % for maize (Zea mays) and 10 % for tomato (Solanum lycopersicum) , while inhibition of root growth was detected in pumpkin (Cucurbita pepo) .
Several studies have demonstrated a potential of fullerenes to increase accumulation of organic contaminants in plants. Accordingly, in cottonwood (Populus deltoides) cuttings cultivated in hydroponics, accumulation of industrial solvent trichloroethylene added to the growth medium was increased by 80 % in the presence of fullerene C60 (15 mg L−1) . The authors speculated that a fullerene-trichloroethylene complex, formed in the nutrient solution was taken up by the plants. In another study  carried out in a vermiculite substrate, fullerene C60 (40 mg pot−1) increased the total plant content of the DDT metabolite dichlorodiphenyldichloroethylene (DDE) in zucchini (C. pepo), soybean (G. max) and tomato (S. lycopersicum) by approximately 30, 45 and 62 %, respectively. Although fullerenes C60 were detected mainly in the root tissue and at the root surface, a conjugated uptake of C60 together with the contaminant was postulated by the authors. Analyses of plant tissues revealed no membrane disruptions, suggesting that the contaminants did not enter the plant simply via damaged tissues. Genotypic differences in the uptake rates of DTT metabolites in the presence of fullerene C60 have been reported in plants grown on a vermiculite-soil mixture  with inhibitory effects recorded for maize (Z. mays) and tomato (S. lycopersicum) but stimulation in soybean (G. max) and zucchini (C. pepo). Interestingly, in a study conducted on a loamy field soil, containing naturally aged DDE residues, no impact of fullerene C60 amendments on contaminant uptake by pumpkin (C. pepo) was detectable . These findings suggest that plant availability of fullerenes and/or organic contaminants depends not only on substrate properties, but also on differences between plant species.
By contrast, fullerols, as OH-functionalized fullerenes, frequently exerted positive effects on plant growth, such as stimulation of cell divisions in green algae cultures of Pseudokirchneriella subcapitata and of hypocotyl growth in Arabidopsis (A. thaliana) . Fullerol seed dressings even increased fruit number, fruit size and final yield by up to 128 % in bitter melon (Momordica charantia), and are also associated with a higher content of bioactive compounds in fruits, such as cucurbitacin-B, lycopene, charantin and inulin . These findings demonstrate perspectives of hydroxyfullerenes to improve crop yields and product quality. However, further investigations on potential food chain contaminations are still necessary, since fullerol residues have been detected in various plant organs including fruits. The exact mechanism behind plant-growth promotion induced by hydroxyfullerenes is not yet clear, but may be at least partially explained by antioxidant properties  connected with the ability of hydroxyfullerenes to accept up to six electrons and distribute them among the aromatic rings, thereby acting as “radical sponges”.
However, not all functionalized fullerenes exhibit stimulatory effects on plant growth. As an example Liu et al.  reported that a water-soluble fullerene-malonic acid derivative (FMAD), C70(C(COOH)2)4-8 added to the growth medium, induced dose-dependent inhibition of root elongation by up to 60 % and deformation of root tips in Arabidopsis (A. thaliana), associated with a disruption of auxin transport in the root tips, aberrations of cell divisions in the root meristematic zone and reduction of intracellular ROS. Growth-inhibitory effects of carboxyfullerenes (C70(C(COOH)2)2-4) have been similarly reported in tobacco (N. tobacum) cell cultures, connected with cell wall deformations and co-induction of oxidative stress . These findings demonstrate that the type of functionalisation is an important determinant for the effects of nanomaterials on plants.
Uptake of fullerenes and fullerols Lin et al.  reported that rice seedlings (O. sativa) grown in hydroponic culture exhibit root uptake of fullerene C70 and translocation to shoots and leaves. The accumulation of C70 was observed in vascular tissues, in surrounding cells and intercellular spaces. Similar to hydroxyfullerenes described above, uptake of fullerenes added to a vermiculite growth substrate was found in root systems of soybean (G. max), tomato (S. lycopersicum) and in both the roots and shoots of zucchini (C. pepo) [141, 146]. Fullerene C60 accumulated mainly in the root tissue, but smaller quantities were detected also in leaves and stems . Uptake of fullerene 14C60 was also reported for radish (Raphanus sativus), grown for 2 weeks in a sand substrate and hydroponic culture, while a rock wool substrate limited the availability of C60 for plant uptake . Although the principal capacity of plant roots to take up fullerenes has been repeatedly demonstrated, unfortunately more detailed studies on plant availability and root uptake under real soil conditions are still lacking [138, 139].
