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ISSN 1990-7478, Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology, 2007, Vol. 1, No. 3, pp. 185–205. © Pleiades Publishing, Ltd., 2007.
Original Russian Text © V.D. Kreslavski, R. Carpentier, V.V. Klimov, N. Murata, S.I. Allakhverdiev, 2007, published in Biologicheskie Membrany, 2007, Vol. 24, No. 3, pp. 195–217.
185
In nature, plants are often subject to deleterious
effects of an immense diversity of environmental fac-
tors, e.g., heat, cold, high salinity of soils, intense light,
etc. All these factors induce stress reactions, which lead
to inhibition of many physiological functions in plant
organisms. As a rule, several such factors act on plants
simultaneously, but stress responses are mediated by
similar protective and adaptive mechanisms. For exam-
ple, cold acclimation can generate osmotic shock [1],
whereas high salinity is often accompanied by ionic
and osmotic stresses [2, 3]. Photoinhibition induced by
salinization, heat or cold shock alters the lipid compo-
sition and fluidity of thylakoid membranes and thus
affords effective protection of cells against stress of
various kinds [4–11].
Extreme temperatures and high salinity stimulate
the production of reactive oxygen species (ROS). In
photosynthesis, ROS are largely formed during elec-
tron transport [12–14] and
ëé
2
assimilation [15] in
chloroplasts. Excess ROS production is one of the rea-
sons for low activity of chloroplast-specific enzymes
with enhanced sensitivity to oxidative stress (OS), low
ATP levels and structural rearrangements in the thyla-
koid membrane [16]. According to the recently pro-
posed hypothetical scheme, the
de novo
synthesis of D1
and other photosynthetic proteins is inhibited by excess
ROS, most probably, in the translation step of
psbA
mRNA, as can be evidenced from the increase in intra-
cellular
ç
2
é
2
[17] and singlet oxygen [18]. Protein
synthesis and, correspondingly, recovery of the photo-
damaged PS II induced by salt stress, high and low tem-
peratures are inhibited in a similar way [19].
ROS generated under stress take part in the transfer
of signals triggering protective and adaptive mecha-
nisms of the cell [20–22], in particular at the level of
photosynthetic reactions [23]. Other universal messen-
gers in the chain transducing stress signals include lip-
ids, proteins, and Ca
2+
[11, 22, 24, 25].
Under moderate stress, PA injuries are usually
reversible and are eliminated with time. However, irre-
spective of its origin, high-level OS generates intense
oxidative processes resulting in lipid peroxidation and
degradation of proteins and nucleic acids [16, 23, 26,
27]. As a result, the damage of PA, first of all, of thyla-
koid membranes, becomes irreversible.
Stress increases the intracellular content of ROS,
which in the case of severe stress triggers irreversible
changes in PS II and other photosynthetic systems [16,
28]. Moderate stress provoked by heat, cold, and salin-
ization is associated with photoinactivation, inhibition
of protein synthesis, and recovery of the photodamaged
PS II, but not with its direct damage [19, 29].
Under physiological conditions, PS II manifests
higher sensitivity to photodamage than many other PA
systems [26, 30, 31]. By illustration, the PS II of the
REVIEWS
Molecular Mechanisms of Stress Resistance
of the Photosynthetic Apparatus
V. D. Kreslavski
a
, R. Carpentier
b
, V. V. Klimov
a
, N. Murata
c
, and S. I. Allakhverdiev
a
a
Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow oblast, 142290 Russia
b
Groupe de Recherche en Biologie Végétale, Université du Québec à Trois-Rivières, C.P. 500, Québec, Canada, G9A 5H7
c
National Institute for Basic Biology, Okazaki 444-8585, Japan
e-mail: vkreslav@mail.ru, suleyman@issp.serpukhov.su
Received January 16, 2007
Abstract
—The mechanisms of action of environmental stress-inducing factors on the photosynthetic apparatus
(PA) of plants are considered. The basic targets for stress produced by heat, cold, salinity, osmotic imbalance,
and high irradiance are analyzed. It is suggested that stress factors have an influence on the composition of thy-
lakoid membranes and inhibit photosynthetic processes. However, recent studies demonstrated that strong light
induces the photodamage to photosystem II (PS II) due to direct action of light on the oxygen-evolving complex.
Stress-induced accumulation of reactive oxygen species (ROS) leads to inhibition of the recovery of the PSII by
suppressing the
de novo
synthesis of photosynthetic proteins. In addition, stress stimulates the synthesis of protec-
tive low-molecular weight compounds (e.g., glycine betaine) and stress proteins. The major mechanisms of accli-
mation and protection of the PA against damaging effects of environmental stress-inducing factors are analyzed
with special reference to cyanobacterial cells and mutants with high or low stress resistance.
DOI:
10.1134/S1990747807030014
Abbreviations
: ROS, reactive oxygen species; HSP, heat shock pro-
teins; GB, glycine betaine; OEC, oxygen-evolving complex; OS,
oxidative stress; LHC, light-harvesting complex; PS, photosystem;
RC, reaction center; PA, photosynthetic apparatus; ETC, electron
transport chain; Chl, chlorophyll; SOD, superoxide dismutase.
186
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KRESLAVSKI et al.
cyanobacterium
Synechocystis
sp. PCC 6803 is much
more sensitive to photoinhibition than PS I [32].
Cells of aerobic microorganisms possess several
protective mechanisms against OS. One of them con-
sists in the activation of an antioxidative protective sys-
tem, which eliminates the negative effect of stress by
converting ROS into nontoxic products [21, 33–36].
The activities of antioxidant enzymes and low-molecu-
lar-mass components increase in response to ROS
accumulation [12, 13, 34, 37], particularly in chloro-
plasts, the main site of ROS formation in plant leaves
This is achieved at the expense of activation of ascor-
bate–glutathione cycle enzymes [14], superoxide dis-
mutase (SOD), Fe and Cu–Zn [36], as well as Fe–SOD,
Cu–Zn–SOD, and other antioxidant enzymes.
Stress initiates the synthesis of many specific “pro-
tective” compounds including heat shock proteins
(HSP), amino acids, osmotically active compounds,
abscisic acid, carotenoids, etc. Changes in the lipid
composition of membranes, e.g., in the ratio between
unsaturated and saturated fatty acids [4–6, 8, 9], also
fulfil a protective function of special interest is
enhanced synthesis of enzyme isoforms resistant to a
particular type of stress. An alternative mechanism con-
sists in inhibition of plant growth and photochemical
reactions in chloroplasts [7]. The toxic products formed
thereupon are excreted from the cell by virtue of their
ability to bind to specific carrier proteins [38] or to be
accumulated in definite cell compartments [7].
The effects of stress on photosynthesis are usually
studied in cell cultures, most frequently, in cultured
cyanobacteria. The main advantage of such cultures is
their ability for oxygenic photosynthesis and similarity
of their PA to those of higher plants [39]. Moreover,
cyanobacteria are easily adapted to stress of any kind
and are devoid of the cytoplasmic membrane, which
prevents the penetration of exogenous compounds
inside the cell. And, last but not least, antioxidative sys-
tems are rather extensively studied [32, 40, 41].
Intracellular regulatory systems are subdivided into
metabolic, membrane and genetic systems. This classi-
fication is arbitrary, of course, since all these systems
are mutually interrelated. Therefore, the mechanisms
underlying the damage and adaptation of plants to
stress are examined at the level of the aforementioned
systems.
Photosynthesis, which provides energy for the vital
activity of plants, is one of the main metabolic mecha-
nisms responsible for the stress resistance of plants. Of
particular interest in the study of photosynthesis are
extreme temperatures and high salinity in combination
with intense or low light, since plants are especially
often exposed to various effects of these factors. As
photosynthesis takes place in chloroplasts, the integrity
and state of thylakoid membranes and efficient func-
tioning of PS play a key role in the resistance and adap-
tation of plants to stress. The effects and mechanisms of
action of some typical environmental stresses are con-
sidered in this review.
PHOTOINHIBITION
If the intensity of the light exceeds that of saturating
values for photosynthesis, the activity of the PA in
plants grown under low-illumination conditions, espe-
cially that of the PS II (manifested as photodamage or
photoinhibition), is decreased [42, 43]. The PS II is the
main target for photoinhibition; The PS I is also sub-
jected to inhibition, however, in a lesser degree [44].
Photoinhibition implements an important protective
function by suppressing electron transport at intense
light and by inducing the formation of photochemically
inactive reaction centers (RC) in the PS II, in which
light energy is transformed into heat energy [43, 44].
