Impact Mechanisms of Humic Acid on the Transmembrane Transport of Per- and Polyfluoroalkyl Substances in Wheat at the Subcellular Level: The Important Role of Slow-Type Anion Channels

Abstract

Per-and polyfluoroalkyl substances (PFASs) have potential to accumulate in crops and pose health risks to humans, but it is unclear how the widely present organic matters in soil, such as humic acid (HA), affect their uptake and translocation in plants. In this study, hydroponic experiments were conducted to systematically disclose the impacts of HA on the uptake, translocation, and transmembrane transport at the subcellular level of four PFASs, including perfluorooctane sulfonic acid, perfluorooctanoic acid, perfluorohexane sulfonic acid, and 6:2 chlorinated polyfluoroalkyl ether sulfonate in wheat (Triticum aestivum L.). The results of the uptake and depuration experiments indicated that HA depressed the adsorption and absorption of PFASs in wheat roots by reducing the bioavailability of PFASs, and HA did not affect the long-range transport of PFASs to be eliminated via the phloem of wheat. However, HA facilitated their transmembrane transport in wheat roots, while the contrary effect was observed in the shoots. The inhibitor experiments coupled with transcriptomics analysis uncover that the increased transmembrane transport of PFASs stimulated by HA is mainly driven by the slow-type anion channel pathways interacting with Ca 2+ -dependent protein kinases (Ca 2+ -CDPK-SLAC1). The promoted transmembrane transport of PFASs might cause adverse effects on the plant cell wall, which causes further concerns.

Novel Insights into the Promoted Accumulation of Nitro-Polycyclic Aromatic Hydrocarbons in the Roots of Legume Plants

“…These results suggest that the accumulated nitro-PAHs in the roots of legumes were hard to eliminate. As has been reported previously, PFOS and PFHxS accumulated in wheat roots could be released into the solutions during the depuration phase, which was driven by the concentration gradients between the roots and solutions . However, among the five sub-PAHs, although nitro-PAHs had the highest log RCF values (Figure S1), they exhibited the lowest elimination rates in legume roots (Table S6).…”

“…A previous study also demonstrated that the uptake of 1-NO 2 -Pyr by wheat roots was inappreciably affected by water channel inhibitors . A similar phenomenon was observed for perfluoroalkanesulfonic acids (PFSAs) such as PFOS and PFHxS. , Water channels, a type of membrane proteins, can transport water and hydrophilic solutes depending on the size of the holes. , Since nitro-PAHs have relatively high hydrophobicity (log K ow > 4.16, Table S1), it is quite difficult for them to be absorbed via water channels. Notably, the concentrations of 9-NO 2 -Ant and 1-NO 2 -Pyr in legume roots were significantly reduced by 29.7–44.2 and 24.5–58.6% in the presence of a H + -ATPase inhibitor (Na 3 VO 4 ), respectively, but not in the roots of gramineous plants (Figure ).…”

“…Similar results were also observed in the 2,4-DNP treatments, in which 9-NO 2 -Ant and 1-NO 2 -Pyr uptake in legume roots were inhibited at rates of 53.2–72.1 and 47.5–55.7%, respectively (Figure ). These results collectively indicate that uptake of nitro-PAHs in legume roots was an energy-dependent active process mediated by plasma membrane H + -ATPase. ,, Such an energy-dependent active process is also generally present in the nutrient uptake by plant roots because nutrients are delivered from a low concentration to a high concentration, thus achieving significant accumulation of nutrients in plant roots . For instance, it has been proven that plants can actively absorb amino acid by amino acid transporters driven by the H + electrochemical gradient produced by H + -ATPase .…”

“…It is well known that the migration of organic pollutants in soil–plant systems plays a crucial role in affecting their environmental behaviors in soil . In recent years, some significant advances have been made in understanding the root accumulation of organic pollutants from contaminated soils. − It is widely accepted that these processes are highly dependent upon the pollutant properties . Hydrophobic organic pollutants possess a tendency to partition into root lipids and thus concentrate in roots .…”

Phloem Redistribution of Pesticide Phenamacril in Plants Followed by Extensive Biotransformation

“…In the 144 h of the plant uptake experiment (Figure S2A), the uptake rate constant ( k 1 , h –1 ) was calculated by the first-order one-compartment model (Text S12). As shown in Table S8, the k 1 of phenamacril in roots (wheat: 0.744 h –1 , rice: 0.547 h –1 ) were 23.6–105.4 times higher than that in shoots (wheat: 0.00706 h –1 , rice: 0.0232 h –1 ), suggesting the mass transfer of phenamacril from roots to shoots was much slower than that from external water to roots. The RCF of phenamacril in wheat (or rice) gradually increased up to 2.7 (or 2.4) mL/g within 144 h (Figure S4A, Table S9), indicating a low-medium accumulation potential in roots.…”