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Photosynthesis Research 53: 229–241, 1997.
c 1997 Kluwer Academic Publishers. Printed in the Netherlands.
Regular paper
Chloroplast redox regulation of nuclear gene transcription during
photoacclimation?
Dion G. Durnford & Paul G. Falkowski
Environmental Biophysics and Molecular Biology Program, Department of Applied Science, Building 318,
Brookhaven National Laboratory, Upton, NY 11973, USA
Received 1 November 1996; accepted in revised form 26 February 1997
Key words: light-harvesting antenna, plastid signal, plastoquinone pool
Abstract
The role of the redox state of ferredoxin/thioredoxin within the chloroplast is well established for the feedback
regulation of enzyme activity in the Calvin cycle. However, evidence has emerged also suggesting that chloroplast
electron transport components regulate plastid and nuclear gene expression. Using the unicellular green alga,
Dunaliella tertiolecta, as a model organism, we have shown that the cell acclimates to changes in growth irradiance
by altering the abundance and activities of photosynthetic components, in particular the light harvesting complexes
(LHC). Pharmacological data suggests that light intensity is sensed through the redox status of the plastoquinone
pool leading to the regulation of nuclear encoded genes, such as Lhcb. This signal may be transduced through a
redox regulated protein kinase that (in)directly interacts with the nuclear transcription apparatus. The redox state of
the plastoquinone pool seems to play a pivotal role in sensing cellular energy status and in regulating photosynthetic
capacity. Other cellular pathways, including carbon fixation, carbohydrate metabolism and nutrient assimilation
have been shown to have feedback influences on photosynthesis, that may be sensed by the redox state of the
plastoquinone pool.
Introduction
All organisms have, to varying degrees, the capacity
to adjust metabolic pathways in response to environmental cues. Physiological acclimation requires signal transduction pathways and feedback mechanisms
that link gene expression to changes in the environment. One of the most important cues for photosynthetic organisms is light. Phytochrome was the first
light responsive element discovered, and the role of
this chromophore in regulating both developmental
and reproductive responses in higher plants is well
described (Smith 1995). There is also compelling
evidence for a blue light receptor(s) in cyanobacteria, eucaryotic algae and higher plants, although the
molecular identity of this chromophore remains elu? The US Government’s right to retain a non-exclusive, royaltyfree licence in and to any copyright is acknowledged.
sive (Short and Briggs 1994). Both phytochrome and
the blue-light responsive elements appear to be much
more sensitive to spectral quality or photoperiod rather
than photon flux densities that are relevant to photosynthetic electron flow. However, some evidence has suggested that photoacclimation responses are transduced
via metabolic signals arising from the photosynthetic
apparatus. Here, we review the evidence for regulation
of nuclear gene expression based on the redox status
of specific carriers in the photosynthetic electron transport chain. For additional information and perspective,
the reader is referred to other reviews on redox control
of gene transcription (Allen 1993; Allen 1995; Levings
and Siedow 1995).
Yoshihiko Fujita, to whom this issue is dedicated, was amongst the first researchers to ascribe
light-induced changes in the photosynthetic electron
transport components to electron transport imbalances.
Fujita and his collaborators’ pioneering work increased
ICPC: PIPS No.: 139262 BIO2KAP
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Figure 1. Dunaliella tertiolecta cultures grown under high (left) and low (right) irradiance. Under high light conditions (in excess of 1500 mol
quanta m 2 s 1 ) the cell contains lower amounts of chlorophyll, a higher content of carotenoids per cell and a chl a/b ratio of around 8. The
deep green culture on the right, containing more chlorophyll per cell, was grown under low light intensity (ca. 70 mol quanta m 2 s 1 ) and
has a chl a/b ratio of around 4. Photograph is courtesy of Dr. Assaf Sukenik.
our understanding of how a cell perceives changes in its
light environment, especially as it relates to the adjustment of photosystem stoichiometry. In this review we
consider Fujita’s observations, along with others, in
the context of the experimental evidence indicating
possible molecular mechanisms for sensing changes in
photon flux density (PFD) and the transduction of the
signal leading to photoacclimatory changes.
