Available online at www.sciencedirect.com
Photorespiration: current status and approaches for metabolic
engineering
Veronica G Maurino1 and Christoph Peterhansel2
Photorespiration results from the oxygenase reaction catalysed
by ribulose-1,5-bisphosphate carboxylase/oxygenase and
serves as a carbon recovery system. It comprises enzymatic
reactions distributed in chloroplasts, peroxisomes and
mitochondria. The recent discovery of a cytosolic bypass and
the requirement of complex formation between some
photorespiratory proteins added additional levels of complexity
to the known pathway. Photorespiration may have evolved in
both, C3 and C4 plants, to prevent an accumulation of toxic
levels of glycolate. Moreover, it is suggested that
photorespiration evolved in cyanobacteria before the origin of
chloroplasts. Synthetic detours, reminiscent of secondary
photorespiratory pathways naturally occurring in
cyanobacteria, were installed in Arabidopsis thaliana to bypass
photorespiration. An enrichment of CO2 in the chloroplast and
positive effects on plant growth raised the question why these
pathways have been lost from higher plants.
CO2/O2 ratio in the chloroplast and the CO2/O2 specificity
factor of RubisCO (V = VC/VO = VC/KC KO/VO [CO2]/
[O2], where KC and KO represent the Michaelis Menten
constants for CO2 and O2, and VC and VO the maximal
velocities for carboxylation and oxygenation), which
indicates the preference of the enzyme for CO2 over O2
and varies between species. The photorespiratory C2 cycle
serves as a carbon recovery system converting 2-PG to 3PGA that can re-enter the reductive cycle. This pathway is
coordinated between four cellular compartments and uses
a multitude of enzymes and transport processes (Figure 1).
Addresses
1
Botanisches Institut, Universität zu Köln, Zülpicher Str. 47b, 50674
Cologne, Germany
2
Institut für Botanik, Leibniz-Universität Hannover, Herrenhäuserstr. 2,
30419 Hannover, Germany
First, 2-PG is dephosphorylated in the chloroplasts
through 2-phosphoglycolate phosphatase (PGLP) and
the glycolate produced is transported to peroxisomes
for further metabolization (Figure 1). A. thaliana (Arabidopsis) possesses two genes encoding active PGLPs, but
only PGLP1 (At5g36700) participates in photorespiraton
[1]. Knock-out mutants of this gene have very low leaf
PGLP activity and cannot survive in normal air but grow
well in a CO2-enriched environment where photorespiration is low [1].
Corresponding author: Maurino, Veronica G ([email protected])
and Peterhansel, Christoph ([email protected])
Current Opinion in Plant Biology 2010, 13:249–256
This review comes from a themed issue on
Physiology and metabolism
Edited by Uwe Sonnewald and Wolf B. Frommer
Current status of the photorespiratory
pathway in the model plant Arabidopsis
thaliana
Chloroplastic production of glycolate and its
peroxisomal conversion into glycine
Introduction
In the peroxisomes, glycolate oxidase (GO) catalyses the
oxidation of glycolate into equimolar amounts of glyoxylate and H2O2. Catalase (CAT) degrades H2O2 and
glutamate:glyoxylate aminotransferase (GGAT) transaminates glyoxylate into glycine, which is further transported to the mitochondria (Figure 1). GO-suppressed
rice showed the typical conditional lethal high-CO2requiring phenotype [2]. Moreover, GO was found to
exert a strong regulation over photosynthesis, possible
through a feedback inhibition on RubisCO activase [2].
Plant photosynthetic carbon metabolism is composed of
two connected pathways: the reductive photosynthetic
carbon metabolism, also known as the C3 or Calvin
cycle, and the oxidative photosynthetic carbon metabolism, also known as the C2 cycle or photorespiratory
pathway (Figure 1). Both cycles are initiated by the action
of ribulose-1,5-bisphosphate carboxylase/oxygenase
(RubisCO) on ribulose-1,5-bisphosphate (RubP). Carboxylation of RubP yields 3-phosphoglycerate (3-PGA),
while its oxygenation leads to the synthesis of one molecule of 3-PGA and one molecule of 2-phosphoglycolate
(2-PG). The 3-PGA/2-PG ratio is determined by the
Arabidopsis has two genes encoding peroxisomal glutamate:glyoxylate aminotransferase (GGAT1, At1g23310
and GGAT2, At1g70580) shown to participate in photorespiration [3,4]. Knock-out mutants of GGAT1 showed a
weak residual GGAT activity, repressed growth in normal
air and high light intensity, but normal growth at elevated
CO2 conditions [4]. This partial photorespiratory phenotype suggests that both, GGAT1 and GGAT2, may
contribute to photorespiration. However, GGAT1 is
highly expressed in both leaves and roots, indicating that
its function is not restricted to photorespiration.