Impact of carbon nanotubes on plants
Compared with fullerenes, many more studies on plant interactions with the various types of carbon nanotubes are available, describing effects on seed germination, early plant growth, cell culture, gene expression and various physiological processes. Concerning toxicity aspects, due to smaller size, SWCNTs seem to be more toxic than MWCNTs, and toxicity is further increased by functionalization of nanotubes . Since CNTs exhibit great tensile strength, mechanical damage of tissues may be induced by piercing effects.
Impact of SWCNTs on plants
Germination A few studies report effects of SWCNTs on germination rate. Stimulation of seed germination in response to SWCNTs treatments (10–40 mg L−1), potentially induced by perforation of the seed coat, has been reported for salvia (Salvia macrosiphon), pepper (Capsicum annuum), and tall fescue (Festuca arundinacea) . Among the tested treatments, the highest germination rates were obtained by applying moderate SWCNT concentrations: e.g.10 mg L−1 SWCNTs for pepper (C. annuum) and 30 mg L−1 of for salvia (S. macrosiphon) and tall fescue (F. arundinacea). However, a similar concentration of SWCNTs (20 mg L−1) did not affect the germination of maize (Z. mays) seeds .
Plant cell culture For SWCNTs added to the growth media of plant cell cultures, positive as well as negative effects have been observed, depending on the applied dosage. In Arabidopsis (A. thaliana) mesophyll cells, low concentrations of SWCNTs (10–50 mg L−1) exerted stimulatory effects on cell growth, while higher concentrations (100 mg L−1) induced the generation of ROS and toxic effects, associated with necrosis and apoptosis . Similar dose-dependent effects including ROS accumulation and programmed cell death (at 25 mg L−1) have been reported for cell cultures of Arabidopsis (A. thaliana) and rice (O. sativa), potentially linked with the small particle size of SWCNTs, since particles of activated carbon did not cause similar damage. . It has been speculated that SWCNTs might penetrate cell walls and cell membranes.
Plant growth and development Effects of SWCNTs have been reported mainly for young seedlings grown in aqueous suspensions or various culture media amended with SWCNTs. Stimulatory effects on early seedling growth have been detected for a range of plant species including fig plants (Ficus carica)  maize (Zea mays)  and tomato (S. lycopersicum) seedlings . A dose-dependent effect of SWCNTs was reported for salvia (S. macrosiphon), pepper (C. annuum) and tall fescue (F. arundinacea) , where 10–30 mg L−1 of SWCNTs increased the formation of seedling biomass, while at 40 mg L−1 SWCNTs exerted negative effects on seedling development. A similar response has been reported for blackberry (Rubus adenotrichos) grown in vitro in a culture medium supplemented with functionalized carboxy-SWCNTs (SWCNTs-COOH) .
However, contradicting effects were observed for short-term applications (24 and 48 h) of SWCNTs functionalized with poly-3-aminobenzenesulfonic acid and non-functionalized SWCNTs in six important crops [cabbage (Brassica oleracea), carrot (Daucus carota), cucumber (C. sativus), lettuce (Lactuca sativa), onion (Allium cepa), and tomato (Solanum lycopersicum)]. Non-functionalized nanotubes inhibited root elongation in tomato (S. lycopersicum) but exerted stimulatory effects on cucumber (C. sativus) and onion (A. cepa). Root elongation in lettuce (L. sativa) was inhibited by functionalized nanotubes, while cabbage (B. oleracea) and carrot (D. carota) were not affected at all . The authors speculated that the variability of the responses may be related (i) with genotypic differences of the test plants and (ii) with differences in seed size, since small-seeded species, such as lettuce (L. sativa), onion (A. cepa), and tomato (S. lycopersicum) appeared to be more sensitive compared with large-seeded species with a lower surface to volume ratio providing a lower surface area for interactions with SWCNTs.
