Environ Sci Pollut Res DOI 10.1007/s11356-015-5003-8
RESEARCH ARTICLE
Effects of bisphenol A on chlorophyll fluorescence in five plants Jiazhi Zhang 1 & Lihong Wang 1 & Man Li 1 & Liya Jiao 1 & Qing Zhou 1 & Xiaohua Huang 2
Received: 16 April 2015 / Accepted: 30 June 2015 # Springer-Verlag Berlin Heidelberg 2015
Abstract The aim of this study was to evaluate the effects of bisphenol A (BPA) on plant photosynthesis and determine whether the photosynthetic response to BPA exposure varies in different plants. Chlorophyll fluorescence techniques were used to investigate the effects of BPA on chlorophyll fluorescence parameters in tomato (Lycopersicum esculentum), lettuce (Lactuca sativa), soybean (Glycine max), maize (Zea mays), and rice (Oryza sativa) seedlings. Low-dose (1.5 or 3.0 mg L−1) BPA exposure improved photosystem II efficiency, increased the absorption and conversion efficiency of primary light energy, and accelerated photosynthetic electron transport in each plant, all of which increased photosynthesis. These effects weakened or disappeared after the withdrawal of BPA. High-dose (10.0 mg L−1) BPA exposure damaged the photosystem II reaction center, inhibited the photochemical reaction, and caused excess energy to be released as heat. These effects were more evident after the highest BPA dose (17.2 mg L−1), but they weakened after the withdrawal of BPA. The magnitude of BPA exposure effects on the chlorophyll fluorescence parameters in the five plants followed the Responsible editor: Philippe Garrigues * Qing Zhou [email protected] * Xiaohua Huang [email protected] 1
State Key Laboratory of Food Science and Technology, Jiangsu Coorperative Innovation Center of Water Treatment Technology and Materials, College of Environment and Civil Engineering, Jiangnan University, Wuxi 214122, China
2
Jiangsu Collaborative Innovation Center of Biomedical Functional Materials, Jiangsu Key Laboratory of Biomedical Materials, College of Chemistry and Materials Science, Nanjing Normal University, Nanjing 210046, China
order: lettuce > tomato > soybean > maize > rice. The opposite order was observed following the removal of BPA. In conclusion, the chlorophyll fluorescence response in plants exposed to BPA depended on BPA dose and plant species. Keywords Bisphenol A . Photosynthetic parameters . Chlorophyll fluorescence . Effects . Five plants
Introduction Bisphenol A [BPA; 2,2-bis (4-hydroxyphenyl) propane] is an important raw material for synthetic resin, polycarbonate plastics, and other industrial products. It has been widely used in the production of infant feeding bottles, paper coating, food and beverage packaging, dental sealants, flame retardants, adhesives, and water pipes (Staples et al. 1998). Global annual BPA production has been reported to be about 6.8 million tons, and the demand for BPA has been increasing rapidly, especially in developing countries (Jandegian et al. 2015). Thus, more and more BPA is being discharged into the environment (Vandenberg et al. 2009). Its potential environmental risk has meant that BPA has attracted more research attention over the past few years (Ferrara et al. 2006). It has also been reported that the concentration of BPA in landfill leachate is up to 17.2 mg L−1 (Yamamoto et al. 2001), which is far beyond the maximum acceptable concentration (1.5 mg L−1) for BPA in drinking water established by the US Environmental Protection Agency (Geens et al. 2011). This means that BPA concentration is potentially a threat to human health and environmental safety (Lim et al. 2009a, b). Previous studies regarding the effects of BPA on plants mainly focused on plant growth (Speranza et al. 2011; Dogan et al. 2012; Adamakis et al. 2013; Qiu et al. 2013; Sun et al. 2013a, b). For example, it was found that
