Introduction

Arsenic (As) is considered one of the most toxic elements in the environment (Otero et al. 2016). Irrigation of agricultural soils with As-contaminated water causes As soil enrichment as well as As bioaccumulation and toxicity (Ruíz-Huerta et al. 2017). As a result, it can enter the food chain and represent a risk to human health (Islam et al. 2016). Reduced CO2 fixation, disorganization of the photosynthetic integral processes, as well as imbalance in nutrient and water absorption are some of the effects that plants can exhibit under As stress (Ali et al. 2009; Zhao et al. 2009). Arsenic also induces reactive oxygen species (ROS) production that leads to lipid peroxidation and can result in plant death (Finnegan and Chen 2012). To counteract ROS stress, plants activate their antioxidant defense system in order to protect their cellular system from harmful effects (Gomes et al. 2014).

Most crops, including tomato (Solanum lycopersicum L.), are sensitive to As stress exhibiting reduced seed germination, reduced growth, and even modified molecular responses (Beesley et al. 2013; Marmiroli et al. 2014; Miteva et al. 2005). Due to its high level of consumption (160 million tons per year in 2013) (FIRA 2017), tomato is economically one of the most important vegetables in the world (Martí et al. 2018). However, safe quality tomato production may be compromised as groundwater contaminated with As has been reported in several countries including India, Vietnam, Mongolia, Greece, Hungary, the USA, Thailand, Ghana, Chile, Argentina, Mexico, Bangladesh, Cambodia, China, Nepal, and Pakistan (Singh et al. 2015). In the case of Mexico, the highest concentrations of As appear in alluvial aquifers in arid and semi-arid areas in northern Mexico (Alarcón-Herrera et al. 2020), where greenhouse tomato production is commonly practiced and irrigation with As-contaminated water may occur.

Silicon (Si) is the second most abundant element on earth’s crust. It is predominantly found as silicon dioxide (SiO2), a non-available form to be taken up by plants. Plant-available Si forms include silicic acid (Si(OH)4) or mono-silicic acid (H4SiO4) (Zargar et al. 2019). Within the plants, and depending on the species, Si accumulates in plant tissue at concentrations ranging from 0.1 to 10% (dry weight) as a polymer of hydrated amorphous silica (Savvas and Ntatsi 2015). Silicon exerts beneficial effects on plant growth and production by alleviating biotic and abiotic stress (Ma and Yamaji 2008). Silicon application under metal stress protects plant structures by compartmentation, co-precipitation, and/or chelation of heavy metals in different parts of the plants, which in turn results on increased plant growth and biomass (Adrees et al. 2015). In the case of As, it can be absorbed by a subclass of aquaporins that participate in Si transport with mobility efficiencies that depend on the species (Allevato et al. 2019).

Nanotechnology is an innovative, novel, and scientific approach that leads to design, manipulation, and development of highly useful nanomaterials (ranging in size from 1 to 100 nm), whose main advantages (compared to bulk forms) include increased surface area to volume ratio, improved (bio)chemical reactivity, and unusual and valuable thermal, mechanical, optical, structural, and morphological properties (Mali et al. 2020; Tyagi et al. 2018). A variety of nanomaterials like silicon nanoparticles (Si NPs), nanopesticides, nanoinsecticides, and nanoemulsions have been developed using nanotechnology. Currently, Si NPs are fabricated by pulse laser irradiation of single-crystal silicon wafers in water (Momoki et al. 2020). Among their applications, Si NPs have shown a protective and promising preventive strategy against hepatoxicity and are useful for the fabrication of multifunctional cotton fabrics with enhanced UV protective, durability, antibacterial, and thermal properties in combination with silver or zinc nanoparticles (El-Naggar et al. 2017; Mohamed et al. 2017). Si NPs are also useful as nanofertilizers and pesticides against pests in maize (El-Naggar et al. 2020).

Si NPs could be also useful to prevent As toxicity and uptake by tomato crops. Studies show that Si NPs prevented Cr accumulation in pea seedlings (Tripathi et al. 2015), increased chlorophyll and carotenoid content as well as plant growth in Pleioblastus pygmaeus in the presence of Pb (Emamverdian et al. 2020), improved the components of the glutathione cycle (antioxidant system non-enzymatic) in Zea mays plants in the presence of As (Tripathi et al. 2016), and increased antioxidant enzymatic activity in Triticum aestivum L. plants in the presence of Cd (Ali et al. 2019). Therefore, while irrigation of tomato plants with As-contaminated water might increase the concentrations of As in soil and plant tissue, Si NPs might help to avoid As translocation and to boost the plant’s biochemical system. Currently, knowledge is particularly scarce regarding the effect of Si NPs in tomato plants irrigated with As-contaminated water and its subsequent phytotoxic effects on the physiological and biochemical properties.

In this study, an experimental design intended to simulate the irrigation of tomato plants with As-contaminated water as well as the application of Si NPs has been tested to better understand the antioxidant response of tomato plants against As in the presence of Si NPs. The objectives of this work were (i) to determine the concentration of As in substrate and plant tissue as a function of the concentration of As in irrigation water, (ii) to evaluate the effect of As contamination on the growth of tomato plants, (iii) to determine the translocation of As at different strata and the effect of Si NPs application in such translocation, (iv) to evaluate As and Si NPs phytotoxicity, and (v) to determine the effect of As and Si NPs on photosynthetic pigments, enzymatic activity, and non-enzymatic antioxidant compounds of tomato plants.

