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Article

Aquatic Ecological Risk Evaluation of Chiral Triazole Fungicide Prothioconazole and Its Metabolite Prothioconazole-Desthio on Lemna minor

by
Yaling Yang
,
Xiaomeng Li
,
Qiyue Tang
,
Liangchi Mei
,
Jian Cao
,
Haiyun Huang
and
Zhaoxian Zhang
*
Key Laboratory of Agri-Food Safety of Anhui Province, College of Resources and Environment, Anhui Agricultural University, Hefei 230036, China
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(23), 16292; https://doi.org/10.3390/su142316292
Submission received: 27 October 2022 / Revised: 28 November 2022 / Accepted: 3 December 2022 / Published: 6 December 2022
(This article belongs to the Special Issue Exposure Sciences and Corresponding Toxicology for Emerging Contaminants)
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Abstract

:
The potential risk posed by the chiral triazole fungicide prothioconazole and its metabolite, prothioconazole-desthio to aquatic ecosystems has attracted attention. At present, the aquatic toxicity of prothioconazole is focused on aquatic animals, and the study of aquatic plants is limited. In this work, the acute toxicity of prothioconazole (PTZ) and its metabolite, prothioconazole-desthio (PTD), to the aquatic plant Lemna minor (L. minor) was evaluated at the enantiomer level. The effects of the prothioconazole and its metabolite enantiomer on the physiological and biochemical indices, including growth rate, photosynthetic pigment content, and antioxidant-defense-enzymes activity, of L. minor were measured to evaluate the potential risk. The results showed that prothioconazole and prothioconazole-desthio possessed obvious stereoselective toxicity to Lemna minor with an LC50 (7 days) of 0.76–5.63 mg/L. The toxicity order was S-PTD > Rac-PTD > S-PTZ > R-PTD > Rac-PTZ > R-PTZ. The S-PTZ, which had the highest toxicity, obviously inhibited the biosynthesis of photosynthetic pigments and the activity of antioxidant-defense enzymes (malondialdehyde, catalase and superoxide dismutase), leading to an increase in MDA content and oxidative damage. The results further confirmed that the metabolism of PTZ in aquatic ecosystems increased its exposure risk, providing data support and a theoretical basis for the risk assessment of PTZ.

