How Does Oxygen Production Relate to the Rate of Photosynthesis

How Does Oxygen Production Relate to the Rate of Photosynthesis

Journal Article

Singlet oxygen production in photosynthesis

Published:

13 August 2004

Abstract

A photosynthetic organism is subjected to photo-oxidative stress when more than light energy is captivated than is used in photosynthesis. In the light, highly reactive singlet oxygen can be produced via triplet chlorophyll germination in the reaction centre of photosystem II and in the antenna system. In the antenna, triplet chlorophyll is produced direct by excited singlet chlorophyll, while in the reaction centre it is formed via accuse recombination of the light-induced charge pair. Changes of the mid-betoken potential of the principal quinone acceptor in photosystem 2 modulate the pathway of accuse recombination in photosystem Two and influence the yield of singlet oxygen production. Singlet oxygen can be quenched by β-carotene, α-tocopherol or can react with the D1 protein of photosystem Ii every bit target. If not completely quenched, it can specifically trigger the up-regulation of the expression of genes which are involved in the molecular defence response of plants against photo-oxidative stress.

Singlet oxygen

Living in an oxygen-rich world carries the potential take chances of oxidative stress. Oxygen in the ground state is not direct a problem because it is relatively stable compared with its intermediates (peroxide (H2Otwo), superoxide

\((\mathrm{O}_{2}^{{\cdot}{-}})\)

and hydroxyl radicals (OH˙)). The relatively stable ground country of oxygen is a triplet state with ii unpaired electrons with the same spin quantum number, each located in different antibonding (π*) orbitals. Oxygen can react by oxidizing another molecule, but, despite its high thermodynamic reactivity, its reactions are kinetically tiresome because of the spin brake. Electron transfer reactions in the presence of oxygen tin give rise to the product of the reactive intermediates, which themselves tin produce different kinds of damage in the prison cell (Halliwell and Gutteridge, 1998).

In addition, the very reactive singlet oxygen can be generated by an input of energy. In this state, the spin restriction is removed and therefore the oxidizing ability of the oxygen is greatly increased. Singlet oxygen is produced past light absorption by photosensitizers and, in plants, particularly by the chlorophylls and their precursors. On the i hand chlorophylls are needed for the utilise of light free energy in photosynthesis, on the other hand, the same molecules carry the potential danger of being a singlet oxygen producer (photosensitizer).
1Otwo
has a brusk half-time of about 200 ns in cells (Gorman and Rodgers, 1992), and reacts with target molecules in the immediate neighbourhood. The possible diffusion altitude of
aneO2
has been calculated to exist up to 10 nm in a physiologically relevant situation (Sies and Menck, 1992).

In the post-obit, the reactions leading to the product of
1O2
in the antenna and reaction centres of the photosynthetic apparatus, the potential target molecules and the protection mechanism avoiding
oneOii
production, are described (Fig. i). In addition, the ‘useful’ role of
oneOtwo
will be discussed, being not simply a dissentious species but also an chemical element of signal transduction bondage leading to the specific expression of stress-related genes.

Fig. i.

Sites of production of singlet oxygen in photosynthesis and its potential targets.

Special properties of chlorophyll

Chlorophyll every bit the principal low-cal-arresting pigment in the low-cal-harvesting circuitous, the inner antenna, and also in the reaction centres, is very efficient in arresting light and has the additional advantage that the excited states are long-lived enough (up to a few nanoseconds) to allow the conversion of the excitation energy into an electrochemical potential via charge separation. If the free energy is non efficiently used, the spins of the electrons in the excited land can rephase and give rise to a lower energy excited state: the chlorophyll triplet state. The chlorophyll triplet state has an even longer lifetime (a few μs under Oii-saturated weather) and can react with
3O2
to produce the very reactive
1O2
if no efficient quenchers are effectually. Chl triplet states may be populated in principle either directly by intersystem crossing (changing of the spin) from a singlet excited chlorophyll, or past accuse recombination reactions (reversal of the charge separation and electron transfer reactions) in the reaction centres.

1O2
formation is favoured under certain physiological conditions like exposure to high light intensities or drought, leading to closure of the stomata and depression COtwo
concentrations in the chloroplasts. Under such weather condition the plastoquinone puddle can exist in a very reduced state, forward electron ship is very limited, and recombination reactions in PSII tin can occur. The kinetically limiting step of the photosynthetic electron ship concatenation is thought to be the quinol oxidation in the Qo
site of the cytochrome
b
vi
f
complex.

Quenching of chl triplet states and photoinhibition of PSII

oneO2
tin can react with proteins, pigments, and lipids and is thought to be the well-nigh important species responsible for light-induced loss of PSII activity, the deposition of the D1 poly peptide (poly peptide of the reaction centre of PSII) and for pigment bleaching (for reviews on photoinhibition, see

Prasil
et al., 1992
;

Aro
et al., 1993
).
oneO2
formation
in vivo
was measured in the leaves of
Arabidopsis thaliana
past the use of a fluorescent dye (
Hideg
et al., 2001
;

op den Campsite
et al., 2003
). Trebst and coworkers (Trebst
et al., 2002) provided evidence that
aneO2
is the of import dissentious species during photoinhibition (i.eastward. the calorie-free-induced loss of PSII activeness and of the D1 protein) of
Chlamydomonas reinhardtii
cells.