Materials and methods

A total of 18 treatments intended to simulate the irrigation of tomato plants with As-contaminated water at six different concentrations (0.0, 0.2, 0.4. 0.8, 1.6, and 3.2 mg L−1) as well as the application of Si NPs at three different doses (0, 250, and, 1000 mg L−1) were tested in tomato plants in twelve replicates to make a total of 216 experimental units (Table S1, Supplementary Material).

Greenhouse experiment: As contamination simulation and Si NPs application

Tomato seeds (Solanum lycopersicum L.) of the var. Hybrid, “Sun 7705,” saladette type, and indeterminate growth were used in this study. Initially, seedlings were placed in a mixture of peat moss and perlite (1:1, v/v), as a growth substrate, in 12 L black polyethylene bags. The growth substrate presented a pH of 6.5, an electrical conductivity of 0.6 dS/m, a cationic exchange capacity of 139 meq/100 g, and an organic matter concentration of 97%. Although As concentrations were not determined in the substrate before the experiment, it was < 2 mg/kg according to the control. A direct irrigation system was then implemented to water the crops for 150 days using the Steiner nutrient solution for crop nutrition (Steiner 1961). An automated irrigation system was used to ensure that each treatment received the same amount of water, approximately 30,000 L during the whole growing season.

Arsenic was supplied as Na2HAsO4.7H2O in irrigation water at 0.0, 0.2, 0.4. 0.8, 1.6, and 3.2 mg L−1 to simulate As-contaminated water. The maximum permissible concentration of As in irrigation water in Mexico is 0.2 mg L−1 (DOF 1997). Si NPs from SkySpring Nanomaterials Inc. were applied via substrate at 0, 250, and 1000 mg L−1 doses every 3 weeks making a total of 6 applications of 10 mL of solution per plant. Si NPs were spherical, between 10 and 20 nm, and presented a surface area of 160 m2 g−1 and a bulk density of 0.08 to 0.1 g cm−3. At the greenhouse, active photosynthetic radiation was 1100 μmol m−2 s−1 at peak hours, average day temperature was 28 °C, and average relative humidity was 61.8%.

Determining As concentrations in substrate and plant tissue

Arsenic concentrations were determined in substrate, root, stem, leaves, and fruit up to the seventh cluster of each plant after 150 days. In order to do so, 6 out of 12 pots were randomly selected per treatment to sample substrate and roots. Each substrate sample was homogenized and air-dried after root removal. Root samples were thoroughly rinsed under running water and air-dried. Samples of stem and leaves were collected from the same pots at three different strata, from which fruit was harvested when tomato brunches matured. Stratum one (S1) covered up to the first cluster of fruit, stratum two (S2) covered up to the fourth cluster of fruit, and stratum three (S3) covered up to the seventh cluster of fruit.

All samples were oven-dried at 80 °C for 72 h, ground with a mortar and pestle, homogenized, weighed, and stored in polyethylene bags until As analysis. Fruit samples were oven-dried for 144 h. Arsenic concentration was determined in three out of the 6 samples by X-ray fluorescence spectroscopy (XRF) in a ThermoScientific Niton FXL instrument with a detection limit of 2 mg/kg according to the 6200 USEPA method (Santos et al. 2017). Reference samples (NIST 1573a for tomato leaves and NIST 2711a and 2709a for soil) and triplicate analyses were carried out for quality control to ensure the reliability of the analytical data. Recovery percentages were 80 ± 10% for NIST 1573a, 85.78 ± 10% for NIST 2711a, and 82.09 ± 10% for NIST 2709a.

Measuring tomato growth and yield

Plant height, number of leaves, stem diameter, and yield were determined in all tomato plants every 15 days after transplantation and until elimination of the plants. Plant height and stem diameter were measured from the first pair of true leaves to the apex with a flexometer and a digital vernier, respectively. The number of leaves was determined by direct count, while the yield was calculated by the sum of the total number of fruits harvested per plant over the 150-day period.

Translocation of As and Si NPs in tomato plants

Translocation of As in tomato plants was calculated for each stratum as the concentration of As in shoots (stem and leaves) divided by the concentration of As in roots times 100 (Vaculík et al. 2013).

Additionally, microscopic analyses were carried out by scanning electron microscopy coupled to energy X-ray dispersion spectroscopy (SEM–EDS) to observe the presence of either As or Si NPs in tomato plant tissue using a ESEM-QUANTA FEG-250 from FEI. Root and leaf tissues from the fresh plant were sampled from a 3.2 mgAs L−1 and 250 mgSi NPs L−1 treatment, rinsed with deionized water, and frozen, until they were mounted in carbon tape in aluminum pins for SEM–EDS analyses.

Phytotoxicity of As

The relative phytotoxicity index (PRI) was calculated using Eq. (1) adapted from Alejandro-Córdova et al. (2017) for aerial and radical dry biomass of plants. To measure the effect of the treatments with As, the PRI of each biomass was compared with the values corresponding to the control treatment (0 mgAs L−1).

$$PRIxi=\frac{CoT}{CT}$$
(1)

where PRI is the relative phytotoxicity index, xi is the radical or aerial biomass, CoT is the contaminated (As and/or Si NPs) treatment, and CT is the control treatment.

