Emerging pivotal role of carbon nanomaterials in abiotic stress tolerance in plants: a mini review

Abstract

In recent years, carbon nanomaterials (CNMs) have received a great deal of attention due to the constantly growing demands in the agricultural sector. In this review, we discuss two major abiotic stresses: drought and salt, which have been extensively researched in terms of their impact on plant growth under CNMs treatments. Drought and salt stress are two of the most important environmental factors that affect plants growth and development. There is still a lot we don’t fully understand about how CNMs accumulates, how plants respond to stress, and how they affect plant growth. Researchers all over the world have worked to uncover more about plants and CNMs interact and what happens when plants are exposed to abiotic stresses. The goal of this review is to give the reader an up-to-date look at how the different CNMs help plants grow when they are stressed by drought or salt. Depending on the recommended dose of CNMs used, different species have different growth and production patterns. Lower CNM concentration levels were observed to boost crop productivity and yield, but greater CNM concentration levels under stress conditions were also observed to reduce these traits. In general, CNMs were proved to be efficient at increasing (water uptake, water transport, seed germination, boosting photosynthetic system and antioxidant activities) and reducing (MDA, H₂O₂ content) while concentration levels were limited; they were found to be less effective at both of these changes when concentrations were high. Taken together, the current state of studies on how CNMs affect the development of plants is encapsulated, and the most important knowledge gaps are also addressed.

Keywords:

• Antioxidant
• chlorophyll
• H₂O₂ content
• MDA
• photosynthesis

1. Introduction

The world's population is predicted to rise to almost 9.6 billion people by 2050, necessitating a 70–100% boost in agricultural productivity to meet the demand for food (Mueller et al., 2012; Rodrigues et al., 2017). However, abiotic stresses on plants are made worse by shrinking fertile land, drought, salinity and the ineffectiveness of current fertilizers and pesticides, which reduces crop yields. For instance, each year crop yield loss from drought and salinity costs billions of dollars (Alabdallah et al., 2021). Therefore, the decline in food production due to drought and salt stress is a deep concern. To ensure food security in a safe and sustainable way, cutting-edge technologies that shield plants from drought and salt stress are required.

Nanotechnology, a prominent field of investment across various research domains, plays a crucial role in the advancement of innovative technologies. Similar to tissue engineering, nanotechnology provides a method for stimulating cell growth and creating complex three-dimensional structures (Harrison & Atala, 2007). Carbon nanomaterilas (CNMs) are receiving a lot of attention because of their potential industrial applications and implementations within this field of nanotechnology. Carbon nanomaterilas (CNMs) are gaining popularity due to their exceptional optical, electrical, mechanical and thermal properties (Srivastava, Gusain, & Sharma, 2015). Over the past two decades, there has been a dramatic development in the synthesizing of CNMs. The CNMs family consists of the following: fullerenes, nano-horns, carbon dots (CDs), carbon nanotubes (CNTs), nano-fibers, single-walled carbon nanotubes (SWCNTs), multi-walled carbon nanotubes (MWCNTs) and graphene (Baptista, Belhout, Giordani, & Quinn, 2015). They show a significant amount of structural variety in addition to a size range that is not entirely limited to the nanoscale (less than 100 nm) in any dimension. The distinctive qualities of the CNMs and their numerous applications as pesticides, seed sprout and growth enhancers, carriers of (phytohormones, herbicides, DNA and fertilizers) to the cells of plants have been detailed (Verma et al., 2018). Despite the fact that research in this multidisciplinary field has shown some promise, it is still absolutely necessary to comprehend the influence that CNMs properties have on specific plant responses to abiotic stresses (Lahiani et al., 2015).

There has been a lack of systematic scientific research investigating the uptake and accumulation of CNMs in different plant tissues. Therefore, we have compiled the most recent scientific literature in the field of plant nanotechnology, with a specific focus on the uptake, translocation and accumulation of CNMs within plant organs. Additionally, we examine their role in influencing plant growth and the plant’s response to induced toxicity. In this review, we analyse the impact of CNMs on plant growth induction, as well as their effects on drought and salt stress responses and crop yields. Furthermore, we provide detailed explanations of the characteristics of individual CNMs in separate sections. The review concludes by suggesting the future research directions for studying CNM–plant interactions in the closing remarks and prospects section.