A limited number of studies linked the effects of plant exposure to SWCNTs on morphological traits with modifications at the molecular level. In maize (Z. mays) grown on Murashige and Skoog medium amended 20 mg L−1 SWCNTs, increased formation of seminal roots was associated with increased expression of the respective genes (SLR1, RTCS), while inhibition of root hair growth was reflected by down regulation of root hair-related genes (RTH1, RTH3). Moreover, similar to plants exposed to stress conditions, SWCNTs could increase histone deacetylation , most likely as a response towards SWCNT accumulation in the root cortex.
Uptake of SWCNTs The process of SWCNT penetration into plant cells has been first described in plant cell cultures. Liu et al.  reported intracellular penetration of water-soluble SWCNTs with a length <500 nm in cell cultures of tobacco (N. tobacum). The nanotubes showed the ability to penetrate both the hard cell wall, and the cell membrane, mediated most probably by means of fluidic-phase endocytosis, since nanotube penetration was minimal in presence of endocytosis inhibitors. Temperature did not affect SWCNT internalization into A. thaliana mesophyll cells and therefore, the authors proposed a non-energy dependent endocytosis pathway . Later, Shen et al.  reported the formation of endocytosis-like structures in the membranes of A. thaliana leaf cells in response to SWCNT (5–30 μm) treatments. Successful intracellular penetration was shown for functionalized magnetic SWCNTs into canola (B. napus) and carrot (D. carota) cells driven by external magnetic forces. This behavior may reflect the potential of SWCNTs for development delivery carriers for biomolecules .
However, less evidence is available for SWCNT uptake by intact plants. In a study by Cañas et al. , none of the functionalized and non-functionalized SWCNTs supplied with the growth medium were found in the root tissues of young seedlings (2–3 days) of six plant species, and SWCNTs were mainly sticking to the external root surface. Accordingly, also in maize (Z. mays) the occurrence of SWCNTs was restricted to the root surface and the intercellular spaces of the root cortex . In studies with cell cultures, it has been demonstrated that events of nanotube penetration occur more frequently with high concentrations of SWCNTs rarely present in experiments with whole plants.
Impact of MWCNTs on plants
Germination In contrast to SWCNTs, stimulatory effects of MWCNTs have been reported for a wider range of different crops. Improved germination rates were described for tomato (S. lycopersicum) (already registered as a patent) [154, 155] and rice (O. sativa) , while germination speed was accelerated in barley (Hordeum vulgare), soybean (G. max), maize (Z. mays) [128, 157] and mustard seeds (B. juncea) . One of the most frequently encountered theories to explain beneficial effects on germination is associated with improved water uptake, demonstrated for tomato (S. lycopersicum) , rice (O. sativa) , and mustard (B. juncea) . Accelerated water flow into the seeds has been related with the ability of CNTs to perforate the seed coat . Later, a concentration-dependent effect of MWCNTs on the expression of aquaporin genes has been reported for germinating seeds of soybean (G. max), barley (H. vulgare) and maize (Z. mays) . Due to a central role of aquaporins in germination, it has been speculated that the beneficial effects of MWCNTs on seed water uptake and germination may be mediated by the described aquaporin effect. However, this assumption is still speculative since additionally to water uptake, aquaporins are involved in many physiological processes including stress responses also induced by CNTs and therefore, more detailed investigation of the involved aquaporin genes is necessary.
