Uptake mechanisms of perfluoroalkyl acids with different carbon chain lengths (C2-C8) by wheat (Triticum acstivnm L.)

Highlights

• Uptake and translocation of PFAAs in wheat depended on their carbon chain length.

• Higher uptake of C2, C3, and C8 PFAAs by wheat roots was observed compared to C4 and C6.

• Accumulation of PFCAs in wheat shoots decreased with their carbon chain length.

• The energy-dependent active process was the main mechanism for the uptake of PFAAs.

• Aquaporins and anion channels also contributed to the uptake of C2 and C3 PFCAs.

Abstract

Organic compounds could be taken up by plants via different pathways, depending on chemical properties and biological species, which is important for the risk assessment and risk control. To investigate the transport pathways of perfluoroalkyl acids (PFAAs) by wheat (Triticum acstivnm L.), the uptake of five perfluoroalkyl carboxylic acids (PFCAs): TFA (C2), PFPrA (C3), PFBA (C4), PFHxA (C6), PFOA (C8), and a perfluoroalkyl sulfonic acid: PFOS (C8)) were studied using hydroponic experiments. Various inhibitors including a metabolic inhibitor (Na₃VO₄), two anion channel blockers (9-AC, DIDS), and two aquaporin inhibitors (AgNO₃, glycerol) were examined. The wheat root and shoot showed different concentration trends with the carbon chain length of PFAAs. The uptake of TFA was inhibited by Na₃VO₄ and 9-AC whereas PFPrA was inhibited by Na₃VO₄, AgNO₃ and 9-AC. For the other four PFAAs, only Na₃VO₄ was effective. These results together with the result of concentration-dependent uptake, which followed the Michaelis-Menten model, indicate that the uptake of PFAAs by wheat is mainly an energy-dependent active process mediated by carriers. For the ultra-short chain PFCAs (C2 and C3), aquaporins and anion channels may also be involved. A competition between TFA and PFPrA was determined during the plant uptake but no competition was observed between these two shorter chain analogues with other analogues, neither between PFBA and PFHxA, PFBA and PFBS, PFOA and PFOS.

Introduction

Perfluoroalkyl acids (PFAAs) including perfluoroalkyl carboxylic acids (PFCAs) and perfluoroalkyl sulfonic acids (PFSAs) are a class of emerging persistent organic pollutants in the environment that have attracted wide attention as global contaminants (Lorenzo et al., 2019; Wang et al., 2018). These substances and mainly their precursors such as fluorotelomers, polyfluoroalkyl phosphates and sulfonamide derivatives have been widely applied in industrial and commercial products due to their unique physical and chemical properties such as chemical, thermal stability and surface activity (Kannan, 2011; Lau, 2012). Once entering the environment, the precursors are transformed to PFAAs (Plumlee et al., 2009; Yin et al., 2018; Blanco et al., 2010). However, PFAAs are highly persistent and can undergo long-distance transport (Scheringer, 2009), and hence, they have been ubiquitously detected in various environmental compartments at high concentrations (Yin et al., 2017; Houde et al., 2006; Venkatesan & Halden, 2013; Shan et al., 2015; Zhao et al., 2017). Due to the feature of persistent organic pollutants (POPs), long chain (≥C8) PFAAs and their precursors have been gradually restricted since 21th century and substituted by short-chain analogues (C4 and C6) (Wang et al., 2015). Consequently, the concentrations of these short-chain PFAAs have been increasing gradually (Li et al., 2018) and their fate has drawn much more attention.

The studies on PFAAs usually do not include the ultra-short chain (C2 and C3) PFCAs, i.e. trifluoroacetic acid (TFA) and perfluoropropionic acid (PFPrA) due to their different origin. TFA and PFPrA's concentrations were in high levels and have been increasing gradually due to the phototransformation of novel refrigerants such as HFC-134a (1,1,1,2-tetrafluoro-ethane) (Wallington et al., 1994; Kanakidou et al., 1995)and its promising replacement HFO-1234yf (2,3,3,3-tetra-fluoropropene) (Luecken et al., 2010). For example, in the rainfall in North America, the concentrations of TFA and PFPrA reached 2400 ng/L and 120 ng/L, respectively, while the concentration of the most concerned PFAA, i.e., perfluorooctanoic acid (PFOA) was only 89 ng/L (Scott et al., 2006). It was found that PFPrA was the primary contaminant together with PFOA and perfluorononaic acid (PFNA) in the rainfall in Japan (Kwok et al., 2010). The continuous and high loads of these ultra-short chain PFCAs lead to their increasing detection frequencies and concentrations in the surface environment (Zai et al., 2015; Zhang et al., 2018; Kazil et al., 2011). In 2012, it was predicted that the concentrations of TFA in surface water bodies could reach 6 mg/L after a 10-year emission of HFO-1234yf, and 15 mg/L after 50 years with extreme concentrations of up to 200 mg/L across North America (Russell et al., 2012).