2. Synthesis of carbon nanomaterials (CNMs)

2.1. Industrial synthesis and chemical functionalization of CNMs

The first fullerenes were created by the evaporation of graphite electrodes in a helium environment (Kratschmer et al., 1990; Kratschmer, 2011). The reactor was later amended by developing an electric arc among both graphite electrodes. The arising root compresses on the reactor’s cold surface, where it is accumulated and refined using boiling toluene, benzene, xylene, or other organic solvents. A black condensate is left behind after the solvents evaporate, and its made up of mostly C60 and C70 fullerenes with only tiny quantities of higher fullerenes.

Arc discharge, laser ablation and chemical vapour deposition (CVD) are the three most common ways to create CNTs (Gore & Sane, 2011). CVD is currently one of the most extensively studied and widely employed methods for producing CNTs (Kumar & Ando, 2010). CVD synthesis is particularly suitable for large-scale CNT production in industrial settings, as it necessitates less sophisticated instrumentation and operates under more forgiving temperature and pressure conditions (Zhang, Huang, Zhao, Qian, & Wei, 2011) (Figure 1).

Figure 1. The diagram illustrates the process of CVD. (A) a simplified depiction of a CVD reactor utilized for synthesizing carbon nanotubes (CNTs); (B) A model showcasing the base-growth mechanism of CNT formation; (C) A model illustrating the tip-growth mechanism of CNT growth.

The process of CVD synthesis involves the breakdown of hydrocarbons into carbon, followed by the synthesis of carbon nanostructures on various substrates doped with catalysts. A typical CVD reactor consists of a reaction chamber, tubes filled with inert gas and hydrocarbon, and a gas meter. Generally, methane is utilized for producing SWCNTs, whereas ethylene or acetylene is employed for manufacturing MWCNTs.

During the production of SWCNTs, the substrate is heated to temperatures ranging from 850 °C to 1000 °C. In contrast, when manufacturing MWCNTs, the substrate is heated to temperatures between 550 °C and 700 °C. Over time, there have been notable advancements in graphene research, accompanied by the development of various techniques for its manufacturing. The initial discovery of graphene sheets by Novoselov et al. (2012) involved a mechanical splitting of graphite using adhesive tape. Nanoscale graphene sheets are the goal of these methodologies, which involve a variety of physical and chemical processes aimed at separating or severing materials like graphite or nanotubes (Jiao, Zhang, Wang, Diankov, & Dai, 2009). CVD synthesis and laser ablation are two additional techniques for producing graphene sheets.

Chemical functionalization allows for an even greater broad scope of carbon-based nanomaterials. In order to alter the physical and chemical properties of nanoparticles (Hirsch & Vostrowsky, 2005), functionalization is commonly used to accomplish this by linking specific molecules to the nanoparticle surface (Hernández-Fernández et al., 2010; Hirsch & Vostrowsky, 2005). The oxidation of CNTs is an example of the functionalization of carbon-based nanoparticles. Here, nanotubes are ultrasonically treated in an acid mixture, which results in the connection of carboxylic functional groups (▬COOH) to the nanotubes' surfaces. Oxidized CNTs are now soluble in water, but they still have the same mechanical and electrical properties as untreated CNTs. In addition, carboxylic groups that are attached to the surface of the nanotubes can act as potential sites for additional functionalization.

