Effects of nanomolar copper on water plants - comparison of biochemical and biophysical mechanisms of deficiency and sublethal toxicity under environmentally relevant conditions

Abstract

Toxicity and deficiency of essential trace elements like Cu are major global problems. Here, environmentally relevant sub-micromolar concentrations of Cu (supplied as CuSO4) and simulations of natural light- and temperature cycles were applied to the aquatic macrophyte Ceratophyllum demersum. Growth was optimal at 10 nM Cu, while PSII activity (Fv/Fm) was maximal around 2 nM Cu. Damage to the PSII reaction centre was the first target of Cu toxicity, followed by disturbed regulation of heat dissipation (NPQ). Only after that, electron transport through PSII (ΦPSII) was inhibited, and finally chlorophylls decreased. Copper accumulation in the plants was stable until 10 nM Cu in solution, but strongly increased at higher concentrations. The vein was the main storage site for Cu up to physiological concentrations (10 nM). At toxic levels it was also sequestered to the epidermis and mesophyll until export from the vein became inhibited, accompanied by inhibition of Zn uptake. Copper deficiency led to a complete stop of growth at “0” nM Cu after 6 weeks. This was accompanied by high starch accumulation although electron flow through PSII (ΦPSII) decreased from 2 weeks, followed by decrease in pigments and increase of non photochemical quenching (NPQ). Release of Cu from the plants below 10 nM Cu supply in the nutrient solution indicated lack of high-affinity Cu transporters, and on the tissue level copper deficiency led to a re-distribution of zinc.