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Plant Physiol, April 2001, Vol. 125, pp. 1558-1566
UPDATE ON PHOTOSYNTHESIS
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INTRODUCTION |
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Plants and algae have a love/hate relationship with light. As oxygenic photoautotrophic organisms, they require light for life; however, too much light can lead to increased production of damaging reactive oxygen species as byproducts of photosynthesis. In extreme cases, photooxidative damage can cause pigment bleaching and death, a phenomenon all too familiar to anyone who has tried to move a houseplant outdoors into full sunlight.
The quantity of the light in natural environments can vary over several orders of magnitude and on a time scale that ranges from seconds to seasons. Because light is such an important environmental parameter, plants have evolved numerous biochemical and developmental responses to light that help to optimize photosynthesis and growth. For example, plants rely on photoreceptors such as phytochrome for shade avoidance responses. Some plants are able to adjust their capacity for harvesting sunlight through leaf and chloroplast movements. During long-term acclimation to changes in light intensity many algae and plants regulate the size of their light-harvesting pigment antennae through changes in gene expression and/or proteolysis. Large antennae are necessary for efficient light capture in limiting light, but they can be a liability when light is abundant or excessive.
On a daily as well as seasonal basis most plants receive more sunlight
than they can actually use for photosynthesis. Under these
circumstances, regulation of light harvesting is necessary to balance
the absorption and utilization of light energy, thereby minimizing the
potential for photooxidative damage. Besides adjusting light
absorption, algae and plants have ways of getting rid of excess light
energy that has already been absorbed. This update will focus on
protective non-photochemical mechanisms that quench singlet-excited
chlorophylls (Chl) and harmlessly dissipate excess excitation energy as
heat. These non-photochemical quenching (NPQ) processes occur in almost
all photosynthetic eukaryotes, and they help to regulate and protect
photosynthesis in environments in which light energy absorption exceeds
the capacity for light utilization. We will summarize progress in
understanding NPQ that has been made since the last Update
article on NPQ appeared in this journal (Horton et al., 1994
).
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NPQ AFFECTS CHL FLUORESCENCE |
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Absorption of sunlight for photosynthesis is accomplished by
light-harvesting pigment-protein complexes (LHCs) that are associated with reaction centers. Light absorption results in singlet-state excitation of a Chl a molecule
(1Chl*), which can return to the ground state via
one of several pathways (Fig. 1).
Excitation energy can be re-emitted as Chl fluorescence, it can be
transferred to reaction centers and used to drive photochemistry, it
can be de-excited by thermal dissipation processes (NPQ), or it
can decay via the triplet state (3Chl*).
Although the triplet pathway can be a significant valve for excess
excitation (4%-25% of absorbed photons; Foyer and Harbinson, 1999
),
3Chl* can transfer energy to ground-state
O2 to generate singlet oxygen
(1O2*), an extremely
damaging reactive oxygen species. At room temperature, Chl fluorescence
mainly originates from photosystem (PS) II, and the yield of
fluorescence is generally low (0.6%-3%; Krause and Weis, 1991
). The
yields of 3Chl* and fluorescence vary in
proportion to the average lifetime of 1Chl*,
which in turn depends on the yields of the other pathways. For example,
the high quantum efficiency of photochemistry in limiting light results
in a decrease, or quenching, of fluorescence that is termed
photochemical quenching (qP). Non-photochemical processes that
dissipate excitation energy also quench Chl fluorescence and are
collectively called NPQ (or qN). A summary of Chl fluorescence quenching processes is given in Table
I.
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In practice Chl fluorescence quenching is usually measured with a
commercial fluorometer that can measure fluorescence yield in the
presence of varying background white light (Fig.
2). Over a wide range of light
intensities, plants are able to maintain a low steady-state
fluorescence yield and 3Chl* yield due to a
combination of qP and NPQ. Thus, qP and NPQ help to minimize production
of 1O2* in the PSII
antenna. The quenching due solely to NPQ can be determined periodically
by measuring the fluorescence during a brief (
1 s) pulse of light
that saturates photochemistry so that there is no quenching anymore due
to qP (Fig. 2).
