Plant cell nanomaterials interaction: Growth, physiology and secondary metabolism

CHAPTER TWO

Plant cell nanomaterials interaction: Growth, physiology and secondary metabolism Mubarak Ali Khana,*, Tariq Khanb, Zia-ur-Rehman Mashwanic, Muhammad Suleman Riaza, Nazif Ullaha, Huma Alid, Akhtar Nadhmane a Department of Biotechnology, Faculty of Chemical and Life Sciences, Abdul Wali Khan University Mardan (AWKUM), Mardan, Pakistan b Department of Biotechnology, University of Malakand, Chakdara, Pakistan c Department of Botany, PMAS Arid Agriculture University, Rawalpindi, Pakistan d Department of Biotechnology, Bacha Khan University, Charsadda, Pakistan e Institute of Integrative Biosciences, CECOS University, Peshawar, Pakistan *Corresponding author: e-mail address: [email protected]

Contents 1. 2. 3. 4. 5.

Introduction Metallic nanoparticles effect development of plants The effect of nanoparticles on plant secondary metabolism Impact of nanomaterials on plant biochemical parameters Applications of nanomaterials during plant in vitro cultures 5.1 Towards callus induction and organogenesis 5.2 Nanoparticles induce somaclonal variations 5.3 Towards controlling contamination 5.4 Size directs the function of nanomaterials in plants 5.5 Concentration affects the function of NPs in plants 6. Adverse effects of nanomaterials on plants 7. Conclusions and future prospects References

23 25 36 37 38 38 40 40 41 42 43 45 46

1. Introduction Nanotechnology has emerged as a promising discipline during the last decade with applications in a plethora of fields. Nanoscale systems by the name “Nanomaterials” as an umbrella term have found diverse applications in bringing innovation to different biological processes. From their potential Comprehensive Analytical Chemistry, Volume 84 ISSN 0166-526X https://doi.org/10.1016/bs.coac.2019.04.005

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2019 Elsevier B.V. All rights reserved.

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to be used as antimicrobial, anticancer agents to their use in sensing disorders and solving agricultural and environmental problems, nanomaterials have infinite applications. In the recent years, nanomaterials have found their way in agriculture sector especially through their significant effects on plants. Whether it be the production of food, medicine or shelter; plants define the dynamics of life and therefore agriculture sector is of pivotal importance to the developing countries. Nanomaterials have primarily been employed in agriculture sector to enhance seed germination and perform genetic alterations to increase growth and yield [1,2]. Their applications to plants are diverse including speedy growth, enhanced production, increased resistance to diseases, and improvements in their physiological and biochemical responses (Fig. 1). Also, the medicinal value of different plants has been highlighted with a wide array of research in this field since long. With

Fig. 1 Illustration of possible routes of entry for NPs into the plant cell system.

Plant cell nanomaterials interaction

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the rapid pace at which the world population is growing, the need for food and medicinal compounds obtained from plants is going to increase sooner than later. However, nanotechnological tools have the potential to speed up the growth of crop plants that can alleviate the food scarcity facing the world and the capability to increase the yield of important medicinal compounds from plants by altering the secondary metabolism [3,4]. Nanomaterials can also add value to the medicinal compounds produced in plant by increasing their potency through conjugation or synergism. Furthermore, nanomaterials can impart pathogen resistance to plants thus reducing the need for toxic insecticides and pesticides [5]. In addition, nanoparticles have the capacity to eliminate microorganisms especially during in vitro cultures that are hampered by microbes, which act as a source of contamination. Nanoparticles have been used in tissue culture media to eradicate bacteria and therefore they enhance the chances of healthy growth of plants. Nanomaterials, in the form of nanoparticles, nanosheets, nanofilms, nanorings, nanorods, nanotubes and several other types have found infinite applications in research. The famous class of nanomaterials is nanoparticles. Nanoparticles are nanoscale small particle like systems that are formed through reduction of certain metal salts and are capable of independent action in a process. Some of the potent nanoparticles include those obtained from metals and metal oxides such as Silver nanoparticles (Ag NPs) and Zinc Oxide nanoparticles (ZnO NPs). These particles have the capacity to penetrate tiny systems and can travel to distant parts within plants to trigger different biochemical and physiological pathways. The size, dimensions and concentration of these nanoparticles have been shown to play significant roles in governing their functions in different plants. Other types of nanomaterials that are used in plants include carbon nanotubes, dendrimers and quantum dots, which have been shown to be beneficial in triggering organogenic responses during in vitro cultures of various plants [6]. This chapter aims to review the prominent effects of nanomaterials on plants including their effects on the physiology, growth, development, and secondary metabolism. It also highlights the effect of nanoparticles supplementation during in vitro cultures of plants. In addition, it gives insight into the role of size and concentration of nanoparticles in plants and outlines various adverse effects associated with the use of nanoparticles in plants.

