Toxic effects and oxidative stress in higher plants exposed to polycyclic aromatic hydrocarbons and their N‐heterocyclic derivatives

Abstract

N-heterocyclic derivatives of polycyclic aromatic hydrocarbons (NPAHs) are widespread concomitantly with their parent analogues and have been detected in air, water, sediments, and soil. Although they were shown to be highly toxic to some organisms, our understanding of their occurrence, environmental fate, biological metabolism, and effects is limited. This study evaluated toxic effects of three homocyclic aromatic hydrocarbons (PAHs-phenanthrene, anthracene, fluorene) and their seven N-heterocyclic derivates on higher terrestrial plants Sinapis alba, Triticum aestivum, and Phaseolus vulgaris. Germinability, morphological endpoints, parameters of detoxification, and antioxidant components of plant metabolism as well as lipid peroxidation were studied in acute phytotoxicity tests. Phytotoxicity of NPAHs was generally more pronounced than the effects of parent PAHs, and it significantly differed with respect to the structure of individual NPAHs. Sinapis alba and T. aestivum were more sensitive plant species than P. vulgaris. Chemicals with the strongest inhibition effect on germination and growth of plants were phenanthridine, acridine, benzo[h]quinoline, and 1,10- and 1,7-phenanthroline. All tested chemicals significantly induced activities of detoxification and antioxidant enzymes (glutathione reductase, glutathione peroxidase, and glutathione-S-transferase) at nanomolar to low micromolar concentrations. Levels of reduced glutathione were induced by all tested chemicals except 1,10- and 4,7-phenanthroline. Furthermore, fluorene, carbazole, acridine, phenanthrene, phenanthridine, benzo[h]quinoline, and 1,7-phenanthroline significantly increased lipid peroxidation. The results of our study newly demonstrate significant toxicity of NPAHs to plants and demonstrate suitability of multiple biomarker assessment to characterize mechanisms of oxidative stress and to serve as an early warning of phytotoxicity in vivo.

Effect of organic pollutant treatment on the growth of pea and maize seedlings

“…The dry biomass of roots in maize was reduced by 85% and in pea by up to 65% and the dry biomass of shoots by 88% in maize and up to 54% in pea. These results are in agreement with Pašková et al [35] who confirmed the negative effect of three PAHs and their N-heterocyclic derivates on the germination and growth of seedling of mustard, barley and common bean. Similarly, Abdel-Latif [36] found a reduction of root and shoot length and biomass of maize seedlings with increasing concentrations of methyl tertbutyl ether as well as in several higher plants cultivated in real soil contaminated with spent oil, which contains also PAHs [37].…”

Stress responses to phenol in Arabidopsis and transcriptional changes revealed by microarray analysis

“…4). Consistent with physiological studies that associated PAH treatment with growth inhibition and oxidative stress (Alkio et al 2005;Pašková et al 2006;Burritt 2008;Liu et al 2009), transcripts related to these were overrepresented among the phenol-responsive genes (Table 1). For instance, three cell wall expansins with known roles in cell wall loosening and cell enlargement (Keller and Cosgrove 1995;O'Malley and Lynn 2000), AtEXPA15, AtEXPB3 and AtEXPA10, were downregulated.…”

Stress signaling in response to polycyclic aromatic hydrocarbon exposure in Arabidopsis thaliana involves a nucleoside diphosphate kinase, NDPK-3

“…It is well established that PAHs cause oxidative stress in plants (Paskova et al 2006;Wang and Zhao 2007;Burritt 2008). In Arabidopsis treated with phenanthrene, a threeringed PAH commonly found in polluted environments, Alkio et al (2005) detected hydrogen peroxide (H 2 O 2 ) and localized cell death, both consistent with oxidative stress.…”

“…It is also possible that the overall physiological damage (Alkio et al 2005;Liu et al 2009) is too great for the plant to efficiently metabolize the toxic PAH molecules. Finally, as phenanthrene causes lipid damage in plants (Paskova et al 2006;Burritt 2008;Liu et al 2009), an increase in organelle membrane permeability could be reducing the high local enzyme concentrations needed to rapidly transform H 2 O 2 . All plants in this study were grown in media containing 2.0 % sucrose that served as an external carbon source.…”