Photoacclimation
We define photoacclimation as reversible phenotypic
changes in activities and/or concentrations of enzymes
or other biosynthetic molecules, such as pigment protein complexes and photosynthetic electron transport
components, that compensate for changes in spectral
irradiance, independent of plant developmental pro-
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cesses (Falkowski and LaRoche 1991). Photoacclimation occurs on a variety of time scales (Falkowski et al. 1994; Anderson et al. 1995). On short time
scales of minutes to hours, plants undergo changes
in response to high frequency (subdaily) variations in
light intensity. These responses include the dissipation of excess excitation energy via xanthophyll cycle
carotenoids (Demmig-Adams and Adams 1996) and
by state transitions where reversible phosphorylation
of LHC II leads to complementary alterations in the
effective absorption cross section of PS II and PS I
(Bonaventura and Myers 1969; Bennett 1983). As we
shall describe, these phenomena are part of a nested
series of photoacclimatory responses, which, on the
longer time scales, can lead to changes in gene expression. The latter requires a signal transduction pathway
that couples an irradiance sensor to both nuclear and
plastid gene expression.
Although many higher plants can photoacclimate
(Anderson et al.1988; Chow et al. 1990; Kim et al.
1993; Anderson et al. 1995), their ability to do so is
limited as compared to algae (Bennett 1987; Falkowski and LaRoche 1991). In higher plants a light gradient can exist within the leaf, generating degrees
of sun and shade adapted chloroplasts within a single plant (Nishio et al. 1994). This gradient reveals
physiological plasticity that is coupled to development
through differentiation. However, many higher plants
have evolutionarily adapted (i.e. are selected) to either
a sun or shade environment and display phenotypes
characteristic of either one or the other light regime
(Boardman 1977). In contrast, algae generally have an
extremely high degree of physiological plasticity that
permits rapid and reversible adjustments to changes in
the average growth irradiance. Green unicellular algae
in particular have a remarkable ability to survive, and
acclimate to, a wide range of irradiance levels. Over the
past several years, we have studied photoacclimation
in the halotolerant chlorophyte, Dunaliella tertiolecta.
This organism is easy to culture, has a single cupshaped chloroplast, lacks a cell wall, does not undergo
sexual recombination (and therefore the study of irradiance responses can be distinguished from developmental processes), and displays changes in photoacclimatory variables such as cellular chlorophyll that are
large and easily measured (Figures 1 and 2).
Within a few hours of a transition from high light
(e.g. 700 mol quanta m 2 s 1 ) to low light (70 mol
quanta m 2 s 1 ), D. tertiolecta redirects the end products of carbon fixation (i.e. carbohydrates) towards
the production of proteins. One of the first detectable
Figure 2. Kinetics of photoacclimation in Dunaliella tertiolecta
following a high light (700 mol quanta m 2 s 1 ) to low light
(70 mol quanta m 2 s 1 ) transition. (A) Changes in chlorophyll
per cell (open triangles) and the Chl a/b ratio (closed circles) over
a 5 day period. (B) Kinetics of LHC II (closed circles) and RC II
changes (open triangles) during a high light to low light transition.
Figure is a modification from Sukenik et al. (1990).
proteins to change is LHC II. A 10 fold decrease in
irradiance induces a 4 fold increase in Lhcb mRNA
within 9 hours, and ultimately leads to a 3-fold increase
in LHC II complexes (LaRoche et al. 1991). Nuclear
run-on transcription and mRNA stability experiments
have established that Lhcb gene expression is regulated at the level of transcription (Escoubas et al. 1995).
The changes in LHC II are subsequently followed by
a net increase in other components of the photosynthetic electron transport chain, such that the ratios of
the components remain unchanged, irrespective of the
growth irradiance (Sukenik et al. 1987a, 1990). A new
steady state level of all photosynthetic components is
reached within ca. 72 h (Figure 2).
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Hypotheses to account for the photoacclimation
response
What is the molecular basis of photoacclimation? At
least three hypotheses can be developed to account
for the light intensity induced changes in Lhc gene
expression. The first postulates a photoreceptor, such
as phytochrome, or a blue light receptor(s) that somehow senses variations in photon flux density and causes
changes in nuclear gene expression. A second hypothesis invokes a feedback from a light intensity regulation
of chlorophyll synthesis (which is confined to the plastid), to either gene expression and/or protein stability.
The third hypothesis proposes a feedback to photosynthetic electron transport or some end product(s) of photosynthetic metabolism that influences gene expression. Let us examine the evidence for each hypothesis
noting that they are not mutually exclusive.
Evidence for a photoreceptor
Photoreceptors are characterized by spectrally-induced
reversible responses that are not directly coupled to
metabolism. The best characterized photoreceptors are
the phytochromes, a conserved family of proteins complexed with an open tetrapyrrole chromophore. The
chromophore is activated through a red light induced
conversion of the Pr to the Pfr form. In higher plants
there are two main types of phytochromes (Furuya and
Schäfer 1996), and there is evidence for two distinct
signal transduction pathways, one involving G protein activation and the other being calcium/calmodulin
dependent (Bowler et al. 1994).