1. Introduction

Prothioconazole (PTZ), a demethylation inhibitor, is a chiral triazole fungicide that can inhibit ergosterol biosynthesis and destroy the biological function of the cell membrane, thereby leading to the death of pathogenic fungi [1,2]. Due to its characteristic of high efficiency and broad spectrum, PTZ has been widely used to control many diseases in cereals, wheat and legumes, especially Fusarium graminearum [3,4]. However, the environmental toxicology issues associated with the use of PTZ have attracted serious attention. Prothioconazole can be rapidly degraded after being applied, forming its main metabolite, PTD [5,6,7]. Compared with its parent compound, PTD has a higher toxicity and can persist in soil, water and crops [5,8]. The initial amount of PTD was 0.152–0.545 mg kg−1 in rice in the Anhui, Hubei, and Guangdong provinces and there was no PTZ in the rice at harvest [9]. The concentration of PTD on wheat in Shandong and Anhui were 0.439 and 0.201 mg kg−1 after 30 d, respectively [10]. The residues of PTD at 14 d were 0.1–0.2 mg kg−1 in tomato, cucumber and pepper [8]. Previous studies showed that PTZ and its metabolite can cause liver-metabolism and gonad disorders, as well as inducing liver steatosis and damage in mice exposed to PTZ (1.5 mg/kg body weight/day) [11]. Prothioconazole and its metabolite also change the structure and composition of the gut microflora in mice, inducing gut dysfunction in mice. [12] The metabolite PTD exhibits greater negative effects than the parent compound [11,12]. In addition, the bioavailability of PTD in lizards was higher than that of PTZ. Both compounds can change the composition and structure of gut microorganisms, affecting the gut barrier function of lizards [13,14]. In addition, PTZ and PTD also possess a strong endocrine-disrupting effect, leading to reproductive and developmental toxicity [15].
Pesticide application can reach surface water through surface runoff, adversely affecting aquatic life [16]. Previous studies showed that PTZ poses a potential risk to aquatic organisms; it was moderately toxic toward zebrafish embryos, destroying cardiac morphology and function, which led to cardiovascular toxicity for zebrafish embryos [17]. Prothioconazole at the exposure concentration of 0.85 mg/L can cause zebrafish-embryo malformation, including yolk-sac and pericardial edemas [18]. In addition, PTZ induced metabolic disorders, resulting in lipid peroxidation for zebrafish embryos [19]. Zhang et al. investigated the acute toxicity of PTZ and its metabolite toward zebrafish, and the results showed that the toxicity of the metabolite was 3.4-fold higher than that of PTZ. Prothioconazole and its metabolite can inhibit the activity of antioxidant enzymes, leading to the accumulation of malondialdehyde (MDA) and oxidative damage [20]. Previous studies on the environmental toxicology of PTZ and its metabolite, PTD, mainly focused on mammals and aquatic organisms. Reports on their effects on aquatic plants are very limited. Therefore, it is of great significance to explore the effects of PTZ and its metabolites on aquatic plants for a systematic risk evaluation of PTZ in aquatic ecosystems.
Duckweeds, which are typical aquatic plants, are freshwater organisms that are widely spread in ponds, lakes and streams in temperate and tropical regions. Duckweeds are extremely important primary producers in aquatic systems and they potentially change the structure, function and stability of these ecosystems [21]. Common species of duckweeds are Lemna minor, Spirodela polyrhiza, Landoltia punctata, Lemna aequinoctialis and Wolffia globose [22]. Duckweeds with the characteristics of small size, simple structure, fast asexual reproduction, strong adaptability and sensitivity to environment chemical compounds are ideal experimental materials in ecotoxicology research. In particular, L. minor has been recommended by the International Organization for Standardization (ISO) and the Organization for Economic Co-operation and Development (OECD) test guidelines [23,24]. Wang et al., revealed the toxic effects of lactofen and its metabolites on L. minor by interfering with photosynthetic pigment biosynthesis and inhibiting antioxidant enzyme activities [24]. Tan et al. investigated the stereoselective toxicity of imazamox toward L. minor using metabonomics and transcriptomics and the results showed that S-imazamox affects the growth of L. minor by acting on multiple metabolic pathways, whereas R-imazamox mainly affected L. minor by acting on photosynthesis and the antioxidant system [25].
Prothioconazole and PTD are composed of a pair of enantiomers with almost identical physical and chemical properties [7]. However, their biological activities, ecotoxicity and environmental behaviors in ecosystems are significantly different. Zhang et al. found that R-PTZ and R-PTD possessed high bioactivity and were preferentially degraded in soil [5,26,27,28]. Moreover, S-enantiomers with substantial endocrine-disrupting effects persisted in the environment [15]. In this study, the acute toxicity of PTZ and its metabolite to L. minor was investigated at the enantiomeric level. The photosynthetic-pigment content and antioxidant-enzyme activities of L. minor exposed to different enantiomers were measured. The results of this study provide a scientific theoretical basis for the systematic evaluation of the exposure risk of PTZ to aquatic plants.

2. Materials and Methods

2.1. Reagents

The PTZ (purity > 99.5%) and PTD (purity > 99.8%) standards were supplied by Anhui Jiuyi Agricultural Co., Ltd. (Hefei, China). The PTZ and PTD enantiomers (purity > 99.0%) were prepared Daicel Chiral Technologies Co., Ltd. (Shanghai, China). The stock standards of PTZ and PTD enantiomers at a concentration of 10,000 mg/L were dissolved in acetone, and the working standard solutions were serially diluted with acetone according to the experimental requirements. Hoagland nutrient solution was purchased from Qingdao Hope Bio-Technology Co., Ltd. (Qingdao, China). Ultra-pure water was prepared using a Milli-Q Advantage A10 ultrapure water system (Millipore, Darmstadt, Germany). Other analytical- or chromatographic-grade reagents were purchased from Business Company Ltd. (Hefei, China).

