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First published online September 19, 2008; 10.1104/pp.108.128439 Plant Physiology 149:195-204 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
High Glycolate Oxidase Activity Is Required for Survival of Maize in Normal Air1,[OA]Department of Biochemistry and Genetics, The Connecticut Agricultural Experiment Station, New Haven, Connecticut 06511 (I.Z., N.P.S., R.B.P.); and Department of Plant Biology (P.B.) and Boyce Thompson Institute for Plant Research (T.P.B.), Cornell University, Ithaca, New York 14853
A mutant in the maize (Zea mays) Glycolate Oxidase1 (GO1) gene was characterized to investigate the role of photorespiration in C4 photosynthesis. An Activator-induced allele of GO1 conditioned a seedling lethal phenotype when homozygous and had 5% to 10% of wild-type GO activity. Growth of seedlings in high CO2 (1%–5%) was sufficient to rescue the mutant phenotype. Upon transfer to normal air, the go1 mutant became necrotic within 7 d and plants died within 15 d. Providing [1-14C]glycolate to leaf tissue of go1 mutants in darkness confirmed that the substrate is inefficiently converted to 14CO2, but both wild-type and GO-deficient mutant seedlings metabolized [1-14C]glycine similarly to produce [14C]serine and 14CO2 in a 1:1 ratio, suggesting that the photorespiratory pathway is otherwise normal in the mutant. The net CO2 assimilation rate in wild-type leaves was only slightly inhibited in 50% O2 in high light but decreased rapidly and linearly with time in leaves with low GO. When go1 mutants were shifted from high CO2 to air in light, they accumulated glycolate linearly for 6 h to levels 7-fold higher than wild type and 11-fold higher after 25 h. These studies show that C4 photosynthesis in maize is dependent on photorespiration throughout seedling development and support the view that the carbon oxidation pathway evolved to prevent accumulation of toxic glycolate.
The oxidation of glycolate to glyoxylate in higher plants is catalyzed by glycolate oxidase (GO; EC 1.1.3.15), an FMN-containing protein (Zelitch and Ochoa, 1953  ). The enzyme is located in the peroxisome and performs an essential step in the operation of the oxidative photorespiratory cycle accompanying photosynthetic CO2 assimilation in C3 plants (Tolbert, 1971, 1997). Glycolate arises from 2-phosphoglycolate, which is produced together with 3-phosphoglycerate by ribulose bisphosphate reacting with O2 as catalyzed by Rubisco (Bowes et al., 1971; Ogren, 2006) in the bundle sheath (BS) cell of C4 plants (Edwards and Walker, 1983). Dephosphorylation of 2-phosphoglycolate yields glycolate that is transported into the peroxisome. In the peroxisome, GO oxidizes glycolate to produce glyoxylate. Transamination of glyoxylate generates Gly that is converted to Ser and CO2 in the mitochondrion (Tolbert, 1971). The Ser gives rise to glyceric acid, which is ultimately converted to 3-phosphoglyceric acid in the mesophyll (M) cell chloroplast (Usuda and Edwards, 1980). Thus, the photorespiratory pathway (Fig. 1
) is a futile process that diverts energy to refixation of photorespired CO2, thereby lowering the quantum efficiency of net carbon assimilation (Zelitch, 2001).
In C3 leaves, production of photorespiratory CO2 decreases net CO2 assimilation by about 25% at 25°C, and photorespiration increases greatly relative to CO2 assimilation at higher temperatures (Peterson, 1983 ; Hanson and Peterson, 1986). In C4 plants such as maize (Zea mays), a carbon shuttle increases local CO2 concentrations in the BS chloroplasts, where Rubisco is located, to levels more than three times higher than those found in M cells of C3 plants. As a result, photorespiration is greatly reduced in C4 tissues (Hatch, 1971; Jenkins et al., 1989; Dai et al., 1993; Laisk and Edwards, 1998).
Several studies point to a low, yet finite, rate of photorespiration in maize. To estimate photorespiration in maize leaves, Zelitch (1973)
A number of conditional mutants with lesions in different steps of the photorespiratory pathway were first obtained by Ogren and coworkers in Arabidopsis (Arabidopsis thaliana; Ogren, 1984
Transgenic tobacco plants were generated that had reduced GO activity through cosuppression of the endogenous GO (Yamaguchi and Nishimura, 2000 In this report, we describe the isolation and characterization of a maize GO mutant caused by an Activator (Ac) insertion in GO1 (go1-m1::Ac). Using Ac as a molecular tag, the GO gene was cloned and sequenced. In addition, mutant seedlings were characterized under both high and low CO2 conditions. Under high CO2 conditions, GO deficiency had no visibly adverse effects on plant growth. However, A was rapidly and linearly diminished in mutants in high light and high O2. When such mutant plants were transferred from growth in high CO2 to normal air in the light, glycolate accumulated linearly for 6 h to levels 7-fold greater than the initial concentration. Plants greatly depleted in GO activity were nonviable when grown at ambient CO2 concentrations. We therefore conclude that photorespiration plays a vital role in C4 photosynthesis.