Photodamage targets and protective mecha-
nisms.
Previous studies showed that light-induced inju-
ries are predominantly localized in RC of the PS II and
are determined by the rates of degradation and resyn-
thesis of D1, one of the key proteins of the PS II [30, 31,
45–47]. This protein is synthesized at much higher rates
in comparison with other intrinsic proteins of the thyla-
koid membrane [48].
As a rule, light-induced injuries of photosystems are
studied in vitro, e.g., in isolated thylakoid membranes.
In intact cells, photodamage is usually accompanied by
a repair of the photodamaged PS II; therefore, photoin-
hibition in vivo is a result of imbalance between the
photodamage and repair of the photodamaged PS II
[17, 29, 49]. Studies with cyanobacterium cells made it
possible to draw a demarcation line between these two
processes. A new concept for photoinhibition of PS II
by light of different intensities has been developed
recently [10, 17, 18, 29, 49–54].
In the paradigm of the new concept, the oxygen-
evolving complex (OEC) or, more precisely, its manga-
nese-containing cluster, is the primary target for photo-
damage, while the photochemical RC is the secondary
target. Another target for ROS is the repair system of
PS II, but not RC [19, 29, 49, 55, 56].
Let us consider these data in more detail. Photosyn-
thetic electron transport yields a vast variety of ROS,
e.g., singlet oxygen, superoxide radicals
( ), ç
2
é
2
,
and OH-radicals [21, 57]. Under excess light, part of
absorbed light energy is not utilized by photosynthesis
as a result of which the rate of ROS production
increases appreciably. There is ample evidence sug-
gesting the involvement of ROS in the photodamage of
PS II [30, 46]. Thus, it was shown that in model sys-
tems, such as thylakoid membranes or PS II particles,
the degradation of the D1 protein is stimulated by OH
radicals [58] and [59, 60]. However, all these stud-
ies were carried out either in vitro or without separation
of the effects of environmental stress on direct damage
to PS II and its repair. This failing was overcome in
O2
–
O
1–
2
BIOCHEMISTRY (MOSCOW) SUPPLEMENT SERIES A: MEMBRANE AND CELL BIOLOGY
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MOLECULAR MECHANISMS OF STRESS RESISTANCE 187
experiments carried out by Murata et al. [10, 17, 18, 29,
52–54] who studied the putative role of ROS in photo-
inhibition of intact cells with a full-value antioxidant
system in vivo. It was found [17] that the OS inducers
such as
ç
2
é
2
and methylviologen suppress the activity
of PS II not directly, but through inhibition of the recov-
ery of the photodamaged PS II. Western blot analysis
demonstrated that the synthesis of the D1 protein is
inhibited in the presence of
ç
2
é
2
and methylviologen.
The results of Northern and Western blotting analysis
suggest that ROS predominantly inhibit the translation
of the
psbA
gene encoding the protein D1 precursor,
which is consistent with the fact that the
katG
–
/
tpx
–
mutant cells with a deficient
ç
2
é
2
-neutralizing system
are highly sensitive to PS II photodamage [17]. It was
also found that
ç
2
é
2
-utilizing enzymes, such as cata-
lase/peroxidase [40] and thioredoxin peroxidase [61]—
katG
and
tpx
gene products, maintain low concentra-
tions of
ç
2
é
2
in cyanobacterium cells. Mutation in the
katG
and
tpx
genes enhances the photodamage of PS II;
however, no such effect is observed in the presence of
the protein synthesis inhibitor chloroamphenicol.
These findings provide additional support in favor of
the crucial role of ROS in inhibition of recovery of pho-
todamaged PS II [17].
A crucial role in this process is played by singlet
oxygen [18, 49]. Photosynthetically generated singlet
oxygen is a potent oxidant inducing the damage of a
vast variety of biologically active photosystem compo-
nents. Visible changes in PS II are induced by high con-
centrations of singlet oxygen in the presence of Rose
Bengal or ethyl eosin. However, in the presence of chlo-
roamphenicol, which stimulated real changes in PS II,
these compounds had no such effect [18]. This indi-
cates that the recovery of photodamaged PS II is inhib-
ited by singlet oxygen. Studies with [
35
S
]methionine-
labeled proteins demonstrated that singlet oxygen
inhibits the activity of photosynthetic proteins includ-
ing that of D1 protein. However, according to Northern
blotting data, singlet oxygen does not influence the
accumulation of the
psbA
RNA encoding the D1 pre-
cursor (Fig. 1). It was conjectured that the activity of
singlet oxygen is specifically manifested in the elonga-
tion step of protein translation [18].
This mechanism is only one of the few mechanisms
responsible for photodamage of PS II in strong light
[18, 45, 49, 55, 62–65]. The most important of them are
as follows [29, 49, 55]:
(1) Damage of the “acceptor side” of PS II.
(2) Damage of the “donor side” of PS II.
(3) Damage by low-intensity light.
(4) Damage by singlet oxygen and/or other ROS.
According to the first and the third mechanisms,
triplet chlorophyll (Chl) is formed in the course of the
electron transport along the electron transport chain
(ETC). In the framework of the “acceptor side” mecha-
nism, this is achieved at the expense of the double
reducing of
Q
A
[64], which favors the formation of trip-
let Chl P680 in RC of the PS II. At low light, this is
accompanied by the recombination of charges between
or and oxidized states
S
2.3
on the donor side of
the PS II [49], which also stimulates the generation of
triplet Chl:
3
ê680 +
3
é
2
ê680 +
1
é
2
[66]. The sin-
glet oxygen formed thereupon causes the degradation
of the D1 protein [45]. Obviously, the “acceptor side”
mechanism fails to elucidate the relationship between
the initial rate of photodamage and light intensity [18,
52]. At low light, the recombination of charges between
or and the oxidized states on the “donor side”
of PS II (
S
2.3
) is accompanied by generation of the trip-
let state of Chl responsible for the production of singlet
oxygen [67]. The “donor side” mechanism is based on
acidification of the lumen as a result of proton transport
with subsequent inactivation of OEC and formation of
the long-living cation-radical,
ê680
+
, responsible for
the degradation of D1 [49, 63, 65]. Supporting evidence
was obtained in experiments with PS II complexes
in vitro.
However, neither the first, nor the second or third
mechanisms are consistent with the in vivo data accord-
ing to which direct photodamage of PS II correlates
with light intensity, but is insensitive to oxygen, and, as
a consequence, to ROS. Moreover, it depends on the
electron transport in the photosynthetic chain, since
inhibition of electron transport by 3,4-dichlorophe-
nyldimethylurea (DCMU) has no effect on the correla-
QA
–
QB
–
QA
2– QB
2–
NaCl
NaCl
H
2
O
2
1
O
2
psbA
genes
psbA
mRNA Pre
-D1-1
Pre
-D1-2
Protein
D1
Degradation
Fig. 1.
A scheme of
psbA
gene expression and protein D1
synthesis (hypothetical targets for inhibiting effects of salt-
and photoinduced stress [50]). Pre-D1-1 and pre-D1-2, pro-
tein D1 precursors. The D1 protein is encoded by
psbA
genes.
188
BIOCHEMISTRY (MOSCOW) SUPPLEMENT SERIES A: MEMBRANE AND CELL BIOLOGY
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KRESLAVSKI et al.
tion between the initial rate of
Synechocystis
photodam-
age and light intensity [18, 52]. Moreover, this correla-
tion is not disturbed either upon oxygen elimination or
during inhibition of electron transport suggesting the
presence of a photoreceptor in PS II. The action spec-
trum of such photoinhibition displays characteristic
bands in the UV and blue regions [55, 68]. The action
spectrum of this photoinhibition was compared to the
absorption spectra of different components of PS II of
thylakoid membranes of higher plants [55]. It was
assumed [18, 49, 52, 68] that absorption of light quanta
by the manganese cluster of OEC with subsequent dis-
sociation of excited manganese ions [55, 56] and for-
mation of the long-living species,
ê680
+
, is the primary
reaction in this photodamage.
ê680
+
is a potent oxidant
(oxidative potential, 1.12 V) [69] able to induce the
degradation of the D1 protein [31].
The conclusion about the crucial role of manganese
clusters in photodamage is consistent with the results
obtained during irradiation of thylakoid membranes of
Thermosynechococcus elongatus
[56], pea and pumpkin
[55] with UV-A and blue light. It was found that PS II
photodamage occurs in two steps. UV and blue light
inactivate OEC at much faster rates than the photo-
chemical RC of the PS II. However, the latter was inac-
tivated upon subsequent illumination with red light. It
is thought that light-induced injuries mainly affect the
OEC components of PS II, which absorb UV and blue
light. It thus appears that the biphasic photodamage
mechanism corresponds to two transient stages of PS II
damage, namely, Stage I (light-induced inactivation of
OEC) and Stage II (inactivation of RC of the PS II by
light (predominantly, red light) absorbed by Chl).
