Distribution of polycyclic aromatic hydrocarbons in subcellular root tissues of ryegrass (Lolium multiflorum Lam.)

Abstract

Background: Because of the increasing quantity and high toxicity to humans of polycyclic aromatic hydrocarbons (PAHs) in the environment, several bioremediation mechanisms and protocols have been investigated to restore PAH-contaminated sites. The transport of organic contaminants among plant cells via tissues and their partition in roots, stalks, and leaves resulting from transpiration and lipid content have been extensively investigated. However, information about PAH distributions in intracellular tissues is lacking, thus limiting the further development of a mechanism-based phytoremediation strategy to improve treatment efficiency.

Results: Pyrene exhibited higher uptake and was more recalcitrant to metabolism in ryegrass roots than was phenanthrene. The kinetic processes of uptake from ryegrass culture medium revealed that these two PAHs were first adsorbed onto root cell walls, and they then penetrated cell membranes and were distributed in intracellular organelle fractions. At the beginning of uptake (< 50 h), adsorption to cell walls dominated the subcellular partitioning of the PAHs. After 96 h of uptake, the subcellular partition of PAHs approached a stable state in the plant water system, with the proportion of PAH distributed in subcellular fractions being controlled by the lipid contents of each component. Phenanthrene and pyrene primarily accumulated in plant root cell walls and organelles, with about 45% of PAHs in each of these two fractions, and the remainder was retained in the dissolved fraction of the cells. Because of its higher lipophilicity, pyrene displayed greater accumulation factors in subcellular walls and organelle fractions than did phenanthrene.

Conclusions: Transpiration and the lipid content of root cell fractions are the main drivers of the subcellular partition of PAHs in roots. Initially, PAHs adsorb to plant cell walls, and they then gradually diffuse into subcellular fractions of tissues. The lipid content of intracellular components determines the accumulation of lipophilic compounds, and the diffusion rate is related to the concentration gradient established between cell walls and cell organelles. Our results offer insights into the transport mechanisms of PAHs in ryegrass roots and their diffusion in root cells.

Figure 1

Concentrations of phenanthrene and pyrene in ryegrass roots as a function of uptake time. C_root means concentrations of phenanthrene and pyrene in ryegrass root.

Figure 2

Dissipation efficiency (%) of phenanthrene and pyrene by ryegrass from aqueous solution as a function of exposure time. The values were defined as ratio of PAH removal to the initial concentration from the aqueous solution. It explained in principle the plant-affected dissipation of phenanthrene and pyrene from solution, and such dissipation was primarily related to plant accumulation and metabolism.

Figure 3

Root concentration factor (RCF) of phenanthrene and pyrene for ryegrass uptake from aqueous solution. Root concentration factor (RCF) describes the capability of roots to accumulate contaminants from the direct contact with the aqueous environment, which is here defined as the ratio of PAH concentration in root (C_root) to that in culture medium (C_solution), i.e., RCF = C_root/C_solution.

Figure 4

Concentrations of phenanthrene (a) and pyrene (b) in root cell walls and organelles as a function of time. C_f means concentrations of phenanthrene and pyrene in root subcellular fractions.

Figure 5

Proportions of phenanthrene (a) and pyrene (b) distributed in cell water soluble fraction, wall and organelle as a function of uptake time. The proportion of PAHs was calculated from the measurement of PAH in each fraction to the total amount in ryegrass root cells.

Figure 6

Subcellular fraction concentration factors (SFCF) of phenanthrene (a) and pyrene (b) for ryegrass root uptake as a function of time 0~240 h. SFCF was defined as the ratio of PAH concentration in subcellular fractions including cell wall and organelle to that in cell water-soluble components.