PRI values > 1 indicate plant adaptation to As and SiO2 NPs and suggest that biomass production was stimulated, while PRI values < 1 indicate As and Si NPs toxicity and suggest that biomass production was inhibited. PRI values equal to 1 indicate plant tolerance to As and Si NPs and suggest that biomass production was not affected compared to the control.

Measuring photosynthetic pigments in tomato plants exposed to As and Si NPs

Fully expanded young leaf tissue from stratum S2 was collected from randomly selected plants at 150 days after plantation for biochemical analysis. After collection, samples were stored at − 20 °C in a freezer, lyophilized at − 84 °C for 72 h, and subsequently ground to fine powder and stored until further analysis. Chlorophylls, antioxidant enzymes, and non-enzymatic antioxidant compounds were analyzed for 6 out of 12 samples.

Photosynthetic pigments (Chl a, chlorophyll a; Chl b, chlorophyll b; and Chl t, total chlorophyll) were determined using a UV–vis spectrophotometer (UNICO Spectrophotometer Model UV2150, Dayton, NJ, USA) using Eqs. (2), (3), and (4) and the absorbances measured at 645 (× Abs645) and 663 (× Abs663) nm (Nagata and Yamashita 1992):

$$Chla\left(mg100{g}^{-1}DW\right)=0.999x\left|{Abs}_{663}\right|-0.0989x\left|{Abs}_{645}\right|$$
(2)
$$Chlb\left(mg100{g}^{-1}DW\right)=-0.328x\left|{Abs}_{663}\right|+1.77x\left|{Abs}_{645}\right|$$
(3)
$$Chlt\left(mg100{g}^{-1}DW\right)=Chla+Chlb$$
(4)

Antioxidant activity of enzymes and non-enzymatic compounds

In a 2 mL Eppendorf tube, 200 mg of lyophilized leaves, 20 mg of polyvinylpyrrolidone, and 1.5 mL of phosphate buffer (0.1 M) with a pH of 7–7.2 were mixed. This mixture was then micro-centrifuged at 12,000 rpm for 10 min at 4 °C. The supernatant was filtered using a nylon membrane and kept refrigerated until determination of antioxidant enzyme activity, glutathione, and proteins using a UV–vis spectrophotometer (UNICO Spectrophotometer Model UV2150, Dayton, NJ, USA) and a microplate (Allsheng, AMR-100 model, Hangzhou, China). In the case of non-enzymatic antioxidant compounds (flavonoids and phenols), another quantity of lyophilized tissue was weighed according to the established methodology for each variable. Six out of 12 plants were analyzed per treatment for all the antioxidant response variables.

Ascorbate peroxidase activity (APX, EC 1.11.1.11) was determined using the methodology described by Nakano and Asada (Nakano and Asada 1981), glutathione peroxidase (GPX, QE 1.11.1.9) with the methodology described by Xue et al. (2001), catalase (CAT, QE 1.11.1.6) using the methodology of Dhindsa et al. (1981), and superoxide dismutase (SOD, QE 1.15.1.1) using a SOD Cayman 706,002® kit.

Total protein quantification (mg g−1 of dry weight (DW)) was carried out according to Bradford’s colorimetric technique (Bradford 1976). Glutathione (mmol 100 g−1 DW) was determined using the method by Xue et al. (2001) by means of a 5,5-dithio-bis-2 nitrobenzoic acid (DTNB) reaction. Flavonoids (mg 100 g−1 DW) were determined using the method by Arvouet-Grand et al. (1994). Phenols (mg g−1 DW) were determined with Folin-Ciocalteu reagent as described in Cumplido-Nájera et al. (2019).

All data were analyzed using the InfoStat statistical package, and an analysis of variance and a Fisher least significant difference test (p ≤ 0.05) were carried out.

Results and discussion

Arsenic in substrate and plant tissue

Arsenic concentrations in substrate were directly proportional to the concentrations of As supplied in irrigation water (Fig. 1a and Table S2, Supplementary Material). Furthermore, As concentration in irrigation water > 0.8 mg L−1 caused As concentrations > 22 mg kg−1 in the substrate, leading to substrate contamination according to Mexican guidelines for As in agricultural soils (DOF 2007) and other international guidelines (i.e., 17 mg kg−1 from Canada) (Canadian Council of Ministers of the Environment 2001).

Fig. 1
figure 1

Arsenic concentration in irrigation water, substrate, tomato plant tissue, and tomato strata. a Arsenic in substrate as a function of As in irrigation water. b Arsenic in substrate and plant tissue (root, steam, and leaves) per stratum for different concentrations of As in irrigation water. c Average As concentration in plant tissue (stem and leaves) as a function of aerial stratums. Lowercase letters indicate significant differences according to the Fisher least significant difference test (p ≤ 0.05, n = 3)

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Total As concentrations in roots, leaves, and stems, at different As exposures, are shown in Fig. 1b and Table S2, Supplementary Material. In general, we found higher As concentrations in the roots than in stems and leaves. Average As concentrations in roots, stems, and leaves were 25.10, 0.80, and 1.47 mg kg−1, respectively. No As was detected in the fruit. According to other studies, roots are the plant organ that tend to accumulate the highest levels of As (Beesley and Marmiroli 2011; Du et al. 2017; Ruíz-Huerta et al. 2017). Arsenic accumulation in root tissue can cause inhibition of the root’s morphological characters (Pandey et al. 2016). Remodelling of root architecture in response to toxic elements can be used by plants as a strategy to adapt to and/or survive toxic elements (Ronzan et al. 2019). Morphological changes could lead to an increase of As in roots, while decreasing As translocation to shoots.