Plants can efficiently take up PFAAs from contaminated environmental media (Blaine et al., 2014a; Yoo et al., 2011; Zhao et al., 2013; Krippner et al., 2014; Felizeter et al., 2012a; Stahl et al., 2009; Felizeter et al., 2014; Blaine et al., 2013), and therefore PFAAs can be transferred to human body via food chains (Blaine et al., 2014b; Heo et al., 2014) and enhance human exposure risks. There were some studies concerning the uptake of PFAAs by plants (Blaine et al., 2014a; Yoo et al., 2011; Zhao et al., 2013; Krippner et al., 2014; Felizeter et al., 2012a; Stahl et al., 2009; Felizeter et al., 2014; Blaine et al., 2013), however, the mechanism of PFAAs uptake by plants remains unclear. Most studies just dealt with the two most concerned analogues, i.e., PFOA and perfluorooctane sulfonic acid (PFOS) (Zhao et al., 2013; Stahl et al., 2009; Lechner & Knapp, 2011). However, the uptake and translocation inside plants of PFAAs should change significantly with the carbon chain length due to the varied chemical and physical properties such as octanol-water partition coeffient (K_ow) and the molecular volume (Blaine et al., 2014a; Krippner et al., 2014). The PFAAs with shorter carbon chain have smaller molecular volume and are more hydrophilic (low logK_ow), and can thus easily penetrate the roots and be transported upwards. On the contrary, long-chain PFAAs like PFOS and PFOA are mostly confined to the surface of roots and easily filtered out by typical barriers of root such as the Casparian strip (Blaine et al., 2014a). Stahl et al. found that root concentration factors (RCF) of PFAAs decreased with increasing chain length from PFBA to PFHxA, then increased markedly between PFHxA and PFUnA by hydroponically grown Lettuce (Felizeter et al., 2012b). It can be predicted that TFA and PFPrA should have high potential to accumulate in plants due to their high water solubility and small molecular size. However, until now, plant uptake of these ultra-short chain PFCAs, i.e. TFA and PFPrA has never been studied together with the long chain analogues (Likens et al., 1997; Cahill et al., 2001).

Plants can uptake chemicals through active and/or passive processes, which mostly depend on the characteristics of the chemical and the plant, and the level in solution (Collins et al., 2006). Active uptake is an energy-consuming process which is mediated by carrier protein, while passive uptake is a process following the gradient of potential energy, driven by mass flow or diffusion (Zhan et al., 2010). Some passive processes are independent of carriers, which occur without any media or via the channels in plant roots such as water channels and anion channels (Sugano et al., 2010; Kong et al., 2007; Wang et al., 2011a). Others are a facilitated passive diffusion, which is mediated by carriers without energy consumption (Sugano et al., 2010; Kong et al., 2007; Wang et al., 2011a). To our knowledge, studies on the uptake mechanisms of PFAAs in plants are scarce. A study carried out by Wen et al. (Wen et al., 2013) found that the uptake mechanisms of PFOA and PFOS in maize were diverse. The uptake of PFOS was a passive process mediated by a carrier, in which aquaporins and anion channels might be involved; while the uptake of PFOA was an energy dependent active process which might occur via anion channels. However, there were no other papers studying the specific uptake processes of PFAAs by plants, such as active or passive uptake processes and further the participation of channels.

In order to fill these knowledge gaps, we focused on five PFCAs including the ultra-short chain (TFA and PFPrA), the short-chain (PFBA and PFHxA), and the long-chain PFOA and PFOS to explore the carbon chain length dependent uptake and translocation by wheat and the mechanisms therein. To our knowledge, this is the first report on the uptake mechanisms of PFAAs including ultra-short chain PFCAs.