Photorespiration
Secondary article
Article Contents
Thomas D Sharkey, University of Wisconsin, Madison, Wisconsin, USA
. Introduction
Photorespiration is the light-dependent release of CO2 from photosynthetic organisms and
is caused by O2 substituting for CO2 in the first step of photosynthetic CO2 fixation.
. Photorespiratory Pathway and Control
. Compartmentation of Photorespiration
. Photorespiration and Global O2 and CO2
Concentrations
Introduction
. Functional Significance of Photorespiration
The enzyme that is responsible for fixing CO2 in photosynthesis, Rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase; EC 4.1.1.39, can also fix O2 (Bowes et al.,
1971). Rubisco favours CO2 over O2 by a factor of up to
100, but the concentration of O2 in the atmosphere is much
higher than that of CO2. As a result, about one molecule of
O2 is fixed by Rubisco for every three molecules of CO2.
When O2 is substituted for CO2, the toxic product
phosphoglycolate results. Plants metabolize phosphoglycolate, but this requires energy and causes the loss of some
reduced carbon as CO2. Thus, photorespiration inhibits
photosynthesis by three mechanisms. First, photorespiration interferes with CO2 fixation at Rubisco; second, it uses
energy that could otherwise be used for photosynthetic
carbon reduction; and third, it causes the release of CO2
from previously fixed carbon (Sharkey, 1988). Photorespiration substantially reduces the efficiency of photosynthesis in most plants, especially crop plants, with a few
exceptions such as Zea mays, which overcomes photorespiration by chemically preconcentrating CO2.
Photorespiratory Pathway and Control
When Rubisco fixes CO2, two molecules of phosphoglycerate are produced; when O2 is used, one phosphoglycerate and one phosphoglycolate are produced (Figure 1).
Photorespiration involves conversion of the phosphorylated phosphoglycolate to the amino acid glycine. This is
followed by the conversion of two glycine molecules (two
carbons each) to the amino acid serine (three carbons) plus
one molecule of CO2 and one of ammonia. Finally, the
serine is converted to glycerate and then phosphoglycerate.
There is a net loss of one CO2 and one ammonia for each
two oxygenation events. The released ammonia must be
refixed and the ammonia cycling that results from
photorespiration accounts for ten times more ammonia
fixation than does protein synthesis.
Because photorespiration detoxifies phosphoglycolate
produced by Rubisco, limiting photorespiration by reducing the capacity for phosphoglycolate metabolism harms
plants. Mutant plants have been generated that lack the
ability to carry out steps in glycolate metabolism. These
plants could be selected because they grew poorly or not at
all in normal air but could be rescued by growth in highCO2 atmospheres, which suppress the oxygenation reaction (Somerville, 1986). Seven different classes of mutants
were recovered, indicating that there are at least seven
proteins that are required for photorespiration that are not
essential for plant growth and reproduction in the absence
of photorespiration.
Because photorespiration is needed to detoxify phosphoglycolate, all hope for reducing photorespiration lies in
improving the specificity of Rubisco for CO2 over O2.
Rubiscos with higher specificity have evolved and the
Rubiscos found in most C3 crop plants today have the
highest specificity of any organism on Earth. However, this
specificity has come at the cost of high catalytic efficiency.
There exist Rubiscos that are much faster than C3
Rubiscos, but they have lower specificities for CO2 over
O2. Given the changes in global CO2 concentration, some
investigators believe there is more to gain by moving a
higher-efficiency Rubisco into C3 plants and accepting the
losses caused by photorespiration in exchange for the
higher capacity of the Rubisco.
Compartmentation of Photorespiration
The reactions of photorespiration occur in three different
compartments in higher plants: the chloroplast, the
peroxisome and the mitochondrion (Figure 1). The reactions begin in the chloroplast with the oxygenation of
ribulose bisphosphate. The phosphoglycolate produced is
dephosphorylated inside the chloroplast and the glycolate
then moves to the peroxisome. Peroxisomes have substantial amounts of catalase to break down hydrogen
peroxide (H2O2). The oxidation of glycolate to glyoxylate
produces H2O2 and reactions that generate H2O2 normally
occur in peroxisomes. The glyoxylate is transaminated to
glycine, which moves to the mitochondrion.