The dangerous triplet state of chlorophylls, which is the origin of the observed
1Oii, can be quenched straight by carotenoids in close proximity. The edge-to-edge altitude between the ii molecules must be less than the van der Waals distance (3.vi Å), i.e. the electron orbitals must take some overlap. In this spin substitution reaction, the triplet country of the carotenoid is formed which can either dissipate the excess free energy straight every bit heat or past physical quenching via enhanced intersystem crossing with
3Otwo
(Edge and Truscott, 1999). This possibility is given in the antenna organization, but not in the reaction centre, although two β-carotene molecules are nowadays in the PSII reaction heart (Telfer, 2002; for the location of the carotenes in the reaction centre, see
Kamiya and Shen, 2003;

Ferreira
et al., 2004
). In the reaction centre, the distance between the carotenes and the triplet chlorophyll is as well large to allow a directly triplet quenching. The redox potential of the redox couple

\(\mathrm{P}_{680}/\mathrm{P}_{680}^{{+}}\)

is very positive and a as well close contact to the carotene would pb to the efficient oxidation of the carotene. Hence the principal role of these β-carotenes is probably the quenching of
iOii
produced via the triplet state of P680
(Telfer, 2002). The latter was generated by charge recombination in PSII of the primary pair, P680Pheo.
1Oii
can react with carotenoids which act as a catalyst, deactivating
1O2.

Some other important antioxidant located in the thylakoid membrane is α-tocopherol. Tocopherol is an efficient scavenger, which becomes oxidized when reacting with
oneO2
(Trebst, 2003). Trebst
et al. (2002) showed that inhibition of tocopherol biosynthesis in
Chlamydomonas
resulted in a stimulation of low-cal-induced loss of PSII activity and D1 protein degradation. This implies that tocopherol comes shut to the site of
1Oii
generation in the reaction centre of PSII.

If
1O2
produced via chl triplet formation in the reaction centre is not quenched by carotenoids or tocopherol, it is very probable that information technology reacts with the D1 protein as a target molecule. The rapid turnover of the D1 protein occurs even at low light intensities (
Keren
et al., 1995
), indicating that there is e’er some
1O2
formation even nether depression or moderate illumination. Singlet-oxygen-generating chemicals produce the same specific fragments of the D1 poly peptide as are found under the conditions of acceptor side photoinhibition (
Okada
et al., 1996
). The degradation of the D1 protein may exist regarded equally a physiological defence force arrangement to prevent uncontrolled damage of PSII. The controlled destruction of the D1 protein seems to be an attractive prophylactic valve to detoxify
1O2
direct at the place of its generation (Trebst, 2003). Damaged D1 protein is degraded and PSII is repaired efficiently by the associates of newly synthesized D1 in the and then-called D1 protein damage–repair cycle (for reviews see

Prasil
et al., 1992
;

Aro
et al., 1993
).

With respect to photoinhibition studies, one has to differentiate between ii experimental conditions chosen in the laboratory for
in vitro
studies: the and then-called acceptor side photoinhibition which is related to the formation of
iiiP680
by charge recombination in PSII, followed by
aneO2
production and the then-called donor side photoinhibition which occurs in PSII with a non-functional or absent-minded water-splitting complex. In this state, photoinhibition is caused by the aggregating of highly oxidizing species like

\(\mathrm{Tyr}_{\mathrm{Z}}^{{+}}/\mathrm{P}_{680}^{{+}}\)

(
Jegerschöld
et al., 1990
;

Blubaugh
et al., 1991
) and is not related to
1O2
production (
Krieger
et al., 1998
).

Triplet chl formation past accuse recombination in the reaction eye of PSII

In the reaction centre of PSII, the first detectable radical pair formed later on excitation by light is

\(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}},\)

with P680
being the primary electron donor and pheophytin the primary electron acceptor (for a contempo review on PSII see

Goussias
et al., 2002
; for the 10-ray structure of PSII, see

Zouni
et al., 2001
;
Kamiya and Shen, 2003;

Ferreira
et al., 2004
). In isolated PSII reaction centres which lack QA
and a functional donor side, the main accuse pair

\(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}\)


recombines and a high yield of P680
triplet is formed (
Durrant
et al., 1990
). In the absence of oxygen, the lifetime of the triplet country is approximately ane ms and shortens in the presence of O2
to approximately 30 μs. This consequence, and the decrease in the stability of the reaction eye and bleaching of chl, were considered to exist indirect evidence for
1Otwo
formation (
Durrant
et al., 1990
).
1Oii
formation was detected straight past its luminescence (
Macpherson
et al., 1993
) and by EPR spin trapping (
Hideg
et al., 1994
).