Irreversible photoinhibition of PS II is manifested
during long-term illumination of
Synechocystis
sp. PCC
6803 cells with high intensity light [10]. If wild type
strain cells are irradiated at light intensity of 2500
µ
M
photons
⋅
m
–2
⋅
s
–1
(20
°
C, 2 h), the inhibition of
é
2
evo-
lution is irreversible and complete, while inactivation
of photochemical RC of the PS II is reversible. In
experiments with
desA
–
/
desD
–
mutants, irreversible
photoinhibition was enhanced at low temperatures
and low viscosity of cell membranes. The results of
Western and Northern blotting studies suggest that
irreversible photoinhibition of these cells was accom-
panied by the synthesis of the D1 precursor, but not
the active form of protein D1. This suggests that long-
term exposure of
Synechocystis
cells to strong light
leads to irreversible photoinhibition of the oxygen-
evolving activity of PS II due to disturbances in the
protein D1 precursor during its modification into the
active form. This effect is enhanced with an increase
in the ratio of saturated/unsaturated fatty acids charac-
teristic of
desA
–
/
desD
–
mutants [10].
It is currently known that electron transport and high
ATP content play a crucial role in the maintenance of
protein synthesis, including that of D1 [30, 31] and are
essential for the repair of PS II in the course of photo-
inhibition, but are not critical in the case of direct pho-
todamage of PS II [18]. Evidence for this hypothesis
was obtained in experiments with cyanobacterium
(
Synechocystis
sp. PCC 6803) cells [53]. It was found
that neither the inhibition of electron transport in PS II,
nor high rates of electron transport in PS I or inhibition
of ATP synthesis influenced the rate of this photodam-
age, which directly correlated only with light intensity.
In contrast, the rates of recovery and synthesis of the
D1 protein decreased after inhibition of ATP synthesis
in both PS I and PS II. However, the results of Northern
blotting and [
35
S
] methionine studies suggest that the
rate of synthesis of D1 protein was increased at the
expense of ATP synthesis. In all probability, the latter
controls the repair of PS II, e.g., at the level of transla-
tion of the
psbA
gene encoding the D1 precursor (Fig. 1),
whereas the extent of the photodamage does not depend
either on the rate of electron transport, or the rate of
ATP synthesis [53].
It thus follows that the antioxidant/oxidant ratio and
the rate of ATP synthesis and electron transport are
equally important for the recovery of the photodam-
aged PS II.
The mechanisms protecting lower and higher plants
against photooxidation are different. The protection of
higher plant leaves against excess light is afforded by
the ability of their PA to dissipate absorbed light energy
by nonphotochemical mechanisms, such as the xantho-
phyll cycle [70–73]. In more detail, the protective
mechanisms of the PA can be presented as follows:
(1) Nonphotochemical dissipation of excess light
energy as one of the most efficient protective mecha-
nisms against photostress. In principle, such dissipation
is manifested in the RC of the PS I and the PS II and in
the antennae [74].
(2) Dissipation of light energy in the light-harvest-
ing complex (LHC) of PS II and low efficiency of its
transfer to the core complex of the PS II. Under these
conditions, the amount of absorbed energy increases in
favor of the PS I due to recovery of the plastoquinone
pool or the cytochrome
b
6
f
complex with subsequent
phosphorylation of LHC and its separation from the
core complex of the PS II [75, 76]. The latter is made
up of six polypeptide subunits (CP-47, CP- 43, D1, D2)
and the heterodimer of cytochrome b559 [77].
(3) Dissipation of excess light energy via the proton
gradient on the thylakoid membrane. This gradient is
formed by cyclic electron flux in the PS I, photorespi-
ration and
é
2
reduction to the anion radicals that
are disproportionated with the formation of
ç
2
é2 and
then water; photoreduced compounds play the role of
electron donors (the so-called water–water cycle) [33].
(4) Quenching of free radicals in the course of OS.
Thus, singlet oxygen is effectively quenched by two
β-carotene molecules coupled with the core complex of
the PS II [78, 79].
O2
–
BIOCHEMISTRY (MOSCOW) SUPPLEMENT SERIES A: MEMBRANE AND CELL BIOLOGY Vol. 1 No. 3 2007
MOLECULAR MECHANISMS OF STRESS RESISTANCE 189
(5) Repair and synthesis of targets photodamaged
by OS, e.g., D1 protein.
(6) Changes in the lipid composition of the thyla-
koid membrane.
(7) Other protective mechanisms including cyclic
electron transport via PS II [80] and PS I [81], aggrega-
tion of thylakoid proteins [82], photorespiration [83],
etc. Cyclic electron transport in the PS I also protects
PS II against photoinhibition [32, 81, 84, 85].
The level of nonphotochemical quenching (NPQ) in
plant leaves is considered as a reliable marker of the
quantity of photosynthetic complexes deactivating light
energy [86] and, correspondingly, their ability to dissi-
pate excess energy, which is not utilized for assimila-
tion of ëé2. The NPQ values in plants grown in the
dark are lower than those grown in strong light, because
in the former case the photodamage of PA in plants that
are less adapted to intense irradiation is more pro-
nounced, presumably due to faster rates of pigment
loss [87].
The nonphotochemical dissipation of light energy in
PS I and PS II increases with light intensity, but the dis-
sipation mechanisms are different [88, 89]. Whereas in
PS I the dissipation of heat energy is exclusively local-
ized in RC and is mediated by oxidation of ê700+ [90],
in the case of PS II the dissipation occurs in both RC
and the antennae [89]. The key role in the dissipation of
excess energy in LHC is played by xanthophyll pig-
ments, predominantly by zeaxanthin formed from vio-
loxanthin upon illumination with high intensity light at
low intrathylakoid pH [91]. Xanthophylls derive energy
from singlet excited Chl and transform it into the heat
by neutralizing triplet Chl and singlet oxygen, i.e., act
as antioxidants. Besides, zeaxanthin enhances the
photo- and thermal stability of membranes by increas-
ing their rigidity [71, 92]. There is evidence that zea-
xanthin inhibits the oxidation of membrane lipids via a
hitherto unknown mechanism [22]. The key role in the
dissipation of light energy is attributed to zeaxanthin,
anteroxanthin, lutein, PSbS (an intrinsic protein of
PS II, which responds to excess light by initiating the
transformation of the energy of absorbed light into the
heat energy), and the proton gradient, ƍ, on the thy-
lakoid membrane [22]. Recent studies based on X-ray
diffraction analysis revealed that two β-carotene mole-
cules bound to the D2 protein in the core complexes of
PS II act as singlet oxygen quenchers and, thus, protect
the proteins against photodamage. Noteworthy, the D2
protein is better protected from photodamage than the
D1 protein [79].
The dissipation of light energy absorbed by Chl into
the heat energy inhibits the generation of singlet oxy-
gen and the superoxide radical , the key participants
in the signaling cascade involving lipids and redox
compounds [22].
The effect of substitution of polyunsaturated fatty
acids for monounsaturated acids on the photoinhibition
O2
–
of electron transport from water to 1,4-benzoquinone in
cyanobacterium (SynechoÒystis sp. PCC 6803) cells was
studied by Tasaka et al. [93]. In the presence of chloro-
amphenicol, the difference between photooxidation
rates in wild type strain and mutant cells with altered
lipid composition was not observed, but the difference
between the repair rates at low light in the absence of
chloroamphenicol was significant. As the high level of
repair was observed only in cells of wild type strains, it
was concluded that the resistance of PA to photoinhibi-
tion increases at the expense of higher repair rates of
photosynthetic reactions and the high degree of unsat-
uration of fatty acids (in this case, at the expense of di-
and trienoic acids) [93, 94].
HEAT STRESS
Long-term exposure of plants to high temperatures
inhibits their growth and productive capacity. The opti-
mum growth temperatures for the majority of plant spe-
cies lie in the range 25–35°ë; at higher temperatures,
the rate of photosynthesis shows a tendency to decrease
[26]. Under these conditions, the temperature of plant
leaves is largely determined by the dose of the light
energy assimilated by the plant, the ability of plant
leaves for cooling at the expense of evaporated water
and their heat capacity. Frequent fluctuations of high
irradiance may strongly damage the plant even at mod-
erate temperatures [95].