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NPQ HAS MULTIPLE COMPONENTS |
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NPQ can be divided into at least three different components
according to their relaxation kinetics in darkness following a period
of illumination, as well as their response to different inhibitors
(Fig. 2; Horton and Hague, 1988
). The major and most rapid component in
most algae and plants is the pH- or energy-dependent component, qE. A
second component, qT, relaxes within minutes and is more important in
algae, but rather negligible in most plants during exposure to excess
light. This component is due to the phenomenon of state transition, the
uncoupling of LHCs from PSII. qT will not be considered further here
because it does not seem to be important for photoprotection (Niyogi,
1999
). The third component of NPQ shows the slowest relaxation and is
the least defined. It is related to photoinhibition of photosynthesis and is therefore called qI.
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RAPIDLY INDUCIBLE AND REVERSIBLE qE QUENCHING IS pH-DEPENDENT |
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Absorption of sunlight that exceeds a plant's capacity
for CO2 fixation results in a buildup of the
thylakoid
pH that is generated by photosynthetic electron transport.
The decrease in pH within the thylakoid lumen is an immediate signal of
excessive light that triggers the feedback regulation of light
harvesting by qE. The control by lumen pH allows induction or reversal
of qE within seconds of a change in light intensity (see Fig. 2), which
is fast enough to cope with natural fluctuations in light intensity
that are due to, for example, passing clouds on a partly sunny day.
The requirement for low lumen pH is evidenced by the
inhibition of qE by uncouplers of the
pH such as nigericin.
Screening for mutants with lower qE levels has uncovered several
mutants that are defective in generation of the
pH due to defects in photosynthetic electron transport. In these mutants qP is also affected
(Shikanai et al., 1999
). However, low lumen pH that induces qE does not
have to be generated by light-dependent reactions. Using isolated
thylakoids it is possible to induce qE in darkness by simply lowering
the pH of the buffer or by generating a
pH via ATP hydrolysis and
reverse proton pumping by the ATP synthase (Gilmore and Yamamoto, 1992
;
Krieger et al., 1992
).
Intensive research during the past several years has led to a
concept of the role of the
pH in qE. A decrease in lumen pH induces
qE through protonation of PSII proteins and activation of xanthophyll
synthesis via a xanthophyll cycle. Together, binding of protons and
xanthophylls to specific sites in the PSII antenna causes a
conformational change that switches a PSII unit into a quenched state
with a short 1Chl* lifetime and a low
fluorescence yield (Gilmore, 1997
). In the following sections we will
describe further the mechanistic details of this pH-dependent switch
and the physiological significance of qE.
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LOW LUMEN pH ACTIVATES A XANTHOPHYLL CYCLE |
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The decrease in lumen pH in excessive light activates the
interconversion of specific xanthophyll pigments (oxygenated
carotenoids) that are mostly bound to LHC proteins. This
interconversion occurs on a timescale of minutes as part of a
xanthophyll cycle, as depicted in Figure
3. All organisms that exhibit qE have a
xanthophyll cycle, of which there are two main types. The violaxanthin
cycle in plants, green algae (Chlorophyta), and brown algae
(Phaeophyceae) consists of the pH-dependent conversion from
violaxanthin, a xanthophyll with two epoxide groups, first to
antheraxanthin (one epoxide group) and then to zeaxanthin (no epoxide
group). Diatoms and most other eukaryotic algae have a different
xanthophyll cycle (the diadinoxanthin cycle) that involves a conversion
from diadinoxanthin (one epoxide group) to diatoxanthin (no epoxide
group). Under certain conditions these algae can be observed to operate
both the violaxanthin cycle and the diadinoxanthin cycle (Lohr and Wilhelm, 1999
).
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In plants the de-epoxidation reaction is catalyzed by
violaxanthin de-epoxidase (VDE). VDE is a 43-kD nucleus-encoded protein that is localized in the thylakoid lumen (Bugos and Yamamoto, 1996
).