Available online 23rd February 2010
1369-5266/$ – see front matter
# 2010 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2010.01.006
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Current Opinion in Plant Biology 2010, 13:249–256
250 Physiology and metabolism
Figure 1
The photorespiratory carbon and nitrogen cycle comprises enzymes and transporters distributed between chloroplasts, peroxisomes, mitochondria
and cytosol. DiT1 and DiT2: dicarboxylate transporter 1 and 2, are the only transporters identified at the genomic level [33,34]. CAT: catalase; GDC:
glycine decarboxylase; GGAT: glutamate:glyoxylate aminotransferase; GLYK: glycerate kinase; GO: glycolate oxidase; GOGAT:
glutamate:oxoglutarate aminotransferase; GS: glutamine synthetase; HPR1: peroxisomal hydroxypyruvate reductase; HPR2: cytosolic
hydroxypyruvate reductase; PGP: phosphoglycolate phosphatase; RubisCO: ribulose-1,5-bisphosphate carboxylase/oxygenase; RubP: ribulose-1,5bisphosphate; SGAT: serine-glutamate aminotransferase; SHMT: serine hydroxymethyl transferase; THF: tetrahydrofolate; 5,10-CH2-THF: 5,10methylene-THF; 3-PGA: 3-phosphoglycerate. The dashed line represents many enzymatic steps.
Mitochondrial conversion of glycine into serine and the
need for ammonia re-assimilation
In the mitochondria, glycine is decarboxylated and deaminated by the glycine decarboxylase complex (GDC)
yielding CO2, NH4+, NADH and 5,10-methylene tetrahydrofolate. The latter is used by serine hydroxymethyltransferase (SHMT) to synthesize serine by transferring
the activated C1 unit onto another molecule of glycine
(Figure 1).
GDC is a hetero-tetramer and Arabidopsis possesses two
genes each encoding for P (At4g33010 and At2g26080)
Current Opinion in Plant Biology 2010, 13:249–256
and L (At3g17240 and At1g48030) proteins, three genes
for H (At2g35370, At2g35120 and At1g32470) proteins
and one gene for the T (At1g11860) protein [5]. Only few
T-DNA-tagged mutants in these genes were analysed
until present. Recent studies showed that individual
knock-outs of the P-protein genes grow normally [6].
In contrast, the combined knock-out of both genes
is lethal even at non-photorespiratory conditions providing evidence that the GDC reaction cannot be bypassed
[6]. GDC seems to be indispensable at least for onecarbon metabolism (Figure 2), by recycling glycine originated from extramitochondrial SHMT. In Arabidopsis,
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Photorespiration Maurino and Peterhansel 251
Figure 2
Simplified scheme illustrating the connection of C1-metabolism to the photorespiratory carbon cycle.
At4g37930 encodes the photorespiratory SHMT1 as
knock-out mutants in this SHMT gene are lethal at
ambient CO2 levels but grow normally at high CO2 [7].
In the course of the GDC reaction, one-quarter of the
bound carbon is lost as photorespiratory CO2 and an
equimolar amount of NH4+ is released, which needs to
be re-assimilated through the glutamine synthetase (GS)/
ferredoxin-dependent glutamate:oxoglutarate aminotransferase (Fd-GOGAT) cycle [8]. The relevance of this
nitrogen re-assimilation pathway was recently confirmed
as mutants in Fd-GOGAT (At5g04140) displayed a
typical photorespiratory phenotype [9].
Peroxisomal production of glycerate and its
chloroplastic phosphorylation into 3-PGA
Glycine generated in the mitochondria is transported to
the peroxisomes where it is converted to glycerate
through the sequential action of serine:glyoxylate aminotransferase (SGAT) and hydroxypyruvate reductase
(HPR1; Figure 1). SGAT is encoded by a single gene
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in Arabidopsis (At2g13360) and its disruption results in
plants that are unviable under normal atmospheric conditions [10]. On the contrary, disruption of HPR1
(At1g68010) caused negligible effects on growth in normal air indicating the existence of an alternative reaction
[11] (see below).
The transport of glycerate to the chloroplasts and its
phosphorylation to 3-PGA by D-glycerate 3-kinase
(GLYK) completes the photorespiratory pathway
(Figure 1). In Arabidopsis, GLYK is encoded by a
single-copy gene (At1g80380). Loss of its function results
in plants that are not viable in normal air [12]. Plant
GLYKs represent a novel protein family as they are
structurally and phylogenetically different from known
GLYKs from non-photosynthetic organisms [12].