Reactive oxygen species, such as ç2é2, play a dom-
inant role even under conditions of moderate heat stress
[11]. ç2é2 production increases significantly with a
rise in temperature, apparently at the expense of high
oxygenase activity of the Rubisco enzyme [11]. Low
concentrations of H2é2 inhibit the activity of fructose
1,6-bisphosphatase and glyceraldehyde 3-phosphate
dehydrogenase, the key enzymes of the Calvin cycle
[96, 97].
Photodamage targets and dark adaptation mech-
anisms. Photosynthesis is one of the major vital func-
tions of green plants susceptible to heat stress [11, 26,
92]. Until recently, PS II was considered to be the most
vulnerable link in photosynthesis [98–100]. However,
even at low photosynthesis rates the PS II damage
(manifested as irreversible reduction of photochemical
activity) induced by moderate heat shock is insignifi-
cant. The photodamage of PS II usually occurs at high
temperatures (45°ë and higher) [11, 101, 102]. Under
conditions of moderate heat shock and at low illumina-
tion, the activity of PS II is recovered in the course of
time [103]. PS II is usually more susceptible to heat
stress than PS I [104, 105].
OEC is a primary target for heat stress on the donor
side of PS II [26, 106]. Its inactivation occurs even at
moderate temperatures and after short-term exposure
[99, 107]. As a rule, such inactivation is fully abolished
after placing the plant under more comfortable thermal
conditions. Such inactivation is due to loss of manga-
190
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KRESLAVSKI et al.
nese ions and OEC-specific proteins and is accompa-
nied by inhibition of electron transport in the photosyn-
thetic chain. The OS-induced loss of some OEC-spe-
cific proteins was corroborated by the results of PS II
studies [107].
The energy transfer from LHC to the core complex
of the PS II is also sensitive to heat stress. The migra-
tion of the LHC from the intergrain space towards stro-
mal lamellae, the site of predominant localization of the
PS I, is observed even at 35°ë; the rate of light quanta
transfer to the PS II decreases under these conditions
[108]. Under moderate heat stress, this process
becomes reversible with a decrease in temperature.
Proton conductivity of thylakoid membranes and
increased rates of photoinduced cyclic electron trans-
port in the PS I can also be provoked by moderate heat
stress [81, 109]. Heat-induced reduction of the depleted
plastoquinone pool in the dark at the expense of stromal
electron donors is among other factors responsible for
enhanced cyclic electron transport in the PS I [11, 110].
The fact that the electron transport from the stroma to
the plastoquinone pool was observed even at 36°ë
[111] led the authors to postulate the existence of a spe-
cific protein possessing an ability to be activated at tem-
peratures above 35°ë and to catalyze electron transport
to plastoquinones.
At temperatures above 40–42°ë, the loss of photo-
synthetic activity is partly due to the inhibition of the
acceptor side of the PS II and lower rates of electron
transport in chloroplasts. Thus, heat stress increases the
relative content of Qb-nonreducing RC [103, 104].
At 42–44°C, the inactivation of the PS II gradually
becomes irreversible, predominantly at the expense of
inhibition of charge separation in RC of the PS II, dis-
sociation of some specific proteins in the core complex
[102, 112, 113], significant reduction of electron trans-
port rates due to structural rearrangements in thylakoid
membranes [114, 115] and disturbances in the system
responsible for ëé2 assimilation [11, 116].
The latter is highly sensitive to heating and is
strongly inhibited even upon moderate heat stress [26,
117]. The heat-induced decrease in the activity of the
Rubisco enzyme, one of the key participants in the
Calvin cycle, was reported by Weis as long ago as 1981
[118]. The decrease in the Rubisco activity under mod-
erate heat stress correlates with the inhibition of photo-
synthesis [119]. Moreover, the efficiency of the non-
photochemical fluorescence quenching and the activity
of the Rubisco enzyme were more sensitive to heat
stress than the quantum yield of the PS II determined by
the ratio Fv/Fm, where Fv is the photoinduced change in
fluorescence and Fm is the maximum fluorescence
[119]. Both processes can be adapted to heat stress
through a gradual increase in the temperature of plant
leaves. The inhibition of the Rubisco enzyme is
achieved due to structural rearrangements in the
Rubisco-activating enzyme (activase), which is
extremely sensitive to high temperatures [120, 121]. It
is suggested that reduction of the photosynthesis rate is
a result of lowering of the Rubisco activity and inhibi-
tion of electron transport [122]. In the latter case, the
decrease in the photosynthesis rate (PN) may be cou-
pled with decrease of content of OEC-specific proteins
[123]. The resulting decrease in the concentration of
OEC-specific proteins (17, 23 and 33 kDa) correlated
with the reduction of PN in maize (Zea mays L.) leaves.
The fact that these proteins are imported to chloroplasts
from the cytoplasm and are encoded by nuclear DNA
[123] is consistent with the results of inhibition of their
transport to chloroplasts induced by heat stress [124].
This suggests that the main effects of high temperatures
on photosynthesis are coupled with changes in the
physico-chemical properties of thylakoid membranes
and the structural organization of the PA [125].
Protection. There exist several molecular mecha-
nisms (slow and fast) whereby plants protect the PA
against heat stress. Slow mechanisms include synthesis
of heat shock proteins, antioxidants, membrane lipids,
etc. [26, 116, 126, 127] and are coupled with elevated
content of antioxidant enzymes (SOD, catalase, perox-
idase, etc.) and low-molecular-mass compounds, which
protect the PA against free radical oxidation [128]. In
addition, SOD and catalase protect PS II-specific pro-
teins against denaturation [101].
Fast mechanisms include separation of the core
complex of the PS II from LHC of the PS II, its further
translocation to the site of the PS I localization and
binding to the PS I [75, 108] as well as stabilization of
the PS II and thylakoid membranes at the expense of
conversion of violoxanthin into zeaxanthin [71, 129]
and some other compounds [11].
Translocation of the PS II LHC from the site of the
PS II localization to the site of predominant localization
of the PS I, i.e., the transition from State 1 to State 2,
represents an alternative protective mechanism against
heat stress; the main prerequisite for this translocation
is phosphorylation of the PS II LHC [75]. At the same
time, heat stress causes dephosphorylation of specific
proteins of the PS II core complex, e.g., D1, D2, and
CP43 [130]. Each of these processes has its own mech-
anism for the regulation of phosphorylation/dephos-
phorylation in thylakoid proteins [11]. Whereas one of
them controls the phosphorylation/dephosphorylation
in the PS II LHC and the transition from State 1 to
State 2, the other one regulates the phosphoryla-
tion/dephosphorylation of other thylakoid proteins.
An immense variety of thylakoid proteins is sub-
jected to phosphorylation/dephosphorylation [131];
therefore, in the majority of cases this process is effec-
tively controlled by heat stress [132].
The cyclic electron transport generated in the PS I
can be stimulated by the ∆pH on the thylakoid membrane
required for regulation of photochemical activity of the
PS II [133]. By diminishing the activity of the PS II, the
∆pH inhibits the generation of ROS and thus prevents their
photodamaging effect on the PS II [134, 135]. A similar
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MOLECULAR MECHANISMS OF STRESS RESISTANCE 191
effect is produced by yet another protective mechanism
of the PA whose effect is exerted through inhibition of
activity of Calvin cycle enzymes.
Attempts were made to establish the systems
responsible for the heat resistance of the PA, particu-
larly in the PS II. Among them, there are heat shock
proteins (HSP) formed in animal and plant cells upon
heating [126, 136, 137], carotenoids involved in the
xanthophyll cycle [71, 78, 79], isoprene [11] and some
other compounds.
There is evidence that specific chloroplast HSP pro-
tect the PS II against thermal injuries [127, 138]. The
addition of purified HSP to chloroplast suspensions
protects the PS II from thermal injuries. Besides, these
proteins play a role in adaptation of the PA to heat
stress.
Expression of HSP genes at high temperatures
depends on the physical state of membranes [139]. It
was found that heat-induced expression of HSP genes
increases with the membrane fluidity. Thus, the expres-
sion of HSP genes increases at high temperatures.
Some of these gene products prevent the disintegration
of membranes [139]. A crucial role in this process is
ascribed to the composition of membrane lipids, to the
ratio of unsaturated and saturated fatty acids, in partic-
ular [5, 6, 140]. Thylakoid membranes of mutant cells
devoid of fatty acids with three double bonds are espe-
cially heat-resistant [141], which is consistent with the
hypothesis that expression of HSP genes is controlled
by changes at the membrane level [142].