In isolated functional reaction centres possessing a complete and fuctional donor and acceptor side, the side by side step of electron transfer afterward the formation of the main radical pair

\((\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}})\)

leads to the reduction of the primary quinone acceptor QA. Subsequently,

\(\mathrm{P}_{680}^{{+}}\)


is reduced by electron donation from the redox active tyrosine TyrZ, which itself obtains an electron from the water oxidizing complex. Forward electron transfer is much faster than accuse recombination reactions. However, charge recombination reactions can occur when the forrard electron transport cannot go along. If the principal quinone acceptor stays reduced because of a block of the forward electron transport (the so-called airtight state of the reaction center), the yield of the primary charge separation is lowered. It has been proposed that the presence of the semiquinone anion

\(\mathrm{Q}_{\mathrm{A}}^{{-}}\)


in airtight PSII may raise the energy of the primary pair by an electrostatic interaction and then that the driving strength of the primary charge separation is decreased compared with open up reaction centres (state of the middle with the oxidized quinone, QA) (van Gorkom, 1985;

Schatz
et al., 1988
). In the closed reaction heart, however, if primary charge separation occurs, it is followed by recombination of the charges. Charge recombination in the primary pair will produce either the singlet ground state of P680
or the triplet country of P680. The triplet state in the reaction eye is not localized directly on P680, i.east. the chlorophyll thought to bear the positive charge, merely delocalized to some other monomeric chlorophyll which is tilted by xxx° compared with P680
(
van Mieghem
et al., 1991
;

Kamlowski
et al., 1996
). In the presence of a large antenna (PSII
in vivo), the yield of the master pair formed in the presence of

\(\mathrm{Q}_{\mathrm{A}}^{{-}}\)


will be low (
van Mieghem
et al., 1995
).

Under reducing conditions, i.e. in the presence of dithionite and lite (
van Mieghem
et al., 1989
) or anaerobiosis and light (
Vass
et al., 1992
), QA
becomes doubly reduced, thereby releasing the negative electrostatic effect on the energy of the principal pair, and a loftier yield of accuse separation, recombination, and P680
triplet germination is observed (
van Mieghem
et al., 1989
). The double reduction of QA
and the high yield of
3P680
formation in such centres have been suggested to have some relevance to photoinhibition (
van Mieghem
et al., 1989
;

Vass
et al., 1992
). The occurrence of double reduced QA, however, has never been shown to occur nether physiologically relevant atmospheric condition.

At cryogenic temperatures (around 20 Grand), different from the situation at ambient temperature, the primary radical pair is formed with a high yield, irrespective of the redox state of QA
and the yield of the triplet land
iiiP680
is loftier both with

\(\mathrm{Q}_{\mathrm{A}}^{{-}}\)

and QAHii
(
van Mieghem
et al., 1995
). The triplet decay is much faster with

\(\mathrm{Q}_{\mathrm{A}}^{{-}}\)


than with QAH2
present. At room temperature, the yield of the primary pair is reduced in the presence of

\(\mathrm{Q}_{\mathrm{A}}^{{-}},\)


but withal, a significant yield of the primary pair is institute in core complexes of
Synechococcus
(about half of that found in reaction centres with double reduced QA) (Schlodder and Brettel, 1988;

van Mieghem
et al., 1995
). Significant amounts of singlet oxygen are produced in PSII with a large antenna nether continuous illumination (
Hideg
et al., 1994
;

Fufezan
et al., 2002
), and they are well-nigh likely linked to chl triplet formation past accuse recombination of the principal pair in PSII and non to chl triplet formation in the antenna. The production of singlet oxygen via chl triplet germination by accuse recombination reaction is shown by the post-obit experiments: (i) the induction of photoinhibition past repetitive single turnover flashes and (2) the outcome of the mid-indicate potential of the redox couple

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\(\mathrm{Q}_{\mathrm{A}}/\mathrm{Q}_{\mathrm{A}}^{{-}}\)


on the yield of singlet oxygen production.

Photoinhibition of PSII by repetitive flashes

If nighttime-adapted PSII is excited by one single turnover wink (a short saturating wink which leads to ane charge separation event in the majority of reaction centres), the state

\(\mathrm{S}_{2}\mathrm{Q}_{\mathrm{B}}^{{-}}\)

is formed, with Sii
being an oxidation land of the Mn cluster, the water oxidizing complex, and QB, the secondary quinone acceptor. In the dark, the charges recombine via the germination of the primary radical. As already described in a higher place, charge recombination of the primary radical pair leads to the production of the singlet and the triplet land of P680. The chl triplet state tin can react with
3O2
leading to the formation of
1O2
which will damage the reaction heart. This flash-induced accuse recombination reaction was exploited to investigate the mechanism of photoinhibition under depression calorie-free
in vivo
(
Keren
et al., 1995
) and
in vitro
(
Keren
et al., 1997
). Keren and coworkers used a series of single turnover flashes, spaced with a dark interval of 32 southward, and measured the degree of photoinactivation and loss of the D1 protein. The dark interval is long plenty to permit charge recombination between the Southward2
or S3
land and

\(\mathrm{Q}_{\mathrm{B}}^{{-}}\)


to occur (the half-time of

\(\mathrm{S}_{2}\mathrm{Q}_{\mathrm{B}}^{{-}}\)


recombination is approximately 20 s;
Rutherford and Inoue, 1984). When they used groups of flashes with 0.one south spacing between the flashes in ane group (for example, ii flashes with 0.1 s interval and and so 32 due south dark interval), they observed photoinhibition later an uneven number of flashes per group and no or little photoinhibition after illumination with an even number of flashes per group. An even number of flashes produced the state S3QBH2
which does not recombine, while subsequently an uneven number of flashes, charge recombination between the S2
or Due south3
state and