Apart from positive effects of MWCNTs on germination, there are also numerous reports claiming the absence of any MWCNT effect in a wide range of different plant species, including radish (R. sativus), rape (B. napus), ryegrass (Lolium perenne), lettuce (L. sativa), maize (Z. mays), cucumber (C. sativus) , wheat (T. aestivum) , mustard (B. juncea), black lentil (P. mungo), and zucchini (C. pepo) . On the one hand, this discrepancy may be attributed to genotypic differences or variability in seed lot quality of the tested seed material but it may also be the test conditions. Interestingly, it has been shown that different techniques of MWCNT application, such as dispersal in agar medium or spraying onto the seed surface did not change the beneficial effects on the germination of barley (H. vulgare), soybean (G. max) and maize (Z. mays) . However, the chemical composition of the growth media used for the germination tests may play an important role. These media can contain simply distilled water [158, 159], but also agar with and without supplementation of mineral nutrients  or even complete media used for plant tissue cultures, such as Murashige-Skoog medium [128, 154], supplemented with minerals, amino acids, vitamins and hormones as bioactive compounds . Moreover, even contaminations of CNTs with catalytic impurities, such as Fe and Al2O3 can exert a stimulatory effects on seed germination .
Plant cell culture Investigations of the influence of MWCNTs on suspension cells of A. thaliana showed toxic effects of MWCNTs (10–600 mg L−1) , reflected by inhibited cell growth and cell viability, decreased chlorophyll content and superoxide dismutase (SOD) activity. Comparing two types of MWCNTs, forming larger and smaller agglomerates, revealed higher toxicity of the smaller particles, confirming again that the size of nanoparticles is an important factor determining their toxicity (see “Impact of SWCNTs on plants” section). Investigations of MWCNT effects on rice suspension (O. sativa) cultures revealed increased ROS formation, associated with reduced cell viability, mitigated by the application of ascorbic acid as an antioxidant , demonstrating once more that oxidative stress is another important determinant of CNT toxicity. Due to the similar size of CNTs and many pathogens, it has been speculated that CNTs are able to induce a pathogen-like hypersensitive response, associated with an oxidative burst, as a defense reaction of plants in response to various kinds of pathogen attacks.
However, positive effects of MWCNTs on plant cell cultures have also been reported. In tobacco (N. tabacum) cells  MWCNTs at a dosage of 100 mg L−1 stimulated biomass accumulation, associated with an upregulated expression of cell cycle genes (after 6 h), cell growth (after 4 days) and water transport (from 24 h to 4 days), while during the rest of the exposure time the gene expression did not differ from cells grown in control (MS medium).
Independent of positive or negative plant responses to MWCNT treatments, the direct cell contact of individual or agglomerated CNTs seems to be a prerequisite for the induction of any effects, with differences in plant sensitivity or different physical parameters of CNTs (diameter, length, degree of aggregation) as determinants for the variable expression of plant responses.
Plant growth and development During seedling development and early growth, positive effects of MWCNTs on root and shoot elongation have been reported for a range of plant species, such as tomato (S. lycopersicum) [151, 154, 166], wheat (Triticum aestivum) , soybean (G. max), maize (Z. mays) , mustard (B. juncea), and black lentil (P. mungo) . A high degree of MWCNT dispersion in the growth medium resulted in more intense stimulation of plant growth as compared to variants containing larger agglomerates of the same MWCNTs , suggesting that a uniform and widely distributed contact of smaller MWCNTs with the plant tissues may be a prerequisite for stimulatory effects on plant growth. In many studies the expression of effects was concentration-dependent (see “Impact of SWCNTs on plants” section), with beneficial effects at lower levels of MWCNT application and inhibition at higher concentrations [127, 160]. As already described for cell culture experiments (see above and “Impact of SWCNTs on plants” section), induction of oxidative stress, associated with ROS formation, membrane damage, electrolyte leakage, mitochondrial dysfunctions, DNA aberration and cell death, has been characterized as determinant for MWCNT toxicity. This was also noted during seedling development and early growth of red spinach (A. tricolor), rice (O. sativa), lettuce (L. sativa) and cucumber (C. sativus) [119, 122, 124] and again small seeds were most sensitive (see also “Impact of SWCNTs on plants” section).
The majority of studies focused on MWCNTs effects on plant growth and development have used hydroponics or agar media as growth substrates, while soil culture has been employed very rarely. Apart from studies on germination and early growth, MWCNT effects have also been investigated in the reproductive stage of plant development. Khodakovskaya et al.  reported a doubling of flower setting and yield in tomato (S. lycopersicum), grown in soil with MWCNT amendments, which was not detectable in control soils simply treated with activated charcoal. On the other hand, De La Torre-Roche et al.  found no indications for effects of MWCNT soil amendments in zucchini (C. pepo) and tomato (S. lycopersicum). This is most likely due to limited mobility of MWCNTs in soil  related with a low probability of CNT contact with plant tissues.