Additionally, we found higher As concentrations in stems and leaves in S1 than in S2 and S3 (Fig. 1c and Table S2, Supplementary Material). The higher the concentration of As in irrigation water, the higher the concentration of As in plant tissue (Fig. 1b and Table S2, Supplementary Material). However, limited As uptake was observed at low As concentration in irrigation water (≤ 0.4 mg L−1), where As was neither found in stems from S2 and S3 at 0.2 and 0.4 mgAs L−1 nor in leaves from S3 at 0.2 mgAs L−1. The strategy developed by tomato plants to tolerate As is avoidance, limiting As transport to shoots and increasing As accumulation in the root system (Carbonell-Barrachina et al. 1997), which in turn plays a fundamental role on As immobilization within plants. The processes that occur in the rhizosphere influence As concentrations and bioavailability, because they involve local changes in redox potential, pH, and organic matter content (Punshon et al. 2017) causing lower As mobility.

Effect of As on tomato growth and yield

At low As concentrations in irrigation water (0.2 mgAs L−1), As caused statistically significant reduced growth and lower number of leaves, as compared to tomato plants irrigated with As-free water and most of other As doses (Fig. 2a, b, and c). Tomato plants irrigated with water containing 0.2 mgAs L−1 of As exhibit toxicity. Similarly, exposure to low doses of Pb (0.05 mg L−1) has been reported to decrease root biomass and induced genotoxicity in lettuce (Silva et al. 2017). Furthermore, it has been reported that As affects grafted melon plants by reducing the number of leaves, leaf area, and aerial dry biomass; however, it did not show to affect fruit biomass (Allevato et al. 2019). In this study, low concentrations of As clearly showed a negative impact on plant growth and number of leaves, but no statistically significant effects were observed in steam diameter and tomato yield (Fig. 2c and d). At higher As concentrations, compartmentalization of As in tomato root tissue might be minimizing its impact on plant growth and metabolism (Carbonell-Barrachina et al. 1997), which in turn could help to explain the findings in Fig. 2.

Fig. 2
figure 2

Arsenic effect in the agronomic variables. a Plant height and b number of leaves as a function of As concentration in irrigation water. c Number of leaves as a function of plant height (the numbers at each point represent the concentration of As in irrigation water). d Stem diameter and e yield as a function of As concentration in irrigation water. f Tomato yield as a function of stem diameter (the numbers at each point represent the concentration of As in irrigation water). Error bars represent the standard deviations, while lowercase letters indicate significant differences according to the Fisher least significant difference test (p ≤ 0.05, n = 12)

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At higher As concentrations in irrigation water (0.4 mgAs L−1), As was tolerable and promoted stem diameter growth and yield, which were statistically higher than those of tomato plants irrigated with As-free water (Fig. 2c, d, and e). However, the highest As doses in irrigation water did not show a statistically significant difference in stem diameter and yield compared to the control (Fig. 2c, d, and e). Enhanced plant growth at high As doses (3.2 mgAs L−1) has been observed in Pteris vittata (Chen et al. 2016), an As hyperaccumulator (Ma et al. 2001) known to cope with As toxicity due to a balance between As detoxification (by efflux of As(III)) and As accumulation [41]. Arsenic effluxes of the order of Pteris vittata have been estimated for tomato plants at relatively low As exposures (0.75 mg L−1) (Chen et al. 2016), which may help to explain why our tomato plants showed higher stem diameter and yield at 0.4 mgAs L−1 compared to the control. The potential for tolerance to metal toxicity of different plant species varies considerably from one species to another as well as between various genotypes (Chandrakar et al. 2016). Generally, crop yields decrease in the presence of As; it has also been reported that the yield of potato tubers (Solanum tuberosum L.) was significantly higher in soils contaminated with As (Codling et al. 2016) as occurred in this study.

Translocation of As and Si NPs in tomato plants

Figure 3 shows the As translocation factor through plant strata and tissues. As translocated up to 34.19% within tomato plants at all As doses (Fig. 3). At 0.2 mgAs L−1, As translocated from roots to stratum S1, exhibiting a preferential accumulation within the leaves (Fig. 3a). At 0.4 mgAs L−1, As translocated all the way up to stratum S2, exhibiting a preferential accumulation within the leaves as well. At higher As doses, As translocated farther from the roots reaching, in some cases, stratum S3 with preferential accumulation of As in the leaves (Fig. 3a). These results imply the flow of As towards higher strata, which was supported by higher concentrations of As in plant tissue (Fig. 1b).

Fig. 3
figure 3

a Arsenic translocation to the aerial parts of tomato plants (stem and leaves per stratum) as a function of As in irrigation water. Images of Si NPs found in the b roots and c leaf trichomes of tomato plants. Arsenic translocation to d stem and e leaves as a function of As in irrigation water and Si NPs. The standard deviations and significant differences among the treatments according to the Fisher least significant difference test (p ≤ 0.05, n = 3) are shown in Tables S3 and S4 (Supplementary Material). * indicates significant differences

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Arsenic translocation within tomato plants might occur similarly to phosphorus (P), as As could enter cells adventitiously through nutrient uptake systems such as phosphate permeases and aquaglyceroporins (Garbinski et al. 2019). Arsenic translocation within tomato plants seems to be enhanced at high As concentrations, a process that seems to occur as P absorption decreases as a result of the contamination (Gomes et al. 2014). Furthermore, it has been shown that As uptake by tomato plants through the root system results in the following accumulation order: Asroot > Asleaf > Asstem > Asfruit (Stazi et al. 2018). In our study, translocation percentages were Asleaf (31.43%) > Asstem (17.07%) > Asfruit (not detected). As mentioned previously, no As was detected in fruits of tomato plants exposed to As (González-Moscoso et al. 2019).