\(\mathrm{Q}_{\mathrm{B}}^{{-}}\)


occurs leading to singlet and triplet P680. This shows that an overall smaller number of flashes (less light absorption in total) can be more damaging than a greater number of flashes. This study was extended using Ca2+-depleted PSII preparations which were not active in water-splitting (
Keren
et al., 2000
). In Ca2+-depleted PSII, the Mn cluster is blocked in the Siii
state (for a review on Ca2+-depleted PSII see
Debus, 1992). In the unmarried turnover flash experiments, the loss of PSII activity was measured and compared with agile samples. No difference between groups of even and uneven numbers of flashes was seen in Caii+-depleted material. Using an uneven number of flashes, the activity loss was much smaller than in active samples. The yield of chief charge separation was not significantly reduced in Ca2+-depleted PSII, even later several single turnover flashes (
Keren
et al., 2000
), implying that a difference in the charge recombination pathway must be responsible for this miracle.

Influence of the redox potential of the quinone acceptor on the yield of singlet oxygen formation

In Ca2+– and also in Mn-depleted PSII not only the water-splitting action is inhibited but, in addition, the mid-signal potential of the

\(\mathrm{Q}_{\mathrm{A}}/\mathrm{Q}_{\mathrm{A}}^{{-}}\)

redox couple is up-shifted past about 150 mV. In PSII with an active h2o-splitting complex, the mid-point potential of the

\(\mathrm{Q}_{\mathrm{A}}/\mathrm{Q}_{\mathrm{A}}^{{-}}\)


couple was found to be −80 mV (Krieger and Weis, 1992;

Krieger
et al., 1995
). In centres with the high potential grade of QA
(Eastward
m
almost +65 mV), forward electron flow from QA
to QB
is energetically disfavoured and electron transfer is therefore unlikely to occur (Fig. 2) (
Johnson
et al., 1995
;

Krieger
et al., 1995
;

Andréasson
et al., 1995
). It was proposed that, in such centres, the shift of the mid-signal potential of QA
influences the pathway of charge recombination within the reaction centre of PSII. In agile PSII, with QA
in its normal, low potential form, charge recombination between the acceptor and the donor side proceeds with a loftier probability via the formation of the primary pair

\((\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}),\)


resulting in the germination of singlet and triplet P680. In centres with the high potential form of QA, the formation of the chief pair is not disfavoured (
Keren
et al., 2000
) and charge recombination may occur via an alternative pathway which does not involve the formation of excited chlorophyll species (Fig. iii; see likewise

Johnson
et al., 1995
;
Rutherford and Krieger-Liszkay, 2001). Every bit already described above, the loss of PSII action after excitation past an uneven number of flashes was about 30% less in Ca2+-depleted PSII than in active PSII. In improver, no singlet oxygen product could exist measured past spin trapping EPR with TEMP under continuous illumination (
Krieger
et al., 1998
). This shows that the change of the mid-bespeak potential of QA
is an important molecular switch for changing the charge recombination pathway within PSII. By changing the mid-betoken potential of QA
from low to loftier potential, the germination of singlet oxygen tin can be avoided.

Fig. 2.

Photosynthetic electron transport. Linear electron flow through PSII (I), cytochrome b6f complex, and PSI are shown. If forward electron transport is blocked, charge recombination reactions occur in PSII leading to the formation of triplet chl which reacts with O2 to 1O2 (II). If the water-splitting complex of PSII is inactivated (prior to photoactivation or after Ca2+-depletion), the mid-point potential of QA is shifted and charge recombination reactions are though to occur to the ground state via a safe route (III). QA ‘low potential’ is shown as a circle, QA ‘high potential’ as a diamond.

Photosynthetic electron transport. Linear electron flow through PSII (I), cytochrome
b
6
f
complex, and PSI are shown. If forrad electron transport is blocked, charge recombination reactions occur in PSII leading to the formation of triplet chl which reacts with Otwo
to
oneOtwo
(II). If the h2o-splitting complex of PSII is inactivated (prior to photoactivation or after Caii+-depletion), the mid-indicate potential of QA
is shifted and charge recombination reactions are though to occur to the ground state via a condom road (III). QA
‘low potential’ is shown as a circle, QA
‘loftier potential’ as a diamond.

Fig. 3.

Schematic diagram of the free energy levels of the states involved in recombination of the \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\mathrm{P}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\) \end{document} radical pair in PSII. The scheme shows the electron transfer reactions after illumination of a dark-adapted PSII. A series of radical pairs is formed, each with a slight loss of energy. The back reactions between these radical pairs require thermal activation and are thus thermodynamically disfavoured. It is assumed that the \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}\) \end{document} radical pair formed by back reaction from \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\mathrm{P}_{680}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\) \end{document} is at a lower energy level than that formed initially from *P680 presumably through some kind of relaxation process. When the \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}\) \end{document} radical is formed by the back reaction from the long-lived \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\mathrm{P}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\) \end{document} state, there is a high probability for the formation of a triplet state \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(^{3}[\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}]\) \end{document} because the spins had time to randomize. The triplet state of this radical pair can recombine rapidly, resulting in 3P680. 3P680 can react with 3O2 forming 1O2. The influence of herbicide binding on the mid-point potential of the redox couple \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\mathrm{Q}_{\mathrm{A}}/\mathrm{Q}_{\mathrm{A}}^{{-}}\) \end{document} is shown (dashed line). When phenolic herbicides are bound, the mid-point potential of \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\mathrm{Q}_{\mathrm{A}}/\mathrm{Q}_{\mathrm{A}}^{{-}}\) \end{document} is shifted by 50 mV to a more negative value and the back reaction via the \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}\) \end{document} radical pair is favoured. When DCMU is bound, then the mid-point potential of \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\mathrm{Q}_{\mathrm{A}}/\mathrm{Q}_{\mathrm{A}}^{{-}}\) \end{document} is shifted by 50 mV to a more positive value and this back reaction is disfavoured and direct recombination to the ground state may occur.

