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Article

Influence of Nonsteroidal Anti-Inflammatory Drugs (NSAIDs) on Photosynthetic Parameters and Secondary Metabolites of Plants from Fabaceae Family

by
Monica Taschina
†,
Cristian Moisa
†,
Andreea Lupitu
,
Dana Maria Copolovici
and
Lucian Copolovici
*
Faculty of Food Engineering, Tourism and Environmental Protection, Institute for Research, Development and Innovation in Technical and Natural Sciences, Aurel Vlaicu University, Elena Dragoi St. No. 2, 10330 Arad, Romania
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Appl. Sci. 2022, 12(13), 6326; https://doi.org/10.3390/app12136326
Submission received: 20 May 2022 / Revised: 18 June 2022 / Accepted: 20 June 2022 / Published: 21 June 2022
(This article belongs to the Section Food Science and Technology)
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Abstract

:

Featured Application

The emission of the volatile organic compounds from plants could be used to indicate plant stress. The current study may help in choosing plants that can remediate soils affected by the presence of NSAIDs.

Abstract

Nonsteroidal anti-inflammatory medications (NSAIDs) are commonly used painkillers, anti-inflammatory agents, and fever reducers. They arrive in the environment from municipal wastewater and/or agriculture waste, affecting growing plants. In our study, the impact of NSAIDs, namely, diclofenac, indomethacin, naproxen, and paracetamol, on four plant species from the Fabaceae family (Cicer arietinum, Pisum sativum, Lens culinaris, and Vicia faba) was tested. The assimilation rate and stomatal conductance decreased for all plants treated with NSAIDs. Chlorophyll and carotenoid contents in the leaves of plants under stress declined by more than 15% compared with the control plants, while the flavonoids and total phenols decreased to a lesser extent. In contrast, the plants treated with NSAIDs emit terpenes and green leaf were volatile, at a level of some nmol m−2 s−1, which could influence the atmospheric reaction and ozone formation.

1. Introduction

Humans’ pharmaceutical compounds make their way into the soil through several routes, including wastewater for irrigation and sewage sludge as fertilizer. After administration, unaltered drugs and their metabolites can also undergo further alteration in sewage due to biological, chemical, and physical processes [1,2]. Municipal wastewater treatment plants could remove microbiological organisms and biodegradable carbon, nitrogen, and phosphorus compounds but have not been built to deal with complex pharmaceutical compounds [3,4]. The soil and groundwater contamination level with drugs depends on soil properties (such as pH, organic matter content, and clay content) and physico-chemical properties of the medicines and their metabolites [5,6]. All NSAIDs have a low acidic character (as their pKa is 4.5 for indomethacin, 4.15 for diclofenac and naproxen, and 9.38 for paracetamol) and may dissociate in solution [7]. As log KOW range from 0.46 for paracetamol to 4.27 for indomethacin, the transport of those drugs in the soil is mainly ruled by the absorption–desorption mechanism [7].
A recent study said that only 31% of hospital wastewater was treated in India [8]. Trace concentration of antibiotics has been found in different hospital effluents in South Africa [9], Brasil [10], and Sweden [11].
Ketoprofen, naproxen, indomethacin, and diclofenac have recently been found in sewage treatment plant effluents in France, Greece, Italy, and Sweden [12]. Relatively high concentrations of diclofenac have been found not only in rivers and lakes [13,14] but also in groundwater and drinking water [15,16,17], with a maximum of 4.9 µg L−1 reported in Pakistan’s lakes [18]. Paracetamol occurrence in the surface waters is quite common and has been found in approximately 75% of natural water [19,20,21]. The highest concentration of paracetamol found in a small river Seke La Paz Bolivia was 227 μg L−1 [21]. Indomethacin has been detected in the primary influents in concentrations between 20 and 100 μg L−1 [22,23]. Ketoprofen is found in rivers, effluents, and wastewater at a level of μg L−1 [24]. The levels of naproxen found in river water and sediments ranged from 0.59 to 2.3 µg L−1 [25].
Nonsteroidal anti-inflammatory drugs (NSAIDs) are toxic to ecosystems. Numerous studies indicate that NSAIDs may harm aquatic life and human health. Compounds can generate oxidative stress in plants at high concentrations or induce hormesis in plants at low concentrations, depending on the kind, concentration, and duration of exposure and the species and stage of development of the plant. For example, diclofenac and ketoprofen are highly toxic for vultures [26]. It has been shown that NSAIDs influence the plant’s development. Hammad et al. [27] discovered that paracetamol has a detrimental effect on Zea mays growth and development. When the dose of paracetamol was raised, the accumulation of paracetamol in maize grain and root grew linearly; however, the protein content of the grain was not impacted by the dose increase. Plants may absorb NSAIDs, water, and nutrients, where they can be stored and transformed into tissues. Research on spring barley (Hordeum vulgare L.) seedlings found that naproxen has significantly influenced the plant’s growth and development. The mixture of diclofenac and naproxen had a moderate effect, and diclofenac had the least impact [28]. After a prolonged period of exposure, the low concentration of paracetamol slowed the development of wheat plants. The paracetamol treatment affected the chlorophyll accumulation with 1.4–22.4 mg L−1 after a 21-day exposure [29]. Separate research showed that lettuce plants (Lactuca sativa L.) treated with high quantities of paracetamol had a considerable drop in photosynthesis and chlorophyll fluorescence, suggesting a possible influence on photosystem II quantum efficiency [30]. It was discovered that indometacin had a dose-dependent effect on algal growth, macromolecular synthesis, and metabolism. Cell division and dry mass production were inhibited when cells were exposed to 10−3 mol L−1 of indomethacin for seven days [31].
The Fabaceae or Leguminosae family, also known as the legume, pea, or bean family, is a vast and commercially significant flowering plant family. Previous articles showed that paracetamol [32] and diclofenac [33] influence the photosynthetic parameters and metabolites concentration of Phaseolus vulgaris L. even at low drug concentrations 0.1 g L−1 for diclofenac and 1 g L−1 for paracetamol)
This study aimed to evaluate the modifications in photosynthetic parameters and secondary metabolites for four species from Fabaceae family (Cicer arietinum, Pisum sativum, Lens culinaris, and Vicia faba) due to their exposure to NSAIDs (diclofenac, indomethacin, naproxen, and paracetamol).