2.2. Plant Material and Cultivation

The L. minor was provided by the Chinese Academy of Tropical Agricultural Sciences Environment and Plant Protection Institute. Some L. minor specimens of similar size (2 ± 0.2 mm) and consistent color were selected and cultured with 1/10 Hoagland nutrient solution for 1 week in an incubator. The culture conditions were as follows: temperature of 25 ± 3 °C, photoperiod of 16 h/8 h (L:D), relative air humidity of 60% and irradiance of 114 µmol·m−2·s−1 provided by fluorescent tubes of TLD 36 W/54 (Philips, Shanghai, China).

2.3. Acute-Toxicity Experiment

An acute-toxicity experiment on PTZ and PTD to L. minor was conducted according to ISO 20079 [23] and OECD guideline 221 [24]. The glass Petri dishes in the experiment were cleaned and autoclaved to prevent the interference of other biotic or abiotic factors. Four healthy L. minor specimens with two fronds were transferred to the nutrient solution containing Rac-, R-, S-PTD and Rac-, R-, S-PTZ at series of concentration (0.05, 0.1, 0.25, 0.5, 1, 5 and 10 mg/kg) in triplicate. The L. minor was cultured under the experimental conditions above and the nutrient solution was changed every day. In addition, a treatment with an equal amount of acetone was conducted to confirm that there was no interference of acetone in the L. minor growth. The number of fronds and the changes in appearance were recorded at 3, 5 and 7 days to calculate the growth-rate inhibition and half-maximal inhibitory concentration (IC50) of the target compound using following equations (Eq.) [25].
The relative growth rate was calculated using Equation (1):
µ = (ln (Nt) − ln(N0))/t
where µ is relative growth rate for time 0 to t; Nt is frond number at real time; N0 is frond number at initial time; t is time period from 0 to t.
The percentage inhibition of growth rate was calculated using Equation (2):
I = (µc − µT)/µc × 100%
where I is percent inhibition of growth rate; µc is elative growth rate of control group; µT is relative growth rate of treatment group.
Finally, the log-concentration-percentage inhibition curve was generated to calculate IC50.

2.4. Physiological and Biochemical Experiment

To investigate the enantioselective influence of PTZ and PTD on photosynthetic pigment biosynthesis, 1 g of healthy L. minor was transferred to 50 mL of medium containing PTZ and PTD enantiomers at three concentration levels of 0.05, 0.5 and 1 mg/L in triplicate. The medium with the tested compound and acetone was renewed every day. After 7 days of culture, the samples were washed with deionized water three times and dried with absorbent paper. The samples were weighed and stored at −80 °C.

2.4.1. Determination of Photosynthetic Pigment Content

First, 0.2 g of L. minor was broken in a precooled mortar with liquid nitrogen and then transferred to a polyethylene centrifuge tube containing 2 mL of 80% acetone. The mixtures were homogenized and centrifuged at 10,000× g for 20 min at 4 °C. The supernatant was collected to measure the absorbance values at 470 nm, 647 nm and 663 nm. The contents of chlorophyll a, chlorophyll b and carotenoids were calculated according to the Lichtenthaler formula [29].

2.4.2. Determination of Antioxidant Enzymes Activities and Lipid Peroxidation

First, 0.5 g of L. minor was prepared in triplicate to measure the antioxidant enzyme activity (CAT, APX and SOD) and MDA content. The samples were homogenized in 1 mL of ice-cold 0.05 M phosphate buffer (pH 7.0) at 4 °C. The homogenate was centrifuged for 10 min at 12,000× g at 4 °C. The supernatants were carefully transferred to 10-milliliter centrifuge tubes to measure the enzyme activity and determine the MDA content using the corresponding kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China), according to the kit instructions.

2.5. Statistical Analysis

Statistical analysis was performed using IBM SPSS Statistics (Version 26, Inc., New York, NY, USA). The statistical significance of the average values in different treatment groups was analyzed using one-time ANOVA (p < 0.05).