Identifying a Maize GO Mutant
The GO mutant was first identified in sandbench screens of Ac-mutagenized families (Kolkman et al., 2005
Genomic sequences flanking the Ac insertion were used to search GenBank and matched genomic DNA (AC187560.5) and mRNA (AY108197). Further BLAST searches indicated the Ac insertion was in exon 7 of a putative GO gene (Fig. 2A ). We reasoned that the mutant phenotype (necrosis and seedling death) was likely caused by accumulation of glycolate and that it may be rescued under high CO2 conditions where photorespiration is minimal. In an attempt to rescue the seedling lethality of homozygous go1 mutants, seedlings were grown under high CO2 conditions (1% to 5% CO2 in air). Under these conditions, the growth and appearance of the mutants could not be distinguished visually from either the heterozygous or homozygous wild-type individuals (Fig. 3 ). Seedlings were routinely grown this way for 30 to 60 d. Soon after germination in high CO2, the phenotype of an individual plant was established using a sensitive GO assay carried out on extracts prepared from discs cut from the first leaf. Later, this phenotype was confirmed on extracts prepared from second or third leaves. As shown in Figure 2B and Table I , seedlings homozygous for the Ac insertion allele showed minimal GO activity. Extracts from heterozygous individuals exhibited intermediate capacities to oxidize glycolate (Table I), indicating that a single functional copy of GO is insufficient to completely rescue the defect in GO activity. Heterozygote plants appear phenotypically normal, complete a full-life cycle, and are not underrepresented among segregating families. Thus, GO activity of heterozygote individuals is sufficient for plant health in normal air under the growth chamber conditions employed here. Plants with the highest GO activities were homozygous for the functional GO1 allele (430-bp band in Fig. 2B). As shown in Figure 2C, wild-type plants accumulated GO mRNA in contrast to the homozygous mutant plants with the low GO activity, consistent with the severe mutant phenotype of the homozygous insertion. When go1 mutant seedlings were transferred from high CO2 to normal air, leaves became necrotic within 7 d, and the seedlings died within 15 d under either growth chamber or greenhouse conditions (Fig. 3B). Taken together these data indicate that the seedling lethality of the mutants is due to the cytotoxic accumulation of glycolate in homozygous individuals due to an Ac insertion in the maize GO1 gene. We therefore named the mutant allele go1-m1::Ac. A phylogenetic analysis of known GOs from Oryza sativa and Arabidopsis reveals two separate protein subgroups (Fig. 4A ) in which the maize GO1 (derived from mRNA PCO065133 gb AY108197) is most similar to proteins encoded by Os07g0152900 (91.0%/96.8% identity/similarity) and At3g14415 (83.7%/94.8%; Fig. 4B).
CO2 Assimilation in Low GO Mutant Is Strongly Inhibited in High O2
To examine the consequences of the loss of GO activity on A, wild-type and go1 mutant leaf tissue was examined under low (1%) and high (50%) O2 conditions (Table II
). Representative results are shown in Figure 5
. Values of A attained relatively stable levels after 20 min in high light and low O2 (Fig. 5). The average value of A attained after 40 to 50 min in 1% O2 was lower for the mutant, but this effect was not statistically significant (P > 0.05; Table II). A similar trend was noted for effect of genotype on intrinsic quantum yield of PSII (Fv/Fm in Table II). Though not visible by eye, leaf-to-leaf variation in Fv/Fm was unusually high among mutant leaves, consistent with the occasional occurrence of mild cytotoxic symptoms. An immediate 3% to 4% reduction in A occurred upon increasing the O2 level from 1% to 50% for both genotypes (Fig. 5). During the remainder of the exposure to 50% O2, the magnitudes of A declined on average by 16% (10% in the example illustrated in Fig. 5) for wild type. A similar inhibition of A at high O2 was observed in maize leaves by Dai et al. (1993)
go1 Mutants Do Not Display a General Disruption in the Photorespiratory Cycle To examine the consequences of a disruption of GO activity on additional reactions of the photorespiratory cycle, go1 mutants were further characterized by providing [1-14C]glycolate to leaf discs in darkness and measuring the 14CO2 produced (Table III ). These results are consistent with parallel assays made on leaf extracts showing that go1 mutants do in fact have a low but measurable activity compared with intermediate and normal plants. An important later step in photorespiration, after oxidation of glycolate, involves the conversion of two Gly to Ser and CO2 (Fig. 1). Leaf discs taken from go1 mutants were tested to determine whether any later step in the pathway was also affected by supplying [1-14C]Gly in darkness. Table IV shows that the rate of formation of [14C]Ser and 14CO2 was similar for all three genotypes. The mean ratio of CO2 produced:Ser formed was 1.02, close to the expected stoichiometry, and an ANOVA showed there was no significant difference in the mean ratios among the three genotypes. Thus, plants with low GO activity were not likely altered in their ability to otherwise complete metabolism of photorespiratory Gly.