Inside the mitochondrion glycine meets one of two fates.
One half of the glycine molecules are taken apart to yield
CO2, ammonia and a one-carbon fragment on tetrahydrofolate. This last compound donates the carbon from the
first glycine to a second glycine molecule to make serine.
The serine leaves the mitochondrion and goes back to the
peroxisome. Here it gives up its amino group, which is used
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1
Photorespiration
RuBP + O2
Phosphoglycolate
COO–
COO–
C
C
OH
C
P
P
Phosphoglycolate
phosphatase
Phosphoglycerate
COO–
Glycolate
C
ADP
OH
Glycerate
kinase
ATP
Chloropast
Cytosol
O2
Glycolate oxidase
COO–
H2 O + 12 O2
H2 O2
C
OH
C
NAD
O
Glutamate
Hydroxypyruvate
reductase
NADH
Glycine amino
transferase
COO–
C
α-Ketoglutarate
COO–
Glycine
OH
Glycerate
COO–
Glyoxylate
C
Peroxisome
C
Hydroxypyruvate
COO–
NH+
3
C
NH+3
OH
C
O
NH+3
Serine glyoxylate
amino transferase
Cytosol
THF
NAD
Mitochondrion
COO–
NADH
Glycine
decarboxylase
NH 3
CO2
Serine
hydroxymethyl
transferase
C
NH+3
C
OH
Serine
C
THF
Figure 1 The carbon reactions of photorespiration occur in three organelles: the chloroplast, the peroxisome and the mitochondrion.
in the transamination of glycolate to glycine, resulting in
hydroxypyruvate.
Hydroxypyruvate is reduced to glycerate, which moves
to the chloroplast. Glycerate in the chloroplast is
phosphorylated to phosphoglycerate. This phosphoglycerate re-enters the carbon metabolism of photosynthesis.
For each two ribulose bisphosphate molecules oxygenated,
three phosphoglycerate molecules plus one CO2 molecule
result (Figure 2).
2
The transamination from serine to glycolate to make
hydroxypyruvate and glycine accounts for half of the
needed ammonia. The other half comes from refixation of
the ammonia released during glycine decarboxylation in
the mitochondrion (Figure 3). The glutamine synthetase/
glutamate synthase (GS/GOGAT) pathway refixes the
ammonia, consuming both ATP and reducing power. This
adds to the energetic cost of photorespiration.
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Photorespiration
2 RuBP + 2O2
Tetrahydrofolate
+
glycine
NAD
NADH
CO2
Glycine
C decarboxylase
THF
NH3
Mitochondrion
Cytosol
Phosphoglycolate
ADP + Pi
Phosphoglycerate
Glutamine
2Fd red
α-Ketoglutarate
ATP
Chloroplast
2Fd ox
Glutamine
synthetase
(GS)
Glutamate
Glutamate
Glutamate
synthetase
(GOGAT)
Glycine
Cytosol
Peroxisome
Serine
CO2
NH3
Glycine
Hydroxypyruvate
Figure 2 The stoichiometry of photorespiratory reactions.
Photorespiration and Global O2 and
CO2 Concentrations
Rubisco is believed to have evolved when the CO2
concentration was very high and O2 was nearly absent
from the atmosphere. The ability of Rubisco to use O2
instead of CO2 was, therefore, not important during early
Rubisco evolution. During the 2 billion years after the
evolution of Rubisco, the CO2 level in the atmosphere fell
almost 90%, but free O2 was still almost nonexistent.
However, about 1.5 billion years ago, O2 gas started to
accumulate in the atmosphere. At 500 million years before
present, the O2 concentration had increased to approximately the levels we have today but CO2 was still high.
Because the interaction between O2 and CO2 is competitive, photorespiration was still not a significant factor in
photosynthetic organisms.
