with Pheoand QAthat eliminates the repulsive interaction between Pheoand QAwithout affecting pri-
mary charge separation.
Inhibition of the donor side of photosystem II close to the water oxidation complex was supported
by the loss of the extrinsic 17-kDa polypeptide associated with the oxygen-evolving complex [31]. Fur-
thermore, it was shown that photosystem II preparations depleted of the 17- and 23-kDa extrinsic
polypeptides were more sensitive to copper and that Ca^2 , a cofactor of the water oxidation complex,
specifically prevented the inhibitory action [34]. Ca^2 also partially prevented the deleterious effects of
copper in whole plants [35]. This might indicate that Cu^2 ions are competing for the Ca^2 binding site
and may replace Ca^2 . Inhibition by copper is also competitive in respect to protons [28,36] and is thus
pH sensitive. It has been suggested that it may bind an unprotonated residue close to the water-oxidizing
system [9].
In the cyanobacterium Spirulina platensis, it was shown that copper had a much more significant in-
hibitory effect on photosystem II photochemistry under illumination in comparison with dark incubation.
It was hypothesized that light may stimulate copper binding at its inhibitory site [29]. On the other hand,
in bean plants, copper was also shown to accelerate the photoinhibition process in photosystem II by in-
creasing the photoinhibition quantum yield and thus decreasing the steady-state concentration of active
photosystem II centers [37]. It was previously proposed that copper might reduce the repair cycle of the
D1 protein of the reaction center of photosystem II [38]. Copper is a relatively good catalyst of free rad-
icals, and its presence is assumed to stimulate oxidative damage in plants. Copper was shown to increase
significantly the concentration of superoxide in both thylakoid membranes and photosystem II prepara-
tions isolated from wheat seedlings exposed to copper [39]. This coincided with the induction of antiox-
idative enzymes even though it was also observed that in the cyanobacterium Anabeana doliolum, the an-
tioxidant system could not significantly protect against copper-induced oxidative damage [40]. From
studies using photosystem II preparations, Yruela et al. [41] proposed that copper strongly interacts with
the accceptor side of the photosystem, near the pheophytin-QAdomain, where it catalyzes the generation
of superoxide and hydroxyl radicals instead of the formation of singlet oxygen usually involved in donor-
side photoinhibition. This results in greater yields of photodamage because hydroxyl radicals are more
deleterious than singlet oxygen.
B. Cadmium
Cadmium is a major environmental contaminant for which no biological function has been described. It
has a number of toxic effects in plants, although the photosynthetic apparatus is particularly susceptible
to this metal. Micromolar concentrations of cadmium were shown to inhibit oxygen evolution and CO 2
fixation in cyanobacteria [42,43]. Cadmium transport into the cells of Synechocystis aquatiliswas pH de-
pendent and was optimal at pH 7.5 [42]. In higher plants, it was suggested that the primary targets of cad-
mium during short exposures of bean plants were more at the Calvin cycle enzyme than at the electron
transport reactions [44,45]. The inhibitory action also depended on leaf maturity [45]. The ultrastructure
of developing chloroplasts in several plant species was shown to be greatly affected by cadmium and large
destruction of the granal structure was observed under illumination [46–48]. The accumulation of chloro-
phylls and carotenoids was retarded by cadmium and some changes in the photosystem II light-harvest-
ing complexes were also reported in radish seedlings, showing that the monomeric content increased fol-
lowing exposure to cadmium at the expense of the oligomeric form [49,50].
In the electron transport system, both photosystems were shown to be affected together with the ATP
synthase/adenosinetriphosphatase (ATPase) [51–53]. The inhibition in photosystem I was proposed to af-
fect the acceptor side of the photosystem at the level of the ferredoxin:NADP-reductase [54]. However,
photosystem II was reported to be much more sensitive than photosystem I [51,52]. A cadmium-tolerant
mutant of Chlamydomonas reinhardtiiwas exclusively affected by the mutation at the level of photosys-
tem II, which also points to the inhibitory action of cadmium in photosystem II [55].
Studies using isolated chloroplasts indicated that the inhibition of photosystem II by cadmium could
be assigned to the donor side of photosystem II [56–58]. However, a location within the reaction center
of the photosystem has also been suggested [59]. In clover and lucerne plants the inhibition was reported
to be removed by artificial electron donors specific for the photosystem such as hydroxylamine and
MnCl 2 , indicating an inhibitory site on the donor side [51]. However, contradictory results concerning the
electron donors were obtained by Atal et al. [52] in wheat seedlings. Still, these authors also postulated
NEGATIVE ACTION OF TOXIC DIVALENT CATIONS 765