2. Metallic nanoparticles effect development of plants Metallic nanoparticles comprising both of metal oxides and pure metals have recently been employed to influence the development of

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different plants. A number of development parameters tested in plants such as germination, growth, biomass accumulation, and biochemical activities have shown varying effects of these metallic nanoparticles in different plants [7]. The effects of nanoparticles in plants vary from beneficial to harmful and from apparent physiological to hidden biochemical changes. When proved beneficial, these nanoparticles enhanced germination, and growth rate leading to increased shoot and root sizes. The nanoparticles may also prove toxic for the plants in terms of deteriorating the seed quality, increased production of reactive oxygen species and changing the genetic and anatomical behaviours of the plants [8,9]. Nanoparticles that have previously been explored for their effects on plant growth include Silver nanoparticles (Ag NPs), Zinc oxide nanoparticles (ZnO NPs), Gold nanoparticles (Au NPs), Silica nanoparticles (SiO2 NPs), Nanoselenium nanoparticles (Se NP), Cerium oxide nanoparticles (CeO2 NPs), Copper and Copper oxide nanoparticles (Cu and CuO NPs), Iron nanoparticles (Fe NPs), Nickel oxide and nickel hydroxide nanoparticles (NiO and Ni(OH)2 NPs), Aluminium oxide nanoparticles (Al2O3 NPs), Indium oxide (In2O3 NPs), Cobalt oxide (CoO, Co2O3, Co3O4 NPs), and Neodymium oxide (Nd2O3 NPs) as indicated in the Table 1. It is also pertinent to note that the function of nanoparticles is defined by the plant species that they are tested upon. Different plant species may respond differently to different nanoparticle types at different concentrations [10]. Among these nanoparticles, ZnO NPs have been shown to boost development in terms of seed germination rate, seedling vigour, early flowering and increased chlorophyll content in different plants such as cucumber [11], green pea [12], peanut [13], and Glycine max L (soybean) [14]. Nanoparticles are also an efficient sources of minerals delivery to plants. The findings of Belluco et al. [15] showed that addition of ZnO NPs as compared to ZnSO4 in the nutrient media increased the shoot height, root length, and the biomass of maize plant. Similarly, elevated levels of chlorophyll and carotenoids were detected as a result of ZnO NPs application in pearl millet [16]. In another study, ZnO NPs were shown to increase shoot and root length by 22.7% and 43.4%, respectively, in cluster bean [17]. Similarly, Silver nanoparticles (Ag NPs) have been found to positively affect growth parameters including seed germination, seedling growth, and fruit yield and weight, in plants such as Cucumis sativus [18]. In a study by Syu et al. [19], Ag NPs activated a number of genes involved in the process of cell division, enhanced the metabolism and upregulated signalling of

Table 1 Impacts of different nanomaterials on plant cellular growth, physiology, and secondary metabolism in industrially important plant species. Nanomaterial S. No. type/composition Plant species

Nanomaterial concentration Size

1.

Silver nanoparticles

Phaseolus vulgaris

20, 25, 50, 100 mg kg 1

2.

Silver nanoparticles

Trigonella foenumgraecum

200 μL of 1 μg mL 1 (w/v)

3.

CuO, ZnO and Fe2O3 nanoparticles

Cicer arietinum 12.5, 25, 50, 100 and 150 mg

4.

ZnO nanoparticle

Gossypium hirsutum

8–21 nm

25–200 mg L– 2–54 nm l

Effect tested

Results

References

To study the effect on crop growth and the physiochemical properties

Dosage of 50 mg kg 1 showed the [47] highest efficacy in improving the plant growth and soil health

To study the effect on the modulation of secondary metabolites

Increased production of major phytochemical Diosgenin (214.06  17.07 g m 1)

[48]

To study the production of Exo-polysaccharides and the growth patterns of Rhizobia

Nanoparticles differentially modified the production of plant growth promoting substances under in vitro conditions in the nodule forming Gram-negative bacterium Rhizobium sp.

[49]

To study the effects on seedlings growth and biomass accumulation, MDA contents detection and measurement of total soluble protein contents, Quantification of photosynthetic pigment, Estimation of antioxidant enzymes activity, Detection of isoenzymes expression pattern by native PAGE analysis

ZnO NPs were able to interact with [50] the meristematic cells and led to the activation of different biochemical pathways that are conducive to biomass accumulation

Continued

Table 1 Impacts of different nanomaterials on plant cellular growth, physiology, and secondary metabolism in industrially important plant species.—cont’d Nanomaterial S. No. type/composition Plant species

Nanomaterial concentration Size

5.

Nano-sized TiO2 Hyoscyamus niger

6.

ZnO nanoparticles

Carthamus tinctorius

0, 10, 100, 500, and 100l mg L–l

7.

Silver nanoparticles

Radish and lettuce

1, 2.5, 5, 10 mg L–l

8.

CeO2 nanoparticles

Cucumis sativus

20, 40, 80, 160, and 320 mg L–1

0, 20, 40 and 10–15 nm 80 mg L–l

Effect tested

Results

References

To study the effect on activation of antioxidant enzymes and the biosynthesis of hyoscyamine and scopolamine

Application of NPs in lower concentrations enhanced the production of HYO and SCO in the plant

[51]

ZnO NPs treatment at different concentrations increased the production of malondialdehyde enzyme. Whereas the production of other enzymes increased as specific concentrations, e.g., guaiacol oxidase (100 mg L 1), polyphenol oxide (10 and 500 mg L 1) and dehydrogenase (1000 mg L 1)

[52]

To study the effect of NPs on elongation of roots in water and soil

Depending on the plant species both positive and negative effects were observed for Ag NPs on the elongation of roots

[53]

Assays for enzyme activity, and to study the effect of NPs on translocation and physiological parameters

NPs application increased the [54] catalyse activity in the roots whereas decreased activity of ascorbate peroxidase was detected in the leaves

50–100 nm To study the effect on plant growth and physiology

8  1 nm

Triticum aestivum

9.

mPEG-PLGAbased nanoparticle

10.

Titanium dioxide Zea mays nanoparticles

0.3 or 1 g L

11.

