Phytotoxicity of chiral herbicide bromacil: Enantioselectivity of photosynthesis in Arabidopsis thaliana
Graphical abstract
Introduction
The past four decades have witnessed the rapid increase of herbicides consumption in China and the proportion of all pesticides has climbed from 20% in 1960 to 48% in 2005 (Zhang et al., 2011, Ye et al., 2009a). This rapid increase is a growing threat to the environment due to their toxic effects on plants of nearby area, despite the primary goal is to enhance the crop productivity. As we know, plants are intimately connected with the natural environment, and their growth is strongly dependent on the availability of light. It has been reported that the photosystem II (PSII) herbicides are the most frequently detected at the highest concentrations and the approximately 50% of commercially available herbicides act by inhibiting the chloroplast electron transport chain (Flores et al., 2013, Jones and Kerswell, 2003). Their mode of action is associated with the perturbation of photosynthetic electron flow which affects carbon fixation. Photosynthesis is important for plants and the disturbance to photosystem may occur before obvious inhibition to growth (Chen et al., 2015). The effects of PSII herbicides on photosynthesis reduce primary production, leading to ecosystem deterioration. Therefore, providing regulators and managers for herbicides is necessary to assess the direct effects of PSII herbicides on photosynthesis.
Chiral herbicide family represents about quarter of the pesticide active ingredients and this ratio has been increased by introducing compounds with more complex structures (Garrison, 2006, Wen et al., 2009, Ye et al., 2009b). Previous studies have reported that chiral herbicides displayed enantioselective disturbance to plants though they share the identical physical and chemical properties due to their different interactions with enzymes and biological receptors in organism (Wang et al., 2007, Qian et al., 2015, Wen et al., 2011, Wen et al., 2010). A few studies have demonstrated that chiral herbicides may disturb the photosynthesis of plants in an enantioselective manner (Qian et al., 2013, Zhang et al., 2013), however, the studies of the enantioselective effect of PSII herbicides on photosynthesis are poorly limited (Omokawa and Takahashi, 1994, Huppatz, 1996).
Bromacil (5-bromo-3-sec-butyl-6-methyluracil, BRO) is a broad spectrum herbicide used for nonselective weed and bush control on non-cropland areas, as well as for selective weed control on a limited number of crops, such as citrus fruit and pineapple. It has been reported to interfere with photosynthesis in the PSII of plants (Retzinger and Mallory-Smith, 1997). It was reported that between 55,000 and 117,000 lb of BRO was used on California citrus crops from 1992 to 2001 (Turner and Branch, 2003). In fact, due to the high mobility in soils, BRO has been detected in groundwater wells and aquatic habitats at levels up to 5 μg/L (Alavi et al., 2008, Mena et al., 2014, Spurlock et al., 2000, Wilson and Boman, 2011), which lead both animals and plants exposed to BRO. Considering the carcinogenic potential shown in the inhibition to growth and nutrient uptake of human cell lines (Hurley, 1998, Venkat et al., 1995, Zilkah et al., 1981), BRO is classified as a possible carcinogen by the US Environmental Protection Agency (Pfeuffer and Matson, 2001).
It should be noticed that BRO is also a chiral compound with a pair of enantiomers for the carbon chiral center (Fig. 1A). The toxicity of BRO to plants has been investigated recently (El-Nahhal and Hamdona, 2015, Liu et al., 2013). But, unfortunately, BRO was studied as race mate and no information is available on the enantioselective toxicity of BRO to plants. In this study, we selected Arabidopsis thaliana as model plants, to learn about the potential enantioselective effect of BRO on plants in terms of photosynthesis and photosynthetic pigment levels, chlorophyll fluorescence parameters and some genes expression of proteins in PSI and PSII were measured. The aim of this study was to detect the effect of BRO on photosystem at enantiomer level and to provide a new sight to evaluate the phytotoxicity of chiral herbicides.
Section snippets
Chiral separation of BRO
Racemate BRO (97% purity) was provided by the Kangbaotai Fine Chemical Company (Wuhan, China). Chiral separation of BRO enantiomers was performed on Waters-2535 series HPLC systems with chiral column (Lux 5u Cellulose-1, 250 × 4.60 mm) purchased from Phenomenex Company (Torrance, CA, USA). The composition of mobile phase was 9:1 of hexane/isopropanol with a flow rate of 0.5 mL/min. 5 μL sample was injected every time for analysis and the temperature of column was 30 °C. Other solvents used in this
Chiral separation and absolute configuration of BRO enantiomers determination
As shown in Fig. 1A, BRO, one of substituted uracil and widely used herbicides, has two enantiomers because of its chiral carbon atom. Unfortunately, there is no report about the chiral separation of BRO so far. Considering the fact that the biological effects (e.g., toxicity, mutagenicity, carcinogenicity and endocrine-disrupting activity) of enantiomers are typically enantioselective (Li et al., 2008), we first performed the chiral separation of BRO by Waters-2535 series HPLC systems with
Acknowledgment
This study was supported by the National Natural Science Foundation of China (No. 21377111) and National High Technology Research and Development Program of China (No. 2013AA065202).