Alternative photorespiratory reactions
In a recent publication, Timm et al. [11] presented
biochemical and genetic evidence that HPR2
(At1g79870) is the cytosolic enzyme that provides a
Current Opinion in Plant Biology 2010, 13:249–256
252 Physiology and metabolism
bypass to the peroxisomal conversion of glycine into
glycerate (Figure 1). This reaction serves as a mechanism
for the utilization of hydroxypyruvate leaking from the
peroxisomes and extends the photorespiratory pathway to
the cytosolic compartment. In line with this, combined
deletion of the peroxisomal and cytosolic reactions is
detrimental to air-grown mutants [11].
Most green algae convert glycolate to glycerate in the
mitochondrium [13]. Knock-out of glycolate dehydrogenase (GlyDH), the first enzyme in this pathway, in Chlamydomonas results in a high-CO2-requiring phenotype
[14]. It has been suggested that this mitochondrial pathway is conserved in higher plants, because an Arabidopsis
protein with homology to Chlamydomonas GlyDH is
targeted to mitochondria [15] and insertion mutants
showed altered photorespiratory properties albeit not
being affected in growth [16]. This view has been
recently challenged by characterization of the Arabidopsis
homolog enzyme [17], which shows a much higher preference for D-lactate compared to glycolate because of an
extremely low catalytic rate with the latter substrate.
Moreover, this enzyme was shown to participate in planta
in the methylglyoxal pathway [17], suggesting that the
ancient photorespiratory pathway has been re-directed to
a new function in higher plants.
Complex regulation of the mitochondrial reactions of
photorespiration
Recently, Jamai et al. [9] reported that Fd-GOGAT, a
component of the photorespiratory nitrogen assimilation
cycle in the chloroplast, is dual targeted to the mitochondria. Here, the protein seemingly does not exert an
enzymatic function, but rather associates with SHMT1.
Furthermore, two 10-formyl THF deformylases (10FDF; At4g17360 and At5g47435), components of the
mitochondrial THF cycle, were shown to be essential
for photorespiration as they oppose the accumulation of
5-formyl THF ([Figure 2]) [18]. This compound
is synthesized by SHMT in a side reaction using
5,10-methenyl-THF as substrate and is a strong inhibitor
of the SHMT activity. It was speculated that the role of
Fd-GOGAT bound to SHMT1 might be to reduce the
sensitivity of SHMT1 to 5-formyl THF or to inhibit its
accumulation [9].
occurs under high light, drought and salt-stress and CO2free air [19,20]. This transfer of reducing equivalents
might also be important for nitrate assimilation [21].
Moreover, photorespiration would be important for avoiding the suppression of the repair of photodamaged photosystem II, as different photorespiratory mutants of
Arabidopsis showed inhibition of the synthesis of the
D1 protein at the level of translation [22]. Finally, through
H2O2 production and pyridine nucleotide interactions,
photorespiration makes a key contribution to cellular
redox homeostasis [23].
Photorespiration is required in all
photosynthetic organisms
The dual function of RubisCO is common to all photosynthetic organisms [24]. It is therefore plausible to
assume that all photosynthetic organisms also require a
pathway for phosphoglycolate conversion. According to
this, genes encoding photorespiratory enzymes are found
throughout the green lineage [13,25]. However, cyanobacteria, algae and higher plants developed mechanisms
for the concentration of CO2 around RubisCO resulting in
an efficient suppression of phosphoglycolate production
(Figure 3). It was assumed that these organisms do not
strictly require photorespiration. Two recent papers have
now falsified this hypothesis. In the first study, Zelitch
et al. [26] isolated a maize mutant with a transposon
integration in the GO1 gene that encodes the major
glycolate oxidase enzyme in maize. Maize is a C4 plant
and, thus, largely suppresses photorespiration by pumping CO2 into the vicinity of RubisCO ([Figure 3]). Unexpectedly, homozygous mutant plants were not capable of
surviving in normal air and required CO2 enrichment for
normal growth. Furthermore, glycolate accumulated in
these plants and photosynthesis was suppressed by high
oxygen concentrations. All these features are reminiscent
of photorespiratory mutants in C3 plants [27]. The low
rates of RubisCO oxygenase activity in C4 plants seemingly produce enough phosphoglycolate to inhibit
photosynthesis when accumulating. This often mentioned, but poorly studied toxic effect of phosphoglycolate and other photorespiratory metabolites on
photosynthesis seems to be equally important for growth
inhibition under conditions of high oxygenase activity as
the loss of CO2 or NH4+ during later steps of the photorespiratory pathway.
Why photorespiration?
