Handbook of Plant and Crop Physiology

(Steven Felgate) #1

progen oxidative decarboxylase only in the presence of oxygen [1]! Moreover, it has been stated that the
oxidation of water in principle requires catalytic amounts of oxygen with a cooperative mode of binding
for its functioning. In an absolutely anaerobic atmosphere, the oxygen-evolving complex (OEC) does not
operate [2]. Photolytic reactions involving, e.g., ultraviolet (UV) light might have played a role in gener-
ating the necessary low oxygen partial pressure at least in ecological niches such as lakes or puddles [3].
With the modern discussion of an increasing carbon dioxide concentration of the atmosphere in
mind, it should be noted that the CO 2 partial pressure of the early atmosphere amounted to some percent
(instead of ppm!). At the time, the photosynthetic organisms were restricted to inorganic salts as electron
donors for light-induced electron transport, and it is assumed that iron and sulfide compounds played a
substantial role. However, on a long-term scale this situation was problematic and unfavorable for the
evolution of higher photosynthetic organisms because (1) the energy required for the oxidation of such
compounds was relatively high and (2) the availability of sufficiently high amounts of these electron
sources was limited. It appeared necessary to evolve an improved system with less energy required and—
most important—to find a ubiquitous electron supply. Such an electron source was finally found with the
simple and almost ubiquitously available and disposable molecule of water (H 2 O). In this context, the
evolutionary significance of hydrogen peroxide in some ecological niches functioning (transitorily) as an
intermediate electron donor between inorganic salts and molecular water has been proposed and dis-
cussed [e.g., 3–5]. However, another problem came up based on some unique properties of the water
molecule. In this context, only the extremely high stability of this molecule will be mentioned. Even in
the modern world with all the technical facilities available today, drastic reaction conditions such as elec-
tric current or high temperatures of about 2000°C or more are needed technically to oxidize the molecule.
Photosynthetic organisms perform oxygenic photosynthesis under physiological conditions and at room
temperature! Although many scientific details of the mechanisms of photosynthetic reactions have been
worked out, many questions remain to be elucidated. Some of the relevant parameters will be referred to
in the respective sections of this chapter. From the multitude of relevant investigations and reviews, only
a few will be mentioned here [3–10] (G Renger, submitted).
Although plants are capable of utilizing abiotic radiation energy (see earlier) and transforming it to
biologically useful forms, they also operate (at the same time or under specific conditions) many oxida-
tive (respiratory) processes. Among these are (completely) different and independent reactions—dark res-
piration, alternative respiration, photorespiration, chlororespiration, and concerted reactions that have
been termed maintenance respiration. It is clear that these reactions require a substantial but “reasonable”
oxygen partial pressure. It must be emphasized that oxygen as such is by far not the “positive” molecule
for plants that it is for animals and human beings; in many cases it is a problematic gas whose partial pres-
sure has to be strictly regulated in order to avoid detrimental effects. Thus, the evolution of oxygenic pho-
tosynthesis—finally reaching an ambient partial pressure of 21% O 2 —made the situation more and more
complex and was in principle a type of ecological catastrophy for the early anaerobic organisms. It must
be kept in mind that the process of water “splitting” oxidizes H 2 O with O 2 being released as a waste prod-
uct, thus substantially increasing the partial pressure of molecular oxygen at endogenous physiological
sites where (unregulated) oxidative processes appeared highly problematic and might result in the unde-
sired oxidation of sensitive vicinal components. (The reaction center pigment of photosystem II, P 680 
has a high positive redox potential of about 1.2 V.) It should be added that in the absence of molecular
oxygen the decay of the P 680 triplet state turned out to be much slower; i.e., the excitation state was more
stable than under oxygenic conditions [11]. Moreover, it is well known that reactive oxygen species are
formed inside the oxygen-evolving complex; P 680 in the triplet state forms singlet oxygen, and this sin-
glet oxygen is not least formed by direct recombination of the radical pair P 680 Pheo[12]. (The ex-
ceptionally high turnover rate of the D1 protein can at least in part be explained by the need for protec-
tion against such detrimental oxidative processes.)
It has been shown that photosystem II of photosynthetic species can interact with atmospheric oxy-
gen, forming a peroxidic component such as hydrogen peroxide (see earlier). This reaction might be
suited to lower the internal partial pressure of oxygen and at the same time to supply an additional elec-
tron donor for the OEC as hydrogen peroxide has been shown to be effectively oxidized by photosystem
II [13–17]. Thus, the interaction of the OEC with molecular oxygen might help to keep the oxygen par-
tial pressure in the immediate vicinity of the enzymatic process at a low level. Taking the arguments to-
gether, it is clear that oxygenic photosynthesis requires small amounts of oxygen but at the same time has
to limit the resulting increasing partial pressure via some regulatory mechanism. The binding of atmo-


300 BADER AND ABDEL-BASSET
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