The evolutionary origin of phytochrome is unclear.
The chromophore has structural similarities to phycobilins, including the covalent bonding of the tetrapyrrole to the protein via a sulfide bridge from cysteine.
Phytochrome-like gene sequences have been reported
in the green alga, Mesotaenium; however, red/far red
reversibility has not been demonstrated (Morand et al.
1993). No phytochrome sequences have been detected
in a genomic library of Dunaliella tertiolecta (Harry
Smith, personal communication), and attempts to isolate the chromophore from green algae have not been
successful (HW Siegelman, personal communication).
Although there is some evidence for phytochromelike proteins in chlorophyte algae, there is little evidence indicating a role for phytochrome in light mediated responses in unicellular algae. Perhaps this should
not be surprising. In aquatic systems, spectral irradi-
ance is highly modified by the medium itself. Absorption and scattering by water leads to rapid depletion
of red and far-red light with depth, but permits a large
fraction of blue and blue/green light to penetrate (Kirk
1994). Hence, chromophores keyed to red/far-red variations would seem to have little value for planktonic cells in aquatic environments. While phytochrome
probably does have cyanobacterial origins (Hughes
et al. 1997), it would appear that the utilization of
this chromophore as a major light responsive element
emerged relatively late in the evolution of photosynthetic organisms, and has been utilized in terrestrial
plants primarily as a sensor of photoperiod rather than
of light intensity (Anderson et al. 1995).
Some cyanobacteria respond to changes in the relative level of red and green irradiance (chromatic
adaptation) by adjusting phycoerythrin and /or phycocyanin levels within the phycobilisome; this response
is thought to be sensed by a photoreceptor (Grossman
et al. 1993). A possible candidate for this receptor has
been identified that has some sequence similarity to
both phytochrome and ethylene receptors (Kehoe and
Grossman 1996). Chromatic adaptation is independent
of electron transport rates in the filamentous cyanobacterium, Calothrix (Campbell et al. 1993), adding further evidence for a light receptor mediated response.
Blue light responses have been more extensively
examined in higher plants and are attributed to the
control of numerous cellular processes (reviewed by
Short and Briggs 1994). In algae, a blue light receptor(s) is implicated in the regulation of LHC expression (Kindle 1987; Humbeck et al. 1988; Hermsmeier
et al. 1991; Melis et al. 1996), cell division (Munzner
and Voigt 1992) and chlorophyll biosynthesis (Matters
and Beale 1995). In Chlamydomonas, the induction
of Lhc expression in blue light is DCMU-insensitive,
suggesting that the signal is independent of photosynthesis (Kindle 1987). However, other studies using
Chlamydomonas and Scenedesmus indicate that light
intensity and light quality are both factors influencing
photoacclimation (Humbeck et al. 1988; Melis et al.
1996).
While reversible spectral responses are often interpreted as evidence for a photoreceptor, in algae it is difficult to distinguish between the effects of light quality
on a specific target molecule and indirect effects on
photosynthetic electron transport (as will be discussed
below). In contrast to higher plant leaves, because
individual algal cells are optically thin, their optical
absorption cross section are highly spectrally dependent. Hence, exposing cells to blue light and red light
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at equal photon fluence rates does not translate to an
equal rate of photon absorption. Rather, for most algal
systems, the Soret bands of the antenna pigments are
more efficient at photon absorption than the Q bands
of chlorophylls; there is virtually no absorption by
cells in far-red light. A physiologically more meaningful test for spectral responses that are independent
of photosynthesis would be to expose cells to different
wavelengths of light at fluence rates that elicit identical
electron transport rates. To our knowledge, such experiments have not been performed. This issue becomes
critical to evaluating potential signal transduction pathways. For example, in cyanobacteria light intensity and
light quality can be manipulated to give the same photoacclimation state; however, the responses have been
correlated with changes in the redox poise of the plastoquinol pool rather than with a photoreceptor (Fujita
et al. 1987; Murakami and Fujita 1991b, 1993).
Evidence for feedback from the chlorophyll
biosynthetic pathway
Regulation of LHC expression during photoacclimation can be hypothesized to occur indirectly through
the light controlled biosynthesis of chlorophyll. Two
metabolic steps were identified as potentially important areas in the regulation of chlorophyll biosynthesis: the synthesis of -amino levulinic acid (ALA) and
the conversion of protochlorophyllide to chlorophyllide (Reinbothe and Reinbothe 1996). The primary
substrate for synthesis of the tetrapyrrole precursor,
ALA, is glutamic acid and its synthesis occurs in a
three step reaction that utilizes ATP, NADPH and a
tRNAglu . One of enzymes involved in this pathway,
glutamate-1-semialdehyde aminotransferase, is tightly
regulated at the transcriptional level indicating a potentially important step in the photo-regulation of chlorophyll biosynthesis (Matters and Beale 1994, 1995).