References (54)
- et al.
Movement of bromacil in a Hawaii soil under pineapple cultivation—a field study
Chemosphere
(2008) - et al.
Changes of soluble protein expression and leaf metabolite levels in Arabidopsis thaliana grown in elevated atmospheric carbon dioxide
Field Crop Res.
(2004) - et al.
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence
Biochimica et Biophysica Acta (BBA)-General Subjects
(1989) - et al.
The function of 33-kDa protein in the photosynthetic oxygen–evolution system studied by reconstitution experiments
Biochimica et Biophysica Acta (BBA)-Bioenergetics
(1985) Parameters of photosynthetic energy partitioning
J. Plant Physiol.
(2015)- et al.
Combined toxicity of pesticide mixtures on green algae and photobacteria
Ecotoxicol. Environ. Saf.
(2013) - et al.
Growth inhibition and effect on photosystem by three imidazolium chloride ionic liquids in rice seedlings
J. Hazard. Mater.
(2015) - et al.
Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method
Methods
(2001) - et al.
Adaptation to salinity as monitored by PSII oxygen evolving reactions in barley thylakoids
J. Plant Physiol.
(1993) - et al.
Reverse chiral discrimination relationships between the inhibitory activity of 1,3,5-triazines on photosystem II and light-independent root growth
Pestic. Biochem. Physiol.
(1994)
Characterization of selected organo-nitrogen herbicides in south Florida canals: exposure and risk assessments
Sci. Total Environ.
Antioxidant defense system responses and DNA damage of earthworms exposed to perfluorooctane sulfonate (PFOS)
Environ. Pollut.
Enantioselective separation and analysis of chiral pesticides by high-performance liquid chromatorgraphy
Trends Anal. Chem.
Stereoselective phytotoxicity of HCH mediated by photosynthetic and antioxidant defense systems in Arabidopsis thaliana
PloS One
Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins
Planta
Growth and photosynthetic responses of ectomycorrhizal pine seedlings exposed to elevated Cu in soils
Mycorrhiza
Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis
P. Natl. Acad. Sci. USA
Phytotoxicity of alachlor, bromacil and diuron as single or mixed herbicides applied to wheat, melon, and molokhia
SpringerPlus
Phytotoxicity of four photosystem II herbicides to tropical seagrasses
PLoS One
Probing the enantioselectivity of chiral pesticides
Environ. Sci. Technol.
Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94
J. Comput. Chem.
Quantifying the inhibitor-target site interactions of photosystem II herbicides
Weed Sci.
Mode of carcinogenic action of pesticides inducing thyroid follicular cell tumors in rodents
Environ. Health Perspect.
Analysis of chiral pharmaceuticals using HPLC with CD detection
Chirality
The dissipation of excess excitation energy in British plant species
Plant Cell Environ.
Phytotoxicity of photosystem II (PSII) herbicides to coral
Mar. Ecol. Prog. Ser.
Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants
Plant Physiol.
Cited by (21)
Research on phytotoxicity assessment and photosynthetic characteristics of nicosulfuron residues on Beta vulgaris L
2024, Journal of Environmental ManagementThe fate, acute, and subchronic risks of dinotefuran in the water-sediment system: A systematic analysis at the enantiomer level
2023, Journal of Hazardous MaterialsEnantioselectivity in the toxicological effects of chiral pesticides: A review
2023, Science of the Total EnvironmentCitation Excerpt :It is worth noting that BRO is also a chiral compound which consists of a pair of enantiomers (Chen et al., 2016b). Experiments showed that enantioselective phytotoxicity of BRO to A. thaliana could be attributed to the difference in the inhibition on photosynthesis processes, including the electron transmission in photosystem I and transcriptional levels of photosynthesis related genes (Chen et al., 2016b). Ethofumesate (ETO) is a chiral post-emergence herbicide applied on specific grasses and broad-leaf weeds (Perovani et al., 2021).
PWC-based evaluation of groundwater pesticide pollution in the Júcar River Basin
2022, Science of the Total EnvironmentEnantioselective effects of the fungicide metconazole on photosynthetic activity in Microcystis flos-aquae
2021, Ecotoxicology and Environmental SafetyCitation Excerpt :Other trans-1R,5R-MEZ treatments were not significantly different from the control on day 8 (p > 0.05). Photosynthetic pigments are the basis for plant photosynthesis, and changes in their content can reflect the growth status of plants (Chen et al., 2016). Chl a plays a crucial role in light capture, energy transfer and light conversion into chemical energy, while carotenoids protect the production of chlorophyll and absorption of light energy (Wang et al., 2020a).
Stress responses and biological residues of sulfanilamide antibiotics in Arabidopsis thaliana
2020, Ecotoxicology and Environmental Safety