2. Materials and Methods

2.1. Plant Material

Experiments were carried out in 2021. Commercial seeds from the following plants: Pisum sativum, Lens culinaris, Vicia faba, and Cicer arietinum were sown in 0.5 L plastic pots filled with commercial garden soil and grown under controlled conditions of light (1000 µmol m−2 s−1), temperature (25 °C), and humidity (60–70%). Plants were watered every second day to pot capacity. The treatments were started after 21 days with plants bearing a minimum of 3 leaves. Every second day, the plants were watered with a 100 mL aqueous solution of NSAIDs (diclofenac, indomethacin, naproxen, and paracetamol) with 0.5 mg L−1 concentration for 20 days. As stated in the figure captions, three to four plants in different pots were used for every experimental group.

2.2. Photosynthetic Measurements

Assimilation rates and stomatal conductance to water vapor were determined with a portable gas exchange system, GFS-3000 (Waltz, Effeltrich, Germany) [34]. This system included a cuvette with an 8 cm2 window area and a leaf chamber fluorimeter with a full window for sample illumination. The leaf was measured under the following conditions: leaf temperature of 25 °C, chamber air humidity of 65%, the light intensity of 1000 µmol m−2 s−1, and CO2 concentration of 400 mmol mol−1. The leaf was stabilized under the standard conditions until stomata opened and steady-state CO2 and water vapor exchange rates were reached. Steady-state values of assimilation rate (A) and stomatal conductance to water vapor (gs) were calculated according to von Caemmerer and Farquhar (1981) [35].

2.3. Volatile Sampling and GC–MS Analyses

A constant flow air sample pump 210-1003 MTX (SKC Inc., Houston, TX, USA) was used to sample volatile organic compounds (VOC) from the gas-exchange cuvette at a flow rate of 200 mL min−1 for 20 min, as previously described [36]. Automated cartridge desorber and a Shimadzu 2010 Plus GC–MS apparatus (Shimadzu Corporation, Kyoto, Japan) were used to analyze the adsorbent cartridges [37,38]. Briefly, The GC carrier gas had a total flow in the column of 1.82 mL min−1. An OPTIMA-624 capillary column (0.25 mm i.d. 60 m, 1.4 µm film, Macherey–Nagel, Düren, Nordrhein-Westfalen, Germany) was employed for the volatile separation using the same program as in [38]. The mass spectrometer was operated in electron-impact mode at 70 eV, in the scan range m/z 30–400, the transfer line temperature was set at 250 °C, and the ion-source temperature at 200 °C. Calculations of volatile emission rates were performed by subtracting background (blank) emissions from those of the leaf samples.