Photorespiration lowers photosynthetic efficiency in that
CO2 and ammonia should be re-assimilated with the
concomitant consumption of both ATP and reducing
power [19]. So why photorespiration? Although the main
function of photorespiration would be the recovery of
carbon diverted by the oxygenase activity of RubisCO
some other functions have also been proposed. By transporting excess reducing equivalents from the chloroplast
photorespiration may be a mechanism for preventing the
over reduction of the stroma, and thus photoinhibition, as
Current Opinion in Plant Biology 2010, 13:249–256
In the second study, photorespiratory mutants of the
cyanobacterium Synechocystis were analysed [28]. Analogous to the situation in maize, oxygen fixation by
RubisCO is also low in cyanobacteria because of an
efficient CO2-concentrating mechanism. Moreover, at
least some cyanobacteria are capable of excreting excess
glycolate [29]. Despite of the low rates of phosphoglycolate synthesis, Synechocystis established three different
routes for the metabolism of this compound (Figure 4):
one pathway reminds of the metabolism that bacteria use
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Photorespiration Maurino and Peterhansel 253
Figure 3
CCM in cyanobacteria, algae and higher plants.
to grow on glycolate as a carbon source, the second
resembles the photorespiratory pathway found in higher
plants, and the third involves the complete oxidation of
glycolate to CO2. Whereas mutants in single pathways
were impaired in growth, only knock-out of all three pathways for glycolate conversion resulted in a conditional
lethal phenotype. These data are important for two
reasons: First, they suggest that the photorespiratory pathway might have evolved before the endosymbiosis of
cyanobacteria forming the first photosynthetic eukaryotes.
Second, a complete interruption of phosphoglycolate
metabolism is probably lethal for all tested photosynthetic
organisms under normal growth conditions independent of
the amounts of phosphoglycolate formed.
Manipulation of photorespiration and growth
In theory, any reduction in photorespiration should
enhance CO2 fixation and therefore growth. However,
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as discussed above, disruption of photorespiration causes
strongly retarded growth of mutant plants. An alternative
is the deviation of some of the phosphoglycolate formed
by RubisCO into alternative pathways. Kebeish et al. [30]
described the installation of the bacterial glycolate oxidation pathway in Arabidopsis chloroplasts that converts
glycolate in three steps to glycerate and thus establishes a
photorespiratory bypass. This pathway includes a CO2
release step analogous to the C2 pathway, but the authors
provided evidence that shifting CO2 release from the
mitochondrium to the chloroplast increased the CO2
concentration around RubisCO and as a result reduced
RubisCO’s oxygenase activity in vivo. Moreover, energy
and reducing equivalents may be saved in the bypass: it
does not include release and refixation of ammonia and
the energy from glycolate oxidation is saved in reducing
equivalents and not burned by the formation of H2O2.
Consequently, transgenic lines showed enhanced shoot
Current Opinion in Plant Biology 2010, 13:249–256
254 Physiology and metabolism
Figure 4
support the view that photorespiration evolved in both,
C3 and C4 plants, to prevent the accumulation of toxic
levels of glycolate, which inevitably occurs if O2 is
present. This together with the still limited knowledge
on metabolite transport during photorespiration and
the potential for biotechnological application will hopefully motivate significant future research efforts in this
field.
Acknowledgements
We thank Andreas Weber for critical reading of the manuscript. This work
was supported by the Deutsche Forschungsgemeinschaft grants MA2379/41 and 8-1 to VGM and PE819/4-1 to CP, both as part of the German
Photorespiration Research Network Promics.
References and recommended reading
Papers of particular interest, published within the period of review,
have been highlighted as:
of special interest
of outstanding interest
The multiple pathways for phosphoglycolate metabolism in
Synechocystis. Phosphoglycolate is converted to glyoxylate in two
enzymatic steps and then further metabolized to 3-phosphoglycerate (3PGA) and/or CO2 by three complementary pathways: blue: bacteria-like
pathway; red: higher plant-like pathway; green: complete oxidation of
glyoxylate to CO2.
and even root biomass production. It remains to be analysed which of the theoretical benefits of the bypass discussed are responsible for the enhanced growth phenotype.
A clue to this question might come from an alternative
approach where glycolate is completely oxidized to CO2 in
the chloroplast using only two enzymatic steps (H Fahnenstich, PhD thesis, University of Cologne, 2008). This
approach shares both the enrichment of CO2 in the chloroplast and the prevention of ammonia release with the
photorespiratory bypass and because of this positive effects
on growth are also evident [31]. Interestingly, both synthetic detours from photorespiration are reminiscent of the
secondary photorespiratory pathways that naturally occur
in Synechocystis [28]. It is of major interest to understand
why these pathways have been lost from higher plants if
synthetic re-engineering of the previous state was successful in augmenting photosynthetic capacity in Arabidopsis
[30]. One reason might be the evolution of specific leaf
architectures in individual species. For example, rice shows
adaptations to maximize the scavenging of photorespired
CO2 and to enhance the diffusive conductance of CO2 [32].
It is speculated that such an ultrastructure could minimize
the benefits obtained from glycolate oxidation in the
chloroplast in this species.
Concluding remarks
Recent studies added additional levels of complexity
to the well-established photorespiratory pathway and
Current Opinion in Plant Biology 2010, 13:249–256
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