ZnO NP

0, 100, 250 <100 nm and 500 mg L–

Mung bean broth

200 nm

1

Magnetic iron nanoparticles

Triticum 100, aestivum L. 200 kg ha 1, var. Wyalkatchem

13.

Iron oxide nanoparticles (FeO NPs)

Trifolium repens

NPs had a promoting role and [55] enhanced the overall plant growth

To study the effect of NPs on the NPs interfered with the [56] growth of growth of leaf and root, transportation of water in the plant transpiration, root hydraulic body and associated leaf responses conductivity and pore size in root cell wall

1

12.

To study the effect of NPs on wheat seedling by analysing morphology and physiology parameters such as seeds vigour index, root vitality and total chlorophyll content

10 nm

0.032, 0.32, 10.2 nm 3.2, mg kg 1, (Fe) 0.01, 0.1 and 1 mg kg 1

The Antifungal activity of NPs against plant pathogen Fusarium graminearum was investigated.

ZnO NPs showed significant antifungal activity

[57]

The effect of NPs enriched biochars on the growth of plant nutrient uptake mycorrhizal colonization and improvement of soil quality were investigated

Phosphorus (P) and nitrogen [58] uptake in wheat shoots were significantly greater for a low application rate of BMCs (100 kg ha 1 ). The present formulation of BMC was effective in enhancing growth of wheat at low application rate (100 kg ha 1)

To study the effect of NPs on plant growth and arbuscular mycorrhizal fungi

At a concentration of 3.2 mg kg 1 [59] the FeO NPs significantly reduced mycorrhizal clover biomass (34%) due to the reduction in the glomalin content and root nutrient acquisition of AMF Continued

Table 1 Impacts of different nanomaterials on plant cellular growth, physiology, and secondary metabolism in industrially important plant species.—cont’d Nanomaterial S. No. type/composition Plant species

Nanomaterial concentration Size 1

Effect tested

Results

References

5.9 (Ag NP) 5.4 (TiO2NP)

To investigate the effect of NPs on the bacteria in the rhizoplane and plant growth during early stage

In wheat plant TiO2 NPs enhanced [60] the germination and seedling growth Furthermore, a significant decrease was observed in the quantity of total rhizoplane bacteria upon the application of positively charged TiO2 NPs, whereas negatively charged Ag NPs and TiO2 NPs had the opposite effect and led to an increase

14.

Silver and Triticum titanium dioxide aestivum, nanoparticles Linum usitatissimum

15.

Iron oxide nanoparticles

Linum usitatissimum

1, 100, and 1000 mg L 1

56 nm

To evaluate the NPs as a nutrient A positive correlation was observed [61] for plant growth between the NPs dose size and the plant growth, which may be due to changes in metabolic activity

16.

ZnO nanoparticles

Triticum aestivum

25 ppm

25 nm

To study the effect of NPs on different morphological features in plant growth

NPs markedly increased shoot and [62] root length, number of leaves and the plant weight. Increase was also observed in the number and weight of gains

17.

Silver nanoparticles

Bacopa monnieri

10 ppb, 100 ppb, 10 ppm, 100 ppm

2–50 nm

To study the effect on plant metabolism, quantification of protein, carbohydrate and phenols, and the analysis of antioxidant enzymes; catalase and peroxidise in the plants body grown in hydroponic solution

Enhanced peroxidase and catalase [63] activity simulated the stress conditions induced by the silver nitrate treatment. No severe toxic effects were observed

100 mg L

Nanoparticles, multi-walled carbon nanotube, aluminium, alumina, zinc, and zinc oxide

Rassica napus 20, 200, 2000 mg L (rape), Raphanus sativus (radish), Lolium perenne (ryegrass), Lactuca sativa (lettuce), Zea mays (corn) and Cucumis sativus (cucumber)

19.

ZnO nanoparticles

9–37 nm Lolium perenne 10, 20, 50, 100, 200, and (ryegrass) 1000 mg L 1

To study the upward translocation Zn content was significantly lower [65] of NPs inside the plant body and in the plant shoots treated with their uptake at the plant cells ZnO NPs as compared to those treated with Zn+2

20.

Silver nanoparticles

Triticum 0, 50 and aestivum, 75 ppm Vigna sinensis, Brassica juncea

35–40 nm

[66] To study the effect on plant Ag NPs treatment had no growth and bacterial populations significant effect on Wheat plant. in the soil Ag NPs increased the root nodulation in cowpea at a concentration of 50 ppm and in brassica enhanced shoot growth at a concentration of 75 ppm. A

21.

Zn Nanoparticles Brassica napus 5, 15, and 25 mg L 1

30–70 nm

To analyse various biochemical and physiological processes, study the effect on in vitro seed germination

18.

1

To study the toxic effect of NPs 5–20 nm on seed germination and plant (CNT), 30–103 nm growth (Al), 13 nm (Al2O3), 19 e36 nm (ZnO), 58 nm (Zn)

IC50 values were calculated for Zn [64] NPs and ZnO NP in different plants. In case of radish the IC50 value was 50 mg L 1 while in case of rape and ryegrass the value was 20 mg L 1

[67] Zn NPs had a positive effect on plant germination and caused the production of antioxidant enzymes such as superoxide dismutase and secondary metabolites. Zn NPs treatment also caused a significant increase in the chlorophyll content Continued

Table 1 Impacts of different nanomaterials on plant cellular growth, physiology, and secondary metabolism in industrially important plant species.—cont’d Nanomaterial S. No. type/composition Plant species

Nanomaterial concentration Size

30 μg m

1

Effect tested

Results

References

22.