However, heat tolerance of plant cells is controlled
not only by HSP, but by other compounds as well [112,
143]. The attempt to estimate the contribution of HSP
and phosphorylation of individual polypeptides in cul-
tured salt-resistant tobacco (Nicotiana sylvestris L.)
cells to cell responses to high salinity and high temper-
atures failed because of the inability to establish a cor-
relation between the synthesis of 70 kDa HSP and high
heat tolerance of N. sylvestris cells [143]. This implies
that heating of cells differing in their heat resistance
yields different sets of polypeptides and low-molecu-
lar-mass compounds, e.g., proline and other cell-pro-
tecting factors, which determine their resistance to heat.
Studies with Chlamydomonas reinhardtii cells carried
out by Tanaka et al. [112] showed that the crucial role
in heat resistance of OEC of the PS II is played by pro-
teins encoded by nuclear and chloroplast genomes
rather than by 70, 60 and 22 kDa HSP. Conceivably,
their stabilization requires the synthesis of extrinsic
proteins of PS II (e.g., PSbU) [144] manifesting coop-
erative activity during stabilization of OEC of the PS II.
Studies with cyanobacterium cells revealed that inacti-
vation of the psbU gene encoding PSbU, an extrinsic
protein of the core complex of the PS II, deprives the
OEC of its ability to be resistant to high temperatures
[144].
The analysis of mechanisms of light-induced recov-
ery of membranes at room temperature [102] and of
PS II recovery in plant leaves exposed to heat shock
[103] revealed that heating of PS II preparations to
40°ë is accompanied by a release of the 33 kDa protein
from the core complexes of the PS II and its repeated
binding to these complexes upon subsequent cooling to
room temperature [102]. An alternative mechanism can
be realized at higher temperatures and consists in deg-
radation and resynthesis of pigment–protein complexes
of the PS II, in the first place, of the antenna complexes
CP47 and CP43 [103]. Under these conditions, the
resynthesis can be coupled with the degradation of
Chl–protein complexes. The mechanism of PS II RC
recovery after exposure to intense light was studied in
sufficiently great detail [31, 39, 145]. However, there is
still no evidence concerning the relationship between
the photochemical activity of PS II and heat-induced
changes at the level of Chl–protein complexes.
Heat stress and photoinhibition. It is known that
under certain conditions illumination protects PA
against heat-induced injuries [146]. One of such induc-
ing factors is photoinduced recovery of the PS II. How-
ever, under combined action of light and heat stress
photoinhibition is sometimes manifested even upon
low-level illumination [26]. Studies of direct photo-
damage of PS II and its further recovery showed that
heat stress inhibits PS II repair in tobacco leaves with-
out any effect on its photodamage [147]. Analysis of
changes in the activity of PS II in wheat seedlings after
heat stress (42°ë, 20 min) in the presence of chlOroam-
phenicol revealed that the rate of photoinhibition of the
PS II, contrary to the rate of the repair of the photosys-
tem, does not depend on thermal treatment [148]. This
finding is consistent with the hypothesis according to
which moderate heat stress is accompanied by the PS II
repair without any effect on its photodamage [19, 29, 49].
The relationship between heat and light-induced
stress, i.e. the effect of preliminary thermal treatment
on the rate of photoinhibition and subsequent exposure
of heat-adapted plants to light, is yet another important
issue. The data available are rather controversial. It was
found, in particular, that heat shock (40°ë) does not
influence the rate of photoinhibition in individual wheat
leaves determined from the rate of electron transport in
isolated wheat chloroplasts [149]. At the same time, the
results of analysis of induction curves for delayed mil-
lisecond and variable fluorescence of intact wheat
leaves exposed to heat shock at 40 and 42°ë with a sub-
sequent recovery at low light and repeated exposure to
heat shock or high-light stress suggest that the PA of
hardening plants is more resistant to repeated heat
shock and photostress [148, 150]. Enhanced resistance
of the PA can be attributed to accumulation of HSP,
which protect the PA against photoinactivation.
In summary, it may be said that the state and struc-
ture of thylakoid membranes play a key role in the pro-
tection of the PA against stress and its acclimation to
high temperatures.
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COLD STRESS
Low temperatures entail uniform compression and
solidification of the membrane lipid bilayer resulting in
inhibition of photosynthesis and respiration, decrease
in membrane permeability (mostly for water), inactiva-
tion of enzymes, retardation of ion exchange and so on.
Solidification of the lipid bilayer induced by cold shock
can be nonuniform as a result of which its barrier func-
tion is impaired and disintegration of membranes
occurs [7].
Biomembranes are the main targets for cold stress.
In the framework of the Lyons hypothesis [151], cold-
induced injuries in plant membranes largely affect
phase transitions of membrane lipids. The liquid-crys-
talline state of membranes is a prerequisite for their
function as a selective barrier between different cell
compartments and the maintenance of proteins in the
active state, while the transition of membrane lipids
from the liquid-crystalline to the solid state is the main
cause of death in heat-loving plants at low tempera-
tures. Phase transitions are controlled by the ratio of
saturated and unsaturated fatty acids. The functional
activity of biomembranes including thylakoid mem-
branes depends on the fatty acid composition of mem-
brane lipids. The changes in the ratio of saturated and
unsaturated fatty acids [7, 94, 140, 151] and the con-
centration of membrane phospholipids (e.g., in thyla-
koid membranes) determine the resistance of plants to
low temperatures. Studies of the damaging effect of
cold stress carried out by Novitskaya et al. [152]
revealed insignificant changes in the ratio of unsatur-
ated and saturated fatty acids, but the content of polar
lipids calculated per unit of protein was decreased. The
decrease in the content of phosphatidylglycerol, an
intrinsic component of chloroplast membranes and
chloroplast lipids (galactolipids and sulfolipids), was
especially well pronounced.
Long-term dark incubation of cucumber leaves at
low temperatures resulted in selective inactivation of
their OEC [153]. Prolonged cold stress at low tempera-
tures was accompanied by dissociation of OEC-bound
extrinsic proteins and manganese ions. However, this
mechanism is fairly ineffective under natural condi-
tions [116]. Cold-induced injuries are especially appar-
ent in chloroplasts and are further aggravated upon sub-
sequent cooling in the light; as a result, chloroplasts
lose their original color due to “bleaching” of chloro-
phyll, formation of lipid droplets and degeneration of
thylakoids [154]. Mitochondria are more resistant to
low temperatures, but photosynthetic electron trans-
port, ëé2 assimilation and surface stomata of plant
leaves manifest the highest sensitivity to cold stress [7,
146].
Protective mechanisms. The mechanism of cold
resistance includes increasing concentrations of water-
soluble proteins and cold-resistant isoenzymes and
maintenance of membrane lipids in the liquid state in
order to keep a high degree of unsaturation and high
phospholipid content. Phase transitions of membrane
lipids from the (quasi)liquid-crystalline to the
(quasi)solid-crystalline state (the so-called sol–gel
transition) result in a drastic decrease of membrane per-
meability [7].
Photosynthesis is more susceptible to low tempera-
tures than respiration, particularly because phase tran-
sitions of membrane lipids in chloroplasts occur at
higher temperatures than in mitochondria.
Phospholipid bilayers of the plasmalemma and
intracellular membranes are the main targets for ROS
generated in plant cells at low temperatures. Therefore,
the membrane composition, first of all, the ratio of
unsaturated and saturated fatty acids, is extremely
important for the resistance and tolerance of plants.
Studies with transgenic cyanobacteria and genetically
transformed tobacco plants revealed that the ratio of
saturated and unsaturated fatty acids is critical for their
cold tolerance. In these studies, the level of unsaturated
fatty acids in chloroplasts was variable, because both
mutant and transgenic organisms were used [155]. At
high degrees of unsaturation, the PA is more resistant to
cold stress than at low-level of unsaturation.
These findings are consistent with the previously
reported close relationship between cold sensitivity of
the PA and the content of cis-unsaturated fatty acids of
phosphatidylglycerol [94, 156]. At 1°ë, the rate of pho-
tooxidation in transformed plant leaves with a lower
content of unsaturated fatty acids was higher in com-
parison with control, while the rate of the PS II recov-
ery in the dark at +17°ë was lower even in the absence
of protein synthesis inhibitors. It was concluded that
cis-unsaturated fatty acids of phosphatidylglycerol
stimulate the recovery of the PS II after photoinhibition
at low temperatures. In addition, high-molecular-mass
alcohols, some amino acids and proteins also contribute
to cold resistance of plants [94]. Some studies devoted
to cold stress [7] are based on the so-called “bioener-
getic concept,” assuming that cold adaptation of thyla-
koid membranes is accompanied by accumulation of
compounds which demand especially high-energy
expenditures and materials (e.g., high-molecular-mass
lipids and proteins) for their synthesis. Ultrastructural
changes in the chloroplast membrane also play a pro-
tective role.