Environ Sci Pollut Res
1.5 mg L−1 BPA improved soybean seedling root and leaf growth, whereas 17.2 and 50.0 mg L−1 BPA inhibited growth (Qiu et al. 2013; Sun et al. 2013a, b). Moreover, 10.0 and 100.0 mg L−1 BPA reduced pea (Pisum sativum) seedling taproot length by 8 % and more than 92 %, respectively (Adamakis et al. 2013). In addition, 10.0 mg L−1 BPA did not affect wheat seed germination and root growth, whereas 50.0 mg L−1 BPA did inhibit seed germination and root growth (Dogan et al. 2012). However, 10.0 mg L−1 BPA could inhibit the occurrence and elongation of the kiwifruit pollen tube, which resulted in deformed pollen tubes (Speranza et al. 2011). However, only a few reports have been published so far about the possible mechanism underlying the BPA effects on plant growth (Qiu et al. 2013). Recently, we found that the effects of BPA on soybean seedling growth were associated with photosynthesis in the leaves and mineral nutrients in the roots (Qiu et al. 2013; Sun et al. 2013a, b; Hu et al. 2014; Nie et al. 2015). Photosynthesis converts light energy into chemical energy in plants, and thus, it plays an important role in plant growth and yields (Ambavaram et al. 2014). Photosynthesis involves a number of physiological processes in plants that capture light energy, induce photochemical reactions, and synthesize organic compounds (Demmig-Adams and Adams 2002). As a good natural probe, chlorophyll fluorescence can be used to obtain a large amount of information about photosynthesis, and therefore, it can be used to analyze the photosynthetic mechanisms in plants (Hu et al. 2014). Under abiotic stress, energy dissipation in plants through chlorophyll fluorescence emission is six times larger than under normal conditions (Rambo et al. 2010). Therefore, the chlorophyll fluorescence technique is also commonly used to analyze the impacts of heavy metals (Dai et al. 2012), herbicides (Gorbe and Calatayud 2012), air pollution (Liu et al. 2007), rare earth elements (Xie et al. 2013), and other abiotic stresses on photosynthesis in plants. Our recent studies revealed that the toxic effects of BPA on soybean seedlings were related to changes in photosynthesis and chlorophyll fluorescence parameters (Qiu et al. 2013; Hu et al. 2014). However, it is not known whether the effects of BPA on plant photosynthesis are the same for all plants or whether the effects vary depending on plant species. In this study, the effects of BPA on the chlorophyll fluorescence reaction in three kinds of global economic crops (rice, soybean, and maize) (Neumann et al. 2010; Zhao et al. 2015) and two kinds of global most consumed vegetables (lettuce and tomato) (Mamatha et al. 2014; Freitas et al. 2015) seedlings were investigated using chlorophyll fluorescence technology. In these selected crops, tomato, lettuce, soybean, and rice are four representative C3 plants (Huang et al. 2006; He et al. 2007; Mamatha et al. 2014), and maize is a typical C4 plant (Bellasio and Griffiths 2014). Our study provides new information that could be used to evaluate the ecological safety of BPA in the environment.
