Phytotoxicity of chiral herbicide bromacil: Enantioselectivity of photosynthesis in Arabidopsis thaliana

https://doi.org/10.1016/j.scitotenv.2016.01.046Get rights and content

Highlights

  • It is necessary to assess the direct effects of PSII herbicides on photosynthesis.

  • Phytotoxicity of bromacil is investigated in an enantiomeric level.

  • Bromacil disturbed enantioselectively the photosystem II of Arabidopsis thaliana.

  • S-bromacil caused severer damage to photosynthesis of Arabidopsis than R-bromacil.

  • Photosynthesis should be considered for phytotoxicity assessment of herbicides.

Abstract

With the wide application of chiral herbicides and the frequent detection of photosystem II (PSII) herbicides, it is of great importance to assess the direct effects of PSII herbicides on photosynthesis in an enantiomeric level. In the present study, the enantioselective phytotoxicity of bromacil (BRO), typical photosynthesis inhibition herbicide, on Arabidopsis thaliana was investigated. The results showed that S-BRO exhibited a greater inhibition of electron transmission in photosystem I (PSI) of A. thaliana than R-BRO by inhibiting the transcription of fnr 1. S-BRO also changed the chlorophyll fluorescence parameters Y (II), Y (NO), and Y (NPQ) to a greater extent than R-Bro. Transcription of genes psbO2, Lhcb3 and Lhcb6 was down-regulated in an enantioselective rhythm and S-BRO caused more serious influence, indicating that S-BRO did worse damage to the photosystem II (PSII) of A. thaliana than R-BRO. This study suggested that S-BRO disturbed the photosynthesis of plants to a larger extent than R-BRO and provided a new sight to evaluate the phytotoxicity of chiral herbicides.

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).

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