Schematic diagram of the free energy levels of us involved in recombination of the

\(\mathrm{P}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\)

radical pair in PSII. The scheme shows the electron transfer reactions after illumination of a nighttime-adapted PSII. A series of radical pairs is formed, each with a slight loss of free energy. The back reactions between these radical pairs crave thermal activation and are thus thermodynamically disfavoured. It is causeless that the

\(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}\)


radical pair formed by back reaction from

\(\mathrm{P}_{680}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\)


is at a lower energy level than that formed initially from *P680
presumably through some kind of relaxation process. When the

\(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}\)


radical is formed by the dorsum reaction from the long-lived

\(\mathrm{P}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\)


country, at that place is a high probability for the germination of a triplet state

\(^{three}[\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}]\)


considering the spins had time to randomize. The triplet state of this radical pair can recombine quickly, resulting in
3P680.
3P680
can react with
3Otwo
forming
1O2. The influence of herbicide binding on the mid-point potential of the redox couple

\(\mathrm{Q}_{\mathrm{A}}/\mathrm{Q}_{\mathrm{A}}^{{-}}\)


is shown (dashed line). When phenolic herbicides are leap, the mid-point potential of

\(\mathrm{Q}_{\mathrm{A}}/\mathrm{Q}_{\mathrm{A}}^{{-}}\)


is shifted by 50 mV to a more negative value and the back reaction via the

\(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}\)


radical pair is favoured. When DCMU is bound, then the mid-bespeak potential of

\(\mathrm{Q}_{\mathrm{A}}/\mathrm{Q}_{\mathrm{A}}^{{-}}\)


is shifted by 50 mV to a more than positive value and this dorsum reaction is disfavoured and directly recombination to the ground state may occur.

This regulation mechanism of PSII may be of physiological importance. PSII is assembled without the Mn cluster and with QA
in the high potential course (
Johnson
et al., 1995
). In the light, during the so-chosen photoactivation process, the Mn cluster is assembled and the mid-signal potential of QA
is switched from loftier potential to the low potential form, which allows linear electron flow. In the state prior to complete assembly of the functional water-splitting complex, PSII is protected confronting photodamage induced by
1O2
formation. Under high low-cal conditions, the alter of the mid-signal potential of QA
may likewise exist involved in the pH-dependent control of PSII activity. In improver to the dissipation of excess energy by the formation of zeaxanthin in the antenna (for a review see
Demming-Adams, 1990), the activity of the electron transfer tin be altered at the level of the reaction heart of PSII (reaction heart quenching). When, in backlog light, the pH in the lumen decreases below a certain threshold value, up to 1 Ca2+
per PSII can exist released and the mid-point potential of QA
is thereby switched to the high potential form (Krieger and Weis, 1992). This was demonstrated in thylakoid membranes, in which a proton gradient was maintained by ATP-hydrolysis in the dark, by measuring the chlorophyll fluorescence at the
F
o-level at different redox potentials equally a measure out for the reduction land of QA
(Krieger and Weis, 1993).

Information technology is nevertheless unclear how the action state of the water-splitting complex at the donor side is continued to the mid-point potential of the quinone at the acceptor side of PSII. 1 possibility is that, upon the release of Ca2+, a structural modify in a poly peptide subunit of the reaction centre and peculiarly at the QA
binding site occurs, which could exist responsible for the observed change in the mid-point potential. It might as well exist possible that cytochrome
b
559
mediates between the donor and acceptor sides. In inactive and non-photoactivated PSII, cytochrome
b
559
is in the depression potential course and changes upon the assembly of the Mn to the high potential form, characteristic for the active PSII (for review, run into
Stewart and Brudvig, 1998). The change of the potential form of cytochrome
b
559
was already observed before the process of photoactivation was fully completed (
Mizusawa
et al., 1997
).

