Engineering plants with carbon nanotubes: a sustainable agriculture approach

Abstract

Sustainable agriculture is an important conception to meet the growing food demand of the global population. The increased need for adequate and safe food, as well as the ongoing ecological destruction associated with conventional agriculture practices are key global challenges. Nanomaterials are being developed in the agriculture sector to improve the growth and protection of crops. Among the various engineered nanomaterials, carbon nanotubes (CNTs) are one of the most promising carbon-based nanomaterials owing to their attractive physiochemical properties such as small size, high surface area, and superior mechanical and thermal strength, offering better opportunities for agriculture sector applications. This review provides basic information about CNTs, including their history; classification; and electrical, thermal, and mechanical properties, with a focus on their applications in the agriculture field. Furthermore, the mechanisms of the uptake and translocation of CNTs in plants and their defense mechanisms against environmental stresses are discussed. Finally, the major shortcomings, threats, and challenges of CNTs are assessed to provide a broad and clear view of the potential and future directions for CNT-based agriculture applications to achieve the goal of sustainability.

Keywords: Agriculture; Antimicrobial activity; Biosensors; Carbon nanotubes; Environmental stress; Gene delivery; Plant growth; Sustainability.

Fig. 1

Schematic illustration of the structure and morphology of CNTs. A Scanning electron microscope (SEM) image of a zigzag shaped SWCNT [74]. B Transmission electron microscope (TEM) image of a MWNT containing a concentrically nested array of nine SWNTs [75]. C SEM image of large amount of helically coiled CNTs [76]. D TEM images of typical coiled CNTs with a nanobell structure [77]. E SEM images of the coiled CNTs > 20 mm in length [77]. F SEM image of array of CNTs grown with zigzag morphology using a three-stage growth process [78]

Fig. 2

Introduction of carbon nanotubes (CNTs). A Timeline of CNT development for applications in the agriculture sector to improve plant growth. CNTs were first discovered by Iijima in 1991 and were first introduced in agriculture in 2008. For sustainable agriculture production, CNTs improve seed germination and growth, exhibit antimicrobial activity, can be used in gene delivery and as biosensors, and protect plants against various environmental stresses. B Diverse applications of CNTs in the agriculture field

Fig. 3

Effects of CNTs during the life cycle of plants. A Schematic representation of the effects of CNTs at various stages of plant growth. B The effect of single-walled carbon nanotubes (SWCNTs), quantum dots (QDs), and SWCNT-QD conjugates on the phenotype of 2-month-old tomato plants grown on a medium supplemented with 0.5 µg/mL QDs, 50 µg/mL SWCNTs, or 50 µg/mL SWCNT-QDs, or without nanoparticles as a control [144]. C Morphological observations of red spinach and lettuce exposed to multi-walled carbon nanotubes (MWCNTs) at concentrations of 0, 20, 200, 1000, and 2000 mg/L in hydroponic culture for 15 days [146]. D Image showing the effects of natural MWCNTs, synthetic MWCNTs, amorphous carbon, and a control group on Eysenhardtia polystachya growth [141]. E Effect of synthetic MWCNTs on the growth of Lupinus elegans [142]. F Effect of water supplied CNTs (50 and 200 µg/mL) on the number of flowers on tomato plants [53]. G Effect of CNTs on the nodule development of plants grown in soil treated with activated carbon (AC), MWCNTs, SWCNTs, and graphene oxide (GO) at low (50 µg/mL) or high (500 µg/mL) concentration for 14 days post-inoculation (dpi), respectively. Nodules on the roots are shown by red triangles. Scale bar = 10 mm [147]

Fig. 4

Systematic illustration of the antimicrobial activity of carbon nanotubes (CNTs) against various pathogens. A Physical interaction of CNTs with microbes leads to membrane damage and the release of biological components. B Images of Escherichia coli cells treated without (left) and with (right) single-walled CNTs (SWCNTs) for 60 min captured using scanning electron microscopy (SEM). Scale bar = 2 μm [162]. c Measurement of cell viability after exposure to SWCNTs (5 g/mL) in a 0.9% NaCl isotonic solution. Image of SWCNT aggregates at the microscopic level from a total cell fluorescence microscope (cells were stained with propidium iodide and DAPI). Using the fluorescence microscope, a fluorescence image of dead cells was captured (stained with propidium iodide only) [162]. D SWCNTs of < 1 μm, 1–5 μm, and ∼5 μm in a deionized (DI) water solution at a concentration of 100 µg/mL. Salmonella cells (6.0 × 10⁸ colony-forming units/mL) were combined with three different lengths of SWCNTs (100 µg/mL) in DI water for 20 min [161]. E Images of Salmonella cells stained with the Live/Dead bacterial viability kit without and with SWCNTs: cells without SWCNTs in the control sample, live (green) and dead (red) cells in the sample of cells with SWCNTs of 1–5 μm [161]. F The synthesis of silver (Ag)–multi-walled CNTs (MWCNTs) and evaluation of their antibacterial activity [180]