Another potential light responsive point in the
chlorophyll biosynthetic pathway is the photocatalyzed
reduction of protochlorophyllide to chlorophyllide
(Reinbothe et al. 1996). In angiosperms, protochlorophyllide oxidoreductase (POR) is light dependent, thus
the completion of the chlorophyll biosynthetic pathway requires light. Many, but not all, algae are able
to synthesize chlorophyll in the dark due to the presence of a light-independent POR. Conifers, which can
also synthesize chlorophyll in the dark, seem to have
both a light-dependent and light-independent form of
POR (see Reinbothe and Reinbothe 1996). The abili-
ty of some organisms, especially algae, to synthesize
chlorophyll in the dark might suggest that low light or
dark induced changes in chlorophyll levels are not solely attributed to the regulatory feedback of protochlorophyllide.
Light intensity induced chlorophyll accumulation
could, in principle, lead to an increased synthesis of reaction centers and antenna complexes that
would be capable of increasing the effective absorption cross section of the photosynthetic apparatus (Ley
and Mauzerall 1982). However, the hypothesis implies
that chlorophyll exerts its control through the posttranslational stabilization of LHC apoproteins and/or
through mRNA stabilization or transcriptional regulation, signaled by a chlorophyll biosynthetic intermediate.
Post-translational stabilization of LHC II apoproteins by the binding of chlorophyll has been reported
for higher plants and green algae (Apel and Kloppstech 1980; Michel et al. 1983). To test if this mechanism could account for the LHC II changes induced
by decreasing irradiance levels, Mortain-Bertand et al.
(1990) blocked the formation of ALA from glutamate
with gabaculine and found that 35 S labeled LHC II
apoproteins were stable in the light. However, the cells
did not accumulate more LHC II apoproteins upon
transfer to low light. These experiments suggest that
while chlorophyll synthesis is not required in Dunaliella for accumulation of LHC II apoproteins, the posttranslational stabilization by chlorophylls is required
for an increase in total cellular LHC II levels during
acclimation to reduced irradiance levels.
LHC synthesis may also be controlled at the
transcriptional level through feedback regulation by
chlorophyll biosynthesis intermediates. In the green
algae Chlamydomonas and Dunaliella, the presence
of gabaculine or levulinic acid did not affect the
normal light induced increase in Lhc mRNA accumulation through dark to light or high-light to lowlight transitions (Johanningmeier and Howell 1984;
LaRoche et al. 1991). These latter results suggested that chlorophyll biosynthesis precursors between
ALA and chlorophyll are not required for the observed,
enhanced rate of Lhc gene expression. However, blocking synthesis at later stages with inhibitors or by mutation caused reductions in the accumulation of Lhc
mRNA following dark to light transitions (Johanningmeier and Howell 1984). These changes were later correlated to transcription rates by nuclear run-on
assays (Jasper et al. 1991) and were interpreted as
evidence that precursors of chlorophyll biosynthesis
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feedback negatively to regulate Lhc transcription and
hence accumulation.
It should be stressed that acclimation to low light is
not equivalent to deprivation of light. Cells entrained
in a light/dark cycle exhibit a diel cycle in cellular
chlorophyll, typically with an increase in chlorophyll
immediately prior to the photophase and a decrease
prior to the scotophase. This rhythm is opposite that
of photoacclimation. Yet cells entrained in a light/dark
cycle acclimate to the average photon flux density to
which they are exposed within a photoperiod (Post et al.
1984). Thus, while the results of LaRoche et al. (1991)
and Johanningmeier and Howell (1984) may appear to
conflict, both studies indicate that chlorophyll biosynthesis is requisite for acclimation to low photon fluence rates; however, the signalling for increased Lhcb
mRNA transcription does not appear to require a
chlorophyll precursor.