The purified VDE enzyme is activated by low pH (Eskling et
al., 1997
), and cloning of the VDE gene revealed that the
enzyme has a Glu-rich region that may be protonated at low pH
(Bugos and Yamamoto, 1996
). Upon acidification of the lumen, VDE
associates with the thylakoid membrane (Hager and Holocher, 1994
) where
it can interact with its substrate violaxanthin. VDE uses ascorbic acid
(vitamin C) to reduce the epoxide group, and it has a
Km for ascorbic acid that is strongly
dependent on pH, probably because ascorbic acid rather than ascorbate
is the actual cosubstrate (Bratt et al., 1995
).
A different enzyme, zeaxanthin epoxidase (ZE), catalyzes the
epoxidation reactions that complete the violaxanthin cycle. ZE is
a flavin adenine dinucleotide-containing,
O2-dependent mono-oxygenase that uses
reduced ferredoxin to epoxidize first zeaxanthin and then
antheraxanthin (Bouvier et al., 1996
). Because of its pH optimum of 8, ZE is thought to be located on the stromal side of the thylakoid
membrane and to be constitutively active. The level of zeaxanthin is
therefore determined by the activity of VDE compared with ZE, with
rapid accumulation of zeaxanthin occurring upon activation of VDE in
excessive light. ZE and VDE are the first known plant members of the
lipocalin family, a diverse group of proteins that bind small
lipophilic molecules and share a conserved tertiary structure of eight
-strands in a barrel configuration (Bugos et al., 1998
).
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XANTHOPHYLLS ARE NECESSARY, BUT NOT SUFFICIENT FOR qE IN VIVO |
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The amount of zeaxanthin synthesized via the violaxanthin cycle is
highly correlated with the level of qE in a large number of plants
under a variety of conditions (Demmig-Adams, 1990
). In a similar
manner, a correlation has been shown between qE and the conversion of
diadinoxanthin to diatoxanthin in diatoms (Arsalane et al., 1994
).
Isolated thylakoids that are devoid of zeaxanthin have been observed to
exhibit high levels of qE (Rees et al., 1992
), but only at lumen pH
values that are lower than those normally occurring in vivo.
The requirement for the xanthophylls in qE has been investigated in
vivo by using inhibitors and mutants. Dithiothreitol has been used
extensively as a remarkably specific inhibitor of VDE and
diadinoxanthin de-epoxidase. Blocking zeaxanthin synthesis in leaves
with dithiothreitol results in inhibition of qE, the extent of
inhibition depending on the plant species examined (Horton et al.,
1994
). Mutants that are unable to convert violaxanthin to
antheraxanthin and zeaxanthin have been isolated from Arabidopsis and
Chlamydomonas (for review, see Niyogi, 1999
). As in the
inhibitor studies, lower levels of qE accompanied the lack of
zeaxanthin in these npq1 mutants. Recent studies using
antisense VDE in tobacco have confirmed the results obtained from
mutant analyses (Chang et al., 2000
).
The alga Mantoniella squamata has an incomplete xanthophyll
cycle, only leading to antheraxanthin in vivo, but still exhibits qE
(Goss et al., 1998
). This implies that the role of zeaxanthin in qE can
be replaced by antheraxanthin in this alga. The involvement of
antheraxanthin in plants had been proposed in earlier studies where
zeaxanthin-independent qE could be explained by taking the amounts of
antheraxanthin into account (Gilmore and Yamamoto, 1993
). Therefore, it
has become a common practice to calculate the level of de-epoxidation
of a given organism as the amount of antheraxanthin and zeaxanthin in
comparison with the total amount of antheraxanthin, zeaxanthin, and violaxanthin.
In addition to antheraxanthin and zeaxanthin, a third xanthophyll,
lutein, has also been implicated in qE. These suggestions were
supported by studies on the Chlamydomonas lor1
mutant, which only lacks lutein and loroxanthin, but shows lower qE
than the wild type (Niyogi et al., 1997
). A similar mutant in
Arabidopsis, lut2, which is defective in the lycopene
-cyclase and therefore lacks lutein, also has less qE (Pogson et
al., 1998
). Double mutants of Chlamydomonas or Arabidopsis
that lack lutein and zeaxanthin are totally devoid of any qE and are
very sensitive to high light (Niyogi et al., 1997
, 2001
). Furthermore,
plants that overexpress the lycopene
-cyclase have an increased
lutein content and show a slight, but significant increase in the rate
of qE induction, even though their xanthophyll cycle pool size is
reduced in comparison with the wild type (Pogson and Rissler,
2000
).