It is estimated that between 450 to 500 million years ago
land plants appeared on Earth followed by a rapid decline
in CO2 in the atmosphere. The relatively low CO2 and high
O2 concentrations would have caused significant rates of
photorespiration for the first time about 450 million years
ago. Between 30 and 50 million years ago, the CO2 level fell
to very low levels and photorespiration was probably a
significant impediment to plant growth. About this time,
the ability to chemically concentrate CO2 by making a
four-carbon carboxylic acid evolved. This C4 pathway
evolved in a number of different plant families independently as a result of the strong evolutionary pressure
exerted by photorespiration (Ehleringer et al., 1991).
Plants that do not use this pathway are called C3 plants
and must cope with photorespiration.
Glyoxylate
Serine
Glycine amino
transferase
Serine glyoxylate amino
transferase
Figure 3 Nitrogen cycling during photorespiration.
Turning to more recent times, the global CO2 concentration has increased by about 20% during this century.
Because of this increase, photorespiration has decreased by
20% worldwide. As the CO2 concentration continues to
increase in the future, photorespiration will continue to
fall. This should lead to increased crop yields. The increases
in plant growth caused by decreased photorespiration are
predicted to exceed any negative effect of increased
temperature (Long, 1991). However, increased CO2 in
the atmosphere could lead to more violent weather, which
could more than offset the productivity gains due to
reduced photorespiration.
In today’s atmosphere, the energetic cost of the CO2
pump of C4 plants is roughly equal to the energetic cost of
photorespiration suffered by C3 plants. However, these
costs are affected by other environmental conditions in
addition to the CO2 concentration in the atmosphere. Most
important is temperature. The rate of oxygenation and
thus photorespiration is stimulated by high temperature
because the specificity of Rubisco for CO2 over O2 is worse
at high temperature. In today’s atmosphere, at 358C, the
cost of photorespiration exceeds the cost of the C4 pump
but at 258C the cost of photorespiration is less than that of
the C4 pump. This is why C4 plants are more common in the
tropics than in temperate regions. At about 308C, the cost
of photorespiration is about the same as the cost of the C4
pump.
As the CO2 concentration in the atmosphere increases,
the temperature at which these two costs are equal will
increase until, at 700 ppm CO2, this crossover point is
estimated to be 428C. In other words, when the CO2
concentration doubles, C4 plants will be favoured only in
extreme environments. This is not to say that C4 plants will
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Photorespiration
become less efficient, rather that C3 plants will become
more efficient as the rising CO2 in the atmosphere
suppresses photorespiration. Thus changes in photorespiration rates could affect competition between C3 and C4
plants and alter species composition and diversity in many
ecosystems.
Functional Significance of
Photorespiration
Photorespiration is clearly deleterious to plants. Often, the
stimulation of photosynthesis that occurs in high CO2
results only from the suppression of photorespiration by
CO2. Does photorespiration provide some evolutionary
advantage over a hypothetical plant lacking photorespiration? Or is photorespiration only a metabolic mistake:
evolutionary baggage reflecting the fact that the global
CO2 concentration was high and O2 concentration was low
when Rubisco evolved (Andrews and Lorimer, 1978)?
While not a unanimous opinion, the general consensus is
that photorespiration is primarily an evolutionary relic.
Rubisco routinely makes a number of metabolic mistakes,
including production of pyruvate (Andrews and Kane,
1991) and xylulose bisphosphate (Edmondson et al., 1990).
Photorespiration and production of other oxidized products of ribulose bisphosphate (Kane et al., 1998) are
further examples.
However, there are two ways that plants benefit from
photorespiration. The first is in the production of the
amino acids glycine and serine. These amino acids can be
found in the phloem transporting carbon from photosynthesizing leaves (Madore and Grodzinski, 1984). While
this is not the only method the plant has for synthesis of
these compounds, the plant can none the less use these
amino acids for protein synthesis. This also provides the
plant with another method of end-product synthesis.
Under some conditions, especially at low temperature,
the processes of starch synthesis and sucrose synthesis may
not go fast enough to process all of the carbon fixed in
photosynthesis. Then, glycine and serine can be additional
end products that allow photosynthesis to go faster than
synthesis of starch plus sucrose. When this happens,
adding O2 will stimulate CO2 uptake as opposed to the
normal situation where adding O2 inhibits CO2 uptake
because of the costs associated with photorespiration
(Harley and Sharkey, 1991).