Zinc and copper Citrus nanoparticles reticulata

23.

Silver nanoparticles

Triticum aestivum

25, 50, 75 and 34 nm 100 mg L

To study the effect on growth of In wheat plant Ag NPs application [69] wheat plant under abiotic heat showed a protective effect against stress heat stress led to an improvement of 5 and 5.4% in root length, 22.2% and 26.1% in shoot length, 1.3% and 2% in plant fresh weight and 0.36% and 0.60% in plant dry weight at concentration of 50 and 75 mg L 1, respectively

24.

Silver nanoparticles

Oryza sativa

25, 50, 75, 34 nm and 100 mg L

To study the effect on the growth Ag NPs showed a dose dependent [70] of rice plant under biotic stress effect where higher concentrations due to Aspergillus of Ag NPs significantly reduced the aflatoxins level whereas the lower concentrations showed no or negligible effects

25.

Silver nanoparticles

Citrus reticulata

10, 20, 30, and 40 ppm

To study the effect on disease incidence against Canker disease

8–32 nm (Zn) 15–30 nm (Cu)

8 nm to 28 nm

To study the effects on in vitro Zn NPs were shown to be more [68] germination and analyse different potent as compared to Cu NPs. Zn biochemical reactions NPs application had a significant effect in improving different germination parameters

At a concentration of 30 ppm Ag NPs provided resistance to the plants against canker disease

[71]

450 nm 1.92  1012 and 3.54  1012 nanoparticles mL 1

To study NPs as carrier systems Increased biological activity was for the delivery of gibberellic acid, observed in plant with NPs as a plant growth hormone compared to those with free hormone

Arabidopsis thaliana

0.5 and 3.0 mg L

70–90 nm

To analyse the chlorophyll, anthocyanin and metal content in plant tissue and study the gene expression profile

Carbon nanoparticles

Triticum aestivum

10 to 150 mg L

20–50 nm

To study the effect on absorption Higher growth rates were observed [74] of water and ionic nutrients and at all the concentrations used, plant growth whereas, 50 mg m 1 concentration was the most suitable

Silver nanoparticle

Arabidopsis thaliana

1, 2, 10, and 100 μM

8–47 nm

To study the effect on plant growth and gene expression

26.

Alginate/ Phaseolus chitosan vulgaris (ALG/CS) and chitosan/ tripolyphosphate (CS/TPP) nanoparticles

27.

Silver nanoparticles

28.

29.

1

1

[72]

[73] Ag NPs caused disruption in the structure of thylakoid membrane and reduced the chlorophyll content and affected the homeostasis of small molecules and water. Furthermore the expression of antioxidant and aquaporin genes was altered due to the application of Ag NPs leading to causing changes in the balance between the oxidant and antioxidant systems

Induced the expression of [19] indoleacetic acid protein 8 (IAA8), 9-cis-epoxycarotenoid dioxygenase (NCED3), and dehydrationresponsive RD22 genes

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different pathways in Arabidopsis thaliana. However, Ag NPs, at large, are generally showed to be less friendly in terms of growth parameters in most of the plants [20]. Furthermore, several studies have reported the positive effect of Ag NPs on antioxidant activity and reactive oxygen species (ROS) suppression in various plants. For instance Nair and Chung [21,22] showed that genes responsible for antioxidant defence system in rice plant were upregulated while a decrease was observed in sugar content, photosynthetic pigments, and root growth. Gold nanoparticles (Au NPs) have been shown to positively affect the growth and development of different plants such as rice, pumpkin, radish and mustard etc. as evident from a number of studies (Fig. 2, Table 1). For example, in a study by Arora et al. [23] treatment of mustard seedlings with Au NPs at a concentration of 10 ppm resulted in enhanced growth accompanied by increased seed yield. Similarly, Au NPs improved seed germination, and changed the miRNA expression in A. thaliana pattern which is responsible for regulation of different plant growth functions resulting in growth and yield enhancement of the plant [24]. Titanium dioxide nanoparticles (TiO2 NPs) application stimulated seed germination and growth of radicle and plumule in seedlings of canola plant [25], enhanced photosynthesis in tomato leaves [26] and increased the total chlorophyll content in cucumber plant [27]. Another study by Hatami et al. [28] showed a positive effect of TiO2 NPs on the germination frequency and vigour of seedling in plants such as Alyssum homolocarpum, Carum copticum, Nigella sativa, Salvia mirzayanii, and Sinapis alba. TiO2 NPs have also been shown to positively impact shoot and root length, biomass accumulation

Fig. 2 Effects of NPs on plant cell growth and physiological responses.