It is interesting that a third kind of xanthophyll cycle involving
lutein-5,6-epoxide has been found in a parasitic plant, Cuscuta
reflexa (Fig. 3). In this plant neoxanthin is missing and is
replaced by lutein-5, 6-epoxide. In high light, lutein-5,6-epoxide is
de-epoxidized to lutein, presumably by VDE, which was previously shown
to use lutein-5,6-epoxide as substrate (Bungard et al., 1999
). The
existence of this new cycle is consistent with the idea that lutein has
a photoprotective function that the epoxide lacks.
Although zeaxanthin is generally necessary for maximal qE in vivo, it
is not sufficient. In mutants that accumulate zeaxanthin constitutively, qE must still be induced by a low pH (Niyogi, 1999
).
This demonstrates that the low pH has an additional role in qE, besides
activation of the xanthophyll cycle.
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A CONFORMATIONAL CHANGE IS INVOLVED IN qE |
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Lowering the pH in the thylakoid lumen not only activates
the de-epoxidation of violaxanthin to zeaxanthin, but it is also necessary for a conformational change in the thylakoid membrane that
can be monitored by absorbance changes. Two high light-induced absorbance changes in leaves or isolated thylakoids are associated with
qE. One absorbance change occurs at 505 nm and is due to the conversion
of violaxanthin to zeaxanthin. The second one at 535 nm
(
A535) depends on both zeaxanthin and low pH
and is thought to be due to a conformational change in the thylakoid
membrane (Krause, 1973
; Bilger and Björkman, 1994
). qE is always
accompanied by the
A535.
Conformational changes have also been inferred from measurements
of Chl fluorescence lifetime distributions, which depend on the
molecular environment of the excited Chl (Gilmore, 1997
). In these
experiments the presence of a
pH alone causes a lifetime shift from
approximately 2 to 1.6 ns. This shift likely reflects a
protonation-dependent conformational change that is independent of
zeaxanthin. When both
pH and zeaxanthin are present, a fluorescence lifetime component at 0.4 ns appears at the expense of the 1.6 ns
component. The amount of the 0.4 ns component is proportional to qE.
Together, the absorbance and Chl fluorescence lifetime results suggest
that a conformational change due to binding of protons and xanthophylls
(maybe zeaxanthin) is necessary for qE.
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THE PsbS PROTEIN IS ESSENTIAL FOR qE |
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Several LHC proteins associated with PSII have been implicated in
qE. In particular the minor LHC proteins CP29 and CP26 were suggested
to be involved in qE based on the relative enrichment of associated
xanthophyll cycle pigments (Bassi et al., 1997
) and binding of
N,N'-dicyclohexylcarbodiimide (Walters et al., 1994
), an inhibitor of qE that reacts with proton active residues. However, these proteins have not been found in some organisms that
exhibit qE such as Mantoniella and diatoms.
To identify proteins involved in qE Arabidopsis mutants have been
isolated that are defective in qE, but have normal xanthophyll levels
(Li et al., 2000
; Peterson and Havir, 2000
). Characterization of one of
these mutants, npq4-1, revealed that a PSII protein, PsbS,
is essential for qE (Li et al., 2000
). PsbS belongs to the LHC protein
superfamily, but it has four transmembrane helices instead of three and
different pigment-binding characteristics (Funk et al., 1995
). Despite
the absence of the PsbS protein, light harvesting is not impaired in
the npq4-1 mutant and the levels of the other LHC proteins
are normal. However, in addition to lacking qE, npq4-1 also
lacks the conformational change monitored by
A535 (Li et al., 2000
).