Unsaturated lipids prevent the inhibition of photo-
synthesis at low temperatures thus favoring the recov-
ery of PS II in the course of photoinhibition. This pro-
cess is mediated by the protein D1 precursor; however,
the detailed mechanism is unknown. Presumably, the
conformation of the pre-D1 protein changes in such a
way that its conversion into the mature form, D1, is sig-
nificantly facilitated [10, 94].
Flavonoids, e.g., epicatechin and epicatechin gal-
late, localized near the membrane surface also possess
protective activity. These compounds manifest pro-
nounced antioxidant properties and protect phospholip-
ids against ROS [157].
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MOLECULAR MECHANISMS OF STRESS RESISTANCE 193
Cold stress and photoinhibition. It is well known
that even low-intensity light can inactivate PA at low
temperatures [70, 146, 158–160]. The extent of photo-
inhibition is largely determined by inactivation of the
PS II RC at all temperatures, but the reasons of the inac-
tivation and its mechanisms are different [146]. There
exist several photoinhibition mechanisms explaining
effects of cold stress [70, 158, 160], in particular:
(1) Low efficiency of energy utilization in the
Calvin cycle leads to high rates of pseudocyclic elec-
tron transport and enhanced production of ROS that
stimulate the degradation of D1 and other RC-specific
proteins.
(2) Low activity of antioxidant enzymes. Thus, the
catalase in cold-sensitive plants, e.g., maize and
cucumber, is photoinactivated at low temperatures
[161].
(3) Low activity of enzymes of xanthophyll cycle.
The synthesis of zeaxanthin, which quenches the exci-
tation energy in the PS II antennae by transforming it
into the heat energy, is suppressed at low temperatures
[70]. Zeaxanthin synthesis in the lumen is induced by
high intensity light at low pH, but it is blocked at low
temperatures.
(4) Inhibition of the PS-II repair at low tempera-
tures. The turnover of the D1 protein, the key compo-
nent of photoinhibition, is lowered at low temperatures
[162] as a result of which the rearrangement of PS II
complexes with inbuilt D1 protein is suppressed. The
hypothesis according to which the recovery of the pho-
todamaged PS II is suppressed by cold stress was cor-
roborated in experiments with Synechocystis [5, 52]
and higher plant cells [19, 29, 46, 156]. Individual rates
of PS II photodamage at intense light and its recovery
at low light were established at different temperatures:
34°C (control), 25, 18, and 10°ë [52]. Low tempera-
tures had no effect on the rate of photodamage, but sig-
nificantly decreased the efficiency of the PS II repair
[19, 29, 46, 52].
At the same time, cold acclimation increases the
resistance of plants to high intensity light and cold
stress, although the mechanism of this phenomenon is
still poorly understood [158]. This is achieved at the
expense of enhanced assimilation of ëé2 in cold-
adapted cells and, probably, higher activity of antioxi-
dant system [160]. This hypothesis is consistent with
the crucial role of flavonoids and carotenoids in the
adaptation of Arabidopsis npq and tt mutants to simul-
taneous action of excess light and low temperatures
[163].
Studies with cyanobacterium cells revealed that
recovery of PS II activity in the dark is one of the major
protective mechanisms during photoinhibition at low
temperatures [10]. Upon irradiation with high intensity
light at 10°ë, the activity of the PS II decreases by
approx. 90%, whereas after 1-h incubation of cyano-
bacterium cells at 34°ë up to 50% of the PS II activity
was recovered even in the presence of the protein syn-
thesis inhibitor lincomycin. The results of [35S]
methionine and Western blotting studies suggest that
recovery in dark is unrelated to protein synthesis but
rather is due to formation of the intermediate form of
photodamaged PS II, viz., PS II (i), which is converted
into the active form, PS II(a), in the dark (Fig. 2). Half
of PS II(i) molecules are recovered under these condi-
tions, whereas the other half is converted into PS II*
responsible for the repair in light. Dark reduction of
PS II activity does not require de novo synthesis of the
D1 protein and takes place only during photoinhibition
at low temperatures [10].
In contrast to low temperatures, at high tempera-
tures and at intense light the repair is light-dependent as
can be evidenced from high values of Kr and Kd for
PS II(a) and PS II* synthesis from PS II(i), respectively
[10].
Desaturation of fatty acids is induced by low tem-
peratures and is one of the key factors in cold acclima-
tion of cells [94]. A crucial role in this process is played
by enzymes, such as desaturases. Whereas wild type
strain of Synechocystis sp. PCC 6803 predominantly
synthesizes polyunsaturated fatty acids, the desA–/desD–
mutant deficient in ∆12 (desA) and ∆6 (desD) genes of
fatty acid desaturases produces exclusively monounsat-
urated fatty acids thus increasing the membrane viscos-
ity [93]. Low fluidity of the cytoplasm in cyanobacte-
rium cells favors the expression of the desaturase gene
at low temperatures [164, 165]. For example, the
expression of the desA gene encoding ∆12-acyl-lipid-
desaturase is usually enhanced at low temperatures, but
increases again with a decrease in the degree of unsat-
uration of fatty acids in the composition of the cytoplas-
mic membrane [142].
Strong
light
PS II(‡) PS II(i) PS II*
Dark repair Kr
Light-dependent
repair
Degradation of D1
Synthesis of pre-D1
Assembly of PS II
Kd
Fig. 2. A hypothetical scheme of the photodamage and
repair of PS II [10, 50–53]. Pre-D1, protein D1 precursor;
PS II(i), intermediate form of photodamaged PS II. PS II(a),
active form of PS II. PS II*, PS II responsible for light
repair. Kr and Kd, constants for PS II(a) and PS II* forma-
tion from PS II(i), respectively.
194
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SALT STRESS
The mechanisms underlying the effects of salt stress
on the PA are still poorly understood. Notwithstanding,
low activity of the PA, particularly during electron
transport, is one of the reasons for growth retardation
and low productivity of plants under conditions of salt
stress [166–168]. The effects of high salt concentra-
tions on metabolism were studied in experiments with
salt-resistant and salt-sensitive plant species including
halophilic plants and cultured cyanobacterium and
plant cells.
It is known that salt stress influences both whole
plants and individual cells and entails both osmotic and
ionic stress [169–171]. Each of these factors has a num-
ber of specific features. Osmotic stress is coupled pri-
marily with water deficit. Its mechanism consists in
reversible inhibition of photosynthetic electron trans-
port by the compression of intracellular volume as a
result of an output of water molecules through water
channels in plasmalemma membrane [3].
The water content in the cytosol decreases as a result
of osmotic stress, while intracellular concentrations of
the salt increase in contrast [3].
Mutations in the aqpZ gene encoding aquoporin, a
specific protein of water channels, restrict osmotic
swelling of cyanobacterium cells. There is an opinion
that in cyanobacterium cells water channels, but not the
lipid bilayer, are most important for transmembrane
transport of water. It follows from these data that
aquoporin-induced swelling of cells is critical for gene
expression under conditions of hyperosmotic shock
[172].
Ionic stress is manifested in excessive accumulation
of Na+ and Cl– ions and low level absorption of other
ions, e.g., K+, Ca2+ [173]. Salt stress leads to water def-
icit, loss of cell turgor and enhanced accumulation of
ions. This, in turn, results in inhibition of enzyme activ-
ity and deceleration of metabolic processes (mostly, of
photosynthesis) and membrane damage [166, 171]. OS
induced by enhanced production of ROS, e.g., rad-
icals, OH-radicals, etc., is yet another cause of mem-
brane damage [174].
In many cases, low efficiency of photosynthesis at
high concentrations of NaCl is coupled with low activ-
ity of PS II (see reviews [167] and [170]) and structural
rearrangements of thylakoid membranes [175]. The
reasons are as follows: (1) low level of light energy
absorption in LHC of the PS II due to translocation of
the LHC from PS II to PS I [75, 108] and binding to the
last, disturbances of the acceptor and donor sides of
PS II [176, 177]; (2) reduced number of RC of the PS II
[178, 179] and degradation of the OEC [2]. However,
there are cases where even high (e.g., 0.55 M NaCl) salt
concentrations have no effect on the activity of the PS
II in Synechocystis cells [180], but increase the activity
of electron transport in the PS I in unicellular algae and
cyanobacteria [180, 181]. The number of RC of the PS I
O2
–
increases under these conditions and, a result of this,
the rate of cyclic electron transport in PS I increases as
well [180]. In cells of the salt-resistant cyanobacterium
Aphanothece halophytica, the rate of ëé2 assimilation
increases [182], while the Chl content can both
decrease and increase even under severe salt stress
[171]. Apparently, higher plants are more adapted to
lower salt concentrations, whereas cyanobacteria are
better adapted to high salinities [173].
