Abstract
Plants encounter various nanomaterials (NMs) as pesticides and fertilizers. It is also possible that nanomaterials reach plants as waste from consumer products and industry. The effects of such NMs on plants have been widely studied, and both positive and negative effects of NMs on plant growth and development have been reported. Recent metabolomics studies suggest that nanoparticles affect the concentration of secondary metabolites in plants by modulating reactive nitrogen/oxygen species, gene expression, and signaling pathways. Secondary metabolites are plant compounds that accumulate in plants through their secondary metabolism. To date, more than 200,000 defined structures of secondary metabolites have been identified, among which many of them possess antibacterial, antifungal, antiviral, anti-inflammatory, hepatoprotective, antidepressant, antioxidant, neuroprotective, and anticancer properties. The application of elicitors is a simple strategy to increase the production of secondary metabolites in plant cell and tissues. The ability of nanomaterials to induce plant secondary metabolism has recently been exploited in the elicitation of pharmaceutically important compounds from various plant species. The ability of different NMs to induce the accumulation of different classes of compounds in the same plant species has also been accomplished. The molecular mechanisms behind the effects of NMs on plant secondary metabolism revealed the putative genes involved in NM-mediated elicitation of various plant compounds in several reports. This chapter reviews the current understanding of the effects of nanoparticles on plant secondary metabolism and the elicitation of pharmacologically important compounds from plant species.
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1 Introduction
In this era of nanotechnology, nanomaterials (NMs) are finding applications in various fields, including science, industry, medicine, and agriculture. Several consumer products, medicines, fertilizers, pesticides, cosmetics, food packings, paints and electronics containing NMs are already on the market.
Plants are exposed to NMs through various pathways. NMs can move to plants as NM-containing wastes that are released into the environment by industries and consumer products in water and soil. The predicted concentration of some nanoparticles (NPs) in soil is: silver (Ag): 0.91–1.8 ng/kg; titanium oxide (TiO2): 0.09–0.24 μg/kg; zinc oxide (ZnO): 0.01–0.03 μg/kg (Sun et al. 2014). On the other hand, recent advances in agriculture use formulations containing NMs such as fertilizers, fungicides and pesticides. The concentration-dependent response to NPs varies greatly among different plant species, which has been reported, for example, for NPs from ZnO: 40–1200 ppm, (Mosquera-Sánchez et al. 2020; Sadak and Bakry 2020) cerium oxide (CeO2): 125–500 ppm, (Rico et al. 2014) copper oxide (CuO): 200–400 ppm, (Wang et al. 2019) and gold (Au): 5 ppm (Kang et al. 2016) to show the effect of nanofertilizers and pesticides. Effective concentrations for plant protection applications range from 2 to 2000 ppm for Ag NPs alone across plant species and pathogens (Elmer and White 2018). Thus, while the application of nanotechnology is expected to revolutionize agriculture, NMs that enter the environment directly as agrochemicals or indirectly as industrial or household wastes are proving to be pollutants with unknown consequences for plants.
Previous studies on various model plant species and crops have shown that NMs affect plant growth and development both positively and negatively depending on their concentration. However, it is known that the biologically relevant concentration of NMs strongly depends on their metallic core, physicochemical properties, substrate and plant species. NMs are known to interfere with metabolic processes and lead to the formation of reactive oxygen species (ROS)/reactive nitrogen species (RNS), damage the structure and function of cell membranes, and reduce enzyme activities and DNA synthesis. Recent literature also suggests that plant secondary metabolism is also affected by NMs.
Secondary metabolism is crucial for plants as they play an indispensable role in plant survival: as protection against herbivores and pathogenic microbes, as signals for symbiotic interactions of plants with beneficial microorganisms, as allelopathic agents in natural habitats for protection against competitors, as physical and chemical barriers against abiotic stressors such as UV radiation, and as endogenous regulators of plant growth regulators.