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WHAT IS THE BIOPHYSICAL MECHANISM OF 1CHL* DE-EXCITATION? |
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The pH- and xanthophyll-dependent conformational change
and the PsbS protein are necessary for qE, but the actual biophysical mechanism of 1Chl* de-excitation is still
unknown. The central and long-standing question is whether the
involvement of xanthophylls is direct or indirect. The xanthophylls may
act indirectly as allosteric regulators of the LHCs that cause a switch
from light harvesting to energy dissipation (qE; Horton et al., 2000
).
In this case the conformational change must somehow facilitate
1Chl* de-excitation, which may occur by internal
conversion of Chl itself to the ground state, releasing excitation
energy as heat. Isolated, detergent-solubilized LHCs can exhibit
pH-dependent Chl fluorescence quenching, which is inhibited by
violaxanthin and promoted by zeaxanthin (Ruban et al., 1997
).
On the other hand, xanthophylls may directly de-excite
1Chl*. This is theoretically possible according
to recent spectroscopic experiments, which showed that isolated
xanthophyll cycle pigments possess a lowest singlet excited state that
is below that of 1Chl* (Polívka et al.,
1999
; Frank et al., 2000
). However, because both violaxanthin and
zeaxanthin could potentially accept energy from
1Chl*, these results do not explain why the
xanthophyll cycle is necessary for qE. In vivo, other factors such as
different binding sites for zeaxanthin and violaxanthin, as well as
distance and orientation of these xanthophylls relative to Chl may be
important in determining if energy transfer occurs. Therefore,
structural rather than energetic differences between zeaxanthin and
violaxanthin are likely to be critical. For example, the xanthophylls
that are important for qE (zeaxanthin, antheraxanthin, lutein, and diatoxanthin) all have a de-epoxidized 3-hydroxy
-ring endgroup (Fig. 3), in contrast to violaxanthin, diadinoxanthin, and other xanthophylls.
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A WORKING MODEL FOR qE |
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Figure 4 shows a summary model for
how qE might function. Under limiting light conditions, qE is not
induced and the PSII antenna is characterized by efficient transfer of
excitation energy to the reaction center (Fig. 4A). Upon high light
exposure, proteins in the antenna become protonated, causing a switch
in the Chl fluorescence lifetime from 2 to 1.6 ns (Fig. 4B). We propose
that one of these proteins is PsbS. At the same time, VDE is activated, but the conversion of violaxanthin to zeaxanthin is slower than protonation. Binding of zeaxanthin to a protonated protein, possibly PsbS itself, causes the formation of a quenching complex, evident in a
further decrease in the Chl fluorescence lifetime to 0.4 ns (Fig. 4C).
To form the quenching complex, a conformational change must occur
within the PSII antenna, perhaps originating in a conformational shift
of PsbS induced by the binding of zeaxanthin and protons. The
conformational change in the antenna can be followed by measuring
A535. Formation of the quenching complex could
involve changes within the dimeric PSII or changes in the interaction of several supercomplexes with each other. Upon a decrease in light
intensity, a decrease in
pH should result in the relatively rapid
de-protonation of the antenna protein(s) and the disassembly of the
quenching complex, changing the fluorescence lifetime back to 2 ns
(Fig. 4D). Zeaxanthin conversion to violaxanthin occurs more slowly.
Therefore, a plant exposed to fluctuating light such as sunflecks is
able to reach maximum qE faster after previous exposure to high light
by directly switching from state D shown in Figure 4 to state C
(Demmig-Adams et al., 1999
).
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qE AND XANTHOPHYLLS ARE IMPORTANT FOR PHOTOPROTECTION |
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The npq mutants have been useful for studying the
photoprotective function of qE during high light stress. The
Arabidopsis mutants npq1 and npq4 are more
sensitive to photoinhibition than the wild type in a short-term
high-light treatment (time scale of hours; Niyogi et al., 1998
; Havaux
and Niyogi, 1999
), suggesting that qE normally functions to protect
PSII. The photoprotective effect of qE may be due to decreased
production of 1O2* and
other reactive oxygen species. qE may also prevent the over-reduction
of the electron transport chain and the over-acidification of the
lumen, which are known to sensitize PSII to photodamage.