Figure 3b and c show the results from SEM–EDS observations. We found Si NPs in root and leaf tissue revealing that tomato plants took up Si NPs through the roots (Fig. 3b) and translocated them to the leaves (Fig. 3c), where they accumulated, at least, in the trichomes.

Figure 3d and e show the translocation of As in the presence of Si NPs. No clear trends could be observed for the translocation of As to stem with increasing Si NPs. In general, however, the translocation of As seemed to decrease towards the leaves with increasing Si NPs. Hence, application of Si NPs results in a decrease of As translocation to tomato aerial parts. Yet, the highest translocation of As occurred towards the leaves at level S1 independent of the Si NPs treatments (Fig. 3a, d, and e). Decreased concentrations of As in the stem, leaf, and husk of brown rice were previously reported after the addition of Si (Li et al. 2018). Furthermore, application of Si to tomato plants results in decreased As accumulation in fruit and in aerial parts (Marmiroli et al. 2014), likely due to stimulation of radical exudates that can chelate metals and reduce their translocation (Kidd et al. 2001), which could explain our results. These exudates include amino acids, organic acids, sugars, and phenolic compounds (Haichar et al. 2014). Si NPs application has been reported to decrease cadmium translocation up to a 60.8% in rice plants (Chen et al. 2018).

In this study, adhesion of Si NPs to plant roots may have helped to restrict, at least partially, As translocation to the aerial part of tomato plants, likely due to increases of root exudates, as it has been reported in other studies using metallic nanoparticles (de Sousa et al. 2019; Ghoto et al. 2020). This hypothesis was supported by the high accumulation of As found in tomato plant roots (Fig. 1b). On the other hand, it has been reported that trichomes from tobacco plants exposed to Cd actively excrete crystals, which help to exclude the toxic element through the main cells of the trichomes (Choi et al. 2001), suggesting that trichomes play an important role in the exudation of Cd crystals through crystallization (Choi et al. 2004). Furthermore, Si NPs have been reported to increase trichome size in Mentha piperita L. (Ali et al. 2019). In the present study, the presence of Si NPs in tomato leaf trichomes may also have contributed to the As detoxification process in our tomato plants.

Effect of As and Si NPs on tomato growth and yield and the relative phytotoxicity index

Figure 4 shows the effect of Si NPs on tomato plant height, number of leaves, stem diameter, yield, and the relative phytotoxicity index. The application of Si NPs did not show significant differences in plant height, number of leaves, and stem diameter (Fig. 4a, b, and c). However, the application of Si NPs showed a significant decrease in tomato yield, in the absence and in the presence of As (Fig. 4d), which accounted for up to 23.31% at 1000 mgSi NPs L−1 and 0 mgAs L−1 and up 27.04% at 250 mgSi NPs L−1 and 3.2 mgAs L−1, respectively.

Fig. 4
figure 4

Arsenic and Si NPs effects in the agronomic variables and the phytotoxicity relative index. a Plant height, b number of leaves, c stem diameter, and d yield as a function of As and Si NPs. Relative phytotoxicity index in e radical and f aerial biomass. Error bars represent the standard deviations, while * indicates significant differences according to the Fisher least significant difference test (p ≤ 0.05, n = 12). The statistical differences among the treatments are shown in Table S5 (Supplementary Material)

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Application of nanoparticles to crops has not shown any clear trend on plant growth. While some studies report positive effects (Elsheery et al. 2020; García-López et al. 2019; Salachna et al. 2019), others report negative effects (Alquraidi et al. 2019; Le et al. 2014; Oukarroum et al. 2013). Nanoparticle geometry and size as well as the type of organic coating seem to induce plant responses that range from biostimulation to toxicity (Jośko and Oleszczuk 2013; Juárez-Maldonado et al. 2019; Zuverza-Mena et al. 2017). While low nanoparticle concentration (< 100 mg L−1) has been reported to increase plant growth (Juárez-Maldonado et al. 2019; Tolaymat et al. 2017), high Si NPs concentrations (100, 500, and 2000 mg L−1) have been reported to cause negative effects on plant physiology (Le et al. 2014). In our study, we used high doses of NPs (250 and 1000 mg L−1). No significant effects were observed in plant growth (plant height, number of leaves, and stem diameter), but significant negative effects were observed in tomato yield, in the absence and in the presence of As.