Influence of herbicides on the mid-bespeak potential of QA
and on singlet oxygen production

The influence of unlike herbicides on the mid-signal potentials of the primary quinone acceptor QA
(Krieger-Liszkay and Rutherford, 1998) and unmarried point mutations in D1 (
Rappaport
et al., 2002
) or in D2 (Vavilin and Vermaas, 2000) tin be used equally a tool to investigate the charge recombination pathways in PSII. Binding of herbicides to the QB
binding site of the D1 protein inhibits linear electron flow and affects the degree of photoinactivation and light-induced deposition of the D1 protein.
In vitro, the urea herbicide DCMU and related herbicides have been reported to retard photodamage (
Keren
et al., 1995
,
1997;

Kirilovsky
et al., 1994
) and deposition of the D1 protein (
Keren
et al., 1995
,
1997;

Nakajima
et al., 1996
;

Jansen
et al., 1993
;
Zer and Ohad, 1995). By contrast with DCMU, phenolic herbicides, which also bind to the QB-binding site, accept the opposite event and stimulate the susceptibility of PSII to light (Pallett and Dodge, 1980;

Nakajima
et al., 1996
) and the degradation of D1 (
Jansen
et al., 1993
). Binding of these herbicides to the QB
binding site influence the mid-bespeak potential of QA. Phenolic herbicides lower the mid-indicate potential past approximately 45 mV and DCMU raises it by nigh l mV (Krieger-Liszkay and Rutherford, 1998). A smaller difference of 60 mV betwixt the redox potential in the presence of bromoxynil and in the presence of DCMU was reported by

Roberts
et al. (2003)

when estimated from the dorsum reaction rate of

\(\mathrm{S}_{two}\mathrm{Q}_{\mathrm{A}}^{{-}}.\)

The issue of the different types of herbicide on the mid-betoken potential of QA
was not merely observed for the low potential form but likewise for the high potential course of QA
(Krieger-Liszkay and Rutherford, 1998). The accented modify in the mid-point potential of QA
by these herbicides was much lower (±50 mV) than the shift induced by inactivation of the water-splitting complex (Ca2+– or Mn-depletion), merely it has, however, a big consequence on the yield of
1O2
production. The molecular ground for the shift of the mid-point potential of QA
by bounden a herbicide to the QB
binding pocket is not understood. FTIR spectra of QA
obtained in the presence of a phenolic herbicide compared with DCMU indicate that the protein surroundings of QA
is slightly modified by the phenolic herbicide. The change seen in the spectra is small and approximately in the range of 1 H-bonding (J Breton and A Krieger-Liszkay, unpublished information).


Fufezan
et al. (2002)

showed that the yield of
oneO2
production in the presence of a phenolic herbicide in active PSII-enriched membrane fragments (with QA
in the low potential form) is twice every bit high as in the presence of DCMU. This effect is already seen at relatively low low-cal intensities (400 μmol quanta grand−2
s−1) and the amount of
1O2
produced increases linearly with increasing lite intensities. In bacterial reaction centres it has been shown that the costless energy gap between the

\(\mathrm{P}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\)

radical pair and the P+BPheo
radical pair has a major influence on the back reaction pathway (
Gunner
et al., 1982
;

Gopher
et al., 1985
;

Woodbury
et al., 1986
;
Shopes and Wraight, 1987). When the gap is smaller than 400 meV, the back reaction via the main pair (P+BPheo) dominates, while under conditions where the gap is greater than this value, a straight recombination pathway dominates

\((\mathrm{P}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}{\rightarrow}\mathrm{PQ}_{\mathrm{A}}).\)


This direct recombination pathway involves electron tunnelling reactions. Based on these observations made with the bacterial reaction centre a model was proposed (Fig. 3) showing the influence of the mid-point potential of QA
on the charge recombination pathway within PSII (Krieger-Liszkay and Rutherford, 1998;
Rutherford and Krieger-Liszkay, 2001). It seems likely that the modulation of the mid-indicate potential of QA
by the land of the water-splitting complex and past the herbicides volition influence the free energy gap between

Popular:   Find the Values of X and Y

\(\mathrm{P}_{680}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\)


and

\(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}.\)


With DCMU information technology is predicted that the increase in the mid-bespeak potential should increase the energy gap and thereby diminish the yield of dorsum reaction via the

\(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}\)


radical pair. By illustration to the bacterial reaction center a direct recombination via

\(\mathrm{P}_{680}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\)


may take place which does non result in the formation of excited singlet or triplet states of P680. This model may explain the lower product of
iO2
observed in the presence of DCMU in centres with low potential QA
(
Fufezan
et al., 2002
) and the absenteeism of
1Otwo
formation in PSII with high potential QA
(
Krieger
et al., 1998
).

On the other hand, the decreased mid-point potential of QA
induced by phenolic herbicides should make the energy gap between

\(\mathrm{P}_{680}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\)

and

\(\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}}\)


smaller and, therefore, the back reaction via the master radical pair and the formation of P680
triplet more likely.


Rappaport
et al. (2002)

investigated the influence of the mid-point potential of the Pheo/Pheo
redox couple on charge recombination between

\(\mathrm{S}_{2}\mathrm{Q}_{\mathrm{A}}^{{-}}\)

and showed that the recombination rate is sensitive to the free energy gap between Pheo and QA. They used mutants of
Synechocystis, in which the mid-signal potential of Pheo/Pheo
was shifted past +33 mV or −74 mV compared with the wild blazon. The mutant with the potential shift of +33 mV showed an increment in the recombination rate

\((\mathrm{P}_{680}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}})\)


by a factor of four (measured as the decay of fluorescence after a saturating flash), while lowering of the mid-point potential slowed down the recombination past the same factor. This demonstrates that accuse recombination via the germination of the primary radical pair