Materials and methods Preparation of BPA solution Based on our previous report (Nie et al. 2015), five doses of BPA solutions (1.5, 3.0, 6.0, 10.0, and 17.2 mg L−1) were prepared. Plant culture and BPA exposure Tomato (Lycopersicum esculentum, Zhongza 9), lettuce (Lactuca sativa, April Man), soybean (Glycine max, Zhonghuang 25), maize (Zea mays, selected white maize), and rice (Oryza sativa, Huaidao 8) seeds were disinfected in 0.1 % HgCl2 solution for 10 min and then rinsed three times with deionized water. The disinfected seeds were placed in a dish covered with three layers of gauze and germinated in an incubator (25±1 °C) with a 12/12-h light/dark ratio. After 1 week, 15 seedlings of each plant type were transplanted into a plastic container (320×215×100 mm) filled with deionized water to avoid microbial pollution based on our preliminary experiments. Preliminary experiments also showed that under this condition, these plants did not show nutrient deficiencies because their seeds might have abundant nutrients (Zienkiewicz et al. 2011). The deionized water was renewed once a day. Two weeks after germination, the seedlings were cultured in one-half strength Hoagland’s solution (pH 7.0) in the greenhouse with a 300 μmol m−2 s−1 photosynthetic photon flux density, at 30/25 °C day/night temperature and with a 12/12-h light/dark ratio. The nutrient solution was renewed every day and aerated two times daily with an electric air pump. Thirty days after germination, the seedlings were transplanted into one of the prepared BPA solutions (1.5, 3.0, 6.0, 10.0, or 17.2 mg L−1). The control plants were cultured in one-half strength Hoagland nutrient solution (pH 7.0) without BPA. The BPA solution and the nutrient solution were renewed every 3 days. The seedlings were exposed to BPA solution for 7 days and then were moved to one-half strength Hoagland solution (pH 7.0) without BPA for 7 days. After 7 days of BPA exposure, followed by 7 days without BPA exposure (BPA withdrawal), the leaves were collected and the chlorophyll fluorescence parameters were measured. Determination of chlorophyll fluorescence parameters Chlorophyll fluorescence parameters of the five plants were measured by pulse-modulated (PAM-210) fluorometer (Walz GmbH, Germany). The determination procedures were performed as described by Guidi et al. (2007). The leaves were first dark-adapted for 30 min; then, the initial fluorescence (F0) was measured after irradiating detective light (710 nm) and determined the minimal fluorescence in the light-adapted state (F’0) under a background of far infrared light for 10 s. Moreover, the steady-state level of fluorescence (Fs) was calculated by Ft–F’0 (where Ft is the instant fluorescence yield), about 20 min after converting to the next higher light level. Photochemical quenching parameter (qP), nonphotochemical quenching parameter (qN), and electron transport rate (ETR) were calculated automatically based on the above known parameters. Statistical analysis All treatment groups were repeated for six times, and all data for the three independent experiments of the mean value± standard error (mean ± SD). The significant differences (p
RESEARCH ARTICLE
Effects of bisphenol A on chlorophyll fluorescence in five plants Jiazhi Zhang 1 & Lihong Wang 1 & Man Li 1 & Liya Jiao 1 & Qing Zhou 1 & Xiaohua Huang 2
Received: 16 April 2015 / Accepted: 30 June 2015 # Springer-Verlag Berlin Heidelberg 2015
Abstract The aim of this study was to evaluate the effects of bisphenol A (BPA) on plant photosynthesis and determine whether the photosynthetic response to BPA exposure varies in different plants. Chlorophyll fluorescence techniques were used to investigate the effects of BPA on chlorophyll fluorescence parameters in tomato (Lycopersicum esculentum), lettuce (Lactuca sativa), soybean (Glycine max), maize (Zea mays), and rice (Oryza sativa) seedlings. Low-dose (1.5 or 3.0 mg L−1) BPA exposure improved photosystem II efficiency, increased the absorption and conversion efficiency of primary light energy, and accelerated photosynthetic electron transport in each plant, all of which increased photosynthesis. These effects weakened or disappeared after the withdrawal of BPA. High-dose (10.0 mg L−1) BPA exposure damaged the photosystem II reaction center, inhibited the photochemical reaction, and caused excess energy to be released as heat. These effects were more evident after the highest BPA dose (17.2 mg L−1), but they weakened after the withdrawal of BPA. The magnitude of BPA exposure effects on the chlorophyll fluorescence parameters in the five plants followed the Responsible editor: Philippe Garrigues * Qing Zhou [email protected] * Xiaohua Huang [email protected] 1
State Key Laboratory of Food Science and Technology, Jiangsu Coorperative Innovation Center of Water Treatment Technology and Materials, College of Environment and Civil Engineering, Jiangnan University, Wuxi 214122, China
2
