Synergistic effects of a photooxidized polycyclic aromatic hydrocarbon and copper on photosynthesis and plant growth: Evidence that in vivo formation of reactive oxygen species is a mechanism of copper toxicity

Abstract

Heavy metals and polycyclic aromatic hydrocarbons (PAHs) are often cocontaminants in industrialized environments, yet little is known about either the extent or mechanisms of their cotoxicity. To address this shortfall, the combined effects of an oxygenated PAH, 1,2-dihydroxyanthraquinone (1,2-dhATQ), and a heavy metal, Cu2+, on photosynthesis and growth of the duckweed (Lemna gibba) were evaluated. Using assays of chlorophyll a fluorescence and photosystem I activity, 1,2-dhATQ inhibited electron transport at the cytochrome b6/f complex. Conversely, Cu2+ alone (at low concentrations) had little effect on photosynthesis. When Cu2+ was combined with 1,2-dhATQ, an increase in transient and steady-state chlorophyll a fluorescence quenching occurred relative to 1,2-dhATQ alone. Treatment of isolated thylakoid membranes with 1,2-dhATQ inhibited whole-chain linear electron transport, measured as O2 consumption using methyl viologen as the electron acceptor. However, Cu2+ plus 1,2-dhATQ resulted in active O2 consumption with or without methyl viologen as an electron acceptor. From these data, we conclude that 1,2-dhATQ renders the plastoquinone pool to a highly reduced state by inhibiting at cytochrome b6/f. Then, Cu2+ is able to mediate the transfer of electrons from reduced plastoquinone to O2, forming reactive oxygen species. At the whole-organism level, when Cu2+ and 1,2-dhATQ were mixed at concentrations that resulted in the above-mentioned impacts on photosynthesis, synergistic inhibition of plant growth was observed. This suggests a catalytic mechanism of toxicity for redox active metals, a process that could be instrumental in explaining their impacts at low concentrations.

Mixtures of metals and polynuclear aromatic hydrocarbons elicit complex, nonadditive toxicological interactions in meiobenthic copepods

“…Response addition and concentration addition were relatively rare. These observations suggest that, at least in binary tests, nonadditive interactions between a variety of metals and PAH occur frequently in benthic copepods and perhaps other aquatic plants [31] and animals [32] and that the combination of Cd and PAH may be especially toxic.…”

Comparing the effects of excess copper in the leaves ofBrassica juncea(L. Czern) andBrassica napus(L.) seedlings: Growth inhibition, oxidative stress and photosynthetic damage

“…Based on these, the photosynthesis of B. juncea was more sensitive to low applied Cu concentration, while B. napus showed susceptibility to more serious excess Cu (25 and 50 µM Cu). Considering the remarkable ROS accumulation detected in the leaves we can assume that chloroplast membranes may suffer Cu-induced peroxidation, which can partially explain the diminution of photosynthetic efficiency [3]. Furthermore, free radicals can damage the photosynthetic apparatus [2] and may also catalyse protein degradation through oxidative modification and increased proteolytic activity [38], which may also lead to the decrease in photosynthesis.…”

Multiparameter-Based Bioassay of 2-(4-Chlorophenyl)-4-(4-methoxyphenyl) Quinazoline, a Newly-Synthesized Quinazoline Derivative, Toward Microcystis aeruginosa HAB5100 (Cyanobacteria)

“…Therefore, it is suggested that that concentrations of CMQ C 5 mg L -1 cause PSII inactivity and linear electron flow blockage in M. aeruginosa, leading to the formation of oxygen radicals and consequent oxidative stress. (Babu et al 2001;Nishiyama et al 2006). A conserved gene in eukaryotes and prokaryoters, prx, encodes the Prx protein that plays an important role in catalyzing the reduction of oxygen radicals, such as H 2 O 2 , alkyl hydroperoxides, and peroxynitrite (Wood et al 2003).…”