The small molecular products that are biosynthesized in plants through their secondary metabolic pathways are called plant secondary metabolites. These compounds are generally classified as terpenes, steroids, phenols, flavonoids and alkaloids and are derived from primary metabolites or as an intermediate in the primary metabolic pathway (Chandran et al. 2020; Pang et al. 2021). Plant secondary metabolites play an important role in plant defense mechanisms against biotic and abiotic stresses (Khare et al. 2020; Mahajan et al. 2020). In particular, phenylpropanoids are involved in the regulation of oxidative stress, free ion chelation, cell wall lignification, and plant defense (Agati et al. 2012). In addition, secondary metabolites are also known to be involved in pest defense (Barlow et al. 2017; Stevenson 2020), signal transduction in plant–microbe symbiosis (Adedeji and Babalola 2020) and plant innate immunity (Piasecka et al. 2015).
Apart from their beneficial effects in plants, many secondary metabolites are economically important as medicines, flavors and fragrances, dyes and pigments, pesticides and food additives. Useful remedies from herbal medicine are due to the presence of various secondary metabolites (Chandran et al. 2020). For example, a recent study showed that 12 pure compounds from Clerodendranthus spicatus (Thunb.) C. Y. Wu ex H. W. Li, an herb widely used in traditional Chinese medicine for the treatment of kidney inflammation, gout, and dysuria, promoted the excretion of uric acid (Chen et al. 2020). More than 500 secondary metabolites have been reported from 46 species of the genus Lycopodium, and these secondary metabolites have been shown to have several medically important bioactivities, including neuroprotective, anti-inflammatory, anti-cancer, antiviral, and antimicrobial activities (Wang et al. 2021).
The quantity of secondary metabolites produced by natural biosynthesis in plants is limited to meet the growing demand of the pharmaceutical industry. Thus, development of alternative biotechnological approaches is necessary to boost production of secondary metabolites (Thakur et al. 2019). Elicitation is one of the most commonly used techniques to enhance the biosynthesis of secondary metabolites (Thakur et al. 2019; Yazdanian et al. 2021).
In recent years, NMs have emerged as novel triggers for inducing biosynthesis of bioactive compounds in plants (Shakya et al. 2019; Rivero-Montejo et al. 2021). Ag NP treatment increased artemisinin content by 3.9-fold in 20-day-old hairy root cultures of Artemisia annua L. (Zhang et al. 2013). Hydroponically grown Bacopa monnieri L. treated with copper-based NPs (Cu) improved antioxidant capacity and showed hormetic increase in the content of saponins, alkaloids, flavonoids and phenols (Lala 2020). Celastrol, a therapeutically important phytochemical, was increased in adventitious and hairy root cultures of Celastrus paniculatus Willd. after treatment with Ag NP (Moola et al. 2021). The elicitation of various classes of bioactive secondary metabolites in Hypericum perforatum L. cell suspension cultures treated with various metal (Ag, Au, Cu, Pd) and metal oxide (CeO2, CuO, TiO2, ZnO) NPs has been recently reported (Kruszka et al. 2022).
In this chapter, we discuss the effects of NMs on secondary metabolism in plants, focusing on signaling events and key medicinal agents that are enhanced by NPs.
2 Plant’s Response to Nanomaterials
Exposure to NMs has been found to induce changes in various physiological, morphological and developmental processes of plants. In general, plant metabolism can be divided into primary (associated with energy and biosynthesis of building blocks) and secondary (more specialized molecules) metabolism (Erb and Kliebenstein 2020). Primary metabolites consist of the products of photosynthesis, glycolysis, the tricarboxylic acid cycle (TCA cycle), biosynthesis of amino acids, lipids, and some natural polymers. Cu NPs minimized the negative effects of drought stress on photosynthetic pigments and promoted plant growth, development and grain yield in Zea mays L. (Van Nguyen et al. 2021). Foliar application of silica (SiO2) and ZnO NPs in Cucumis sativus L. significantly increased chlorophyll content and various amino acids and modulated carbon metabolic processes in leaves (Li et al. 2021). For example, increased melatonin synthesis by application of ZnO NPs helped in controlling drought-induced damage in Z. mays (Sun et al. 2020). Melatonin is a secondary metabolite and is known to improve stress tolerance in plants by stimulating antioxidant activities (Marioni et al. 2008; Debnath et al. 2020). The quality, visual attractiveness and nutritional properties of Punica granatum L. sap have been found to be affected by the reduction of bioactive compounds such as anthocyanins and punicalagin under drought stress (Mena et al. 2013). Spraying leaves with selenium NPs increased phenolic content and improved the quality of drought-affected fruits of P. granatum (Zahedi et al. 2021).