Plant cell nanomaterials interaction

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and quantity of chlorophyll in rapeseed plant [29]. Nanoparticles of Silicon oxide (SiO2 NPs) were shown to improve growth parameters, seed stability, seed germination, seedling growth, higher yield of proteins, phenolics and chlorophyll content in several plants including maize [30] tomato [31], lentils [32] and sun flower [32]. A study by Tripathi et al. [33] showed that preaddition of SiO2 NPs had a protective effect against UV-B stress in wheat seedlings suggesting their potential to be used as a substitute of abiotic stress tolerance agent. Selenium nanoparticles (Se NPs) have been used in plant systems in controlled concentrations. Haghighi et al. [34] found that both Se (bulk) and Se NPs were able to increase tomato plant growth. Comparison of Se NPs with selenate in Nicotiana tabacum showed that Se NPs stimulated organogenesis and increased the development of root system by up to 40% while no such effect was observed in case of aqueous selenate [35]. Kim et al. [36] found that the use of nano zero valent iron facilitated the elongation of root system in A. thaliana. Application of γ-Fe2O3 NPs in transgenic plants led to increased activities of superoxide dismutase (SOD) and peroxidase (POD) enzymes [37]. Application of Fe2O3 NPs in Quercus macdougallii had a positive effect on seed germination, plant growth, biomass, and chlorophyll content [38], improved iron deficiency chlorosis and endorsed the plant growth in water melon [2] and increased the yield of leaves in common bean plants [39]. Ma et al. [40] investigated the effects of CeO2 and In2O3 NPs in A. thaliana (L.) at physical and molecular levels. CeO2 NPs addition considerably increased plant biomass and higher concentration of CeO2 NPs led to the increased production of anthocyanin but showed little effect on root elongation. CeO2 NPs for instance were observed to increase biomass in barley plant as reported by Rico et al. [41]. Apart from nanoparticles, other types of nanomaterials can also influence the growth of plants. For instance, semiconductor NPs known as Quantum Dots (QDs) are used in biological and industrial processes. It was shown that CdSe QDs were able to bind to the cellulose of the cell wall in Picea omorika (a coniferous tree) and hence can be used as a biomarker for whole cell wall [41a]. Santos et al. [42] conducted tests related to DNA repair on alfalfa cells and showed the cytotoxic and genotoxic potential of CdSe/ZnS QDs in these cells. Their exposure affected the antioxidant defence system and programmed cell death in wheat seedlings [43]. However, mutants of A. thaliana upon exposure to engineered nanomaterial in the form of cadmium sulphide (CdS) QDs displayed greater tolerance level as compared to the wild type plants [44].

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Similarly, there are nanosized spherical macromolecules known as dendrimers. One such example is the generation 4 (G4) PAMAM dendrimer that has shown to cause a significant decrease in Chlamydomonas reinhardtii cell viability. Exposure of green microalgae to a PAMAM dendrimer resulted in altered gene expression, especially those involved in photosynthetic and antioxidant processes which led to enhanced ROS production [45]. Normal seed germination was shown to be affected in monocotyledonous and dicotyledonous plants including ryegrass, tomato, and lettuce as a result of application of amine-terminated G3 PAMAM dendrimer [46].

3. The effect of nanoparticles on plant secondary metabolism Plants produce several important secondary metabolites which are primarily used as their defence compounds. The medicinal value of secondary metabolites to humans is also well established. The medicinal value of these metabolites has called for the need for their enhanced production in plants. Some of the strategies used for improving the content of secondary compounds through plant cell and organ cultures include altering the culture medium composition, providing precursors and elicitors and altering the environmental conditions [75–77]. Nanomaterials among other strategies can also be employed for the increased production of these compounds. It has been suggested through various studies that the application of nanoparticles to plants and their cultures in vitro can elicit the production of important secondary metabolites. For instance, the addition of aluminium oxide (Al2O3) nanoparticles significantly enhanced the phenolic content in cell suspension cultures of tobacco [78]. Various types of nanoparticles have been shown to enhance the quantity of secondary metabolites (Fig. 4, Table 1). In a study by Al-Oubaidi and Mohammed-Ameen [79] the quantities of essential oils increased in the callus cultures of Calendula officinalis when exposed to Ag NPs. Similarly, the addition of titanium oxide (TiO2) nanoparticles enhanced the quantity of chlorogenic acid, cinnamic acid, gallic acid, o-coumaric acid, and tannic acid in the callus cultures of Cicer arietinum [80]. Furthermore, combined application of different nanoparticles has also been proven to be effective in enhancing the metabolite content in plants. For instance, maximum accumulation of total phenolic compounds was observed in Prunella vulgaris calli established in response to the addition of Au-Ag NPs (1:3) [81].

Plant cell nanomaterials interaction

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The various types of nanoparticles employed for the enhancement of secondary metabolites production in plants include Ag NPs, ZnO NPs, CuSO4 NPs, Fe NPs and TiO2 NPs [82]. Specific secondary metabolites enhancement through application of these nanoparticles include anthocyanins in Arabidopsis thaliana seedlings [19], steviol glycosides in shoot cultures of Stevia rebaudiana [83], rosmarinic acid and caffeic acid in Satureja khuzestanica shoot cultures [84], artemisinin in hairy root cultures of Artemisia annua [85], taxol in Corylus avellana cell suspension culture [86], atropine in hairy root cultures of Datura metel [87], aloin in Aloe vera suspension cells [88], hyoscyamine and scopolamine in hairy root cultures of Hyoscyamus reticulatus [89], and capsaicin in Capsicum frutescens cell suspension cultures [90]. The exact mechanism of speeding up the secondary metabolism by nanoparticles is yet to be established. One possible mechanism includes the generation of reactive oxygen species (ROS) by the nanoparticles which ultimately trigger the secondary metabolism to cope with the stress induced by ROS. Another mechanism of enhancing their production is by up-regulating the expression of various genes involved in the biosynthesis of secondary metabolites. Kaveh et al. [91] reported the upregulation of genes involved in the thalinol biosynthetic pathway in Ag NPs treated plants. Conclusively, nanoparticles have been shown to significantly affect the production of bioactive compounds in different plants and plant cell cultures and hence can be employed as standard elicitors in plant cell, tissue and organ cultures to produce valuable metabolites.