A second way that photorespiration can be useful to the
plant is as an alternative electron sink when CO2 is not
available. The light-dependent reactions of photosynthesis
produce reduced compounds used in photosynthetic
reactions. Management of reducing power developed as a
result of absorbing sunlight is an important concern for
plants. When the energy in sunlight is not managed
properly, leaves are damaged. Leaves exposed to excess
4
light can take hours to days to regain all of their capacity
for photosynthesis, a phenomenon called photoinhibition.
The primary management method appears to involve the
xanthophyll zeaxanthin, but photorespiration can also
help manage excess light, especially during drought. When
plants have too little water, the stomata on the leaves close,
restricting water loss but at the same time restricting CO2
entry. The CO2 concentration inside the leaf quickly falls to
the compensation point, where photosynthesis goes just
fast enough to fix the CO2 released in photorespiration. As
the falling CO2 concentration inhibits photosynthesis,
photorespiration increases. Because photorespiration requires about the same amount of energy as photosynthesis
(per ribulose bisphosphate consumed), the energy consumed by photosynthesis plus photorespiration remains
roughly constant as the stomata close and photorespiration replaces photosynthesis (Stuhlfauth et al., 1990).
These two functions of photorespiration can be demonstrated. However, it is unlikely that these two functions
provided an evolutionary constraint leading to photorespiration, because the basic mechanism of oxygenation
of ribulose bisphosphate evolved at a time when there was
no free O2. It is possible that these two functions are now
important to the plant and provide evolutionary pressure
to maintain photorespiration despite its costs to the plant.
However, in both cases, there already exist mechanisms
that can perform the required function better than
photorespiration. In the first case, the capacity for starch
and sucrose synthesis far exceeds the capacity for glycine
and serine synthesis. In the second case, the mechanism of
dissipating excess light that involves zeaxanthin can
dissipate much more energy than can photorespiration in
most leaves. Thus, while these two functions of photorespiration may be useful to the plant, the overall effect of
photorespiration is deleterious: plants would be better off
without photorespiration.
If photorespiration is primarily a metabolic mistake,
perhaps it can be eliminated through genetic engineering.
So far it has been possible to make the specificity of
Rubisco worse through genetic methods. While disappointing in themselves, these results show that it is possible
to manipulate the processes that lead to photorespiration.
Perhaps some day it will be possible to engineer a plant that
lacks photorespiration. In the meantime, increasing global
CO2 concentrations will suppress photorespiration.
References
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ribulosebisphosphate carboxylase/oxygenase. Journal of Biological
Chemistry 266: 9447–9452.
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Bowes G, Ogren WL and Hageman RH (1971) Phosphoglycolate
production catalyzed by ribulose diphosphate carboxylase. Biochemical and Biophysical Research Communications 45: 716–722.
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net
Photorespiration
Edmondson DL, Kane HJ and Andrews TJ (1990) Substrate isomerization inhibits ribulosebisphosphate carboxylase-oxygenase during
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C-photoassimilate transport from leaves of Salvia splendens L. Plant
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Further Reading
Artus NN, Somerville SC and Somerville CR (1986) The biochemistry
and cell biology of photorespiration. CRC Critical Reviews of Plant
Sciences 4: 121–147.
Canvin DT (1990) Photorespiration and CO2-concentrating mechanisms. In: Dennis DT and Turpin DH (eds). Plant Physiology,
Biochemistry and Molecular Biology, pp. 253–273. Harlow. Longman
Scientific and Technical.
Husic DW, Husic HD and Tolbert NE (1987) The oxidative
photosynthetic carbon cycle or C2 cycle. CRC Critical Reviews of
Plant Sciences 5: 45–100.
Ogren WL (1984) Photorespiration pathways, regulation, and modification. Annual Review of Plant Physiology 35: 415–442.
Tolbert NE (1997) The C2 oxidative photosynthetic carbon cycle. Annual
Review of Plant Physiology and Plant Molecular Biology 48: 1–23.
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