3. Results and Discussion

3.1. Enantioselective Acute Toxicity

The results of the growth-inhibition experiments showed that there was no effect of acetone as a solvent on the L. minor growth. The L. minor was exposed to varying degrees of damage, including the visible chlorosis of fronds and gradual break-up of the colony; moreover, it sank to the bottom of the culture dish after it was treated with different PTD and PTZ enantiomers. A morphological change from chlorosis to disintegration is a typical symptom of L. minor exposure to pollutants. Figure 1 shows the growth-rate inhibition of L. minor by serial concentrations of PTZ and PTD enantiomers. The metabolite, PTZ, possessed higher toxicity than the parent compound, suggesting that the metabolism of PTD in aquatic ecosystems increases the exposure risk. Zhang et al. investigated the acute toxicity of PTZ and PTD to zebrafish and their results showed that the toxicity of the metabolite PTD with an LC50 of 1.31 mg/L was 3.5-fold that of PTZ [20]. In fact, PTZ was quickly transformed into PTD in water, where, driven by biotic and abiotic factors, it was slowly degraded [27]. Therefore, the reason for the high toxicity of the metabolite may be its environmental persistence. There was remarkable enantioselectivity according to the growth-inhibition rates of L. minor. The S-PTD and R-PTZ possessed the highest and lowest inhibition rates, respectively.
To accurately evaluate the toxicity of PTZ and PTD enantiomers to L. minor, their LC50 values were calculated at different time points. As shown in Table 1, the toxicity of PTZ and PTD increased with time, whether it was the racemate or enantiomer, while the LC50 values of the analytes at 3, 5 and 7 days were 7.59–20.36, 2.57–12.32 and 0.76–5.63 mg/L, respectively. The order of toxicity was S-PTD > Rac-PTD > S-PTZ > R-PTD > Rac-PTZ > R-PTZ. The S-enantiomers exhibited higher toxicity than the R-enantiomers. The S-PTZ was 2.7-fold more toxic than the R-PTZ, while the S-PTD was 2.9-fold more toxic than the R-PTD at 7 days. Zhai et al. measured the LC50 values of PTD enantiomers, revealing that S-PTD with an LC50 (7 days) of 0.49 mg/L exhibited higher toxicity than the R-enantiomer [30]. Our results agree with previous reports. According to the present study, the PTZ shows stereoselective acute and chronic toxicity toward aquatic organisms, mammals and reptiles, particularly the metabolite, PTD. Therefore, it is extremely important to improve and strengthen the risk assessment and management control of PTZ for ensuring ecological safety and human health.

3.2. Effect of PTZ and PTZ Enantiomer on Dry Weight and Photosynthetic Pigment

The biomass production of plants is predominantly determined by the function of photosynthetic organs [31,32]. It was reported that pesticides could affect the dry weights of plants. Triazolinone herbicide carfentrazone-ethyl treatment caused a significant reduction in the dry weights of water lettuce and water hyacinth [33]. Wang et al. confirmed that the inhibition of lactofen and its metabolites via photosynthetic processes was the most important mechanism underlying the toxic effects to L. minor [25]. Therefore, the effect of PTZ and PTD enantiomers at exposure concentrations of 0.05, 0.5 and 1 mg/L on the dry weight and photosynthetic pigment of L. minor was measured according to available assay methods. As shown in Figure 2 and Figure S1, the variation trend of the dry weight of L. minor was basically similar to that of the photosynthetic pigment exposed to different enantiomer concentrations, suggesting that the growth inhibition of L. minor by PTZ and PTD might be achieved by affecting photosynthesis. The inhibition rate of the metabolites was higher than that of the PTZ, which was consistent with the results of the acute-toxicity assay. Higher concentrations of enantiomers inhibited the biosynthesis of chlorophyll and carotenoids more significantly. The S-enantiomer showed a higher inhibition rate than the R-enantiomer. The inhibition rates of the S-PTD at the exposure concentration of 1 mg/L on the dry weight, chlorophyll and carotenoid of the L. minor were 42.4%, 38.3% and 32.3%, which were 2.7-, 4.8- and 2.2-fold the rates of the R-PTZ; the inhibition rates of the S-PTZ at the exposure concentration of 1 mg/L with the highest toxicity were 70.2%, 67.5% and 40.7%, respectively, which were 1.9-, 3.3- and 3.1-fold the rates of R-PTZ, respectively. The effects of the PTD and PTZ enantiomers at an exposure concentration of 0.05 mg/L on the dry weight and physiological parameters of the L. minor were not significant. The S-PTZ, Rac-PTD and S-PTD at an exposure concentration of 0.5 mg/L significantly inhibited the dry weight and photosynthetic pigment content of the L. minor.