2.4. Chromatographic Analysis of Photosynthetic Pigments

Samples of 4 cm2 of the plant’s leaves were placed in liquid nitrogen, and using ice-cold acetone (70 percent), the pigments were extracted, as previously described [39]. Chlorophyll a, chlorophyll b, and β-carotene were evaluated using the UHPLC (NEXERA8030, Shimadzu, Japan) equipped with a diode array detector (DAD), using the procedure described before [39]. A Nucleosil 100-3 C18 reversed-phase column (4.0 mm i.d. 150 mm column length, 3 µm particle size, Macherey–Nagel, Düren, Nordrhein-Westfalen, Germany) was used. The solvents used for the chromatographic elution consisted of buffered ultra-pure water (0.1 M sodium phosphate buffer, pH = 8) (A) and HPLC grade acetone (B). The chromatographic elution program followed the same procedure as in [39].

2.5. Total Phenolic Content–Folin Ciocalteu Method

The extracts were obtained by macerating fresh leaves in 60% methanol for seven days at a temperature of +4 °C. All extracts were filtered through a PTFE membrane with a pore size of 0.45 µm. Folin–Ciocalteu’s method was used to determine the total phenolic content, as described in [40].

2.6. Flavonoid Content

The methanolic extracts obtained previously were used to determine the flavonoid content using a previously published method [41].

2.7. Statistical Analysis and Data Handling

One-way ANOVA followed by Tukey’s multiple comparisons test was performed using GraphPad Prism, version 9.4.0, for Windows (GraphPad Software, San Diego, CA, USA, www.graphpad.com (accessed on 10 May 2022)). All analyzes were performed in triplicate, and the results were reported as mean.

3. Results

3.1. The Influence of NSAIDs on Photosynthetic Parameters

The assimilation rates of all species were affected by NSAIDs regardless of the type of drugs (Figure 1). Control plants’ assimilation rate decreased by at least 50% for plants treated with 0.5 mg L−1 NSAIDs. The assimilation rates were differently affected by NSAIDs treatment in different species. For example, in the case of Lens culinaris, the assimilation rates were statistically different for all medicines (p < 0.05). At the same time, for Cicier arientinum there were no differences between naproxen, indomethacin, and paracetamol treatments (p = 0.947).
Stomatal conductance to water vapor was affected by NSAIDs for all species (Figure 2). In the case of Lens culinaris plants, stomatal conductance to water vapor decreased drastically from 83.7 ± 2.7 mmol m−2 s−1 in the control plants to 18.3 ± 2.1 mmol m−2 s−1 in plants treated with paracetamol.

3.2. The Emission of Volatile Organic Compounds from Plants for Plants Affected by NSAIDs

The plants from the Fabaceae family are not monoterpenes emitters in physiological conditions. There is a low emission of monoterpenes from plants under NSAID stress with no clear trend regarding drug type (Figure 3). The limonene is dominant in emission for all species, while camphene and β-ocimene show the lower emission.
In contrast, 1-hexanol (a green leaf volatile) emission increased significantly (p < 0.05) compared with the control for all plant species treated with NSAIDs (Figure 4). The higher emission of 1-hexanol was from plants treated with paracetamol 0.038 ± 0.001 nmol m−2 s−1 with no statistical differences between the species (p = 0.729).

3.3. The Influence of NSAIDs on Chlorophylls and β-Carotene

The chlorophyll a concentrations in the leaves of all four species decreased for plants treated with NSAIDs (Figure 5). The chlorophyll a concentration of control plants varied from 556 ± 35 mg m−2 in Pisum sativum to 293 ± 25 mg m−2 in Lens culinaris. There were no statistical differences between different drug treatments in the case of all species.
The chlorophyll b concentrations in leaves were influenced by NSAIDs treatments (Figure 6). In the case of Cicer arietinum treated with diclofenac, the concentration of chlorophyll b decreased by more than 45% compared with control leaves. The medium chlorophyll b concentration for all species was 237 ± 119 mg m−2. Generally, there were no statistical differences between the different types of drug treatments.
The concentrations of β-carotene in the leaves of all four species decreased for plants under NSAIDs stress (Figure 7). Despite the chlorophylls, the β-carotene concentration in control plants did not differ significantly across species (varied between 27.1 ± 3.0 mg m−2 in Lens culinaris and 23.4 ± 1.9 mg m−2 in Cicer arietinum).