\((\mathrm{P}_{680}^{{+}}\mathrm{Pheo}^{{-}})\)


is a meaning process in PSII reaction centres in which forward electron flow is blocked. In add-on they demonstrated that the direct charge recombination pathway which does not involve the repopulation of the chief pair is significant in the mutant with the lowered mid-indicate potential of Pheo/Pheo. In a unlike set of experiments, mutations in the CD loop of the D2 protein were made in
Synechocystis
(Vavilin and Vermaas, 2000). These mutants show a temperature shift and a decrease in intensity in the thermoluminescence ring originating from

\(\mathrm{S}_{ii}\mathrm{Q}_{\mathrm{A}}^{{-}}\)


recombination. This was interpreted as an increment of the proportion of the directly recombination pathway of the

\(\mathrm{P}_{680}^{{+}}\mathrm{Q}_{\mathrm{A}}^{{-}}\)


pair which does non lead to the germination of an excited chlorophyll.

Accuse recombination and chl triplet formation in the reaction centre of PSI

In PSI, under reducing atmospheric condition when the iron sulphur clusters are prereduced or when vitamin K1 is removed from the reaction centre, charge recombination reactions likewise occur leading to the triplet country of P700
at room temperature (for a review meet
Brettel, 1997). In PSI, the lifetime of the state
3P700
is about 6 μs and is not shortened by
3O2, indicating that P700
is screened from O2
(Sétif
et al., 1981).

iO2
production by the cytochrome
b
half dozen
f
complex

Illumination of the isolated cytochrome
b
half dozen
f
complex results in the formation of
aneO2, as shown past spin trapping techniques and the effects of azide, a
1Oii
quencher, and D2O, which extends the lifetime of
1O2
(
Suh
et al., 2000
). Information technology was shown by

Suh
et al. (2000)

that the Fe-S cluster of the Rieske protein and not the cytochromes are responsible for the
1O2
product in the light. The extent to which
1Oii
generated past the cytochrome
b
half dozen
f
complex contributes to photoinhibition of PSII is unclear. The cytochrome
b
6
f
complex contains, in addition to the other cofactors, one chlorophyll with an unknown function. In principle, this chlorophyll could too be involved in
1O2
formation interim as a photosensitizer.

Chlorophyll triplet and singlet oxygen production in the antenna

Chlorophyll triplet states and consecutive
1Otwo
formation is not only produced by charge recombination in the reaction centre, merely too by intersystem crossing from a singlet excited chlorophyll in the antenna. In addition, excited states of chlorophyll precursors can lead to the formation of
oneO2.

In isolated poly peptide/pigment complexes, the rate of intersystem crossing is significant (Kramer and Mathis, 1980) and the formation of triplet chlorophylls in the antenna has been shown
in vitro. These states can be distinguished by their spectroscopic characteristics from the triplet chlorophyll in the reaction center and they do not depend on the redox potential of the medium (
Santabarbara
et al., 2002
). 2 of these triplet states are probably generated in the core complex while the 3rd one may be generated in the light-harvesting complex (
Santabarbara
et al., 2002
). Formation of
1Otwo
from isolated LHCII has been shown
in vitro
by spin trapping with TEMP (
Rinalducci
et al., 2004
). Singlet oxygen may also play a role in the deposition of low-cal-harvesting proteins. The deposition of LHCII is much slower than the degradation of the D1 protein (
Lindahl
et al., 1995
), only modifications of the poly peptide are already visible later a few hours of low intensity illumination (100 μmol quanta m−2
s−i) in the isolated complex (Zolla and Rinalducci, 2002). Deposition of LHCII releases a large number of chl. Light-induced harm might occur from such chl which is energetically uncoupled from the antenna, and will give a loftier triplet chl and, therefore, possibly loftier
aneOtwo
yield. Nevertheless, experimental evidence for the product of
oneO2
past triplet formation in the antenna and their involvement in the lite-induced damage in PSII
in vivo
in mature leaves is still missing. In the antenna
3chl will exist efficiently quenched by nearby carotenoids, so that
3chl, although formed with a college probability than by accuse recombination in the reaction heart, will rarely be a problem.

Production of triplet chlorophyll and
oneO2
may play a role during the transition from etioplasts to chloroplasts. In greening material, disorganized chlorophyll may act every bit a photosensitizer (
Marder
et al., 1998
). Oxygen uptake by thylakoid membranes, isolated from greening material, was measured. Oxygen uptake was significantly quenched by β-carotene and α-tocopherol, indicating that production of singlet oxygen was measured by this method (
Caspi
et al., 2000
). Protochlorophyllide acts also as photosensitizer, as shown for the
Arabidopsis
mutant
flu
(
op den Military camp
et al., 2003
). In this mutant, a protein is inactivated which plays a key office during the negative feedback control of chlorophyll biosynthesis. Equally a issue, the mutant accumulates free protochlorophyllide in the dark. In this study, the production of
iO2
was shown in leaves by quenching of the fluorescent dye DanePy
in vivo
subsequently a night–low-cal transition of the plants (
Hideg
et al., 1998
;

op den Camp
et al., 2003
). Information technology was besides shown previously, by the use of herbicides which cake the protoporphyrinogen oxidase, that protoporphyrin IX is a photodynamic pigment which produces high amounts of
1O2
in the lite (Becerril and Duke, 1989).

iO2
may also be produced by free chlorophyll and chlorophyll degradation products which may be produced during strong photoinhibition. If the light-induced damage exceeds the controlled D1 deposition and repair of PSII, further protein degradation of chl binding subunits may lead to the product of free chls, which are unsafe photosensitizers. These free chls may be jump by ELIP (Early Calorie-free Induced Proteins) proteins (Adamska, 1997) or by proteins like WSCP (Water Soluble Chlorophyll Protein) (
Schmidt
et al., 2003
). The binding of chl to the WSCP reduces the yield of
1O2
production by a nonetheless unknown mechanism. This protein is an unusual chl-bounden protein in the sense that information technology does non bind carotenoids, but, nevertheless, efficiently protects spring chl against photodegradation and reduces the yield of
oneOii
product.