Evidence for feedback from photosynthetic
electron transport
The first clue implicating a role of the chloroplast electron transfer components in the control of nuclear gene
expression came from the observations of Beale and
Appelman (1971) who reported that when Chlorella
cultures were grown in the presence of sublethal concentrations of DCMU (0.5-510 6 M) cellular chlorophyll increased. As LHC II, let alone its gene sequence,
had not yet been discovered, the interpretation of these
results was limited to a vague understanding that photosynthetic metabolism influenced the abundance of pigments within the cell. Subsequent studies confirmed
the increase in chlorophyll per cell in other unicellular green algae (Nau and Melis 1992; Escoubas et
al. 1995). Koenig (1990) reported that the addition
of atrazine to Anacystis cultures, led to an increased
synthesis of phycocyanin, a component of the light
harvesting phycobilisome complexes, that mimicked
a shade acclimated phenotype. Koenig suggested D1
somehow sensed light intensity.
Fujita and colleagues explored the interaction
between photosynthetic electron transport and the regulation of photosynthesis in cyanobacteria by taking
advantage of the strong spectral differences in the optical absorption cross sections of the two photosystems
in these organisms. Using different spectral qualities
of irradiance, rather than pharmacological inhibitors,
they were able to demonstrate alterations in PS I/PS
II stoichiometry (Fujita et al. 1987; Murakami and
Fujita 1991a, b, 1993). In Synechocystis, light quality and quantity induced similar changes (Murakami
and Fujita 1991a). This was hypothesized to occur in
order to maintain an optimal quantum efficiency, and
was somehow regulated via the redox state of the plastoquinone pool or the Cyt b6 f complex; hence it was
central to the photoacclimation process.
The effects of DCMU on gene expression were
examined by Escoubas et al. (1995), who reported
that the addition of the herbicide to high-light grown
cultures of D. tertiolecta induced a two fold increase
in Lhc mRNA levels. These changes resembled a
response to a reduction in the light intensity (LaRoche
et al. 1991) correlating DCMU action to the process
of photoacclimation as observed with cyanobacteria
(Koenig 1990). Moreover, since DCMU specifically
acts within the chloroplast by inhibiting the reduction
of plastoquinol (Trebst 1980), these data provided a
specific link between chloroplast function and the regulation of nuclear gene transcription.
When D. tertiolecta cultures were grown in the
presence of DBMIB (10 7 M) at low light intensity,
photosynthetic electron transport was reduced by half
though there was little observable effect on respiration
(Escoubas et al. 1995). Application of the inhibitor
resulted in a reduction in the amount of chlorophyll per
cell and a 75% decrease in the steady state Lhc mRNA
levels even though the cultures were maintained under
low light conditions. DBMIB prevents the reoxidation
of plastoquinol (Trebst 1980) and mimicks an increase
in light intensity that is antithetic to the response seen
with DCMU treatment under high light. The inverse
effects of DCMU and DBMIB strongly suggest that
the balance between the reduced and oxidized forms
of plastoquinone are involved in the sensing of light
intensity.
Signal transduction and nuclear-chloroplast
interactions
In Dunaliella the changes in nuclear encoded Lhc
mRNA levels in response to chloroplast specific
inhibitors of photosynthetic electron transport demonstrate that a plastid to nucleus signal must exist. Evidence suggesting the existence of such a signal or
‘plastid factor’ originally arose through the examination of photooxidative stress in plant seedlings
(Oelmüller 1989; Taylor 1989). Seedlings deficient
in carotenoids, either through mutation or norflurazon treatment, were exposed to high light to induce
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photooxidation. Under non-photooxidative light conditions (ie. grown under low intensity white light or farred light) the seedlings accumulate both chlorophyll
and Lhc mRNA (Oelmüller and Mohr 1986; Burgess
and Taylor 1987). However, upon exposure to high
intensity light, chlorophyll is destroyed through photooxidation and there is a rapid reduction in the amount
of detectable Lhcb, RbcS, and plastocyanin mRNA
(Mayfield and Taylor 1984; Oelmüller and Mohr 1986;
Burgess and Taylor 1987). This was attributed primarily to transcriptional changes (Burgess and Taylor
1988). These studies addressed chloroplast biogenesis,
not photoacclimation, and are complicated by the fact
that the seedlings have an independent energy source.
Moreover, one of the Arabidopsis GUN mutants (for
genomes uncoupled) that expresses Lhcb genes under
norflurazon induced photooxidation, has wild type levels of Lhcb expression under a variety of light quality, quantity and exogenously applied sucrose levels in
mature plants (Susek et al. 1993). This indicates that
there may be a separate signal transduction pathway
for chloroplast development and photoacclimation.