Jiangsu Collaborative Innovation Center of Biomedical Functional Materials, Jiangsu Key Laboratory of Biomedical Materials, College of Chemistry and Materials Science, Nanjing Normal University, Nanjing 210046, China
order: lettuce > tomato > soybean > maize > rice. The opposite order was observed following the removal of BPA. In conclusion, the chlorophyll fluorescence response in plants exposed to BPA depended on BPA dose and plant species. Keywords Bisphenol A . Photosynthetic parameters . Chlorophyll fluorescence . Effects . Five plants
Introduction Bisphenol A [BPA; 2,2-bis (4-hydroxyphenyl) propane] is an important raw material for synthetic resin, polycarbonate plastics, and other industrial products. It has been widely used in the production of infant feeding bottles, paper coating, food and beverage packaging, dental sealants, flame retardants, adhesives, and water pipes (Staples et al. 1998). Global annual BPA production has been reported to be about 6.8 million tons, and the demand for BPA has been increasing rapidly, especially in developing countries (Jandegian et al. 2015). Thus, more and more BPA is being discharged into the environment (Vandenberg et al. 2009). Its potential environmental risk has meant that BPA has attracted more research attention over the past few years (Ferrara et al. 2006). It has also been reported that the concentration of BPA in landfill leachate is up to 17.2 mg L−1 (Yamamoto et al. 2001), which is far beyond the maximum acceptable concentration (1.5 mg L−1) for BPA in drinking water established by the US Environmental Protection Agency (Geens et al. 2011). This means that BPA concentration is potentially a threat to human health and environmental safety (Lim et al. 2009a, b). Previous studies regarding the effects of BPA on plants mainly focused on plant growth (Speranza et al. 2011; Dogan et al. 2012; Adamakis et al. 2013; Qiu et al. 2013; Sun et al. 2013a, b). For example, it was found that
Environ Sci Pollut Res
1.5 mg L−1 BPA improved soybean seedling root and leaf growth, whereas 17.2 and 50.0 mg L−1 BPA inhibited growth (Qiu et al. 2013; Sun et al. 2013a, b). Moreover, 10.0 and 100.0 mg L−1 BPA reduced pea (Pisum sativum) seedling taproot length by 8 % and more than 92 %, respectively (Adamakis et al. 2013). In addition, 10.0 mg L−1 BPA did not affect wheat seed germination and root growth, whereas 50.0 mg L−1 BPA did inhibit seed germination and root growth (Dogan et al. 2012). However, 10.0 mg L−1 BPA could inhibit the occurrence and elongation of the kiwifruit pollen tube, which resulted in deformed pollen tubes (Speranza et al. 2011). However, only a few reports have been published so far about the possible mechanism underlying the BPA effects on plant growth (Qiu et al. 2013). Recently, we found that the effects of BPA on soybean seedling growth were associated with photosynthesis in the leaves and mineral nutrients in the roots (Qiu et al. 2013; Sun et al. 2013a, b; Hu et al. 2014; Nie et al. 2015). Photosynthesis converts light energy into chemical energy in plants, and thus, it plays an important role in plant growth and yields (Ambavaram et al. 2014). Photosynthesis involves a number of physiological processes in plants that capture light energy, induce photochemical reactions, and synthesize organic compounds (Demmig-Adams and Adams 2002). As a good natural probe, chlorophyll fluorescence can be used to obtain a large amount of information about photosynthesis, and therefore, it can be used to analyze the photosynthetic mechanisms in plants (Hu et al. 2014). Under abiotic stress, energy dissipation in plants through chlorophyll fluorescence emission is six times larger than under normal conditions (Rambo et al. 2010). Therefore, the chlorophyll fluorescence technique is also commonly used to analyze the impacts of heavy metals (Dai et al. 2012), herbicides (Gorbe and Calatayud 2012), air pollution (Liu et al. 2007), rare earth elements (Xie et al. 2013), and other abiotic stresses on photosynthesis in plants. Our recent studies revealed that the toxic effects of BPA on soybean seedlings were related to changes in photosynthesis and chlorophyll fluorescence parameters (Qiu et al. 2013; Hu et al. 2014). However, it is not known whether the effects of BPA on plant photosynthesis are the same for all plants or whether the effects vary depending on plant species. In this study, the effects of BPA on the chlorophyll fluorescence reaction in three kinds of global economic crops (rice, soybean, and maize) (Neumann et al. 2010; Zhao et al. 2015) and two kinds of global most consumed vegetables (lettuce and tomato) (Mamatha et al. 2014; Freitas et al. 2015) seedlings were investigated using chlorophyll fluorescence technology. In these selected crops, tomato, lettuce, soybean, and rice are four representative C3 plants (Huang et al. 2006; He et al. 2007; Mamatha et al. 2014), and maize is a typical C4 plant (Bellasio and Griffiths 2014). Our study provides new information that could be used to evaluate the ecological safety of BPA in the environment.