2.2. Naturally occurring CNMs

Carbon-based nanomaterials that occur naturally have also been observed (MacKenzie, See, Dunens, & Harris, 2008; Velasco-Santos, Martínez-Hernández, Consultchi, Rodríguez, & Castaño, 2003), in addition to nanomaterials that have been artificially manufactured. CNTs were found in a mixture of coal and petroleum (Velasco-Santos et al., 2003). Su and Chen (2007) and Mracek, Fagan, Stengelin, and Hesjedal (2011) utilized volcanic lava as a substrate and catalyst for the production of SWCNTs using the CVD technique. The lava contained particles of metal oxides. The authors hypothesized that this method offers evidence for the creation of nanotubes under natural circumstances whenever the temperature increases to extremely high levels, such as during the eruption of a volcano. In addition to CNTs, there is evidence that fullerenes can be found in geological materials. Low concentrations of fullerenes (2% w/w) have been found in the naturally occurring mineral shungit from Karelia (Buseck, Tsipursky, & Hettich, 1992; Parthasarathy, Srinivasan, Vairamani, Ravikumar, & Kunwar, 1998). It is interesting to note that the spherical structure of fullerenes does not appear to be confined to the case of CNMs only. Recently, fullerene-like structures have been characterized in the pollen grains of Hibiscus rosa-sinensis. These structures are thought to have putative functions for high stability and adaptive characteristics, both of which are crucial for the process of pollination (Andrade et al., 2014).

3. Carbon nanoparticles improve abiotic stress tolerance

With the world's population growing, the biggest challenge is to increase agriculture productivity on the land that is already being used. In this case, nanotechnology can be a very useful tool. Because the climate is always shifting, both biotic and abiotic are always bringing stress on plants. Many abiotic stresses, like drought and salt stress, can limit the growth, development and yield of plants (Alabdallah et al., 2021; Duhan et al., 2017; Hasan, Skalicky, et al., 2021) (Figure 2).

Figure 2. A schematic shows the sources and CNMs impact on the crop abiotic stress tolerance in plants.

3.1. CNMs improve the drought stress tolerance in plants

Water deficits alter numerous plant characteristics at the cellular, physiological and molecular levels, including photosynthetic activity, biomass and ROS production. Excessive ROS production causes injury to DNA, proteins and cell membranes (Hasan et al., 2020; Hasan, Skalicky, et al., 2021b; Rahman et al., 2022). Regulating ROS production and maintaining ROS concentrations stability is crucial (Ahmed et al., 2023; Liu et al., 2023). It is well established that many CNMs, including fullerene and its derivatives, contribute significantly to a plant's ability to withstand abiotic stress (Khan, Mobin, Abbas, AlMutairi, & Siddiqui,2017; Borišev et al., 2016). Optimal fullerol concentrations aid plants in resisting the deleterious effects of osmotic stress (Panova et al., 2016). The concentrations of H₂O₂ and malondialdehyde (MDA) in maize decreased under PEG treatment, as was also concluded by Liu et al. when fullerol was prevalent. Because of its spherical cage-like structure, fullerene is able to scavenge reactive oxygen species (ROS), which play an important role in plant abiotic stress tolerance, especially drought (Wei & Wang, 2013). Numerous findings have shed light on fullerene and its derivatives’ function as potent ROS detoxifying substances (Akhtar, Ahamed, Alhadlaq, & Alshamsan, 2017). Depending on the concentration of nanoparticles used, foliar application of fullerenol may help mitigate the oxidative impacts of drought stress (Borišev et al., 2016). Seed germination was significantly boosted by priming with fullerol at 10 and 100 mg L⁻¹ under drought treatments (15% PEG). Fullerol applied directly to B. napus seedlings increased their above-ground dry weight and photosynthesis when grown in drier soil conditions (Xiong, Li, Wang, Zhang, & Naeem, 2018) (Table 1).

Table 1. Impact of CNMs on plant growth and development under drought and salt stress.

