Bypassing the photorespiratory pathway is regarded as a way to increase carbon assimilation and, correspondingly, biomass production in C
3 crops. Here, the benefits of three published photorespiratory bypass strategies are systemically explored using a systems-modeling approach. Our analysis shows that full decarboxylation of glycolate during photorespiration would decrease photosynthesis, because a large amount of the released CO
2 escapes back to the atmosphere. Furthermore, we show that photosynthesis can be enhanced by lowering the energy demands of photorespiration and by relocating photorespiratory CO
2 release into the chloroplasts. The conductance of the chloroplast membranes to CO
2 is a key feature determining the benefit of the relocation of photorespiratory CO
2 release. Although our results indicate that the benefit of photorespiratory bypasses can be improved by increasing sedoheptulose bisphosphatase activity and/or increasing the flux through the bypass, the effectiveness of such approaches depends on the complex regulation between photorespiration and other metabolic pathways.In C
3 plants, the first step of photosynthesis is the fixation of CO
2 by ribulose bisphosphate (
RuBP). For every molecule of CO
2 fixed, this reaction produces two molecules of a three-carbon acid, i.e., 3-phosphoglycerate (
PGA), and is catalyzed by the Rubisco enzyme. A small portion of the carbon in
PGA is used for the production of Suc and starch, whereas the remainder (i.e. five-sixths) is used for the regeneration of
RuBP (). The regeneration of the Rubisco substrate
RuBP in the Calvin-Benson-Bassham (
CBB) cycle ensures that ample
RuBP is available for carbon fixation (
Bassham, 1964;
Wood, 1966;
Beck and Hopf, 1982). Rubisco is a bifunctional enzyme that catalyzes not only
RuBP carboxylation but also
RuBP oxygenation (
Spreitzer and Salvucci, 2002).
RuBP oxygenation generates only one molecule of
PGA and one molecule of 2-phosphoglycolate (
P-Gly;
Ogren, 1984). The photorespiratory pathway converts this
P-Gly back to
RuBP in order to maintain the
CBB cycle.
Open in a separate windowSchematic representation of the C3 photosynthesis kinetic model with three different photorespiratory bypass pathways. The bypass described by
Kebeish et al. (2007) is indicated in blue, the bypass described by
Maier et al. (2012) in pink, and the bypass described by
Carvalho et al. (2011) in green. The original photorespiratory pathway is marked in orange, and CO
2 released from photorespiration (including the original pathway and bypass pathways) is indicated in red. 2PGA, 2-Phosphoglyceric acid; ASP, Asp; CIT, citrate; ICIT, isocitrate; PGA, 3-phosphoglycerate; DPGA, glycerate-1,3-bisphosphate; GAP, glyceraldehyde 3-phosphate; DHAP, dihydroxyacetone phosphate; SBP, sedoheptulose-1,7-bisphosphate; S7P, sedoheptulose-7-phosphate; Ri5P, ribose-5-phosphate; Ru5P, ribulose-5-phosphate; FBP, fructose-1,6-bisphosphatase; F6P, fructose 6-phosphate; Xu5P, xylulose-5-phosphate; G6P, glucose-6-phosphate; G1P, glucose-1-phosphate; ADPG, ADP-glucose; F26BP, fructose-2,6-bisphosphate; UDPG, uridine diphosphate glucose; SUCP, sucrose-6F-phosphate; SUC, Suc; PEP, phospho
enolpyruvate; OAA, oxaloacetate; PGCA, phosphoglycolate; GCA, glycolate; GOA, glyoxylate; GCEA, glycerate; MAL, malate; PYR, pyruvate; GLU, glutamate; KG, alfa-ketoglutarate; GLN, Gln; HPR, hydroxypyruvate; RuBP, ribulose bisphosphate; SER, Ser; GLY, Gly; TS, tartronic semialdehyde.In higher plants,
P-Gly is dephosphorylated to glycolate, which is transferred into the peroxisomes, where it is oxidized to hydrogen peroxide and glyoxylate. Then, glyoxylate is aminated to produce Gly, which is subsequently transferred to the mitochondria. There, two molecules of Gly are converted into one Ser plus one CO
2 and one NH
3 (
Ogren, 1984;
Peterhansel et al., 2010). The Ser is ultimately converted back to
PGA (
Tolbert, 1997). CO
2 and NH
3 are gasses that can escape to the atmosphere (
Sharkey, 1988;
Kumagai et al., 2011), and the loss of carbon and nitrogen essential for biomass accumulation will decrease the efficiency of photosynthesis and plant growth (
Zhu et al., 2010). Fortunately, both substances are partially reassimilated in the chloroplast, but this results in decreased photosynthetic energy efficiency. At 25°C and current atmospheric CO
2 concentrations, approximately 30% of the carbon fixed in C
3 photosynthesis may be lost via photorespiration and the size of this loss increases with temperature (
Sharkey, 1988;
Zhu et al., 2010). As a result, photorespiration has been regarded as a pathway that could be altered to improve photosynthetic efficiency (
Zelitch and Day, 1973;
Oliver, 1978;
Ogren, 1984;
Zhu et al., 2008,
2010).There are several approaches that may be used to alter photorespiration to improve photosynthetic efficiency. First, it might be possible to increase the specificity of Rubisco to CO
2 versus oxygen (
Sc/o;
Dhingra et al., 2004;
Spreitzer et al., 2005;
Whitney and Sharwood, 2007). However, previous studies have shown that there is an inverse correlation between
Sc/o and the maximum carboxylation rate of Rubisco (
Jordan and Ogren, 1983;
Zhu et al., 2004), and there are some indications that the
Sc/o of different organisms may be close to optimal for their respective environments (
Tcherkez et al., 2006;
Savir et al., 2010). Second, a CO
2-concentrating mechanism could be engineered into C
3 plants. For example, introducing cyanobacterial bicarbonate transporters (
Price et al., 2011) or introducing C
4 metabolism could be used to concentrate CO
2 in the vicinity of Rubisco and, thereby, suppress the oxygenation reaction of Rubisco (
Furbank and Hatch, 1987;
Mitchell and Sheehy, 2006). Past efforts to introduce a C
4 pathway into C
3 plants have focused on biochemical reactions related to C
4 photosynthesis without taking into account the anatomical differences between C
3 and C
4 plants, which may have been responsible for the limited success of such endeavors (
Fukayama et al., 2003). Recently, there has been renewed interest in engineering C
4 photosynthetic pathways into C
3 plants, with efforts focusing on understanding and engineering the genetic regulatory network related to the control of both the anatomical and biochemical properties related to C
4 photosynthesis (
Mitchell and Sheehy, 2006;
Langdale, 2011).Transgenic approaches have been used to knock down or knock out enzymes in the photorespiratory pathway. Unfortunately, the inhibition of photorespiration by the deletion or down-regulation of enzymes in the photorespiratory pathway resulted in a conditional lethal phenotype (i.e. such plants cannot survive under ambient oxygen and CO
2 concentrations but may be rescued by growing them under low-oxygen or high-CO
2 conditions; for review, see
Somerville and Ogren, 1982;
Somerville, 2001). Another approach to reduce photorespiration is to block (or inhibit) enzymes in this pathway using chemical inhibitors.