To estimate tomato plant tolerance to the stress induced by As and Si NPs as determined by radical and aerial biomass production, the PRI was estimated. Nearly all PRI values were higher than 1 at all As doses in the absence of Si NPs, suggesting that tomato plants showed adaptation to As (Fig. 4e and f). Apparently, under conditions of contamination of As, tomato plants develop a detoxification system that allows them to tolerate As. Similar findings have previously been reported (Carbonell-Barrachina et al. 1997). An interesting observation was higher PRI values for aerial dry matter compared to radical dry matter, suggesting lower toxicity to As in the aerial system, which proved tolerance to As at 3.2 mgAs L−1 and 1000 mgSi NPs L−1. It is known that metal toxicity can decrease as the result of the “dilution effect,” which accounts for the dilution of the concentration of the toxic metal within the plant by increasing plant biomass (Masood et al. 2012). In this study, the dilution effect might have helped to cope with As. The more generation of biomass, the lower the toxicity. In contrast, in the presence of Si NPs, nearly all PRI values were lower than 1 at all As doses suggesting that tomato plants exhibit toxicity in the presence of Si NPs (Fig. 4e and f).

Modification of the photosynthetic pigments in tomato plants exposed to As and Si NPs

Figure 5 shows the concentration of chlorophyll a, chlorophyll b, and total chlorophyll in tomato leaves in the presence of As and Si NPs.

Fig. 5
figure 5

Photosynthetic pigments a chlorophyll a, b chlorophyll b, and c total chlorophyll in the leaves of tomato plants. Error bars represent the standard deviations, while lowercase letters indicate significant differences according to the Fisher least significant difference test (p ≤ 0.05, n = 6)

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All chlorophylls were significantly higher than the control at any As doses in the absence of Si NPs (Fig. 5). Chlorophyll a increased up to 34.55% at 3.2 mgAs L−1, while chlorophyll b increased up to 63.9% at 0.8 mgAs L−1 (Fig. 5a and b). No significant differences in chlorophylls were observed within As treatments.

While several studies have shown a decrease in chlorophylls due to effects of As in different plant species (Azeem et al. 2017; Miteva et al. 2005; Pandey and Gupta 2015), increases in chlorophyll content were also reported in plants of Borreria verticillata due to exposure to different As concentrations (Campos et al. 2014). This might be the result of plants stressed by abiotic factors, improving leaf photosystem II (PSII), reaction center activity, electron transport, light harvesting complexes, and adequate heat dissipation in order to maintain leaf photosynthetic performance under stress (Jiang et al. 2014).

Regarding the effect of Si NPs, in the absence of As, only the dose of 1000 mgSi NPs L−1 showed a significant effect on the chlorophyll content, which accounted for up to 76% in total chlorophyll, 48.5% chlorophyll b, and 35.5% chlorophyll a (Fig. 5).

Increases in chlorophylls, as a result of NPs application, were reported elsewhere (Ali et al. 2019; Tripathi et al. 2015). In rice plants, ZnO NPs proved to increase the concentration of chlorophyll a and b by 69% and 44%, respectively, at the highest dose of NPs (100 mg L−1) compared to the control (Ali et al. 2019). The supply of Si NPs in pea leaves improved the photosynthetic pigments under Cr stress (Tripathi et al. 2015), as nanomaterials can improve the functional properties of organelles and photosynthetic organisms, which, in turn, can enhance the use of solar energy and biochemical detection (Giraldo et al. 2014). Chlorophyll content can be increased by silicon, as open PSII reaction centers allow electron transport by excitation energy (Zhang et al. 2018).

In this study, all chlorophylls were significantly higher than the control (0 mgAs L−1 and 0 mgSi NPs L−1) at any As and Si NPs dose (Fig. 5), indicating an improved photosynthetic capacity of tomato plants due to As and Si NPs. No significant differences were observed among As and Si NPs treatments (Fig. 5), except for chlorophyll b, which showed a significant increase at 3.2 mgAs L−1 and 250 mgSi NPs L−1 compared to the highest dose of As.

The interaction of As and NPs has been reported to improve the content of chlorophylls and carotenoids in Brassica juncea compared to the treatment with only As (Praveen et al. 2018). However, this same interaction decreased the content of chlorophylls compared to the absolute control (Praveen et al. 2018). Chlorophylls have also been reported to increase in Pisum sativum plants when they interact with Cr-Si NPs, compared to treatment with only Cr. However, this interaction was not statistically different than the absolute control (Tripathi et al. 2015), indicating that Si NPs can maintain or increase, as in our case, photosynthetic capacity in the presence of metalloids.

Antioxidant activity of enzymes and non-enzymatic compounds

Antioxidant enzymatic activity showed significant differences among treatments for ascorbate peroxidase (APX), glutathione peroxidase (GPX), catalase (CAT), and superoxide dismutase (SOD) (Fig. 6).

Fig. 6
figure 6

Enzymatic antioxidant activities of a APX, b GPX, c CAT, and d SOD in tomato leaves as a function of As and Si NPs. TP, total proteins; ND, not detected. Error bars represent the standard deviations, while lowercase letters indicate significant differences according to the Fisher least significant difference test (p ≤ 0.05, n = 6)

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Statistically significant increased enzymatic activity in tomato leaves was observed for APX and CAT at the lowest (0.2 and 0.4 mgAs L−1) and highest (1.6 and 3.2As mg L−1) As doses, respectively (Fig. 6a and c). CAT activity increased up to 137.12% at 3.2 mgAs L−1 (Fig. 6c). In contrast, statistically significant decreased enzymatic activity was observed mostly for GPX at higher (> 0.4 mgAs L−1) As doses and in some cases for SOD at intermediate (0.4 to 0.8 mgAs L−1) As doses (Fig. 6b and d).