Cistron expression in response to
1O2
formation

In that location are recent reports in the literature that, equally a response to
1Otwo
production, genes are specifically up-regulated which are involved in the molecular defence response of the plant against photo-oxidative stress (
Leisinger
et al., 2001
;

op den Army camp
et al., 2003
; B Fischer, personal communication).

Leisinger
et al. (2001)

showed that, in the presence of photosensitizers like Rose Bengal, a glutathione peroxidase homologous factor from
Chlamydomonas
is transcriptionally up-regulated past
1Otwo, while the mRNA level of this gluthathione peroxidase is simply weakly expressed by exposure to superoxide or peroxide.

Op den Camp
et al. (2003)

used the flu mutant of
Arabidopsis
to prove that the accumulation of protochlorophyllide and thus the loftier yield of
1O2
formation past transferring these plants from dark to light rapidly activated a number (70) of genes. By contrast, other reactive oxygen species like superoxide did not rapidly up-regulate the expression of these genes. In the
influenza
mutant,
1O2
is produced peripherally at the membrane surface and tin can, therefore, react with compounds of the stroma. Nether natural atmospheric condition,
1O2
volition be produced within the reaction centre of PSII and volition react with dissimilar target molecules than in this mutant. Fischer, even so, using inhibitors of the photosynthetic electron transport, studied
1O2
formation in PSII and simply found a significant upward-regulation of the glutathione peroxidase homologous factor from
Chlamydomonas
(B Fischer, personal advice).

The question arises how an extremely short-lived molecule like
1Oii
can give ascension to a betoken that tin can be transmitted to the nucleus to regulate gene expression. Some other reactive oxygen species like superoxide or peroxide take been shown to act direct as 2nd messengers in the regulation of expression of the oxidative stress response genes such as gutathione peroxidases, glutathione-South-transferases, and ascorbate peroxidase (for reviews see

Mullineaux
et al., 2000
;

Vranová
et al., 2002
). Considering of the brusk lifetime of
1O2, it tin be excluded that it oxidizes a component of a betoken transduction chain directly. Instead reaction products originating either from the D1 protein degradation or products of chlorophyll degradation can exist envisaged every bit signal molecules. It has been shown that chlorophyll precursors like Mg-protoporphyrin Nine can human activity as a signalling molecule in a signalling pathway betwixt the chloroplasts and the nucleus (
Strand
et al., 2003
). By analogy, one tin can also speculate that a chlorophyll degradation product such equally pheophytin, chlorophyllide, or pheophorbide (for chl degradation, come across

Matile
et al., 1999
) may act as a signalling molecule. Such a molecule could be transported out of the chloroplast to the cytosol past an ABC protein where it mediates a indicate to the nucleus to regulate the expression of genes. It has been shown that a functional ABC protein is required for the transport of protophorhyrin IX (
Møller
et al., 2001
). It was likewise shown that an ABC transporter in the tonoplast membrane can transport chlorophyll catabolites to the vacuole (
Lu
et al., 1998
), making it likely that such a transport mechanism is also present in the chloroplast envelope membrane.

Alternatively, lipid peroxides may role as signalling molecules considering unsaturated fatty acids are the preferred targets of
iO2. However, no increase in
1Otwo-mediated non-enzymatic lipid peroxidation could exist found in the
flu
mutant, which accumulates protochlorophyllide and shows a higher yield of
1Otwo
formation than wild-type plants (
Op den Military camp
et al., 2003
). Linolenic acid was rapidely oxidized upon illumination of the
flu
mutant, merely the oxidation patterns observed were indicative for enzymatic oxidation and not for not-enzymatic oxidation by
1Otwo. In general, fat acid-derived signals may be involved in signalling pathways connected with jail cell death and the expression of stress-related genes (Weber, 2002).

Abbreviations: chl, chlorophyll; DCMU, 3-(3,4-dichlorophenyl)-i,1-dimethylurea; P680, main electron donor in PSII; Pheo, pheophytin (primary electron acceptor in PSII); PS, photosystem, QA, main quinone acceptor in PSII; QB, secondary quinone acceptor in PSII; TEMP, two,ii,6,6-tetramethylpiperidine-i-oxyl; TyrZ, redox active tyrosine of the D1 poly peptide; Southward2, Siii, oxidation states of the Mn cluster.

I thank North Bondarava, B Fischer, C Fufezan, S Panahandeh, A Telfer, and A Trebst for stimulating discussions and critical reading of the manuscript.

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How Does Oxygen Production Relate to the Rate of Photosynthesis

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