Accumulation of phenanthrene by roots of intact wheat (Triticum acstivnm L.) seedlings: passive or active uptake?

Abstract

Background: Polycyclic aromatic hydrocarbons (PAHs) are of particular concern due to their hydrophobic, recalcitrant, persistent, potentially carcinogenic, mutagenic and toxic properties, and their ubiquitous occurrence in the environment. Most of the PAHs in the environment are present in surface soil. Plants grown in PAH-contaminated soils or water can become contaminated with PAHs because of their uptake. Therefore, they may threaten human and animal health. However, the mechanism for PAHs uptake by crop roots is little understood. It is important to understand exactly how PAHs are transported into the plant root system and into the human food chain, since it is beneficial in governing crop contamination by PAHs, remedying soils or waters polluted by PAHs with plants, and modeling potential uptake for risk assessment.

Results: The possibility that plant roots may take up phenanthrene (PHE), a representative of PAHs, via active process was investigated using intact wheat (Triticum acstivnm L.) seedlings in a series of hydroponic experiments. The time course for PHE uptake into wheat roots grown in Hoagland solution containing 5.62 microM PHE for 36 h could be separated into two periods: a fast uptake process during the initial 2 h and a slow uptake component thereafter. Concentration-dependent PHE uptake was characterized by a smooth, saturable curve with an apparent Km of 23.7 microM and a Vmax of 208 nmol g(-1) fresh weight h(-1), suggesting a carrier-mediated uptake system. Competition between PHE and naphthalene for their uptake by the roots further supported the carrier-mediated uptake system. Low temperature and 2,4-dinitrophenol (DNP) could inhibit PHE uptake equally, indicating that metabolism plays a role in PHE uptake. The inhibitions by low temperature and DNP were strengthened with increasing concentration of PHE in external solution within PHE water solubility (7.3 muM). The contribution of active uptake to total absorption was almost 40% within PHE water solubility. PHE uptake by wheat roots caused an increase in external solution pH, implying that wheat roots take up PHE via a PHE/nH+ symport system.

Conclusion: It is concluded that an active, carrier-mediated and energy-consuming influx process is involved in the uptake of PHE by plant roots.

Figure 1

Time course of phenanthrene uptake by roots of wheat seedlings through 36 h. Roots were incubated in Hoagland nutrient solution (pH 5.5) containing 5.62 μM phenanthrene at 25°C. Data points represent mean and SD values of triplicates. Error bars do not extend outside all data points. fr wt, Fresh weight.

Figure 2

Concentration dependence of phenanthrene uptake into intact wheat roots. Phenanthrene concentrations varied from 0 to 6.74 μM in Hoagland nutrient solutions (pH 5.5). Data points represent mean and SD values of triplicates. Error bars do not extend outside all data points. fr wt, Fresh weight.

Figure 3

Concentration-dependent uptake of phenanthrene at 25 and 4°C in intact wheat roots. Phenanthrene concentrations in Hoagland nutrient solutions (pH 5.5) ranged from 0 to 6.74 μM. Data points represent mean and SD values of triplicates. Error bars do not extend outside all data points. fr wt, Fresh weight.

Figure 4

Concentration-dependent uptake of phenanthrene in intact wheat roots with the presence and absence of 2,4-dinitrophenol (1 mM), a common metabolic inhibitor. Phenanthrene concentrations in Hoagland nutrient solutions (pH 5.5) ranged between 0 and 6.74 μM. Data points represent mean and SD values of triplicates. Error bars do not extend outside all data points. fr wt, Fresh weight. DNP, 2,4-dinitrophenol.

Figure 5

Uptake competition between phenanthrene and naphthalene in wheat roots. Hydroponic solution was Hoagland nutrient solution (pH 5.5). PHE, Hoagland solution contained 2.81 μM phenanthrene. NAP, Hoagland solution contained 3.91 μM naphthalene. PHE (PHE+NAP), Hoagland solution contained 2.81 μM phenanthrene and 3.91 μM naphthalene, and phenanthrene uptake was detected. NAP (PHE+NAP), Hoagland solution contained 2.81 μM phenanthrene and 3.91 μM naphthalene, and naphthalene uptake was detected. Data points represent mean and SD values of triplicates. fr wt, Fresh weight. PAHs, Polycyclic aromatic hydrocarbons. PHE, Phenanthrene. NAP, Naphthalene.