According to the literature, APX activity increases in the presence of aluminum (100 μM L−1) stress in cucumber plants, but it is inhibited at very high doses (1000 and 2000 μM L−1) (Pereira et al. 2010), while CAT production is stimulated in plants in response to the presence of trace elements as an important mechanism to prevent oxidative damage (Mittler 2002). GPX activity has been reported to decrease considerably in Myracrodruom urundeuva plants when exposed to high As doses (100 mg kg−1) (Gomes et al. 2014). It has been reported that SOD activity decreased in Cicer arietinum plants exposed to As concentrations of 30 and 60 mg kg−1, as the As treatment did not cause concentrations of superoxide that could affect the plant (Gunes et al. 2009).

Enzymes are susceptible to oxidative explosions and carbonylation of proteins, when plants are exposed to trace elements (Romero-Puertas et al. 2002). In our study, the enzymatic activity showed different responses due to an As exposure that ranged from an increase of enzymatic activity at low doses to an inhibition and an increase of enzymatic activity at high doses. It has been observed that antioxidant activity increases initially with increasing metal accumulation, but that it inhibits gradually within a few days (Kalita et al. 2018). The enzyme activity can, however, be maintained or even increased during As exposure at high concentrations (500 μM) (Shri et al. 2009).

In the absence of As, application of Si NPs to tomato plants showed stimulatory effects on APX and GPX enzymatic activities in tomato leaves (Fig. 6a and b), reaching up to a 94.4% increase of GPX at 1000 mgSi NPs L−1. CAT enzymatic activity showed non-significant effects as a result of Si NPs application, while SOD showed a decrease down to 49.10% at 1000 mgSi NPs L−1 (Fig. 6c and d). Similar results have been reported for silver nanoparticle application to Brassica juncea plants, which increased the APX, GPX, and CAT enzymatic activity (Sharma et al. 2012). In this study, improved antioxidant enzymatic activity and reduced production of reactive oxygen species (ROS), as determined by increases of APX and GPX in the presence of Si NPs, may result in less stress to the plant. SOD decreases may be due to the fact that it is the first line of defense, which may be catalyzing free radicals produced in plants (Gill and Tuteja 2010), which, in turn, could decrease its activity.

Application of Si NPs to tomato plants irrigated with As-enriched water showed a statistically significant increase in APX enzymatic activity at low As concentrations (0.2 and 0.4 mg L−1) for any Si NPs doses as compared to the control (Fig. 6a). Increased APX enzymatic activity was also observed at 0.8 mgAs L−1 and 1000 mgSi NPs L−1 (Fig. 6a). In contrast, the interaction of As and Si NPs caused a statistically significant decrease in GPX enzymatic activity at any As and Si NPs doses, compared to the control, with the exception of 0.4 mgAs L−1 and Si NPs application (Fig. 6b), which decreased to undetectable concentrations at 3.2 mgAs L−1 (Fig. 6b). No significant differences were observed for CAT enzymatic activity among As and Si NPs treatments (Fig. 6c) except at 0.2 mgAs L−1 and 1000 mgSi NPs L−1 and 0.4 mgAs L−1 and 250 mgSi NPs L−1, where CAT enzymatic activity increased compared to the control. Either non-statistically significant or statistically significant decreases were observed for SOD enzymatic activity with no clear trends among the different As and Si NPs treatments (Fig. 6d) although seven out of ten interactions cause decreased SOD activity.

Decreases in SOD and GPX may be the result of high As exposure as well as the result of additional stress imposed to tomato plants by the high doses of the Si NPs applied (250 and 1000 mg L−1). It has been reported that the activities of antioxidant enzymes decrease at high concentrations of metals (Adrees et al. 2015). Increases in enzyme activity are generally reported when the NPs interact with a metal or metalloid, e.g., the application of zinc oxide nanoparticle at relatively low doses (25 mg L−1) proved to increase SOD activity in Leucaena leucocephala seedlings exposed to cadmium and lead (Venkatachalam et al. 2017). In comparison, our NPs concentrations were much higher, which could have influenced the negative effect observed. On the hand, the reactivity and toxicity of NPs can increase by sorption of other chemical compounds on their surface (Madannejad et al. 2019). As for the decrease in GPX, it may also be due to the decrease in glutathione content presented in Fig. 7a, because this compound is a substrate for this enzyme.

Fig. 7
figure 7

Non-enzymatic antioxidant activities of a glutathione, b flavonoids, c phenols, and d total proteins as a function of As and Si NPs. Error bars represent the standard deviations, while lowercase letters indicate significant differences according to the Fisher least significant difference test (p ≤ 0.05, n = 6)

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In addition to defensive enzyme systems that deal with ROS production, other non-enzymatic antioxidants exist in plant cells (Cao et al. 2004), such as glutathione, vitamin C, phenolic acids, carotenoids, and flavonoids, as a natural response of plants against stress (Kasote et al. 2015). In this study, the content of non-enzymatic compounds in tomato leaves exposed to doses of As and Si NPs showed significant differences between treatments (Fig. 7).