Of special importance in the analysis of mecha-
nisms of salt stress is the demarcation line between
osmotic and ionic stress and the role of K+/Na+ and
water channels (aquaporins). These phenomena were
investigated in experiments with thylakoid membranes
as well as with Synechocystis sp. PCC 6803 [8] and Syn-
echococcus sp. PCC 7942 cells [2, 3, 9]. Incubation of
Synechococcus cells in the presence of 0.5 M NaCl was
accompanied by two photoinhibition effects, viz., rapid
reversible decrease of OEC activity and electron-trans-
port activities of the PS I and the PS II (Phase I) and
their subsequent slow irreversible loss (Phase II) [2, 3].
As regards duration and magnitude of effect of photo-
inhibition, the fast (1 h) phase corresponds to the
osmotic effect produced by 1 M sorbitol or 0.5 M NaCl.
This suggests that the drastic decrease of PS II activity
is coupled with the osmotic effect of high salt concen-
trations. The slow phase seems to be coupled with the
effect of ionic stress: in the presence of Na+ ions and
water channel blokators, the damaging effect of NaCl is
absent. A prominent role in photosynthetic reactions in
cyanobacteria and their resistance to salt stress is
played by Na+/H+ antiporters, K+/Na+ exchangers and
water channels (aquaporins) [3, 8]. Considering that the
osmotic effect of NaCl is reversible, while the ionic
effect is irreversible, it was suggested that Na+ ions pro-
voke the degradation of a system responsible for the
recovery of PS II following its exposure to salt stress. It
is also probable that three peripheral proteins coupled
to the core complex of PS II, such as the 33 kDa protein,
cytochrome c550 and protein PsbU [144], and stabiliz-
ing the core complex dissociate at high NaCl concen-
trations, and consequently PS II becomes inactivated
[2, 3, 8].
Similar regularities, including the biphasic kinetics
of changes in the photochemical activity were estab-
lished during incubation of cyanobacterium (S. platen-
sis) cells in the light and in the dark in the presence of
different concentrations of NaCl [176]. The salt-
induced changes in the photochemical reactions occur-
ring in PS II were distinctly biphasic. The first phase
was independent of light and was characterized by a
fast decline of PS II activity and its subsequent recov-
ery. In the second phase, the gradual decrease of PS II
activity was observed only in the light, while the
decrease in PS II activity was more pronounced after
illumination of cells with more intensive light.
It should be noted in summary that high concentra-
tions of NaCl not only inhibit the OEC activity, but also
BIOCHEMISTRY (MOSCOW) SUPPLEMENT SERIES A: MEMBRANE AND CELL BIOLOGY Vol. 1 No. 3 2007
MOLECULAR MECHANISMS OF STRESS RESISTANCE 195
diminish the efficiency of electron transport in the
PS I [3].
Salt stress and photoinhibition. In nature, salt
stress is often accompanied by photostress, as a result
of joint action, effect of the salt stress on the PA can be
enhanced. This takes place both in unicellular photo-
synthesizing organisms, e.g., Chlamydomonas rein-
hardtii [183], Synechocystis sp. PCC 6803 [50], S. lat-
ensis [176, 177], etc., and in the leaves of higher plants
[171, 184]. The targets for stress are variable. Strong
light induced the photodamage of Synechocystis sp.
PCC 6803 PS II, while salt stress suppressed its recov-
ery without any direct damage of PS II [50], which is
consistent with the regularities established in photoin-
hibition studies [10, 17, 18, 49, 53, 54]. Radiolabeling
studies showed that salt stress inhibits de novo synthe-
sis of D1 and many other photosynthetic proteins [18,
50], while the results of Northern and Western blotting
analysis suggest that salt stress inhibits the transcrip-
tion and translation of the psbA gene encoding the D1
protein and suppresses the activity of genome at the
translation and transcription levels (see [19, 29, 49]).
Excess light and salt stress have a synergistic influ-
ence on the activity of the PS II [50], whereas salt stress
in the dark may have no effect on the activity. Thus,
Synechocystis sp. PCC 6803 PS II was found to be resis-
tant to the effect of salt stress alone. The activity of
PS II did not change even after 15-h incubation of cells
with 0.5 M NaCl in the dark [8].
Heat shock and salt stress. In some cases, salt
stress increases the resistance of the PS II to heat shock
[185, 186] without any effect on the electron transport
in the PS II of the halophytic plants Suaeda salsa [185]
and Artemisia anethifolia [186], apparently due to
increased resistance of LHC, OEC and RC of the PS II
to heat shock.
Adaptation and protection. Salt-resistant plants
(halophytes) possess several mechanisms of protection
against salinization, e.g., low rates of Na+ absorption,
predominant accumulation of Na+ ions in vacuoles and
their enhanced excretion via special channels [187].
Studies in which ionic and osmotic stresses were
interpreted as independent phenomena, e.g., with Syn-
echocystis cells, established that salt and hyperosmotic
stresses control the expression of definite sets of genes
responsible for acclimation. Salt stress activates the
slr1390 and slr1604 genes encoding FtsH metallopro-
teases responsible for direct degradation of the D1 pro-
tein in photodamaged PS II and the ÒtpA genes encod-
ing CtpA catalyzing the C-terminal cleavage of the pro-
tein D1 precursor [188, 189]. No induction of ctpA
genes takes place during hyperosmotic stress. Presum-
ably, light intensity is a critical factor, which deter-
mines the adaptation of plants to high salinity: the dam-
aging effect of salt stress can be enhanced in strong
light [50, 52]. The rate of repair of a damage, which is
determined by the rates of photosynthesis and respira-
tion, plays a role as well. Enhanced energy supply of
Synechococcus sp. PCC 7942 cells in the presence
of light and exogenous glucose and its effect on
NaCl-induced inactivation of the PA are detailed in
[54]. Incubation of Synechococcus sp. cells with 0.5 M
NaCl results in initial short-term decrease of the oxy-
gen-evolving activity of PS II and the rate of electron
transport in the PS I followed by a further slower
decrease (Phase II). Both light and exogenous glucose
protect the PS I and the PS II against the second phase
of NaCl-induced inactivation. The protective effects of
light and glucose are eliminated in the presence of a
phosphorylation uncoupler and the protein synthesis
inhibitor lincomycin. Light and glucose had an equal
influence on NaCl-induced inhibition of Na+/H+ anti-
porters (Fig. 3). After exposure of cells to 0.5 M NaCl
in the absence of light, the photosynthetic and anti-
porter activities are partly recovered in the light in the
presence of exogenous glucose; this recovery is pre-
vented by lincomycin. These findings suggest that
enhanced energy supply during photosynthesis or res-
piration required for protein synthesis in plant cells
plays a crucial role in the recovery of the PA and Na+/H+
antiporters under high salinity conditions (Fig. 3) [54].
In addition to energy supply, a prominent role in the
resistance of the PA to salt excess is played by the state
of thylakoid membranes [171]. The ratio of saturated
and unsaturated fatty acids and the phospholipid com-
position of membranes is one of such critical factors [8,
9, 26, 155]. Studies of the role of unsaturated fatty acids
in the resistance of the PS II to salt stress [8, 9] demon-
strated that cyanobacterium cells capable to synthesize
polyunsaturated fatty acids manifested higher resis-
tance to salt stress. The Synechocystis mutant deficient
in the desA and desD genes encoding ∆12 and ∆6 desat-
urases contains fewer unsaturated fatty acids and, cor-
PS II
Na+
H+
H+
Na+
Na+
ATP
ADP
Na+
Plasmalemma
Thylakoid
membrane
Fig. 3. A hypothetical scheme of effects of Na+ ions and
unsaturated fatty acids of membrane lipids on the oxygen-
evolving activity of PS II in cyanobacterial cells [2, 3, 8, 9,
54].
196
BIOCHEMISTRY (MOSCOW) SUPPLEMENT SERIES A: MEMBRANE AND CELL BIOLOGY Vol. 1 No. 3 2007
KRESLAVSKI et al.
respondingly, manifests higher sensitivity to salt stress.