4. Impact of nanomaterials on plant biochemical parameters The changes brought about by the application of metallic nanoparticles sometimes may not be apparent in terms of physiology, but they may translate into the enhanced biochemical features including the antioxidant activity [92]. For instance, Iannone et al. [93] reported that magnetite nanoparticles (Fe3O4 NPs) enhanced the activity of different antioxidant enzymes such as catalase (CAT), superoxide dismutase (SOD) and peroxidase (POD) in wheat plants. These antioxidant enzymes form the defence system of plants and are used to quench ROS generating free radicles. The activation of these enzymes by nanoparticles defines their capacity to enhance antioxidant activities in plants. Application of CeO2 NPs at higher concentration resulted in the increased CAT activity in leaves of Prosopis juliflora velutina [94].

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Furthermore, Sharma et al. [95] reported that incorporation of Ag NPs into MS basal medium at a concentration of 50 mg L 1 decreased the production of hydrogen peroxide, proline, and Malondialdehyde (MDA) in seedlings of Brassica juncea by causing the activation of antioxidant enzymes. Another study reported that Ag NPs treatment altered the antioxidant enzymes content and expression profile of different genes that are involved in the biosynthesis of auxin, abscisic acid and ethylene. The study of Alharby et al. [96] showed that ZnO NPs application mitigated the effects of NaCl in tomato plant by upregulating antioxidant enzymes such as glutathione peroxidase (GPX) and SOD. In another study, ZnO NPs have been reported to alter genetics of the plant thus enhancing the antioxidant enzymes [97], which imparts antimicrobial potential and thus has a role in disease protection. Servin et al. [98] showed that ZnO NPs application in cluster beans led to alterations in the total protein, lipid and chlorophyll contents as compared to plants treated with ZnO. Similarly, ZnO NPs exposure increased the protein content, photosynthetic pigment levels, and upregulated the expression level of SOD and peroxidase (POX) isoenzymes thus increasing the activity of antioxidant enzymes in cotton plant [99].

5. Applications of nanomaterials during plant in vitro cultures 5.1 Towards callus induction and organogenesis Nanoparticles have been shown to positively affect the production of callus, shoots, roots including adventitious roots and hairy roots in the in vitro cultures of plants. Previous studies have shown that NPs have a positive impact on callus induction, somatic embryogenesis, shoot regeneration, shoot multiplication, and root growth (Fig. 3, Table 1). This effect is supposed to be associated with the altered gene expression, ethylene inhibition and ROS generation in response to the application of nanoparticles. For instance, Aghdaei et al. [100] reported that supplementation of growth medium with Ag NPs increased percentage of shoot induction, and callus formation from stem explants of Tecomella undulata. The increased number of shoots has been attributed to the inhibition of ethylene by Ag NPs. Nonetheless, Ag NPs have been proven effective in vitro through different effects on growth parameters such as shoot regeneration of Vanilla planifolia [101], high frequency callus formation (89%) in Solanum nigrum [102], callus proliferation in Prunella vulgaris [81], and increased embryogenesis (50%) in Linum usitatissimum [103]. Similarly, Au NPs have also been shown to positively affect the in vitro cultures of Linum usitatissimum in terms of increased embryogenesis (70%)

Plant cell nanomaterials interaction

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Fig. 3 In vitro application of different types of NPs in plant cell cultures for production of biomass and important secondary products. Source: Redrawn from S.K. Verma, A.K. Das, M.K. Patel, A. Shah, V. Kumar, S. Gantait, Engineered nanomaterials for plant growth and development: a perspective analysis, Sci. Total Environ. 630 (2018) 1413–1435.

[103] and that of Prunella vulgaris in terms of increased callus proliferation [81]. Similar effects have been observed in case of ZnO NPs during in vitro cultures. For instance, Javed et al. [83] showed that ZnO NPs were able to trigger the highest frequency of shoot formation (89.6%) in Stevia rebaudiana while maximized plant regeneration and callus growth were observed in case of tomato [96]. ZnO NPs have also been reported to trigger the formation of maximum somatic embryos from banana explants and increased shoot and root length from these embryos as compared to control [104]. Other nanoparticles such as copper sulphate nanoparticles (CuSO4 NPs) employed during in vitro cultures of Verbena bipinnatifida seedlings led to an increase in the root and shoot length [82]. CuO NPs and Co NPs were shown to increase the number and length of shoots in Mentha longifolia [105]. CuO NPs also were also able to promote organogenesis in rice cultivars [106]. Other than nanoparticles, nanomaterials such as carbon nanotubes have also been shown to enhance callus induction from leaf explants of Satureja khuzestanica which was shown to be as result of upregulation of different genes involved in the process of cell division and cell wall elongation [84].

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5.2 Nanoparticles induce somaclonal variations The application of certain external agents during the growth of plant in vitro, can give rise to various changes as compared to the wild type plant. These changes in the plant biochemistry and physiology are called as somaclonal variations. In vitro derived plantlets may have altered genetics such as mutated DNA and changed chromosome structure [107]. This results in varied phenotypes such as altered plant size, flower colour, resistance and secondary metabolite production in plants. Nanoparticles have been shown to alter plants in a way to induce somaclonal variations. For instance, Kokina et al. [108] demonstrated that supplementation with carbon nanoparticles resulted in a higher number of tetraploid cells with high level of methylated DNA in callus cultures of L. usitatissimum. Similarly, Ag NPs were shown to induce changes in protein and DNA profile of Solanum nigrum calli that resulted in altered appearance of callus cultures [102]. These variations like all other somaclonal variations may be advantageous and disadvantageous.