4.2 NPs as Elicitors of Phytopharmaceuticals
Controlled elicitation is a strategy to increase the production of important secondary metabolites. As described in the previous sections, plants recognize different types of NMs and induce their secondary metabolism, which opens a new opportunity to improve the production of pharmaceutically important compounds in medicinal plants (Marslin et al. 2017; Shakya et al. 2019; Kruszka et al. 2020; Rivero-Montejo et al. 2021). Elicitation of several classes of secondary metabolites such as glucosinolates, terpenes and alkaloids have been reported to be obtained using NPs. The chemical structure of some pharmaceutically important secondary metabolites elicited using NMs is shown in Fig. 6.2.
Some of the pharmaceutically important secondary metabolites elicited from medicinal plants using NMs; (1) naringenin, (2) apigenin (R1 = H, R2 = OH, R3 = H, R4 = OH, R5 = H, R6 = H), (3) cirsimaritin (R1 = H, R2 = OMe, R3 = OMe, R4 = OH, R5 = H, R6 = H), (4) xanthomicrol (R1 = OMe, R2 = OMe, R3 = OMe, R4 = OH, R5 = H, R6 = H), (5) kaempferol (R1 = H, R2 = OH, R3 = H, R4 = OH, R5 = OH, R6 = H), (6) isokaempferide (R1 = H, R2 = OH, R3 = H, R4 = OH, R5 = OMe, R6 = H), (7) quercetin (R1 = H, R2 = OH, R3 = H, R4 = OH, R5 = OH, R6 = OH), (8) catechin, (9) chlorogenic acid, (10) cichoric acid, (11) atropin, (12) hyoscyamine, (13) scopolamine, (14) artemisinin, (15) carnosic acid, (16) tanshinone, (17) γ-mangostin, (18) garcinone B, (19) emodin, (20) fusaroskyrin. (Figure constructed by D. Kruszka)
4.2.1 Flavonoids
Flavonoids are natural bioactive compounds found predominantly in various parts of plants and have been attributed to various pharmacological and therapeutic properties (Panche et al. 2016). In Momordica charantia L., an increase in flavonoid concentration induced by 5 mg/L Ag NPs was observed (Chung et al. 2018c). Stimulation of Thymus daenensis Celak. plant cells with SWNT increased the total flavonoid content (Samadi et al. 2021). Quercetin is an important and abundant flavonoid from plants with rich pharmaceutical properties such as antitumor, anti-infective, anti-inflammatory and antioxidant activities (Qi et al. 2020). Increased quercetin content was observed in shoots and roots of Nigella arvensis L. treated with 50 mg/L NiO NPs (Modarresi et al. 2020). The level of several flavonoid aglycones like apigenin, kaempferol and quercetin was increased upon treatment with the Ag, Au, Cu and Pd NPs treatment, whereas flavonoid glucosides like quercetin 3-O-hexoside or quercetin 3-O-malonylhexoside was elicited by CuO NPs treatment in H. perforatum L. cell suspension cultures, (Kruszka et al. 2022). Anthocyanins are another subgroup of flavonoids and play an important role in the nutraceutical, pharmaceutical and food industries. After the application of ZnO NPs in the shooting culture of Lilium ledebourii (Baker) Boiss., an increase in anthocyanin concentration was observed, and the effect of polyphenol induction was dose-dependent (Chamani et al. 2015). Similarly, stimulation with SiO2 NPs increased the concentration of the anticancer flavonoids xanthomicrol, isocaempferide, and cirsimaritin in the hairy roots of Dracocephalum kotschyi Boiss. (Nourozi et al. 2019b). Treatment of D. kotschyi cell suspension cultures with Fe3O4 magnetite NPs increased the content of rosmarinic acid, naringin, carvacrol, rutin, quercetin, apigenin and thymol (Taghizadeh et al. 2021).
