Excess Copper Predisposes Photosystem II to Photoinhibition in Vivo by Outcompeting Iron and Causing Decrease in Leaf Chlorophyll

Eija Pätsikkä , Marja Kairavuo , Frantisek $S$ er $s$ en , Eva-Mari Aro , and Esa Tyystjärvi ^*

Plant Physiology and Molecular Biology, Biocity A, University of Turku, FIN--20014 Turku, Finland (E.P., M.K., E.-M.A., E.T.); and Faculty of Natural Sciences, Comenius University, 84215 Bratislava, Slovakia (F. $S$ .)

^* Corresponding author; email: esatyy{at}utu.fi.

Photoinhibition of photosystem II was studied in vivo with bean (Phaseolus vulgaris) plants grown in the presence of 0.3 (control), 4, or 15 µM Cu²⁺. Although photoinhibition, measured in the presence of lincomycin to block concurrent recovery, is faster in leaves of Cu²⁺-treated plants than in control leaves, thylakoids isolated from Cu-treated plants did not show high sensitivity to photoinhibition. Direct effects of excess Cu²⁺ on chloroplast metabolism are actually unlikely, because the Cu concentration of chloroplasts of Cu-treated plants was lower than that of their leaves. Excess Cu in the growth medium did not cause severe oxidative stress, collapse of antioxidative defenses, or loss of photoprotection. Thus, these hypothetical effects can be eliminated as causes for Cu-enhanced photoinhibition in intact leaves. However, Cu treatment lowered the leaf chlorophyll (Chl) concentration and reduced the thylakoid membrane network. The loss of Chl and sensitivity to photoinhibition could be overcome by adding excess Fe together with excess Cu to the growth medium. The addition of Fe lowered the Cu²⁺ concentration of the leaves, suggesting that Cu outcompetes Fe in Fe uptake. We suggest that the reduction of leaf Chl concentration, caused by the Cu-induced iron deficiency, causes the high photosensitivity of photosystem II in Cu²⁺-treated plants. A causal relationship between the susceptibility to photoinhibition and the leaf optical density was established in several plant species. Plant species adapted to high-light habitats apparently benefit from thick leaves because the rate of photoinhibition is directly proportional to light intensity, but photosynthesis becomes saturated by moderate light.

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