Type of Stress	Plant Species	CNMs treatment	Stress level	Impact	References
Drought Stress	Dodonaea viscosa L.	MWCNTs (10, 30, 50, 100 and 200 mg L^−1)	PEG 6000 (0, −4, −8, −12 MPa)	Improve seed germination rate, stem, root length, fresh and dry weight	Yousefi, Kartoolinejad, and Naghdi (2017)
	Hyoscyamus niger	SWCNTs (50–800 g mL^−1)	PEG (0.5–1.5 MPa)	Increased shoot and root length, vigour index, protein content, antioxidant enzyme (SOD, POD CAT, APX) activities and decreased MDA, H2O2 content	Hatami, Hadian, and Ghorbanpour (2017)
	Brassica napus L.	Fullerol (1–100 mg L^−1)	15% PEG	Improved germination percentage, mean germination time, gas exchange parameters, antioxidant enzyme activities and declined superoxide anion, MDA and H2O2 content	Xiong et al. (2018)
	Beta vulgaris L.	Fullerenol (700 and 70 µmol L^−1)	60 ± 70% of RWC, 20 ± 30% of RWC, 10 ± 20% of RWC	Reduced MDA content and improved antioxidant enzyme activities	Borišev et al. (2016)
	Cucumis sativus L	MWCNT and Shungite (0.067%)	Withheld water	Increased plant height, sensitivity to ABA, antioxidant enzyme activities and upregulated drought stress-related marker genes	Kim, Lee, Ku, and Lee (2019)
	Arachis hypogaea	Carbon nanodots (180 mg L^−1)	20% PEG-6000	Increased growth conditions, SOD, CAT, POD activities and decreased MDA content	Su et al. (2018)
	Alnus subcordata	MWCNTs (0, 10, 30, 50 and 100 mg L^−1)	drought stress (0, −2, −4, −6, −8 and −10 MPa)	Improved shoot length, root length, dry weight, seed germination rate and seed vigour index	Rahimi, Kartoolinejad, Nourmohammadi, and Naghdi (2016)
	Hordeum vulgare L. var. Afzal	MWCNTs (0, 500, 1000 and 2000 mg L^−1)	PEG 6000 (0, −0.3 and −0.6 MPa)	Increased germination percentage, germination rate, root length, shoot length	Karami and Sepehri (2017)
	Zea mays L.	CDs (5 ml, 5 mgL^−1)	35% soil moisture	Increased shoot and root fresh weight. Improved net photosynthetic rate and carbohydrate content	Yang et al. (2022)
	Glycine max L.	CDs (5 mg kg^−1)	30% soil moisture	Improved the nitrogen fixing ability and water uptake	Wang et al. (2022)
Salt Stress	Triticum aestivum cv. Ujala-2016	Fullerenol (0, 10, 40, 80 and 120 nM)	0 and 150 mM NaCl	Improved SOD, CAT, APX, POD activities and decreased H2O2, MDA content	Shafiq, Iqbal, Ali, and Ashraf (2021)
	Triticum aestivum cv. Ujala-2016	Fullerol (0, 10, 40, 80 and 120 nM)	0 and 150 mM NaCl	Increased shoot and root length, fresh weight, dry weight, chlorophyll content, gas exchange parameters	Shafiq, Iqbal, Ashraf, and Ali (2020)
	Hordeum vulgare L.	Polyhydroxy fullerene (14 mg L^−1)	75 mM NaCl	Increased root and shoot length and decreased oxidative stress	Panova et al.
	Lactuca sativa	Water soluble CNPs (0.3%)	150, 200 mM NaCl	Enhanced germination percentage, leaf, root length, number of leaf, number of lateral roots, biomass, and chlorophyll content	Baz et al. (2020)
	Ocimum basilicum L.	MWCNTs (0, 25, 50, and 100 mg L^−1)	0, 50 and 100 mM NaCl	Improved plant height, fresh, dry weight, chlorophyll content, antioxidant enzyme activities	Gohari et al. (2020)
	Gossypium hirsutum, Catharanthus roseus	CBNs, graphene (50, 100, 200, 500, and 100 µg mL^−1)	50 mM NaCl for Catharanthus roseus and 100 mM NaCl for Gossypium hirsutum	Enhanced germination percentage, seedlings length, fiber weight	Pandey, Anas, Hicks, Green, and Khodakovskaya (2019)
	Solanum lycopersicum L.	CNTs and graphene (50, 250, and 500 mg L^−1)	50 mM NaCl	Improved chlorophyll content, ascorbic acid, proteins, glutathione, phenols, antioxidant enzyme activities, and decreased MDA and H2O2 content	González-García et al. (2022)
	Sophora alopecuroides	SWCNHs, ZnO NPs (50 or 100 mg L^−1)	100 mM NaCl	Increased plantlet height, fresh weight, protein content, and metabolites,	Wan, Wang, Bai, Wang, and Xu (2020)
	Sorghum bicolor L., Panicum virgatum L.	CNTs, graphene (50,100, 200, 500, and 1000 µg ml^−1)	0, 50, 100, 150, 200, 300, 400 mM NaCl	Decreased Na^+ ions	Pandey et al. (2018)
	Brassica napus cv. Zhongshuang 11	MWCNTs (20 mg L^−1)	125 mM NaCl	Increased plant height, root length, fresh weight, NO production, and upregulated antioxidant, ion-balance-related genes	Zhao et al. (2019)
	Vitis sp. cv. Rasha	CQDs, Pro-CQDs NPs (0, 50, and 100 mg L^−1)	100mM NaCl	Enhanced fresh, dry weight, chlorophyll florescence, antioxidant enzyme activities, and declined electrolyte leakage (%), MDA, H2O2 content	Gohari et al. (2021)
	Solanum lycopersicum L.	COFA (5 mg L^−1)	0, 20, and 40 mM	Improved growth conditions, proline content, SOD and CAT activities	Alluqmani and Alabdallah (2022)