4.2.2 Phenolic Acids
Phenolic acids are an important group of plant secondary metabolites with a wide range of bioactivities, including anticancer, anti-inflammatory, neuroprotective, antioxidant, and antimicrobial activities (Kiokias et al. 2020). The phenolic acids, such as chlorogenic acid, coumaric acid, gallic acid, and tannic acid, were accumulated after the callus of Prunella vulgaris L. was exposed to Ag, Au, and Ag/Au NPs (Fazal et al. 2016). Moreover, Ag NPs induced the biosynthesis of phenolic acids more strongly than AgNO3 in the hairy root culture of Cucumis anguria L. (Chung et al. 2018b). Ag and Cu NPs stimulated the secretion of hydroxycinnamic acid and hydroxybenzoic acid derivatives from H. perforatum cells into media of cell suspension cultures (Kruszka et al. 2022).
4.2.3 Glucosinolates
Glucosinolates are a group of Sulphur-containing hydrophilic secondary metabolites found primarily in members of the Brassicaceae and related families (Poveda et al. 2020; Wu et al. 2021). Glucosinolates exhibit some pharmacological bioactivities such as anti-inflammatory, antimicrobial, cholinesterase inhibitory, antioxidant and anticancer properties (Maina et al. 2020). Ag NPs induced biosynthesis of glucosinolates, a group of compounds responsible for response to pathogen attack, in addition to phenolic compounds in seedlings of Brassica rapa L. (Thiruvengadam et al. 2015). Treatment of hairy roots of Chinese cabbage with CuO NPs increased the accumulation of glucosinolates (Chung et al. 2018c). Moreover, the extracts of hairy roots released showed higher antimicrobial activity compared to the control.
4.2.4 Terpenoids
Terpenes and terpenoids are biogenic volatile organic compounds of plant secondary metabolites with high biological activity against various human diseases (Kim et al. 2020). The production of monoterpenes (linalool and linalyl acetate) in shoot cultures of Mentha longifolia L. grown under the influence of Co (0.8 mg/L) and Cu (0.5 mg/L) NPs (Talankova-Sereda et al. 2016). They reported that the higher production of essential oils corresponded with the growth index (Talankova-Sereda et al. 2016). Artemisinin, one of the important pharmaceutical compounds used as antimalarials, was induced by 2.5 and 5 mg/L Co NPs in A. annua cell culture (Ghasemi et al. 2015). Similar results were obtained after stimulation of A. annua hairy root culture by Ag-SiO2 core–shell nanostructures (Zhang et al. 2013). A stimulatory effect of 8–21 nm Ag NPs on the increased production of diosgenin was observed in Trigonella foenum-graecum L. seedlings (Jasim et al. 2017). ZnO NPs (0.1–10 mg/L) increased the biosynthesis of rebaudioside-A and stevioside in shoot cultures of Stevia rebaudiana (Bert.), in addition to the induction of oxidative stress (Javed et al. 2017). Similarly, chitosan nanofibers and cellulose nanofibers increased the production of betulinic acid and betulin in cell suspension cultures of Betula pendula Roth (Vahide et al. 2021).
4.2.5 Alkaloids
Alkaloids are a large group of plant secondary metabolites with nitrogen atom(s) in their structure that exhibit a wide range of medicinally important bioactivities (Eguchi et al. 2019). Ag NPs induced the biosynthesis of atropine alkaloid in hair root culture of Datura metel L. and the highest level of atropine was detected after 48 h of treatment (Shakeran et al. 2015). This NP -based elicitor was better than AgNO3 and two other biotic elicitors (Staphylococcus aureus F. J. Rosenbach and Bacillus cereus Frankland & Frankland). Hyoscyamine and scopolamine levels were significantly increased 24 h after application of 450–1800 mg/L Fe2O3 NPs in the hairy root culture of Hyoscyamus reticulatus L. (Moharrami et al. 2017). SiO2 NPs triggered the production of tropane alkaloids (hyoscyamine and scopolamine) in hair root cultures of two Hyoscyamus species namely, H. reticulatus and H. pusillus L. (Hedayati et al. 2020). Cell suspension cultures of Corylus avellane produced more taxol and baccatin III after treatment with 5 mg/L Ag NPs (Jamshidi and Ghanati 2017). Available examples of the elicitation of pharmaceutically important secondary metabolites using NPs are summarized in Table 6.3.