Fig. 5

Carbon nanotubes (CNTs) serve as carriers for genetic material or drug delivery. A The image on the left illustrates the stability of DNA loading on polyethyleneimine (PEI)-single-walled carbon nanotubes (SWCNTs), whereas the image on the right represents the instability of DNA loading on PEI-SWCNTs, with significant SWCNT agglomeration [186]. B Infiltration of leaves with DNA-loaded PEI-SWCNTs. By infiltrating a higher volume of DNA-PEI-SWCNT solution, the area of penetration can be enhanced [186]. C Confocal microscopy images of wild-type Nicotiana benthamiana (Nb), arugula, wheat, and cotton leaves infiltrated with DNA-PEI-SWCNTs to measure green fluorescent protein (GFP) expression levels in the leaf lamina of each plant species. Scale bars = 50 μm [185]. D Stomata pores allow plasmid DNA (pDNA)–SWCNT complexes to enter the leaf mesophyll. Electrostatic interactions help to condense negatively charged pDNA on the positively charged surface of chitosan-complexed SWCNTs [45]. E Atomic force microscopy (AFM) image of a 1:1 pDNA:CSCOV–SWCNT complex with representative height; 1:6 pDNA:CSCOV–SWNT AFM height image standard deviations (n = 3) are represented by the error bars [45]. F Fluorescence confocal micrographs of isolated protoplasts demonstrate yellow fluorescent protein (YFP) expression from pDNA coupled to CSCOV–SWCNTs (1:6 pDNA:SWCNT w/w ratio) after 24 h [45]. G CNT-mediated DNA delivery into isolated protoplasts and subsequent GFP expression. Enzymatic cell wall degradation extracts of intact and healthy protoplasts from arugula leaves [193]. H Protoplasts incubated with DNA-CNTs display robust GFP expression in the nuclei, whereas protoplasts cultured with free pDNA without CNT nanocarriers do not show strong GFP expression. Red boxes represent areas of interest that are highlighted and expressed with bright-field, GFP, and overlay channels. Scale bars = 25 μm [193]

Fig. 6

Applications of carbon nanotubes (CNTs) as biosensors. A The plant serves as a fluidic device and an environmental sampler. Water and other analytes are carried by the roots into the stem and toward the leaf tissues via the plant vasculature when the leaves transpire. Bombolitin II-modified single-walled carbon nanotubes (B-SWCNTs), serving as an active sensor, and polyvinyl alcohol-modified SWNCTs (P-SWCNTs), serving as a reference sensor, infiltrate the leaves via the abaxial surface on each side of the leaf midrib [206]. B After infiltration, SWCNTs are found within the leaf parenchyma tissues, as evidenced by the fluorescence detected when the leaf was excited at 785 nm. Scale bar = 0.2 mm [206]. C Because of the nanomaterial carbon lattice, analyte interaction with SWCNT sensors generates fluctuations in near-infrared (NIR) fluorescence intensity or wavelength shifts. H₂O₂ monitoring in vivo was accomplished using SWCNT NIR fluorescence intensity fluctuations in Arabidopsis leaf slices with high spatial (> 0.5 m) and temporal (> 0.5 s) resolution [208]. D Plant leaves embedded with SWCNTs act as nitroaromatic detectors, such as for picric acid. Internal controls consist of P-SWCNTs (black arrows), whereas B-SWCNTs (red arrows) monitor picric acid in real time with high spatiotemporal resolution [206]. E Plant subcellular sensors based on smart nanobiotechnology can monitor plant chemical signaling using phenotyping technology, which could aid in the selection of desirable plant features for high yield and stress tolerance [211]

Fig. 7

Schematic representation of the uptake and translocation mechanisms of carbon nanotubes (CNTs) via different routes in crops. A Different routes of entry of CNTs into crops, including foliar and root entrance. B CNT movement in several organs of plant leaves and roots. C Transmission electron microscopy characterization of multi-walled carbon nanotube (MWCNT) uptake in broccoli plants cultivated for 7 days with MWCNTs (10 mg/L) in nutrient solution. Arrows point to MWCNTs in the intercellular space, vacuole, and cytoplasm of the roots and stems [54]. D Spectroscopic characteristics of individual CNTs to detect CNT aggregates in tomato flowers using Raman scattering [53]. E Raman spectroscopy to identify MWCNT translocation inside soybean plants. Slices of various plant tissues, including the leaves, stems, roots, and seeds, were prepared and studied using Raman spectroscopy and point-by-point mapping of selected locations [229]. F Raman spectroscopy to identify MWCNT translocation inside maize plants. Slices of various plant tissues, including the tassels, leaves, stems, roots, and seeds, were prepared and studied with Raman spectroscopy using point-by-point mapping of selected locations [229]

Fig. 8

Defense mechanism of carbon nanotubes (CNTs) against environmental stresses. A The effect of CNTs on the phenotype of Catharanthus plants grown in the presence of carbon-based nanomaterials (CBNs) at day 0, 7, and 15 of water-deficit stress [134]. B Long-term application of CBNs to saline soil reduced salt stress toxicity and increased Catharanthus growth and yield. CBNs were added to saline soil and had a favorable effect on flower production in Catharanthus. C After incubation, transmission electron microscopy images of spores with deionized (DI) water and multi-walled carbon nanotubes (MWCNTs). Microscopy images of spores treated with and without (control) MWCNTs, MWCNTs-COOH, MWCNTs-OH, and MWCNTs-NH₂. The MWCNTs around the spores and the magnified location are indicated by red arrows [242]. D Photographs of Podosphaera pannosa-infected rose leaves after exposure to 50 and 200 mg/L MWCNTs. Scanning electron microscopy images of rose leaves infected with P. pannosa after treatment with 50 and 200 mg/L MWCNTs [260]. E Foliar application of CNTs to combat tobacco mosaic virus (TMV) and develop resistance in Nicotiana benthamiana [181]