3.3. Antioxidant-Enzyme Activities

Plant oxidative stress is caused by the accumulation of reactive oxygen species, formed by the imbalance between oxidation and antioxidation [34]. It is a common response of plants to biotic and abiotic stresses. Moderate oxidative stress is of great significance to improve plants’ adaptability to the environment, but excessive oxidative stress can damage plant growth. Antioxidant enzymes in plants can remove reactive oxygen species and protect plants from oxidative stress [35]. Previous studies have shown that exogenous compounds can inhibit the activities of antioxidant enzymes in plants and increase the content of malondialdehyde (MDA), leading to lipid peroxidation [36,37]. Therefore, we investigated the effects of PTZ and PTD enantiomers on the activities of superoxide dismutase (SOD), ascorbate peroxidase (APX) and catalase (CAT) as well as the MDA content, in L. minor. As shown in Figure 3 and Figure S2, there were no significant differences in SOD activity in most cases at a low exposure concentration of 0.05 mg/L. However, the Rac-PTD, S-PTZ and R-PTD enantiomers at high exposure concentrations of 1 mg/L could significantly induce CAT activity. However, the Rac-PTD and S-PTD at the exposure concentration of 1 mg/L could inhibit the activity of the SOD and CAT of L. minor, with inhibition rates of 19.2–33.1% and 45.1–46.9%, respectively. Similarly, the MDA content of L. minor was high in the aforementioned groups. At different exposure concentrations, the Rac-PTZ, Rac-PTD and R-PTD induced APX activity. The R-PTZ and S-PTD at the concentrations of 0.5 and 1 mg/L also induced APX activity. Only the S-PTD at 1 mg/L inhibited the APX activity, with an inhibition rate of 36.1%. Both the S-PTD and the Rac-PTZ induced an increase in MDA content at different exposure concentrations.
The changes in the activities of CAT, SOD and APX suggest that they might play a protective role against the oxidative stress induced by PTZ and its metabolite enantiomers. The response of L. minor was consistent with an excitatory effect, exhibiting a dose-response phenomenon characterized by low-dose stimulation and high-dose inhibition. Plant cells exposed to low doses may accelerate cell division and, thus, increase biomass to dilute the internal concentration of the toxicant, which can be seen as the first sign of perturbation.

4. Conclusions

Aquatic plants, as primary producers, play important roles in aquatic ecosystems, such as oxygen production, nutrient cycling, water quality control and sediment stabilization. However, the pesticide contamination of surface waters poses a considerable danger to aquatic plants. In this study, the stereoselective effects of PTZ and PTD on the aquatic plant L. minor were investigated at the enantiomeric level, which further demonstrated that the degradation of PTZ in water increased its exposure risk. Meanwhile, the acute toxicity of PTZ and PTD enantiomers to L. minor was significantly different. The S-PTZ with high toxicity and environmental persistence inhibited the photosynthetic pigment biosynthesis and antioxidant enzyme activity of the L. minor, leading to lipid peroxidation and death. On the basis of previous reports, it is recommended to use pure R-PTZ instead of Rac-PTZ to reduce the exposure risk of PTZ to the ecosystem and human health.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su142316292/s1, Figure S1: Influences of Rac-PTZ, R-PTZ, S-PTZ, Rac-PTD, R-PTD and S-PTD on the (A) relative dry weight, (B) relative chlorophyll content, (C) relative carotenoid content of L. minor after 7 days of exposure (compared with control). * means significant difference (p < 0.05); Figure S2: Influences of the PTD and PTZ enantiomers on (a) SOD relative activity, (b) APX relative activity, (c) CAT relative activity and (d) MDA relative content of L. minor after 7 days of exposure (compared with control). * means significant difference (p < 0.05).