After several days in high light, the npq1 mutant showed
more photooxidative bleaching and lipid peroxidation than
npq4 (Havaux and Niyogi, 1999
). Similar to npq1,
antisense tobacco plants that lack VDE showed a significant increase in
photoinhibition and a decrease in pigment content when subjected to
high light or a combination of moderate light and water stress in a
growth chamber (Verhoeven et al., 2001
). When transferring npq1
lut2, an Arabidopsis double mutant missing zeaxanthin and lutein,
into high light even more photooxidative bleaching and premature
senescence was visible (Niyogi et al., 2001
). These results indicate
that xanthophylls have a function not only in qE, but also in the
protection of the thylakoid membrane against photooxidative damage.
Zeaxanthin may directly protect the thylakoid membrane against
photooxidation. Thylakoid membranes are enriched in polyunsaturated fatty acids that are particularly susceptible to
1O2*-initiated lipid
peroxidation reactions. Generation of
1O2* within leaves
infiltrated with the photosensitizing chemical eosin caused severe
lipid peroxidation in mature leaves of npq1, but not in
wild-type leaves, suggesting that the photoprotective role of
zeaxanthin is not restricted to the LHCs (Havaux et al., 2000
).
Zeaxanthin may be an important antioxidant in the thylakoid membrane
bilayer itself, where it could scavenge reactive oxygen species and/or
terminate lipid peroxidation chain reactions. Zeaxanthin and lutein
slowed down the lipid peroxidation in artificial membranes made from
egg yolk lecithin in response to a peroxyl radical generator (Sujak et
al., 1999
). Investigating the antioxidant roles of zeaxanthin and
lutein has important implications not only for thylakoids, but also for
retinal membranes of the primate macula lutea where these xanthophylls
are found specifically. Zeaxanthin could also have a structural
function in the lipid bilayer itself. This xanthophyll has been shown
to decrease the fluidity of the membrane (Tardy and Havaux, 1997
), and
a decrease in fluidity could be important by lowering the penetration
of reactive oxygen species inside the thylakoid.
In summary, qE protects PSII against short-term high light and
fluctuations in light intensities, whereas xanthophylls have an
additional photoprotective role in longer-term high light. Although the
light sensitivity of the npq mutants of Arabidopsis and the
VDE antisense plants of tobacco has been demonstrated clearly, these
mutants are remarkably tolerant of strong light. In particular, young
leaves of the npq mutants are quite resistant to high light
or oxidative stress (Havaux et al., 2000
; Niyogi et al., 2001
),
suggesting that other important photoprotective mechanisms like
tocopherols or other antioxidants can compensate at least partially for
the lack of qE and/or xanthophylls.
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qI QUENCHING IS INVOLVED IN LONG-TERM DOWN-REGULATION OF PSII |
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Under more prolonged, severe light stress qE is replaced by a
sustained, slowly reversible component of NPQ, called qI. In contrast
to qE, qI is much less characterized and might be due to a mix of
photoprotection and photodamage. Chl fluorescence measurements can help
to distinguish between photoprotective mechanisms and photoinhibition.
The min-imum fluorescence level in the dark-adapted state,
Fo (see Fig. 2), is decreased in direct
proportion to the maximal fluorescence, Fm,
by the photoprotective quenching like qE, whereas photoinhibition
normally increases the Fo level while decreasing the Fm level (Gilmore et al.,
1996
).
Overwintering plants show an acclimation to the cold by increasing the
xanthophyll pool size, as well as by having an increased retention of
zeaxanthin and antheraxanthin that is associated with qI (Demmig-Adams
et al., 1999
). Overwintering snow gum trees appear to form special
Chl-quenching complexes that dissipate excess excitation energy
(Gilmore and Ball, 2000
). Measurements of Chl fluorescence lifetime
distributions of this qI state have revealed lifetime changes that are
similar to those observed during qE, but that are reversed only
gradually at room temperature (Gilmore and Ball, 2000
). Induction and
reversal of qI in these overwintering leaves may involve major
reorganization of pigment-protein complexes in the thylakoid membrane.