3.4. The Change in Total Flavonoids Concentration for Plants Affected by NSAIDs

The leaf flavonoid concentrations of all four species were lower for plants treated with NSAIDs than for the control plants (Figure 8). The concentration of flavonoids in the control leaves for all species varied between 80.6 ± 5.5 mg rutin equivalents/mL in Pisum sativum and 68.1 ± 5.1 mg rutin equivalents/mL in Lens culinaris with an average of 74.2 ± 5.4 mg rutin equivalents/mL. Different plant species reacted differently to drug stress. For example, Cicer arietinum total flavonoids were more affected by paracetamol than indomethacin, while in Lens culinaris the indomethacin significantly decreased the total flavonoids compared with paracetamol (p < 0.05).

3.5. The Influence of NSAIDs on Total Phenols Content in the Leaves of Fabaceae Plants

NSAIDs treatments do not affect the total phenols concentration for some Fabaceae family species but decrease others (Figure 9). The most pronounced decrease in total phenols concentration was found in Lens culinaris plants (164 ± 14 mg Eg gallic acid/L for plants treated with diclofenac compared with 296 ± 27 mg Eg ac gallic/L for control plants).

4. Discussion

The plants’ behavior was reported to be dose-dependent [42,43]. The concentration of NSAIDs used in this study was chosen to be lower than the maximum values determined for the drugs found in the environmental [21,22,23].
NSAID-induced alterations in the photosynthetic machinery as assimilation rates and stomatal conductance to water vapor decrease for all species. A similar pattern was determined in Lactuca sativa plants treated with 0.76 g L−1 paracetamol [30] and in bean plants treated with 0.30 g L−1 paracetamol [32]. Interestingly, there were differences in the assimilation rates for plants treated with different medicines, but no pattern could be observed. Generally, diclofenac influence lowers the carbon uptake over naproxen or paracetamol. Diclofenac’s poor translocation rate to other parts of the plants could explain its low lipophilicity [44]. It has been demonstrated that reducing the assimilation rate depends on drug type and administration dose [33,39,45]. Such patterns have even been demonstrated in green algae, such as S. obliquus [45,46], Chlorella, and Desmodesmus spinosus [47], suggesting that NSAIDs seem to impact chloroplast and mitochondrial function, resulting in lower oxygen consumption. Since all NSAIDs have the same adverse effects on the assimilation rate, all such drugs may have phytotoxicity potential. In addition, the lower activity of PSII reaction centers is probably linked to the suppression of photosynthesis.
Stomata are the entry points for transpiration, photosynthesis gas exchange, and microbial penetration into the leaves of the plants. Stomatal closure is an effective defense mechanism against biotic [48] and abiotic stressors, such as drought [41,49], ozone [50], and high temperature [51]. Moreover, many studies have shown that plants exposed to harmful metal concentrations have decreased stomatal conductance (or increased stomatal resistance). For example, stomatal conductance and density are significantly reduced in Setaria veridis treated with cadmium ions [52]. In our experiment, stomata conductance to water vapor decreased for plants treated with NSAIDs. There were no clear trends for different drugs among the species. The same behavior has been found in plants treated with antibiotics but only at high concentrations [39]. This could be explained by the fact that long-distance water transport is inhibited, which results in a decrease in leaf water content and a water deficit in the leaves over time [53]. Such a decrease in stomatal conductance could be linked with the reduction of the synthesis of abscisic acid (ABA) and associated with reduced chlorophyll content [39,54].
NSAID-induced changes in plant photosynthetic pigment content have been documented in the literature, which shows that various plant species are more or less sensitive to these drugs. Still, the pharmaceutical dosage may also play a role. Relatively low concentrations of diclofenac and naproxen determine a decrease in the total chlorophyll in the leaves of vegetables as Atriplex patula L., Spinacia oleracea L., and Lactuca sativa L. [43]. Only 2 mg L−1 diclofenac determines a drop in the maximum quantum efficiency of PSII and the activity of PSII and a decrease in the content of the photosynthetic pigments for maize (Zea mays L.) and tomato (Solanum lycopersicum L.) plants [55]. Reduced levels of photosynthetically active pigments in plants under NSAIDs stress are directly linked to lower photosynthesis intensity levels and lower carbon uptake [56]. An alteration in the chlorophyll a/b and carotenoid/total chlorophyll ratios may indicate a reduction in PSII light-trapping activity and the initiation of antioxidant response.