Materials and methods Preparation of BPA solution Based on our previous report (Nie et al. 2015), five doses of BPA solutions (1.5, 3.0, 6.0, 10.0, and 17.2 mg L−1) were prepared. Plant culture and BPA exposure Tomato (Lycopersicum esculentum, Zhongza 9), lettuce (Lactuca sativa, April Man), soybean (Glycine max, Zhonghuang 25), maize (Zea mays, selected white maize), and rice (Oryza sativa, Huaidao 8) seeds were disinfected in 0.1 % HgCl2 solution for 10 min and then rinsed three times with deionized water. The disinfected seeds were placed in a dish covered with three layers of gauze and germinated in an incubator (25±1 °C) with a 12/12-h light/dark ratio. After 1 week, 15 seedlings of each plant type were transplanted into a plastic container (320×215×100 mm) filled with deionized water to avoid microbial pollution based on our preliminary experiments. Preliminary experiments also showed that under this condition, these plants did not show nutrient deficiencies because their seeds might have abundant nutrients (Zienkiewicz et al. 2011). The deionized water was renewed once a day. Two weeks after germination, the seedlings were cultured in one-half strength Hoagland’s solution (pH 7.0) in the greenhouse with a 300 μmol m−2 s−1 photosynthetic photon flux density, at 30/25 °C day/night temperature and with a 12/12-h light/dark ratio. The nutrient solution was renewed every day and aerated two times daily with an electric air pump. Thirty days after germination, the seedlings were transplanted into one of the prepared BPA solutions (1.5, 3.0, 6.0, 10.0, or 17.2 mg L−1). The control plants were cultured in one-half strength Hoagland nutrient solution (pH 7.0) without BPA. The BPA solution and the nutrient solution were renewed every 3 days. The seedlings were exposed to BPA solution for 7 days and then were moved to one-half strength Hoagland solution (pH 7.0) without BPA for 7 days. After 7 days of BPA exposure, followed by 7 days without BPA exposure (BPA withdrawal), the leaves were collected and the chlorophyll fluorescence parameters were measured. Determination of chlorophyll fluorescence parameters Chlorophyll fluorescence parameters of the five plants were measured by pulse-modulated (PAM-210) fluorometer (Walz GmbH, Germany). The determination procedures were performed as described by Guidi et al. (2007). The leaves were first dark-adapted for 30 min; then, the initial fluorescence (F0) was measured after irradiating detective light (710 nm) and determined the minimal fluorescence in the light-adapted state (F’0) under a background of far infrared light for 10 s. Moreover, the steady-state level of fluorescence (Fs) was calculated by Ft–F’0 (where Ft is the instant fluorescence yield), about 20 min after converting to the next higher light level. Photochemical quenching parameter (qP), nonphotochemical quenching parameter (qN), and electron transport rate (ETR) were calculated automatically based on the above known parameters. Statistical analysis All treatment groups were repeated for six times, and all data for the three independent experiments of the mean value± standard error (mean ± SD). The significant differences (p