While the exact nature of this plastid factor(s) is
unknown, some of its characteristics can be inferred
indirectly using chlorophyll per cell as an indicator
for photoacclimation in Dunaliella. In Dunaliella, a
high light to low light transition results in a three fold
increase in the amount of chlorophyll per cell that correlates to changes in Lhc mRNA abundance (LaRoche
et al. 1991) and an increase in transcription (Escoubas
et al. 1995). However, the addition of sub-micromolar
amounts of the cytosolic phosphatase inhibitors okadaic acid, microcystin-LR or tautomycin prevents the
increase in chlorophyll per cell by about 44%, partially inhibiting the normal photoacclimatory response.
This suggests that phosphorylation of a protein in the
cytosol or nucleus is involved in the light intensity
induced signal transduction pathway.
It was proposed that in Dunaliella Lhc gene transcription was repressed under high irradiance and activated under low light (LaRoche et al. 1991). Several putative regulatory motifs were detected in a
Dunaliella Lhc promoter by homology to those found
in higher plants and were hypothesized to be involved
in light intensity mediated control (Escoubas et al.
1995; Terzaghi and Cashmore 1995). Utilizing the
electrophoretic mobility shift assay, a DNA binding
complex, found only in high light cellular extracts,
was identified (Escoubas et al. 1995; Durnford and
Falkowski, unpublished data). Binding specificity was
localized to a 100 bp region at or near a G-box motif
(Durnford and Falkowski, unpublished data). This
motif has been implicated in light mediated responses
for a variety of nuclear encoded genes (Terzaghi and
Cashmore 1995). Binding kinetics of this DNA-protein
complex during light transition experiments are correlated with Lhc mRNA levels suggesting a regulatory
role for the DNA binding protein during photoacclimation (Durnford and Falkowski, unpublished data).
Molecular basis of redox regulation: The protein
phosphorylation hypothesis
A sudden change in light intensity will immediately
cause an imbalance in the electron flow between PS II
and PS I. Upon a transfer to a higher irradiance (Figure 3B) there is an over-excitation of PS II resulting
in a reduction of the plastoquinone pool that exceeds
its reoxidation by the cytochrome b6 f complex. This
imbalance in the redox state is sensed by a thylakoid
bound protein kinase(s) (Bennett 1991; Allen 1992).
Once activated, the thylakoid kinase(s), are known to
phosphorylate LHC II. This induces a state II condition where a population of phosphorylated LHC II
becomes dissociated from the PS II reaction center
(Bonaventura and Myers 1969; Bennett 1983). Consequently, the excitation pressure at PS II is reduced,
alleviating the imbalance in electron transport sensed
through the redox state of the plastoquinone pool. A
similar activation pathway may occur if these shortterm adjustments are not sufficient to fully compensate
for the imbalance in the redox status. Electron transfer through the plastoquinone pool is the rate limiting
step of the light reactions and is an ideal sensor site,
as it functions like a capacitor, storing electrons and
buffering against minor variations in the redox rates at
Qa and the Cyt b6 f complex.
Signal transduction could conceivably involve a
chloroplast phosphoprotein intermediate (CPP, Figure 3A) that is released from the membrane upon
phosphorylation (Bhalla and Bennett 1987). The mode
of signal transduction between the chloroplast and
nucleus is unknown although the phosphatase inhibitor
experiments suggest the involvement of a phosphorylation cascade. Lhc gene repression under high light
intensity may be mediated by the specific interaction
of cis-acting regulatory proteins binding to the Lhc
promoter. There is evidence correlating an increase
in light intensity to the rapid appearance of a specific
DNA binding protein and a reduction in mRNA levels, suggestive of a repressor (Durnford and Falkows-
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236
Figure 3. A working hypothesis for the molecular basis of photoacclimation in Dunaliella tertiolecta. In the low light acclimated state (A)
Dunaliella contains a larger number of reaction centers and increased levels of LHC II. Lhc transcription rates and mRNA abundance are
high under such conditions. Upon a transition to a high light environment (B), the plastoquinone pool becomes reduced (PQrd ) due to excess
excitation energy. Under such conditions the redox active LHC II kinase(s) (LK) would become activated and induce state transitions via the
reversible phosphorylation of LHC II. The activation of the same or a similar redox sensitive kinase may initiate a signal transduction pathway
involving a chloroplast phosphoprotein (CPP). A phosphorylation cascade may trigger the repression of Lhc gene transcription, preventing the
accumulation of unnecessary transcripts. These processes eventually lead to a new steady state level of components acclimated to the higher
irradiance level (C). In a reverse transition, the plastoquinone pool would become predominantly oxidized (PQox ) due to the reduced availability
of light. This would cause an inactivation of the kinase and signal the resumption of Lhc transcription through a removal of the DNA binding
complex (D).
ki, unpublished data). Lowering light intensity and
consequently permitting the re-oxidation of the plastoquinone pool would relax the redox signal (Figure 3D).