Alteration of morphological traits in plants treated with MWCNTs is often associated with changes in gene expression and also with damage of DNA and chromatin structures. Ghosh et al.  reported DNA damage, micronucleus formation and chromosome aberration in onion roots (A. cepa) in response to MWCNT treatments. In a study with tomato roots (S. lycopersicum) , application of MWCNTs to the growth medium triggered overexpression of various biotic stress-related genes, such as subtilisin-like endoprotease, meloidogyne-induced giant cell protein, threonine deaminase, and this was also observed after SWCNT treatments in maize (Z. mays) seedlings . Similarly, the increased expression of aquaporins (water channel proteins) reported for seedlings of tomato (S. lycopersicum) [151, 166], soybean (G. max.), maize (Z. mays), and barley (H. vulgare) with MWCNTs seed treatments may reflect a common stress response . In tomato seedlings (S. lycopersicum), up-regulation of aquaporin gene expression was triggered by highly dispersed MWCNTs with different functional groups attached to the surface, while MWCNTs in the form of large aggregates remained ineffective . Taken together the findings suggest that CNTs are acting as stress factors with the ability to induce plant defense responses and hormesis effects, or toxicities depending on the intensity of the stimulus.
Uptake of MWCNTs Despite the fact, that the diameter and length of MWCNTs are frequently greater than the size of fullerenes and SWCNTs, plant uptake and internal translocation has been reported also for MWCNTs. The majority of such studies have been carried out in hydroponics or agar-like growth media. Multiwalled nanotubes can penetrate not only cells of developing seedlings, but even rigid seed coats by perforation and creation of new pores . For instance, MWCNTs with a diameter range of 15–40 nm were detected in germinating seeds of barley (H. vulgare), soybean (G. max) and maize (Z. mays) . Once nanotubes have passed the seed coat, contact with the radicle and other seedling organs is possible. Accordingly, small diameter MWCNTs (<13 nm), present in the germination medium, could penetrate cell walls and were later detected in the roots of wheat (T. aestivum)  and red spinach (A. tricolor) seedlings . Wild and Jones  demonstrated that MWCNTs with a diameter of 110–170 nm could pierce the epidermal cell wall and thus penetrate up to 4 μm into the cytoplasm of wheat (T. aestvcum) root hairs. MWCNTs taken up by plant roots were even detected in the xylem and in phloem cells . A root to shoot translocation of MWCNTs is most probably driven by transpiration  as demonstrated for wheat (T. aestivum) and rapeseed (B. napus) . In soil-grown tomato plants MWCNTs have been detected in vegetative shoot organs and even in the flowers . Figure 4 summarizes the evidences of plant uptake and internal translocation of carbon-based nanomaterials.
Impact of graphene on plants
Similar to other classes of nanomaterials, uptake into seeds and seedlings , plant growth stimulation [173, 174] at low concentrations (e.g. 5 mg L−1) and growth inhibition in plants exposed to higher doses (≥50 mg L−1) as a response to oxidative stress  has been also demonstrated for graphene.
A very detailed investigation of oxidative stress, induced by different concentrations of graphene oxide in faba bean (V. faba) seedlings was performed by Anjum et al. [176, 177]. They showed that low and high concentrations of GO applications (100, 200 and 1600 mg L−1) impaired the antioxidative glutathione metabolism  and increased the amount of ROS . Interestingly, graphene oxide applied in moderate concentrations (400 and 800 mg L−1) increased the glutathione pool  and reduced the formation of ROS , which was explained by an improved seed water content. Amendments of graphene oxide to native soils also reduced the activity of soil enzymes (xylosidase, 1,4-β-n-acetyl glucosaminidase, and phosphatase), which is probably related to its antimicrobial properties, but the microbial biomass was not affected . Additionally, indirect toxicity of GO has been reported in wheat (T. aestivum) acting via increased phytotoxicity of arsenic (As) . Mechanical damage of the cell wall and plasma membrane caused by the graphene oxide sheets, contributed to increased As uptake, which led to toxicity and further changes in metabolism. Similarly, mechanical damages of cell wall and other organelles (chloroplasts) due to GO treatments as well as enhanced formation of ROS have been detected in algal cells [180, 181]. Thus, the published data suggest that the main mechanisms of graphene toxicity are based on (i) mechanical damage of cells and tissues caused by the sharp edges of graphene sheets and (ii) formation of ROS which in small doses can also induce hormetic effects.
