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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Complexation and Toxicity of Copper in Higher Plants. I. Characterization of Copper Accumulation, Speciation, and Toxicity in Crassula helmsii as a New Copper Accumulator^1,[W],[OA]

Universität Konstanz, Mathematisch-Naturwissenschaftliche Sektion, Fachbereich Biologie, D–78457 Konstanz, Germany (H.K., B.G.); University of South Bohemia, Faculty of Biological Sciences and Institute of Physical Biology, CZ–370 05 eské Budejovice, Czech Republic (H.K.); University of Utrecht, Department of Inorganic Chemistry and Catalysis, 3584 CA Utrecht, The Netherlands (A.M.); Scottish Association for Marine Science, Dunstaffnage Marine Laboratory, Oban, Argyll PA37 1QA, Scotland, United Kingdom (F.C.K.); and EMBL Outstation Hamburg, Deutsches Elekronen-Synchrotron, D–22603 Hamburg, Germany (W.M.-K.)

The amphibious water plant Crassula helmsii is an invasive copper (Cu)-tolerant neophyte in Europe. It now turned out to accumulate Cu up to more than 9,000 ppm in its shoots at 10 µM (=0.6 ppm) Cu²⁺ in the nutrient solution, indicating that it is a Cu hyperaccumulator. We investigated uptake, binding environment, and toxicity of Cu in this plant under emerged and submerged conditions. Extended x-ray absorption fine structure measurements on frozen-hydrated samples revealed that Cu was bound almost exclusively by oxygen ligands, likely organic acids, and not any sulfur ligands. Despite significant differences in photosynthesis biochemistry and biophysics between emerged and submerged plants, no differences in Cu ligands were found. While measurements of tissue pH confirmed the diurnal acid cycle typical for Crassulacean acid metabolism, ¹³C measurements showed values typical for regular C3 photosynthesis. Cu-induced inhibition of photosynthesis mainly affected the photosystem II (PSII) reaction center, but with some unusual features. Most obviously, the degree of light saturation of electron transport increased during Cu stress, while maximal dark-adapted PSII quantum yield did not change and light-adapted quantum yield of PSII photochemistry decreased particularly in the first 50 s after onset of actinic irradiance. This combination of changes, which were strongest in submerged cultures, shows a decreasing number of functional reaction centers relative to the antenna in a system with high antenna connectivity. Nonphotochemical quenching, in contrast, was modified by Cu mainly in emerged cultures. Pigment concentrations in stressed plants strongly decreased, but no changes in their ratios occurred, indicating that cells either survived intact or died and bleached quickly.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Hendrik Küpper (hendrik.kuepper{at}uni-konstanz.de).

^[W] The online version of this article contains Web-only data.

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www.plantphysiol.org/cgi/doi/10.1104/pp.109.139717

^* Corresponding author; e-mail hendrik.kuepper{at}uni-konstanz.de.

Received April 9, 2009; accepted July 20, 2009; published July 29, 2009.