Elsevier

Environmental Pollution

Volume 285, 15 September 2021, 117246
Environmental Pollution

Perfluorooctanoic acid (PFOA) changes nutritional compositions in lettuce (Lactuca sativa) leaves by activating oxidative stress

https://doi.org/10.1016/j.envpol.2021.117246Get rights and content

Highlights

  • PFOA changes nutritional compositions in lettuce leaves.

  • Non-enzymatic and enzymatic antioxidants were employed to cope with PFOA in leaves.

  • Transpiration, stomatal conductance and leaf net photosynthetic rate were changed.

  • Global detoxifying mechanism to PFOA in lettuce leaves was proposed.

Abstract

Perfluorooctanoic acid (PFOA) is a typical persistent organic pollutant commonly detected in ecosystem. Insights into the risks of PFOA in crops, from the perspectives of food nutritional compositions, are sparse. In this study, the physiological responses to PFOA induced oxidative stress were investigated in lettuce (Lactuca sativa) leaves hydroponically exposed to 5 and 50 μg/L PFOA. The effects on photosynthesis and nutritional compositions were characterized. 35.1 and 316.7 ng/g dry weight PFOA were bio-accumulated in lettuce leaves under exposure to 5 and 50 μg/L PFOA, respectively. PFOA led to exposure-dependent over-generation of reactive oxidative species (ROS; H2O2, 8.1%–38.7%; radical dotOH, 11.3%–26.4%; radical dotO2, 3.1%–22.8%) in leaves. Both non-enzymatic and enzymatic antioxidants were activated to scavenge ROS. Nevertheless, metabolomics results indicated some nutritional compositions in lettuce leaves were elevated by environmentally relevant concentrations of PFOA. Both primary metabolites, such as carbohydrates in the tricarboxylic acid cycle and amino acids, and secondary metabolites, such as bioactive (poly)phenol and alkaloid compounds, were significantly up-regulated. Leaf net photosynthetic rates were stimulated and intercellular CO2 concentration was decreased. A thorough scheme on the interaction between PFOA and lettuce leaves was proposed as well, to enhance the understanding of PFOA risks in crops.

Introduction

Chemical contamination in agricultural environment is a non-ignorable factor affecting food production in current era (Ramón and Lull, 2019). Perfluorooctanoic acid (PFOA) is a synthetic, highly stable perfluoroalkyl substances used in manufacturing industrial and household products, from water resistant coatings for carpets and fabrics to fast food contact materials, fire-resistant foams, paints, and hydraulic fluids (Giesy and kannan, 2002). Due to the long-time application, a large amount of PFOA has been released into environment (Xiang et al., 2020). With the increase of global urbanization, especially in developing countries, PFOA contamination in agricultural environment is getting worse (Yuan et al., 2018; Li et al., 2019; Wu et al., 2020).

Widespread occurrence of PFOA in agricultural environments causes its bioaccumulation in crops globally (Jian et al., 2017; Sunderland et al., 2019; Menger et al., 2020). PFOA was detected at shocking levels in crops in fields using contaminated water for irrigation or sewage sludge as soil conditioner (Blaine et al., 2014; Jian et al., 2017; Li et al., 2019; Liu et al., 2019). For instance, PFOA was measured at 298 ng/g dry weight (dw) in the leaves of lettuce (Lactuca sativa ‘Multy’) irrigated with reclaimed water containing 5.83 μg PFOA/L. (Blaine et al., 2014). In wheat (Triticum aestivum L.) grown in biosolid-amended soils, PFOA was measured at 34.6, 15.9, 2.6 and 3.3 ng/g dw in root, straw, husk and grain, respectively (Wen et al., 2014). PFOA has been a common abiotic stress encountered by agriculture worldwide (Li et al., 2020a).

Over-generations of reactive oxygen species (ROS) and resulting oxidative stress in crops are common outcomes under contaminated circumstances, which constitutes a primary cause of crop loss and nutritional impairment worldwide (Zhao et al., 2020). However, a recent study reported that maintaining a basal level of ROS, between cytostatic and cytotoxic level, enables proper redox biological reactions and the regulation of numerous processes essential for cells (Mittler, 2017). Previous studies reported that low levels of PFOA exposure increased the growth rate and biomass of crops, albeit high levels of PFOA exposure inhibited the crop growth (Sharma et al., 2020; Yang et al., 2015; Zhou et al., 2016). For example, Zhou et al. (2016) reported low PFOA exposure (<0.2 mg kg−1) contributed the seedling growth and root length of wheat (Triticum aestivum L.). However, the underlying mechanisms of PFOA stimulated growth, especially from the physiological and metabolic perspectives, is unclear so far.

In this study, lettuce (Lactuca sativa) was cultivated in hydroponic media spiked with PFOA at 5 and 50 μg/L for 10 days. The over-generation of ROS, oxidative damages and antioxidative defenses were systematically determined in lettuce leaves to reveal the underlying rationales for the alterations of nutritional compositions by PFOA exposure. The alterations of both primary and secondary metabolites in lettuce leaves were tracked using liquid chromatography mass spectrometry (LC-MS) based metabolomics profiling. The photosynthesis process was characterized by gas exchange, chlorophyll fluorescence and photosynthetic pigments.

Section snippets

Chemicals

Calibration standards for PFOA quantification and spiking PFOA (98.5%) in exposure assay were purchased from Wellington Laboratories (Guelph, Ontario, Canada) and Dr. Ehrenstorfer (Augsburg, Bavaria, Germany), respectively. Assay kits were purchased from Nanjing Jiancheng Bioengineer Ins (Nanjing, China).

Plant cultivation and exposure

The strategies for germination and growth of lettuce (Lactuca sativa) were described in a previous study (Li et al., 2020b). Hydroponic media was adopted to supply nutrition for lettuces,

PFOA bioaccumulation and lettuce growth

The amounts of PFOA bioaccumulation in lettuce leaves were 35.1 and 316.7 ng/g dw under the exposure levels of 5 and 50 μg/L PFOA, respectively (Fig. 1a). Leaf biomass (Fig. S1) showed no significant difference between two treatment groups and the control group. The amounts of PFOA bioaccumulation in the present study (Fig. 1a) were agreement to the values previously reported in crops grown in polluted regions. PFOA bioaccumulations up to 20–195 ng/g dw were found in vegetables (lettuce,

Conclusions

In this study, the alterations in nutritional compositions in lettuce under PFOA stress were investigated by monitoring oxidative stress, photosynthesis and metabolisms. Under the exposure to PFOA at environmentally relevant levels, the intermediates in amino acid, TCA cycle, (poly)phenol and alkaloid metabolisms in lettuce leaves were up-regulated. H2O2, radical dotOH and radical dotO2 were overexpressed by PFOA in a dose-dependent manner. Although non-enzymatic and enzymatic antioxidants were activated in leaves,

CRediT author statement

Pengyang Li: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Visualization, Writing - original draft. Zhiyong Xiao: Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision. Xiaocan Xie: Data curation, Investigation, Resources. Zhifang Li: Investigation, Resources. Hongju Yang: Investigation; Xiao Ma: Investigation; Jiang Sun: Funding acquisition, Project administration, Resources, Supervision. Jiuyi Li: Project

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We sincerely thank Professor Lijuan Zhao of State Key Laboratory of Pollution Control and Resource Reuse, Nanjing University for suggestions of experiment design. This study was supported by the National Natural Science Foundation of China (51978037), the Fundamental Research Funds for the Central Universities (2020YJS135), Beijing Agricultural Science and Technology Project (PXM 2021-036207-000005) and Beijing Municipal Finance Project for Beijing Academy of Science and Technology (PXM

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