5.3 Towards controlling contamination Besides their direct effect on the growth nanoparticles have also found applications in facilitation of in vitro cultures. Nanoparticles have proved to be highly effective in controlling microbial contamination during in vitro cultures. Microbial contamination is one of the most commonly encountered problem when it comes to plant tissue culture as it hampers the seed germination, overgrow explants and thus compromises the efficiency of the propagation system even before its initiation. Contaminants arise from lab equipment, water used in the process or the explant used. Different strategies including surface sterilization of explant, disinfection of equipment through chemicals such as mercuric chloride (HgCl2), hydrogen peroxide (H2O2), ethanol and, UV light and even antibiotics have been employed against these microorganisms [109]. However, the disinfectants can adversely affect the in vitro plant cultures due to their deteriorating effects on seed germination, and plant growth and development. Furthermore, endophytic bacteria are present in the seeds and explants of certain plants which cannot be eliminated easily. Antibiotics in different combinations are often employed to get rid of endophytic contaminants [109]. However, not all antibiotics are plant-friendly, and they may cause toxic effects in plants. Metal nanoparticles have been shown to eliminate both exogenous and endogenous contaminants effectively [110]. Various nanoparticles including

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Ag NPs, Al2O3 NPs, CuO NPs, Fe3O4 NPs, Au NPs, MgO NPs, Ni NPs, Si NPs, SiO2 NPs, TiO2 NPs, and ZnO NPs have demonstrated strong antimicrobial properties [111]. Ag NPs were first employed by Abdi et al. [112] to control bacterial growth during in vitro cultures of Valeriana officinalis. The results showed 89% bacteria-free cultures with no adverse effects on shoot multiplication and rooting. In another study, Mahna et al. [113] reported that the Ag NPs (100 mg L 1 for up to 5 min) resulted in 100% removal of contamination from seeds, leaves and cotyledons of Arabidopsis, potato and tomato, respectively. Similarly, woody plants are resilient in terms of contaminant removal. It is reported that in vitro cultures of woody plants are not easily decontaminated using the normal sterilization methods. Ag NPs have been shown to be highly effective in the removal of bacterial contaminants from woody plants such as olive plants. Rostami and Shahsavar [114] reported the complete removal of contaminants when olive plants were treated with Ag NPs (100 mg L 1) compared to 51.4% through conventional disinfection (70% Ethanol followed by 10% Clorox). It is pertinent to note that the conventional disinfection usually kills the explant when the exposure time is higher while Ag NPs were reported to have none or minor negative effects on explants. Other nanoparticles used for this purpose include TiO2 NPs in shoot culture of potato and tobacco cultures [115], and Zn NPs or ZnO NPs in the Murashige and Skoog plant growth medium for contamination-free cultures [116]. The need of the time is to explore the optimal dose for different nanoparticles and to assess their synergism with antibiotics or other disinfectants so as to devise the best possible remedy against microbial contaminants.

5.4 Size directs the function of nanomaterials in plants It is axiomatic to state that the function of nanomaterials is directed by their size. It is observed through the diverse applications of nanomaterials that, size guides their success in almost all the instances. Considering their applications in plants, various studies have reported different results when nanomaterial of different sizes were applied to plants. For instance, Mousavi Kouhi et al. [117] reported that ZnO NPs (approx. 50 nm in size) were more growth-friendly with lesser inhibition of rooting from seedlings of rapeseed compared to ZnO macroparticles and Zn+2 ions which inhibited root growth to a higher extent. Different studies are available which have studied the size dependent responses of nanoparticles in various plants [19] as

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indicated in Table 1. Mustafa and Komatsu [118], reported that Ag NPs having 15 nm average particle size enhanced the growth of soybean compared to smaller (2 nm) or higher (up to 80 nm). This effect was found to be related to the synthesis of mitochondrial proteins. Proteomic analysis revealed that the abundance of voltage-dependent anion channel protein was increased upon exposure to 135 nm Al2O3 NPs. It was, therefore, concluded that varying sizes of Ag NPs have varying effect on growth parameters and physiology of plants. Similarly, in case of CeO2 NPs, size was found to result in altered biotransformation in Lactuca plants and reduced toxicity of different CeO2 NPs [119]. Furthermore, although it is already established that the nanoparticles are effective antimicrobial agents and play a prominent role during in vitro cultures, the potential of NPs in the getting rid of microbial contamination has also been shown to depend on their size and dimensions. Several studies have reported that size is a defining factor for the potency of nanoparticles in killing microbes during in vitro cultures.

5.5 Concentration affects the function of NPs in plants Nanoparticles can act in a concentration dependent manner and the effects of the NPs on plant growth and seed germination is directly related to their concentrations. In some cases, higher concentrations may prove helpful for the growth while in majority of the cases higher concentrations have deteriorating effect on plants. In a study by Helaly et al. [104], it was found in banana plants that the shoot regeneration frequency was enhanced with an increase in concentration of ZnO NPs. Similarly, it was reported that high concentration (up to 20 mg L 1) of ZnO NPs applied through foliar spray increased the biomass of alfalfa, cucumber and tomato plants [120,121]. Application of other nanoparticles such as CeO2 NPs (250 mg L 1) and In2O3 NPs (500 mg L 1) resulted in a significant increase in the biomass accumulation of A. thaliana seedlings [68]. However, generally, lower concentrations of nanoparticles have been found to be more plant-friendly. For example, lower concentrations of ZnO NPs were shown to be more beneficial during seed germination in wheat [122]. Lower concentrations are favourable since they do not hamper cell division and seedling growth as reported by Raskar and Laware [123] in onion. Similarly, lower concentration of ZnO NPs (1 mg L 1) applied to Stevia rebaudiana cultures resulted in an elevated level of steviol glycosides. However, higher concentrations of ZnO NPs (1000 mg L 1) reversed the positive effects of these nanoparticles [83]. Higher concentrations of nanoparticles have been shown to produce