Some part of the persistent qI induced by low temperature is actually
better described as sustained qE because it is pH-dependent. By adding
nigericin, an uncoupler, this kind of qI can be relaxed quickly
(Gilmore and Björkman, 1995
). It may be due to the maintenance of
the
pH by the reverse proton pumping catalyzed by the ATP-synthase (Gilmore, 1997
). Therefore, in contrast to normal qE it relaxes only
slowly in darkness.
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CONCLUSIONS AND FUTURE DIRECTIONS |
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Much has happened since the last Update on this topic
was published in this journal (Horton et al., 1994
). Based on
physiological studies, the main function for qE seems to be the
protection of PSII from photoinhibition. However, when qE is impaired,
other mechanisms are able to compensate for long-term acclimation, at least in the absence of additional stresses. Further studies using qE
mutants are necessary to test the ecological importance of qE and to
uncover other important photoprotective mechanisms that complement qE.
The PsbS protein is an essential component of the mechanism of qE. PsbS itself may be the site of qE in the antenna, or it may function in concert with other LHC proteins. To understand how PsbS actually functions in qE, its location within the antenna, as well as possible proton- and pigment-binding sites within PsbS have to be determined. Characterization of additional mutants or the use of reverse genetics may provide insights into the involvement of other proteins.
Another new development in the field has been the finding that both zeaxanthin and violaxanthin are potential acceptors of excitation energy from 1Chl*. In the future it will be important to design experiments that enable measurement of the energy levels of xanthophylls in their native protein environment and ultimately to determine if there is a direct energy transfer from Chl to a xanthophyll. The application of new and diverse techniques, from chemistry to genetics to ecology, will be necessary to understand qE, a nearly ubiquitous response of photosynthetic eukaryotes to excess light energy.
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ACKNOWLEDGMENTS |
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We thank Adam Gilmore, Peter Horton, Barry Pogson, and Harry Yamamoto for sharing results prior to publication and Alba Phippard and Jae Pasari for critical reading of the manuscript. We apologize to colleagues whose work we were not able to cite due to space limitations.
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FOOTNOTES |
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Received September 27, 2000; accepted November 19, 2000.
1 This work was supported by the Searle Scholars Program/The Chicago Community Trust, by the U.S. Department of Agriculture-National Research Initiative Competitive Grants Program, and by the U.S. Department of Energy.
* Corresponding author; e-mail niyogi{at}nature.berkeley.edu; fax 510-642-4995.
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X.-P. Li, A. M. Gilmore, and K. K. Niyogi Molecular and Global Time-resolved Analysis of a psbS Gene Dosage Effect on pH- and Xanthophyll Cycle-dependent Nonphotochemical Quenching in Photosystem II J. Biol. Chem., September 6, 2002; 277(37): 33590 - 33597. [Abstract] [Full Text] [PDF] |
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C. Kulheim, J. Agren, and S. Jansson Rapid Regulation of Light Harvesting and Plant Fitness in the Field Science, July 5, 2002; 297(5578): 91 - 93. [Abstract] [Full Text] [PDF] |
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J. Lavaud, B. Rousseau, H. J. van Gorkom, and A.-L. Etienne Influence of the Diadinoxanthin Pool Size on Photoprotection in the Marine Planktonic Diatom Phaeodactylum tricornutum Plant Physiology, July 1, 2002; 129(3): 1398 - 1406. [Abstract] [Full Text] [PDF] |
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L. Xiong, H. Lee, M. Ishitani, and J.-K. Zhu Regulation of Osmotic Stress-responsive Gene Expression by the LOS6/ABA1 Locus in Arabidopsis J. Biol. Chem., March 1, 2002; 277(10): 8588 - 8596. [Abstract] [Full Text] [PDF] |
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P. Muller-Moule, P. L. Conklin, and K. K. Niyogi Ascorbate Deficiency Can Limit Violaxanthin De-Epoxidase Activity in Vivo Plant Physiology, March 1, 2002; 128(3): 970 - 977. [Abstract] [Full Text] [PDF] |
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J.-D. Rochaix Assembly, Function, and Dynamics of the Photosynthetic Machinery in Chlamydomonas reinhardtii Plant Physiology, December 1, 2001; 127(4): 1394 - 1398. [Full Text] [PDF] |
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