Under drought conditions, fullerol treatments of 1–100 mg L⁻¹ significantly increased the leaf ABA level and activated ABA biosynthesis by down-regulating expression of the ABA catabolic gene CYP707A3 (Xiong et al., 2018).

Plants have developed effective defense mechanisms, such as enhancing the antioxidant system, in order to combat injuries caused by oxidative stress (Abdulmajeed et al., 2021; Hasan, Skalicky, et al., 2021; Jahan et al., 2022). These defense mechanisms enable plants to counteract the excessive production of reactive oxygen species (ROS) and safeguard cells from oxidative stress (Hasan et al., 2023; Jahan et al., 2023). When confronted with oxidative stress, plants activate their internal antioxidant system, consisting of enzymatic antioxidants such as peroxidase (POD), various isozymes of superoxide dismutase (SOD), peroxiredoxins, and catalase (CAT). Additionally, the main subcellular compartments contain all the necessary components of the ascorbate-glutathione cycle, including ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), and glutathione reductase (GR) (Hasan, Skalicky, et al., 2021; Hasan et al., 2022). Antioxidant enzyme stimulation to protect plants from oxidative stress has been linked to fullerol (Xiong et al., 2018).Carbon nanodots (CDs) have garnered a lot of interest because of their promising future uses in food production (Su et al., 2018; Yang et al., 2022). Despite being subjected to drought, peanut (Su et al., 2018) and maize (Yang et al., 2022) growth was shown to increase under CDs treatments in previous studies. Under drought conditions, plants treated with CDs showed a rise in photosynthetic rate, SOD, CAT, and POD activities, and a reduce in MDA content (Su et al., 2018; Yang et al., 2022).

The two most common types of synthetic carbon nanoparticles used extensively in agriculture are SWCNTs and MWCNTs, respectively (Hatami et al., 2017; Rahimi et al., 2016; Yousefi et al., 2017). Hyoscyamus niger was treated with SWCNTs (50–800 gmL⁻¹), and the results showed a rise in water uptake, antioxidant enzyme activities, up-regulation of mechanisms involved in starch hydrolysis, and a decrease in oxidative injury (H₂O₂ and MDA content) in the expose of drought (0.5–1.5 MPa). Increases in germination rate, mean germination time (MGT), root and stem lengths, and total biomass have been observed when MWCNTs were added to the growing medium (Yousefi et al., 2017). In Alnus subcordata seedlings under all levels of drought stress, Rahimi et al. (2016) found that nano priming at a concentration of 100 mgL⁻¹ of MWCNTs resulted to the maximum germination rate as well as the maximum levels of seed vigour index, root and stem lengths etc.

3.2. CNMs improve the salt stress tolerance in plants

Salt stress has emerged as a significant limitation, exerting detrimental effects on crop productivity, particularly in arid and semiarid regions (Alluqmani & Alabdallah, 2022). Extensive research has revealed the vulnerability of crops to the deleterious consequences of salinity stress, impacting their crucial morphological, physiological, and biochemical attributes. Consequently, it is evident that the overall performance of plant systems is compromised under salt stress conditions. However, in recent years, CNMs have gained widespread utilization in agricultural fields subjected to salt stress.