Author Contributions

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

Funding

This research was funded by the Natural Science Research Project of Higher Education of Anhui, grant number KJ2020A0127.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Growth-inhibition curves of PTZ and PTD enantiomers against L. minor (n = 8).
Figure 1. Growth-inhibition curves of PTZ and PTD enantiomers against L. minor (n = 8).
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Figure 2. Effects of Rac-PTZ, R-PTZ, S-PTZ, Rac-PTD, R-PTD and S-PTD on the (a) dry weight, (b) chlorophyll and (c) carotenoids of L. minor after 7 days of exposure. * means significant difference (p < 0.05).
Figure 2. Effects of Rac-PTZ, R-PTZ, S-PTZ, Rac-PTD, R-PTD and S-PTD on the (a) dry weight, (b) chlorophyll and (c) carotenoids of L. minor after 7 days of exposure. * means significant difference (p < 0.05).
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Figure 3. Influences of the PTD and PTZ enantiomers on (a) SOD, (b) APX and (c) CAT activities and (d) MDA content of L. minor after 7 days of exposure. * means significant difference (p < 0.05).
Figure 3. Influences of the PTD and PTZ enantiomers on (a) SOD, (b) APX and (c) CAT activities and (d) MDA content of L. minor after 7 days of exposure. * means significant difference (p < 0.05).
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Table
Table 1. Enantioselective acute toxicity of PTZ and its metabolite PTD against L. minor.
Table 1. Enantioselective acute toxicity of PTZ and its metabolite PTD against L. minor.
Chemical Compound3 d5 d7 d
R2LC50
(mg/L)		95% CIR2LC50
(mg/L)		95% CIR2LC50
(mg/L)		95% CI
Rac-PTZ0.9910.519.23–11.560.965.635.06–6.450.962.362.07–3.15
R-PTZ0.9820.3618.26–24.320.9712.3210.23–13.580.945.634.68–6.38
S-PTZ0.958.697.21–9.050.934.363.86–5.120.932.061.23–2.98
Rac-PTD0.979.368.23–10.080.953.323.09–4.870.930.980.76–1.18
R-PTD0.9316.5915.69–18.750.929.267.97–10.120.962.232.06–3.56
S-PTD0.947.596.98–8.450.942.571.89–3.450.980.760.62–0.81
CI: Confidence Intervals.
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Yang, Y.; Li, X.; Tang, Q.; Mei, L.; Cao, J.; Huang, H.; Zhang, Z. Aquatic Ecological Risk Evaluation of Chiral Triazole Fungicide Prothioconazole and Its Metabolite Prothioconazole-Desthio on Lemna minor. Sustainability 2022, 14, 16292. https://doi.org/10.3390/su142316292

AMA Style

Yang Y, Li X, Tang Q, Mei L, Cao J, Huang H, Zhang Z. Aquatic Ecological Risk Evaluation of Chiral Triazole Fungicide Prothioconazole and Its Metabolite Prothioconazole-Desthio on Lemna minor. Sustainability. 2022; 14(23):16292. https://doi.org/10.3390/su142316292

Chicago/Turabian Style

Yang, Yaling, Xiaomeng Li, Qiyue Tang, Liangchi Mei, Jian Cao, Haiyun Huang, and Zhaoxian Zhang. 2022. "Aquatic Ecological Risk Evaluation of Chiral Triazole Fungicide Prothioconazole and Its Metabolite Prothioconazole-Desthio on Lemna minor" Sustainability 14, no. 23: 16292. https://doi.org/10.3390/su142316292

APA Style

Yang, Y., Li, X., Tang, Q., Mei, L., Cao, J., Huang, H., & Zhang, Z. (2022). Aquatic Ecological Risk Evaluation of Chiral Triazole Fungicide Prothioconazole and Its Metabolite Prothioconazole-Desthio on Lemna minor. Sustainability, 14(23), 16292. https://doi.org/10.3390/su142316292

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