This could lead to the reverse cellular response, alleviating the repression of Lhc gene expression and allowing for the synthesis of additional antennae during photoacclimation.
Coordination between electron transport and gene
regulation
Photosynthetic electron transport is sensitive to many
environmental and cellular metabolic cues in addition to light. Amongst these are temperature, nutrient
availability, and carbon metabolite levels. All of these
cues have observed effects on photosynthetic rates and
chloroplast protein levels. Understanding the interactions between these diverse pathways and signals is
essential to fully comprehend the regulation of cellular processes. Let us first consider the photosynthesis-
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237
irradiance response and later relate it to the above mentioned environmental and cellular cues.
At low PFD, the rate of photon absorption by PS II
is a product of the functional absorption cross section,
PSII , and spectral irradiance, I. As irradiance increases to a saturated value (Pmax ), the assimilation rate of
electrons is determined by the product of the number
of photosynthetic units, n, and the maximum turnover
rate 1/ . There is a single point on the photosynthesisirradiance (PI) curve where the rate of photon absorption exactly balances that of electron consumption:
PSII I = n=
(1)
The irradiance level at which this balance occurs is the
intercept of the initial slope of the PI curve divided by
Pmax , and is sometimes designated Ik in the biophysical literature. The rate limiting step in light saturated
photosynthesis is carbon fixation, not photosynthetic
electron transport (Sukenik et al. 1987b). A transition
from a low- to a high-light environment would necessitate a reduction in the number of reaction centres and/or
the size of the contributing light-harvesting antennae
in order to avoid chronic photoinhibition as a result of
feedback from the dark reactions (Smith et al. 1990).
It should be noted that Rubisco is not a light-regulated
gene in Dunaliella, hence changes in growth irradiance
lead to marked changes in the ratio of photosynthetic
electron components to Rubisco. The changes in these
ratios are linearly correlated with 1/ (Sukenik et al.
1987b, Fisher et al. 1989). Thus, in principle, any process that affects the assimilation of photosynthetically
generated electrons in PS II could lead to a feedback to
the biosynthetic components of the electron transport
chain via the redox poise of the PQ pool.
Temperature acclimation studies in algae can also
be interpreted with regard to Equation 1. Temperature acclimation responses in different algae are variable; however, they usually involve changes in a
number of cellular processes, including alterations in
maximum photosynthetic rates, the optimum temperature for photosynthesis, and changes in the activity
of Rubisco and other Calvin cycle enzymes (Davison 1991). Generally, the chlorophyll content per cell
decreases with reductions in growth temperature (Morris and Glover 1974; Thompson et al. 1992) though
little change (Morris and Glover 1974; Levasseur et
al. 1990) or even an increase in chlorophyll per cell
(Mortain-Bertrand et al. 1988) has been observed in
some species.
Manipulations of both light intensity and temperature with green algal cultures demonstrate that a high
light-acclimated phenotype, defined by a high chlorophyll a/b ratio and low amounts of chlorophyll per
cell, can be induced under low light conditions simply by decreasing the growth temperature (Maxwell et
al. 1994). This light/temperature regime caused reductions in LHC II protein and steady state mRNA levels
that were correlated to the ‘excitation pressure’ at PS
II (i.e. the product of PSII and I) and, consequently,
the redox state of the plastoquinone pool (Maxwell et
al. 1995).
Under low temperature conditions, the rate of
enzyme mediated reactions is expected to decrease
significantly (Davison 1991), causing reductions in
the carbon fixation rate and consequently increasing
. The cell could acclimate by an increase in the ratio
of Calvin cycle enzymes to electron transport components (Mortrain-Bertrand et al. 1988), thus decreasing
. Alternatively, the functional absorption cross section (PSII ) could be reduced by limiting the energy
transfer efficiency to PS II (Levasseur et al. 1990) or
reducing the LHC II antennae size to prevent over excitation of the photosystems (Davison 1991; Maxwell
et al. 1995). Both types of responses are predicted
through the equation based on the PI curve. In this
sense, the response to temperature is similar to the
phenotypic changes observed during photoacclimation
(Davison 1991) that may be responding to a common
cellular signal originating from the plastoquinone pool.
However, thermal and photoacclimation are not entirely equivalent responses and regulatory differences are
apparent (Machalek et al. 1996).
Metabolic coordination
Photoacclimation requires the coordination of both
nuclear and chloroplast gene expression in order to
synthesize both reaction center and antennae complexes. Thioredoxin, which undergoes a reversible,
photosynthesis-dependent reduction of a disulphide
bond, is important in the regulation of the reductive
pentose phosphate cycle, and functions by altering the
redox state of several key enzymes (Buchanan 1991).