Zelitch (1966,
1974,
1979) reported that net photosynthesis increased by inhibiting glycolate oxidase or glycolate synthesis. However, other groups showed that the inhibition of glycolate oxidase or Gly decarboxylation led to the inhibition of photosynthesis (
Chollet, 1976;
Kumarasinghe et al., 1977;
Servaites and Ogren, 1977;
Baumann et al., 1981). It turns out that plants cannot efficiently metabolize photorespiratory intermediates without a photorespiratory pathway, and suppression of this pathway inhibits the recycling of carbon back toward
RuBP, which is necessary for maintaining the
CBB cycle (
Peterhansel et al., 2010;
Peterhansel and Maurino, 2011). Moreover, the accumulation of toxic metabolic intermediates (e.g.
P-Gly) can strongly inhibit photosynthesis (
Anderson, 1971;
Kelly and Latzko, 1976;
Chastain and Ogren, 1989;
Campbell and Ogren, 1990). This may explain why earlier attempts to block or reduce photorespiration have failed to improve carbon gain.Instead of reducing photorespiration directly, a promising idea is to engineer a photorespiratory bypass pathway. Such a pathway would metabolize
P-Gly produced by
RuBP oxygenation but minimize carbon, nitrogen, and energy losses and avoid the accumulation of photorespiratory intermediates.
Kebeish et al. (2007) introduced the glycolate catabolic pathway from
Escherichia coli into Arabidopsis (
Arabidopsis thaliana); we will subsequently call this type of bypass the Kebeish bypass. In such transgenic plants, glycolate is converted to glycerate in the chloroplasts without ammonia release (). Previous studies suggested that this pathway theoretically requires less energy and shifts CO
2 release from mitochondria to chloroplasts (
Peterhansel and Maurino, 2011;
Peterhansel et al., 2013); experimental results indicated that the bypass allowed for increased net photosynthesis and biomass production in Arabidopsis (
Kebeish et al., 2007). There are reports of two other photorespiratory bypass pathways in the literature (
Carvalho, 2005;
Carvalho et al., 2011;
Maier et al., 2012). In the Carvalho bypass (
Carvalho, 2005;
Carvalho et al., 2011), glyoxylate is converted to hydroxypyruvate in the peroxisome. Similar to the Kebeish bypass, the ammonia release is abolished, one-quarter of the carbon from glycolate is released as CO
2 in the peroxisomes, and three-quarters of the carbon from glycolate is converted back to
PGA. However, this pathway has only been partially realized in tobacco (
Nicotiana tabacum); that is, the enzyme of the second reaction of this pathway was not detectable in the transgenic plants, and plants expressing this pathway showed stunted growth when grown in ambient air (
Carvalho et al., 2011). The Maier bypass (
Maier et al., 2012) is characterized by complete oxidation of glycolate in the chloroplasts. Initial results suggested that the photosynthesis and biomass of transgenic Arabidopsis with this pathway were enhanced (
Maier et al., 2012).Recently, the design and benefits of the three bypass pathways were reviewed (
Peterhansel et al., 2013), and it was suggested that a photorespiratory bypass can contribute to an enhanced photosynthetic CO
2 uptake rate by lowering energy costs and minimizing carbon and nitrogen losses. However, a systematic and quantitative analysis of the potential contributions of these different factors to photosynthesis improvement has not yet been conducted. Systems modeling can help to design new metabolic pathways and improve our understanding of biochemical mechanisms (
McNeil et al., 2000;
Wendisch, 2005;
Zhu et al., 2007;
Bar-Even et al., 2010;
Basler et al., 2012). Such models have been used successfully to gain insight into the photosynthetic metabolism (
Laisk et al., 1989,
2006;
Laisk and Edwards, 2000;
Zhu et al., 2007,
2013;
Wang et al., 2014). In this study, we use an extended kinetic model of C
3 photosynthesis based on earlier work by
Zhu et al. (2007) to systematically analyze the potential of three photorespiratory bypass pathways for improving photosynthetic efficiency (
Supplemental Model S1). In addition, we determined under what conditions such bypass pathways may lead to increased photosynthesis and biomass production in C
3 plants and how to further improve the photosynthesis of plants with such a bypass. Our analysis suggests that the benefit of a photorespiratory bypass varies dramatically if it is engineered into different crops.
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