Biochimica et Biophysica Acta 848 (1986) 41-47 41
Elsevier
BBA 41896
Reversible and irreversible effects of alkaline pH on Photosystem II
electron-transfer reactions
James Cole, Michael Boska, Neil V. Blough * and Kenneth Sauer
Department of Chemistry and Chemical Biodynamics Laboratory, Lawrence Berkeley Laboratory, University of California,
Berkeley, CA 94720 (U.S.A.)
(Received June 12th, 1985)
Key words: Oxygen evolution; ESR; Photosystem II; pH effect; Electron transport; (Spinach chloroplast)
Incubation of highly active, O2-evolving PS II preparations at alkaline pH inhibits donor side electron-trans-
fer reactions in two distinct fashions, one reversible the other irreversible. In both cases, 0 2 evolution is
inhibited, with concomitant loss of the light-induced multiline and g = 4.1 EPR signals and an increased
steady-state level of EPR Signal II induced by continuous illumination. However, the inhibition that is
observed between pH 7.0 and 8.0 is readily reversible by resuspension at low pH, while above pH 8.0 the
effect is irreversible. In addition, under repetitive flash conditions the ms decay kinetics remains largely
unchanged at pH < 8.0 but shows about a 2-fold increase in amplitude and is slowed at pH above 8.0. The
irreversible component of inhibition most likely can be attributed to the loss of Mn and the 16, 24 and 33
kDa proteins. The reversible component may be mediated by displacement of CI - from an anion-binding site
by OH - or by titration of ionizable groups on the protein(s) associated with water-splitting. We propose that
the reversible inhibition blocks electron transfer between the O2-evolving complex and an intermediate which
serves as the direct donor to Signal II, while the irreversible inhibition blocks the reduction of Signal II by
this intermediate donor species.
Introduction
The loss of the water-splitting activity of chlo-
roplast membrane preparations at alkaline pH in
the presence of uncouplers has been observed by a
number of investigators [1-4]. From these experi-
ments it has been concluded that it is the internal
thylakoid pH which controls water-splitting activ-
ity and photosynthetic electron flow through PS II
by its effect on the O2-evolving apparatus located
* Present address: Department of Chemistry, Woods Hole
Oceanographic Institution, Woods Hole, MA 02543, U.S.A.
Abbreviations: Mes, 4-morpholineethanesulfonic acid; Hepes,
4-(2-hydroxyethyl)-l-piperazineethanesulfonic acid; Tricine,
N-[2-hydroxy-l,l-bis(hydroxymethyl)ethyl]glycine; Chl, chloro-
phyll; DCBQ, 2,5-dichlorobenzoquinone; PS, Photosystem.
on the lumenal side of the membrane [1]. The flash
illumination study of Briantais et al. [3] indicates
that the target for alkaline inactivation is the S2
state of the oxygen-evolving complex.
Highly active PS II preparations [5-7] offer an
excellent means of examining the effect of pH on
the water-splitting reactions. Because the lumenal
surface of the membrane is exposed to the external
medium in these preparations [7], the direct in-
fluence of pH on the water-splitting apparatus can
be investigated without interference from an inter-
vening membrane barrier. Kuwabara and Murata
[6,8] found that suspension of PS II preparations
in Tricine buffers at pH > 8.0 produced a loss of
02 evolution [6], the release of the 33, 24 and 16
kDa proteins [8] and a significant decrease in the
Mn content [8], indicating a substantial perturba-
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