In general, glutathione decreased significantly compared to the control (Fig. 7a) suggesting that tomato plants’ antioxidant capacity may be sensitive to the phytotoxic effect of As (Zvobgo et al. 2019), as GSH-related antioxidant defenses may be affected in response to As tolerance (Huang et al. 2012). Flavonoid content decreased when tomato plants were exposed to 0.4 and 1.6 mgAs L−1, but it was not significantly different to the control at other As doses (Fig. 7b). It has been reported that As stress can inhibit flavonoid synthesis in Panax notoginseng plants (Liu et al. 2016). However, many of the biological roles of flavonoids are attributed to their potential cytotoxicity, antioxidant abilities, and also preventing the formation of ROS by chelating metals (Pourcel et al. 2007). Regarding the effect of As on the content of phenols, no significant differences were observed in the presence of As, except at 1.6 mgAs L−1 where phenol content decreased (Fig. 7c). Plant phenols play an important role in the defensive response of plants including excessive concentrations of toxic metal(loid)s (Woźniak et al. 2017). It has been reported that exposure of different forms of As and their combinations increased the content of phenols in Ulmus laevis Pall (Drzewiecka et al. 2018), but decreases have also been reported in Ocimum basilicum plants (Saeid et al. 2014). In our study, tomato plants seemed to adapt to As stress conditions as phenol content did not change. However, total protein content decreased at any As dose (Fig. 7d). Biswas et al. (2016) reported that As exposure at 4 mg L−1 in two rice cultivars decreased total protein content down to 48.56% and 68.34%. Apparently, when trace metal concentrations were high, higher generation of ROS and therefore greater oxidative stress and lower protein production were observed as a result of a greater oxidative damage by trace element presence (Gupta et al. 2009; Sanal et al. 2014). Arsenic causes toxic effects on proteins as a result of its binding to sulfhydryl groups and interaction with the catalytic regions of enzymes (Zhao et al. 2009).

The effect of Si NPs in the absence of As showed at 250 mg Si NPs L−1 decreased glutathione content (Fig. 7a), which also increased the content of phenols by 25.77% (Fig. 7c). The application of Si NPs did not show a significant effect on flavonoid content; however, Si NPs doses decreased total proteins (Fig. 7b and d). It is well known that metallic oxide nanoparticles influence the development of plants. While some species do not show any physiological change, others show variations in the antioxidant system (Siddiqi and Husen 2017). The impact of metallic oxide nanoparticles can be positive or negative depending on the type of nanoparticle, their size, and the concentration used (Torrent et al. 2020).

In this study, As–Si NPs interactions showed a decrease in glutathione content as a function of the concentration of As and Si NPs (Fig. 7a). Glutathione is a crucial non-enzymatic antioxidant which stabilizes the membrane’s structure within the cell and reduces the negative impact of toxic cellular products (Tripathi et al. 2016). However, As and metallic NPs can decrease their content in plants as occurred in this study.

The interaction 0.2–1000 mg L−1 of As and Si NPs decreased the content of flavonoids. This reduction also occurred in plants exposed to 1.6 and 3.2 mgAsL−1 and Si NPs. However, the highest dose of As (3.2 mgAs L−1) in interaction with Si NPs increased the content of flavonoids (Fig. 7b). The increased content of flavonoids induced by high doses of As and Si NPs was likely due to flavonoid production under conditions of severe stress in order to inhibit the generation of ROS (Ni et al. 2017). On the other hand, it has been reported that flavonoid contents of hyper-accumulative plants under As treatments were higher than the control (Wang et al. 2010).

The phenol content was only decreased when the plants were exposed to the interaction 0.8–250 mg L−1 of As and Si NPs, respectively; the rest of the interactions showed no statistically significant differences compared to the control (Fig. 7c). Total phenolics, which are a class of compounds that can eliminate reactive oxygen species (ROS) and are indicators of antioxidant stress responses, have proved to show no change in their content for any type of NPs (Song et al. 2019). The level of unchanged phenols suggested that tomato plants showed no response to stress after exposure to As and Si NPs.

We observed that proteins decreased significantly in all interactions (Fig. 7d). A decrease in protein content in leaves and roots in the Brassica juncea plant has been reported when iron oxide nanoparticles are used in interaction with As (Praveen et al. 2018).

In conclusion, irrigation of tomato plants with As-contaminated water caused As substrate enrichment and As bioaccumulation in roots, steam, and leaves showing that the higher the concentration in irrigation water, the farther the contaminant flowed and translocated through the different tomato strata. Furthermore, within each stratum, As accumulated preferentially in leaf tissue as compared to stem tissue. Arsenic concentrations in tomato fruit were always found below the detection limit (2 mg kg−1). Low As concentrations in irrigation water (0.2 mg L−1) caused decreased plant growth and number of leaves, while higher As concentrations in irrigation water (0.4–3.2 mg L−1) did not show a phytotoxic response. In fact, at higher As concentrations, tomato yield increased. We additionally found that application of Si NPs decreased As translocation, tomato yield, and root biomass. Most likely, lower root biomass accounted for lower As uptake and lower yield. Surprisingly, the combined effect of As and Si NPs at high concentrations (3.2 mg L−1 and 1000 mg L−1) suggested adaptation of tomato plants to As according to the relative phytotoxicity index (PRI), increased production of photosynthetic pigments, and improved activity of CAT and APX. Comprehensively, the application of Si NPs to tomato plants decreased As translocation, stimulated the activity of APX, and increased the photosynthetic capacity of tomato plants that resulted in tomato plant adaptation at high As concentrations in the presence of Si NPs. Results from this study contribute to better understanding the effects of As and nanotechnology on staple foods and show the possible impact that As and nanoparticles could have on tomato production in places where tomato production and the presence of this contaminant in groundwater are common basis.