Nanoparticles formed of fullerenol (also known as polyhydroxy fullerene) could be useful for reducing the oxidative stress caused by salinity in plants (Shafiq et al., 2021). It is well established that fullerenols, like naturally occurring antioxidants, can neutralize a wide variety of reactive oxygen species (ROS) (Sachkova, Kovel, Churilov, Stom, & Kudryasheva, 2019). Under salinity stress, wheat seedlings aided from fullerenol nano-priming because it increased antioxidant enzyme activities and lowered ROS generation and lipid peroxidation. Additionally, Panova et al. revealed that polyhydroxy fullerene increases root and shoot length and reduce oxidative stress in barley seedlings, thereby enhancing salinity tolerance. Seed germination in lettuce plants was greatly enhanced by pre-treatment with water-soluble CNPs, even when the plants were subjected to salt stress (150 mM NaCl). Nanoparticles (NPs)-like quantum dots (QDs) are gaining popularity because their key characteristics in the range of 2–10 nm range, making them ideal candidates for use as carriers (Bai, Purcell-Milton, & Gun’ko, 2019). Advantages of various QDs for plants have been reported in multiple studies (Li et al., 2018). Gohari et al. (2021) found that the chlorophyll florescence and activities of antioxidant enzymes were all greater, while electrolyte leakage (%), MDA, and H₂O₂ content were all lower. When applied at the optimal concentration (50 mg L⁻¹), MWCNTs-COOH have the potential to reduce the detrimental impacts of salinity stress by boosting the levels of non-enzymatic (i.e. phenolic content) and enzymatic (i.e. ascorbate peroxidase (APX), catalase (CAT) and guaiacol peroxidase (GP) activity) antioxidant components (Gohari et al., 2020).

4. Future perspective

Applications of CNMs at maximum allowable levels have been shown to improve germination and seedling growth, expedite photosynthesis process and nitrogen metabolism, alter miRNA expressions and total proteins, and cause positive changes in gene expression in a variety of crops. These benefits encourage the application of CNMs in the proper quantity to help crops grow better. SWCNTs, MWCNTs, fullerenes and its hydroxyl derivatives (fullerols) have all gained the interest of plant biotechnologists for their potential uses in managing plant growth. The potential environmental benefits of MWCNTs for crop production suggest they may be a useful tool for addressing problems with plant growth and yield that are currently hindering agricultural progress. If these problems are resolved, then the production could be improved. The use of CDs as a fertilizer, for instance, has the potential to introduce in a number of new possibilities in the field of nanobiotechnology. The CDs also provide a great way to see plant tissues, which aids in determining their phyototoxicity. This information is crucial before recommending the use of special CNMs in agriculture.

The exogenous application of CNMs has demonstrated its potential in enhancing plant tolerance to abiotic stress across diverse species. However, there remains a significant knowledge gap regarding the molecular mechanisms that underlie the complex interplay of positive and negative effects of CNMs in plants. The relationship between the diverse properties of CNMs and their influence on the expression of essential genes and proteins involved in plant development remains elusive. Consequently, the specific mechanisms by which CNMs impact plant development at the molecular level are not yet understood. To address these gaps, future studies should focus on investigating the role of CNMs physicochemical characteristics in the root system, as well as their translocation within different plant organs. Such research endeavours will contribute to a comprehensive understanding of CNMs effects on plant physiology and development.

5. Conclusion

In this article, the effects of CNMs on different plant systems under drought and salt stress are tried to be summed up. The potential of CNMs for advancing plant sciences is substantial. Because of the extremely small size of CNMs, they are able to pass through the seed coat and the cell wall of the plant. This can cause modifications in the plant’s physiological and metabolic processes, which can subsequently result in higher in biomass and grain yield despite adverse conditions. One of the concerns that need to be carefully addressed in this sector is the phytotoxicity that has been observed in some of the cases. Controlling the concentrations and doses is one way to address this issue and avoid further injury. Despite these drawbacks, CNMs have a lot of potential as a low-cost strategy for boosting crop production and abiotic stress tolerance in the future.

Acknowledgments

We are thankful to Department of Biology, College of Science, Imam Abdulrahman Bin Faisal University and Department of Physics, Faculty of Applied Science, Umm Al-Qura University for their valuable support.

Disclosure statement

No potential conflict of interest was reported by the authors.