For ecotoxicological studies, it is recommended to use an appropriate range of CNM concentrations with respect to the study objectives. However, the experimental concentrations of CNMs used to investigate potential consequences of CNM release as environmental contaminations (ppb range), in many cases largely exceed the levels arising from model calculations (ppt range). On the other hand, in studies aiming at the development of agricultural or biotechnological CNM applications, substantially higher concentrations frequently need to be investigated according to the envisaged product design. Therefore, a clear definition of study objectives is essential to obtain valuable results.
Another important methodological issue is the availability of reliable techniques for CNMs detection in plant tissues. Qualitative methods of CNM detection in plant samples comprise light microscopy, transmission and scanning electron microscopy (TEM and SEM) able to detect carbon nanotubes, fullerenes and graphene particles in plant samples. Light microscopy was used as an easily available technique for visualization of MWCNT aggregates in contact with Arabidopsis (A. thaliana) cell cultures or for the detection of MWCNTs at the root surface of red spinach (A. tricolor) seedlings, grown in CNT-amended nutrient solution . However, light microscopy only allows detection of large CNMs aggregates but not individual CNM particles.
A significantly higher resolution can be obtained using TEM, which has been used for detection of graphene oxide in the tissues of wheat (T. aestivum) seedlings , the presence of graphene inside the husk of tomato (S. lycopersicum) seeds , localization of C70 in rice (O. sativa) leaves , MWCNTs in root and leaves of maize (Z. mays) and soybean (G. max.) seedlings . Challenges related to TEM comprise low contrast between CNMs and plant tissue structures [130, 151], a complicated sample preparation and the need for analysis of large numbers of samples. Use of fluorescent labels attached to CNTs can significantly improve the feasibility of microscopic techniques . However, this type of chemical CNT functionalization can also lead to alterations of their physicochemical properties associated with altered effects on plants .
Scanning electron microscopy is another technique to visualize CNMs: it has been used to detect graphene sheets at the root surface of red spinach (A. tricolor), cabbage (B. oleracea) and tomato (S. lycopersicum) seedlings  and of MWCNTs associated with red spinach (A. tricolor) roots . However, the resolution of SEM techniques is often smaller than in TEM. Visualization of CNMs at the surface or inside plant tissues can provide important information on interactions of CNMs with plant cells and cell structures, internalization mechanisms of CNMs, and transport and distribution of CNMs within the plant, with particular importance for the development of vehicle systems.
Alternative technique to identify the presence of carbon nanotubes in plant samples is Raman spectroscopy. In contrast to TEM, this method does not produce false negative results, but it cannot provide detailed information on intracellular CNM location. Therefore, both techniques are frequently used for complementary analyses. A combination of Raman spectroscopy and TEM was employed for detection of CNTs in tomato (Solanum lycopersicum) , wheat (Triticum aestivum)  and red spinach (Amaranthus tricolor)  seedlings and in tobacco (Nicotiana tabacum) cell cultures .
A promising novel approach for detection of MWCNTs in plant tissues is based on a combination of photothermal and photoacoustic mapping developed by Khodakovskaya et al. . The method has demonstrated high sensitivity, and the obtained results were confirmed by optical imaging. In another study, infra-red (IR) spectroscopy was used for detection of fullerols in bitter melon , since fullerols exhibit specific infra-red absorption features.