Non-stressed plants from the Fagaceae family do not produce monoterpenes. In contrast, many plant species have monoterpenes in response to environmental stressors [57,58,59], and the stress-induced monoterpene emissions correlate with terpenoid gene transcription initiation [60]. This study’s monoterpene emissions from the NSAIDs tested showed no significant differences. This finding implies that the pathway flux into monoterpene synthesis was independent of NSAID type after induced monoterpene emission.
The emission of green leaf volatiles (C5 and C6 aldehydes and ketones) is mainly due to biotic or abiotic stress factors acting on plants. Indeed, the emission of different green leaf volatiles has been found for plants under drought, temperature [61], flooding, or herbivores [62]. The plants treated with paracetamol have been shown to have the highest emission of 1-hexanol, followed by diclofenac stressed plants. The findings of this study provide more evidence that green leaf volatiles emissions are a highly sensitive predictors of how plants react to NSAIDs.
The flavonoid concentration in leaves decreases for all plants treated with NSAIDs. The same results have been reported for the treatment of wheat with a high concentration antibiotics solution [63]. During times of oxidative stress brought on by variables in the surrounding environment, one of the roles of flavonoids is to lessen the impact of reactive oxygen species [64]. Such behavior demonstrates that a persistent effect of drugs can impair the antioxidative capacity of the foliage, which indicates that the foliage’s ability to defend itself gets depleted [65].
Important plant constituents with redox characteristics and antioxidant action are phenolic compounds. Their concentrations in leaves usually increase during short-time oxidative stress (see [66] for review), but in the case of prolonged stress, the total concentration of phenolic compounds could decrease [67]. In our experiment, the concentration of total phenolic compounds decreased for plants under stress conditions for some species. In contrast, for others (such as Vicia faba), the phenolic compounds were disturbed only in plants treated with naproxen. Such a decrease in the antioxidant capacity has been found in Atriplex patula L. plants treated with naproxen [43]. Such behavior is correlated with reducing the content of carotenoids and flavonoids.
From the principal component analysis (PCA) plot with only photosynthetic parameters and photosynthetic pigments (Figure 10, Data in Supplementary Table S1), the Cicer arietinum plants were the most influenced by the presence of NSAIDs, while the Pisum sativum plants were less disturbed. It has already been shown that chickpea plants are sensitive to soil salinity [68] and temperature [69], and the present study demonstrates, once again, its sensitivity to abiotic stresses.
From the PCA plot with all available data (Figure 11), the clustering of control plants could be seen compared with the treated plants. Even more, the Pisum sativum plants express high sensitivity to NSAIDs, but there is no clear pattern for the other species.

5. Conclusions

This research shows the impact of four significant organic contaminants (diclofenac, indomethacin, naproxen, and paracetamol) on the composition and ultrastructure of food-producing plants. Photosynthetic parameters, chlorophyll, carotenoids, polyphenols, and flavonoids were all reduced due to NSAIDs exposure. In contrast, the emission of different terpenes and green leaf volatiles involved in secondary aerosol formation were enhanced even for plants not known to be volatile compound emitters.

Supplementary Materials

The following supporting information can be downloaded at: www.mdpi.com/article/10.3390/app12136326/s1. Table S1. The characteristics of different plants species treated with NSAIDs (raw data for Figure 1, Figure 2, Figure 3, Figure 4, Figure 5, Figure 6, Figure 7, Figure 8, Figure 9, Figure 10 and Figure 11).