The content of unsaturated fatty acids in mutant cell
membranes strongly increases the resistance of the
PS II to salt stress due to expression of the desA gene in
Synechocystis [9].
Vacuolar ATPase involved in the transport of cat-
ions, e.g., Na+, into vacuoles, plays a prominent role in
the resistance to salinity and acclimation [190]. In
cyanobacterium cells, the role of a factor responsible
for the Na+ efflux from the cytoplasm is played by cyto-
plasmic ATPase [171].
Many endogenous low-molecular mass compounds,
e.g., proline, choline, choline betaine, glycine betaine,
sugars, multiatomic alcohols [191–195], silicon [196],
etc., effectively protect plants against salinization.
Their main distinctive feature is the ability to be accu-
mulated in cells in large amounts without any detriment
to membranes or enzymes [197]. The quaternary
ammonium derivatives choline and proline are zwitter-
ions. They bear a compensated charge (+, –) and are
easily bound to proteins and membrane components of
a cell. There is an opinion that at low water content
osmotically active compounds protect lipids and pro-
teins by acting as water substitutes. This maintains the
hydrophilic–hydrophobic orientation of membrane
phospholipids and prevents protein aggregation [197].
Apart from low-molecular compounds, an impor-
tant role in protection against salt stress is played by
antioxidant enzymes. The activity of the most of them
increases during salt stress [174].
GROWTH RETARDANTS
AND BETAINES PROTECT PA AGAINST
ENVIRONMENTAL STRESS
The ability of plants and plant systems to suppress
the damage and/or to recover after stress is of extreme
importance for their survival and productivity. Stress-
induced injuries are minimized through application of
growth-regulating factors, such as growth retardants
and abscisic acid. Growth retardants significantly
enhance the resistance of plants to drought, cold, salin-
ity, ozone and UV-B [192, 198, 199]. Various types of
retardants and their action mechanisms are described in
a review [199]. Treatment of plants with growth retar-
dants increases the activity of antioxidant system and
enhances its ability to neutralize oxidants. For example,
treatment of wheat plants with the triazole type retar-
dant S-3307 stimulates accumulation of lipophilic anti-
oxidants in microsomal membranes [198] and dimin-
ishes their susceptibility to ozone injuries. Our studies
showed [200] that pretreatment of bean seedlings with
growth retardants, e.g., choline choloride and chloro-
choline chloride, increases the resistance of their PA to
high-temperature stress and UV-B irradiation. In plant
leaves, retardants stimulate the activity of antioxidant
enzymes, e.g., SOD and ascorbate peroxidases, and
increase the concentrations of carotenoids and UV-B-
absorbing pigments, thus increasing their resistance to
stress. These effects are characteristic of not only
leaves, but also of isolated chloroplasts, but the effects
were manifested not earlier than within the first 6 hours.
Apparently, cholines stimulate the activity of genes
responsible for the synthesis of antioxidants and stress
protectors, such as flavonoids and carotenoids whose
concentration in the cells increases after treatment with
choline compounds [200]. Cholines stimulate the activ-
ity of phytohormones e.g., cytokinins [201] and absci-
sic acid (Bukhov et al., unpublished data) protecting the
PA against stress.
The aforementioned synthesis of low-molecular
protective compounds including osmoprotectors (pro-
line, putrescins, salicylic acids, betaines, etc.) is one of
the main routes to acclimation of the PA to stress [202,
203]. Many plants, e.g., Chenopodiaceae, Gramineae
and salt-resistant cyanobacteria, accumulate large
amounts of glycine betaine [204]. The latter is espe-
cially well known as an osmoprotector by virtue of its
ability to be accumulated in eukaryotic and bacterial
cells under definite conditions [205]. Similar to other
osmotically active substances, glycine betaine main-
tains high levels of protein activity in cells. Like many
other proteins endowed with chaperonic activity, the
trimethylamine derivatives choline and glycine betaine
protect citrate synthase against thermal denaturation
and stimulate its renaturation by urea in vitro [205],
however, only when sufficiently high (above 50 mM)
concentrations of exogenous trimethylamine are used.
Glycine betaine reactivates the Rubisco enzyme after
denaturation by salt stress and acts as an osmoprotector
for proteins and damaged membranes by promoting
stability of hydrophobic domains of enzymes [204]. In
addition, glycine betaine increases the stress-resistance
of the é2-evolving system and ATP synthesis [106],
attenuates the effects of heat-induced inhibition of the
PS II [193] and protects it against heat-induced injuries.
The hypothetical mechanism of glycine betaine con-
sists in stabilization of membrane proteins, manganese
clusters and peripheral proteins of the PS II (Mr = 33,
23, 17 kDa) [193].
It is interesting to note that sodium bicarbonate
added to chloroplast or subchloroplast suspensions pre-
pared from the PS II stabilizes the structure of manga-
nese cluster [206].
In all probability, betaine maintains certain electron
transfer reactions in RC of the PS II, e.g., pheophytin
recovery and P680 oxidation [193]. Glycine betaine pro-
tects the PS II D1/D2/Cytb559 complex against photo-
damage and heat-induced inactivation [194].
Studies with Synechococcus cells transformed by
the codA gene involved in glycine betaine synthesis
demonstrated that PS II of glycine betaine-synthesizing
microorganisms manifest enhanced resistance to heat
and photoinactivation (Allakhverdiev et al., unpub-
lished data).
BIOCHEMISTRY (MOSCOW) SUPPLEMENT SERIES A: MEMBRANE AND CELL BIOLOGY Vol. 1 No. 3 2007
MOLECULAR MECHANISMS OF STRESS RESISTANCE 197
Accumulation of glycine betaine in cyanobacterium
cells to concentrations of 60–80 mM can be responsible
for cell resistance to low temperatures and recovery of
their photoinactivated PA [170].
Very often, glycine betaine and its derivatives act
nonspecifically as osmolytic agents and protectors of
certain proteins and membranes. Choline compounds
are effective at lower concentrations; their effects are
basically mediated by activation of specific genes.
INTERACTION OF SEVERAL STRESS FACTORS.
CROSS TOLERANCE
It is known that long-term exposure to one type of a
stress leads to non-specific increase of the plant resis-
tance commonly referred to as cross adaptation [137,
207]. For example, in cold- and heat-adapted plants the
sensitivity to photoinhibition is decreased [159], which
can partly be attributed to higher activity of protective
antioxidant compounds of high- (enzymes) and low-
molecular weight compounds [128, 208] involved in
neutralization of ROS causing the damage of the PA
and other cell structures. HSP is also known to play a
role in the resistance of the PS II to heating in strong
light [209]. Moreover, the lipid composition of mem-
branes changes upon OS induced by heating, cooling or
salt stress, which may be important for cross adaptation
of the PA. Other mechanisms include high regeneration
rates of the D1 protein, high rates of energy dissipation
via a proton gradient in thylakoid membranes and high
activity of xanthophyll cycle enzymes.
Irradiation with moderate doses of UV-B also
ensures high resistance of the PA to other types of OS,
apparently at the expense of augmented synthesis of
phenolic derivatives, stress-specific proteins and other
protective compounds [210].
A crucial role in cross adaptation of PA is played by
ROS, e.g., ç2é2, a key participant in the adaptation of
leaves to high intensity light [211]. In addition, hydro-
gen peroxide stimulates the synthesis of HSP and
increases tolerance to heat shock and low temperatures
[14]. Low concentrations of ç2é2 control the expres-
sion of certain genes and stimulate adaptation to stress,
while high concentrations of hydrogen peroxide pro-
voke cell injuries [27, 212].
Altogether, these data clearly demonstrate that high
resistance of the PA of plants is a key factor in their
adaptation to stress. Therefore, the construction of
stress-resistant transgenic plants using methods of
genetic engineering is a task of superior importance. A
hypothetical scheme of ways to increasing the resis-
tance of the PA to environmental stress is shown in
Fig. 4 in the example of stress-resistant transgenic
plants [7, 22, 140, 195]. As can be seen, transgenic
plants synthesize large amounts of protective com-
pounds of low-molecular weight, including osmolytes,
hormones, antioxidants and/or stress proteins as well as
transcription factors. Moreover, increased resistance of
the PA to stress can be achieved through modification
of the lipid composition of thylakoid membranes and
augmented synthesis of high-molecular weight com-
pounds such as lipids and proteins.
ACKNOWLEDGMENTS
This work was financially supported in part by Russian
Foundation for Basic Research (grant no. 05-04-49672)
and the Molecular and Cell Biology Programs from
Russian Academy of Sciences.
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