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deteriorating effects on growth and development of different plants. Dimkpa et al. [124] showed that higher concentration (1000 mg L 1) produced yellow coloration of beans that represents harbouring of Pseudomonas chlororaphis in roots of beans. ZnO NPs in higher concentrations (up to 1500 mg L 1) added to in vitro cultures of Brassica nigra, inhibited seed germination, root and shoot lengths significantly. Similarly, higher concentrations of Ag NPs were shown to cause a reduction in both root and shoot length of A. thaliana [125], Au NPs (100 ppm) hampered the growth of A. thaliana [23], CeO2 NPs (250 mg L 1) and In2O3 NPs (1000 mg L 1) decreased seedling growth and increased ROS in A. thaliana [126]. High concentrations of Zn in plant system in the form of ZnO NPs leads to toxic effects on the growth of plants. In cabbage application of ZnO NPs resulted in a dose dependent inhibition of seed germination [92]. The concentrations of nanoparticles also affect secondary metabolism in plants. Higher concentrations of ZnO NPs (1000 mg L 1) lowered stevioside production in shoot cultures of Stevia rebaudiana [127]. Similarly, another study by Chamani et al. [128] demonstrated that the production of specific secondary metabolites is dependent upon the concentration of nanoparticles applied. Their study showed that the highest content of flavonoids, phenolic compounds and anthocynanins was produced in MS medium having lower concentrations of ZnO NPs (25, 75 and 100 mg L 1) (Fig. 4).

6. Adverse effects of nanomaterials on plants Nanoparticles have proved to be highly beneficial in plant growth and development as well as their defence response. However, there are reports on the adverse effects of nanoparticles on growth parameters of various plants. For example, Zn is needed by plants in concentrations of up to 0.05 mg L 1 for their normal developmental process. Higher levels of Zn in plants can causes toxic effects [120,121]. In a study by Li et al. [129], ZnO NPs demonstrated a retarding effect on tomato growth and biomass accumulation, potentially by altering important cellular processes that in turn caused oxidative damage. Similarly, nanoparticles were shown to be important for the growth and yield of Soybeans but, exposure to ZnO NPs and the resulting genotoxicity also damaged the leaves of soybeans decreasing total chlorophyll concentration in leaves [130]. In another study, microparticles of ZnO were found superior to ZnO NPs when applied to wheat shoots. It was also found that owing to

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Fig. 4 The proposed mechanism of action of NPs on growth, cell signalling and secondary metabolism in plant cell cultures.

the small size of ZnO NPs, greater toxicity was caused in roots of wheat [131]. While increase in ZnO NPs increased the number of abnormal cells in garlic cultures [132]. The exposure time is also important during the application of nanoparticles in plants. Permanent or long-term exposure to nanoparticles have a detrimental effect on plants. For instance, prolonged exposure of alfalfa to ZnO NPs inhibited the growth and accumulation of biomass in the plant [133]. Another aspect of the detrimental role of nanoparticles

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is the disturbance they cause in the rhizosphere. ZnO NPs, for example, kills soil microbes thus affecting the nitrogen and carbon fixing role they play in Phoenix dactylifera [134]. In addition to ZnO NPs, other nanoparticles such as Ag NPs, Au NPs, CuO NPs, CeO2 NPs, and Al2O3 NPs have also shown detrimental effect in various plant species. Ag NPs have been reported to destroy cell morphology in Asian rice [135], and increase pollen lethality in kiwi plant [136]. Similarly, Au NPs decreased the growth and induced biochemical stress in Brassica juncea [137] which is linked with increased ROS formation as a response to Au NPs supplementation during growth. Au NPs supplementation also resulted in dark roots, yellow leaves and decreased biomass during in vitro cultures of Barley [138]. The detrimental effects in response to exposure to CuO NPs include reduced shoot and root growth of soybean, lignification of root cells in A. thaliana [21,22], hampered seed germination in cucumber [139], and decreased germination rate and biomass in Oryza sativa [140]. In addition to the above, other nanoparticles and their toxic effects include CeO2 NPs induced smaller and weaker tomato seedlings [141], altered nutritional value of coriander [142], and Al2O3 NPs induced decreased cell viability through ROS generation in tobacco cell suspension cultures [78].

7. Conclusions and future prospects It is undoubtedly safe to say that nanobiotechnology has emerged as very promising tool to manipulate plants for the benefit of mankind. From beneficial to detrimental effects on plants, nanotechnological tools have the potential to alter the history of plant-based products forever. From disinfection to enhanced germination, growth and yield and to increased secondary metabolism and enhanced defence system, nanotechnology has already offered a viable platform for agriculture biotechnology. Now, with increased beneficial and reduced adverse effects, nanomaterials can be the real saviours of the era. Further research is needed to provide an insight into the adverse effects of nanomaterials on different parameters of plants. Optimization needs to be done for better yields from plants. With the introduction of new types of nanomaterials with time, it is important to evaluate the applications of all these types in plants to find the superior types in terms of higher beneficial effects and negligible harmful effects on plants.

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