Author Contributions

Conceptualization, M.T. and L.C.; methodology, M.T., C.M., A.L. and D.M.C.; software, C.M., A.L. and D.M.C.; validation, C.M., A.L. and L.C.; formal analysis, M.T., C.M., A.L. and D.M.C.; investigation, M.T., C.M., A.L. and L.C.; resources, L.C.; data curation, C.M. and L.C.; writing—original draft preparation, M.T. and L.C.; writing—review and editing, A.L., D.M.C. and L.C.; supervision, L.C.; project administration, L.C.; funding acquisition, L.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by CNFIS-UEFISCDI, project number PN-III-P4-ID-PCE-2020-0410.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors thank Brenda Crystal Svinti for the professional editing of this paper.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. The assimilation rate from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of four independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
Figure 1. The assimilation rate from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of four independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
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Figure 2. Stomata conductance to vapor water from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of four independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
Figure 2. Stomata conductance to vapor water from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of four independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
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Figure 3. The emission rates of monoterpenes from leaves from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of three independent measurements.
Figure 3. The emission rates of monoterpenes from leaves from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of three independent measurements.
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Figure 4. The emission rates of 1-hexanol from leaves from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of three independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
Figure 4. The emission rates of 1-hexanol from leaves from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of three independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
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Figure 5. Chlorophyll a concentration from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of four independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
Figure 5. Chlorophyll a concentration from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of four independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
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Figure 6. Chlorophyll b concentration from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of four independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
Figure 6. Chlorophyll b concentration from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of four independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
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Figure 7. β-carotene concentration from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of four independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
Figure 7. β-carotene concentration from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of four independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
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Figure 8. Flavonoids concentration from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The plants were treated for ten days. The values are averages of three independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
Figure 8. Flavonoids concentration from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The plants were treated for ten days. The values are averages of three independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
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Figure 9. Total phenols concentration from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of three independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
Figure 9. Total phenols concentration from Pisum sativum (a), Lens culinaris (b), Vicia faba (c), and Cicer arietinum (d). Plants in 0.5 L pots filled with commercial garden soil were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. The values are averages of three independent measurements. Data sharing different letters are significantly different (p < 0.05), while data sharing the same letters are not significantly different (p > 0.05).
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Figure 10. The principal component analysis plot (PCA) with photosynthetic parameters and pigments of plants in 0.5 L pots filled with commercial garden soil that were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. PCA 1 and 2 explain 84.5% of the variation (61.9% and 22.6%, respectively). See Supplementary raw data in Table S1.
Figure 10. The principal component analysis plot (PCA) with photosynthetic parameters and pigments of plants in 0.5 L pots filled with commercial garden soil that were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. PCA 1 and 2 explain 84.5% of the variation (61.9% and 22.6%, respectively). See Supplementary raw data in Table S1.
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Figure 11. The principal component analysis plot (PCA) of plants in 0.5 L pots filled with commercial garden soil that were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. PCA 1 and 2 explain 70.23% of the variation (55.7% and 14.5%, respectively). See Supplementary raw data in Table S1.
Figure 11. The principal component analysis plot (PCA) of plants in 0.5 L pots filled with commercial garden soil that were treated by watering 100 mL of 0.5 mg L−1 NSAIDs every second day over a total of 20 days. PCA 1 and 2 explain 70.23% of the variation (55.7% and 14.5%, respectively). See Supplementary raw data in Table S1.
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Taschina, M.; Moisa, C.; Lupitu, A.; Copolovici, D.M.; Copolovici, L. Influence of Nonsteroidal Anti-Inflammatory Drugs (NSAIDs) on Photosynthetic Parameters and Secondary Metabolites of Plants from Fabaceae Family. Appl. Sci. 2022, 12, 6326. https://doi.org/10.3390/app12136326

AMA Style

Taschina M, Moisa C, Lupitu A, Copolovici DM, Copolovici L. Influence of Nonsteroidal Anti-Inflammatory Drugs (NSAIDs) on Photosynthetic Parameters and Secondary Metabolites of Plants from Fabaceae Family. Applied Sciences. 2022; 12(13):6326. https://doi.org/10.3390/app12136326

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Taschina, Monica, Cristian Moisa, Andreea Lupitu, Dana Maria Copolovici, and Lucian Copolovici. 2022. "Influence of Nonsteroidal Anti-Inflammatory Drugs (NSAIDs) on Photosynthetic Parameters and Secondary Metabolites of Plants from Fabaceae Family" Applied Sciences 12, no. 13: 6326. https://doi.org/10.3390/app12136326

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