Despite numerous examples of evidence for the uptake of carbon nanomaterials into plant organs, only limited information exists concerning the quantities of CNMs taken up by plants. However, in the recent past significant progress has been made in the development of techniques for CNMs quantification; fullerene C60 has been quantified in zucchini (C. pepo) stems using high-performance liquid chromatography (HPLC) with UV–vis spectroscopic detection . Another method for CNT quantification inside plant samples, based on microwave-induced heating  has demonstrated extraordinarily high accuracy associated with low detection limits (<0.1 μg) and is now registered as a patent . Also, radio-labeled CNMs have been employed to quantify CNMs in plant tissues. Application of 14C-labeled C60 to radish (Raphanus sativus) grown in sand and hydroponic culture, revealed plant uptake of 7 % of the applied fullerene dosage. In a study with wheat (T. aestivum) and rapeseed (B. napus) exposed to 14C-radiolabeled MWCNTs (10–100 mg L−1) in a hydroponic culture medium  it was demonstrated that less than 0.005 ‰ (≈ 200 ng g−1 plant dry matter) of the total applied nanomaterial, was taken up and translocated within the plants without beneficial or detrimental effects. The high discrepancy between the externally applied amount of CNTs and the fraction really taken up by the plants, as well as typical features of carbon nanomaterials, such as agglomeration or sedimentation in suspensions and surface adsorption to solid substrates, which can vary considerably depending on the composition of the incubation media , demonstrate that the simple indication of application concentrations is easy to use but only of little informative value with respect to the real effective dosage.
Moreover, frequently pristine nanomaterials are used in test systems to investigate their interactions with living organisms. This scenario hardly reflects realistic natural conditions, since depending on the composition of the incubation medium, carbon nanomaterials can undergo significant conformational changes (e.g. agglomeration) with significant impact on their properties in terms of bioavailability or toxicity [118, 152]. To define realistic application conditions, much more information is required concerning the behavior of the various types of nanomaterials in soils and planting substrates. For comparative analyses, the development of standardized test systems would be urgently needed. It has been also recommended to pay more attention to selected controls  by also including positive controls in addition to the commonly used negative controls, as well as other carbon (activated carbon) and non-carbon (contaminants in CNTs) controls that will eliminate any possible artifacts.
Most carbon nanomaterials can be taken up by plants. This is frequently associated also with internal translocation;
Small amounts of absorbed nanomaterials can induce physiological responses;
At higher external concentrations, frequently detrimental effects on plant growth are observed, while lower levels of carbon nanomaterials (<100 mg L−1) exert beneficial or no effects;
Induction of oxidative stress by formation of ROS seems to be a major common mechanism of phytotoxicity induced by carbon nanomaterials, while beneficial effects are probably based on hormesis, which is frequently observed during exposure to toxic agents at sub-toxic levels (e.g. glyphosate, Al3+, pathogens), and often based on induction and strengthening of stress defense systems [176, 177]; in the case of improved seed germination there is also a stimulation of water uptake;
Chemical (functionalization) or conformational (agglomeration) modifications of carbon nanomaterials can significantly influence their toxicity potential;
In many studies of CNM phytotoxicity tested dosages significantly exceed the expected environmental concentrations.
As a major challenge for the future, a more comprehensive and systematic survey of the key factors important for interactions of the various carbon nanomaterials with living organisms and the environment will be important for both risk evaluation and the characterization of potential applications.
double-walled carbon nanotubes
functionalized single-walled carbon nanotubes
oxidized multi-walled carbon nanotubes
water soluble MWCNTs
- C60, C70:
chemical vapor deposition
fullerene-malonic acid derivative
reactive oxygen species
- DI water:
- MS medium:
Murashige and Skoog medium
natural organic matter
transmission electron microscopy
scanning electron microscopy
- IR spectroscopy:
high performance liquid chromatography
OZ wrote the manuscript and prepared figures and tables. The manuscript was edited and improved by both authors. All authors read and approved the final manuscript.
The author (OZ) would like to thank the Ministry of Science, Research and the Arts of Baden-Württemberg and the Education, Audiovisual and Culture Executive Agency of the European Union for financial support. Furthermore, the authors are grateful to two anonymous referees for helpful remarks.
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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