Thioredoxin has also been implicated in the translational regulation of the chloroplast encoded psbA transcript (D1 protein) in the green alga Chlamydomonas
(Danon and Mayfield 1994). In this study a purified
protein complex could be induced to bind to the 50
untranslated region of the psbA mRNA transcript by
reduction of the extract with DTT or with a reduced
thioredoxin preparation. Artificially oxidizing the puri-
pres712b.tex; 4/11/1997; 11:22; v.7; p.9
238
fied mRNA protein complex (RNP) eliminated binding of the complex in vitro. These results are consistent with environmental factors that could control the
translation of the psbA protein via the redox state of
thioredoxin. Such factors as light, temperature or CO2
supply could therefore couple the rate of photosynthetic electron transport to plastid gene expression.
The processes of photosynthetic electron transport, CO2 fixation and nitrogen metabolism are tightly
coupled due to the requirements for ATP, reductant
and protein cofactors such as ferredoxin or thioredoxin. The assimilation of nitrate for the biosynthesis
of amino acids and other molecules requires photosynthetically reduced ferredoxin. In plants and algae,
nitrogen limitation suppresses many cellular functions,
including chlorophyll and protein synthesis, and the
expression of photosynthesis-related genes (Turpin
1991; Huppe and Turpin 1994). In Chlamydomonas,
nitrogen limitation reduces protein and chlorophyll
levels, as well as the expression of Lhc and RbcS nuclear encoded transcripts, while increasing the formation
of starch (Plumley and Schmidt 1989). These responses resemble acclimation to high light, suggesting common or interacting sensing and signal transduction
pathways for the control of nuclear gene expression. In
another green alga, Selenastrum, the ATP dependent
assimilation of NH4 + induces a reversible state transition, a short-term photoacclimation response (Turpin
and Bruce 1990). The decreased requirement for reductant and ferredoxin in this process, as compared to
nitrate uptake, is thought to limit the rate of photosynthetic electron transport, causing a plastoquinone
redox state-mediated state transition in an attempt to
compensate for changes in . In principle, this provides
a mechanism linking nitrogen metabolism to photosynthesis through a feedback regulatory network although
it does not preclude the existence of other regulatory
points.
The processes of starch synthesis, typically occurring in the light, and degradation, occurring in the dark,
are keyed to the cellular energy status and are tightly
regulated to prevent futile cycling within the chloroplast. The addition of an exogenous energy source such
as glucose or acetate has an inhibitory effect upon photosynthetic rates, and on the accumulation of chlorophyll and nuclear transcripts in light-grown cultures
(reviewed by Sheen 1994; Koch 1996). Both Lhc and
RbcS gene expression in algae and plants are negatively
affected in the presence of an exogenous carbon source
(Kindle 1987; Kilb et al. 1996), and this is likely a universal response to the addition of carbon metabolites
(Sheen 1994). Run-on transcription assays (Krapp et
al. 1993) and promoter deletion studies (Sheen 1990)
utilizing photosynthetic genes demonstrated that these
responses are transcriptionally regulated by specific
factors. Hexokinase substrates appear to be pivotal in
the feedback regulation of sugar metabolism; hexokinase somehow signals changes in cellular energy status, which in turn regulates photosynthetic components
(Jang and Sheen 1994). However, it will be difficult
to distinguish between regulatory contributions from
sugar metabolic enzymes and those signals originating
as a result of feedback to photosynthesis.
The complex interactions linking cellular metabolism, nutrient assimilation and photosynthesis to regulatory processes in the nucleus are summarized in
Figure 4. Research directed towards understanding the
regulatory feedback and signal transduction interactions involved in acclimation to light and other environmental cues is in its infancy. Understanding the interactions between these regulatory pathways is essential
to elucidating how photosynthetic organisms integrate
multiple environmental cues simultaneously in order to
coordinate the synthesis and maintenance of the myriad
of proteins and secondary gene products that constitute
the photosynthetic apparatus.
Figure 4. Summary of proposed interactions between cellular
metabolism and photosynthesis in the control of nuclear and chloroplast gene expression. The figure suggests a complex web of interaction controlling gene expression through a feedback to photosynthesis as well as direct, independent signals for the sensing of cellular
energy status.
pres712b.tex; 4/11/1997; 11:22; v.7; p.10
239
Acknowledgments
This research was supported by the US Department of
Energy under contract No. DEAC02-76CH00016.
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