4.2.6 Xanthones
Xanthones are bioactive secondary metabolites that possess antibacterial, antifungal activities, and could inhibit acetylcholinesterase, butyrylcholinesterase and tyrosinase (Badiali et al. 2018; Tusevski et al. 2018). Xanthones also possess neuroprotective activities (Xu et al. 2016; Velingkar et al. 2017). Ag, Au, Cu, Pd and CuO NPs stimulated accumulation of prenylated derivatives of xanthones (γ-mangostin, garcinone B and hyperxanthone C), whereas glycosylated xanthones (eg.: mangiferin, homomangiferin, neomangiferin) content was increased after Au, Cu and Pd NPs treatment in cell suspension system of H. perforatum L. (Kruszka et al. 2022).
4.2.7 Anthraquinones
Antidepressant activities of H. perforatum L. extracts are attributed to naphthodianthrones/ anthraquinones such as hypericin or pseudohypericin (Velingkar et al. 2017). Hypericin content was increased by TiO2-perlite nanocomposite treatment in H. perforatum L. shoot cultures (Ebadollahi et al. 2019). Emodin and emodin anthrone contents were respectively increased by Pd and CeO2 NPs treatment in H. perforatum L. cell suspension cultures (Kruszka et al. 2022). In the above study, a 98.6-fold increase of fusaroskyrin after Ag NP treatment was also reported.
5 Conclusion and Prospects
Plant secondary metabolites play an important role in plant’s fitness and adaptation. Therefore, alteration of secondary metabolism by NPs could affect crop quality and agricultural productivity. The pharmacological properties of several medicinal plants are attributed to the crude extracts or decoctions and not to the individual compounds. Therefore, any alteration in the secondary metabolism of medicinal plants would affect their pharmacological potential and market value. Among the numerous compounds accumulated in plants, many of them possess antibacterial, antifungal, antiviral, anti-inflammatory, hepatoprotective, antidepressant, antioxidant, neuroprotective and anticancer properties. A better understanding of the effects of NPs on plant secondary metabolism would allow us to develop strategies to help plants cope with the increasing presence of NPs in the environment and to develop new molecular pharmaceutical tools (Fig. 6.3).
The potential effects of secondary metabolic changes caused by NMs on other associated plant parameters. NMs can enter plants in both intentional and unintentional ways. Although changes in secondary metabolism could affect plants' ability to protect themselves against pathogens, herbivores, and adverse environmental conditions, as well as their ability to communicate with beneficial microbes, more research is needed to understand the exact consequences (Figure constructed by G. Franklin)
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Acknowledgements
This work was supported by the National Science Centre (NCN), OPUS project Reg. No. 2016/21/B/NZ9/01980. RKS and DK are recipients of PhD and postdoctoral fellowships, respectively, from this project. DM and GF acknowledge the NANOPLANT project, which received funding from the European Union's Horizon 2020 research and innovation program under grant agreement No. 856691. The authors thank Mr F. Gerin Danny, Kings College London, for his help in figure 6.3 drawing.
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Selvakesavan, R.K., Kruszka, D., Shakya, P., Mondal, D., Franklin, G. (2023). Impact of Nanomaterials on Plant Secondary Metabolism. In: Al-Khayri, J.M., Alnaddaf, L.M., Jain, S.M. (eds) Nanomaterial Interactions with Plant Cellular Mechanisms and Macromolecules and Agricultural Implications. Springer, Cham. https://doi.org/10.1007/978-3-031-20878-2_6
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