Glycolate Accumulates in Normal Air in the Low GO Mutant
Though considerable phosphoglycolate is produced by the Rubisco oxygenase reaction, a high GO activity keeps the free glycolate concentration at low steady-state levels in leaves, and even when glycolate concentration increased greatly in short-term experiments in tobacco treated with an inhibitor of GO, the phosphoglycolate concentration was unaffected (Zelitch, 1965
When seedlings were transferred from growth in high CO2 to normal air under the same growth conditions, glycolate concentration in the leaves increased rapidly and linearly for at least 6 h in go1 mutants to a level of 6.3 µmol glycolate/g fresh weight, a 7-fold increase (Fig. 6). After a total of 25 h in air, the glycolate concentration increased to 10.0 µmol glycolate/g fresh weight, an 11-fold increase over the initial concentration. An increase in glycolate concentration in maize leaves induced by photorespiratory inhibitors was accompanied by a decrease in A (González-Moro et al., 1997 ), and a level of 4.0 µmol glycolate/g fresh weight was sufficient to completely abolish A. This inhibitory glycolate concentration was reached after about 3 h in normal air in mutant leaves (Fig. 6). The linear increase in glycolate in go1 mutants (Fig. 6) is consistent with the linear loss of A capacity in 50% O2 and high light (Fig. 5).
Consistent with lower rates of oxygenation of ribulose bisphosphate, it has often been noted that in C4 plants, the enzymes of the photorespiratory pathway, including GO, are present at much lower levels than in C3 plants (Edwards and Walker, 1983 ; Dai et al., 1995). For example, the GO specific activity in C3 grasses is approximately 10-fold greater than in maize (Ueno et al., 2005), and we have also found (I. Zelitch, unpublished data) that on a leaf area basis, maize has about 10% as much GO activity as the C3 tobacco leaf. Nevertheless, no mutant has previously been described in a C4 plant in which GO, or any other gene underlying an enzymatic step of the photorespiratory pathway, was defective. We have shown here that a homozygous disruption of the GO1 gene produces a conditional lethal mutation. This mutant is analogous in its phenotype to other mutants that disrupt enzymatic steps in photorespiration, as previously described for Arabidopsis and other C3 species (Ogren, 1984, 2006) and shows that a functional photorespiratory pathway is essential for maize seedling development.
As shown in Figure 1, glycolate is an early intermediate following the oxygenation of ribulose-1,5-bisphosphate. To examine the effects of glycolate accumulation on carbon assimilation in maize, González-Moro et al. (1997)
Three isoforms of GO have been identified in maize. Two isoforms are localized to the BS, representing 80% of the total activity, and one to the M cells (Popov et al., 2003 As we have discussed, photorespiration in maize is normally low, but our results confirm that it is not entirely absent, so we must conclude that the CO2-concentrating mechanism in the BS cells does not completely suppress Rubisco-catalyzed oxygenation of ribulose bisphosphate, the primary source of glycolate (Figs. 1 and 6).
This conclusion is consistent with previous studies (Dai et al., 1995
The reaction catalyzed by GO is the only known route for processing of glycolate. Hence, our results show that accumulation of glycolate is a causal agent leading to inhibition of metabolic processes associated with A in C4 photosynthesis. The results strongly support the view that an important function of GO and the photorespiratory pathway is the avoidance of buildup of toxic levels of glycolate, as has previously been suggested (González-Moro et al., 1997
The question has often been posed: does photorespiration have a function? There is some evidence that glycolate can strongly inhibit QA/QB electron transfer by displacement of bicarbonate bound to the non-heme iron in PSII (Petrouleas et al., 1994
Ogren (1984)
Ac Mutagenesis and Cloning of GO1
The go1 mutant was identified in sandbench screens of lines segregating newly transposed Ac elements. To identify an Ac-containing restriction fragment polymorphism, genomic DNA was fractionated using EcoRI and resolved on a 0.8% agarose gel prior to transfer to nylon membranes as previously described (Kolkman et al., 2005
Growth of Plants in High CO2 Plants were grown in an environmental control chamber under an 18-h-light/6-h-dark photoperiod and 250 µmol photons m–2 s–1 light provided by sodium vapor lamps. The temperature regime was 30°C light/20°C dark. Eight plastic pots (each 2.2 L in volume) were filled with moistened sterile Promix-BX (peat-based medium containing perlite, vermiculite, and limestone), and the pots were placed in a tray containing water. Four seeds of a population segregating for GO activity were placed in each pot. A portable chamber (total gas volume 219 L) covered with clear plastic was placed over the pots and 1% to 5% (v/v) CO2 in air was continuously pumped into the middle of the chamber at 1 L min–1. Care was taken to avoid simultaneous exposure to actinic light and normal air during plant growth. A complete nutrient solution containing 800 mg L–1 nitrogen, Jack's Fertilizer (J.R. Peters Co.), and 7 mg L–1 chelated iron was added to each pot weekly, and at the same time the foliage was sprayed with the same nutrient solution containing 200 mg L–1 disulfosuccinic acid (Na salt) to "wet" the leaves. After replacing the portable chamber, the pots were flushed with high CO2 for 2 h in darkness before the lights were turned on again.
Four 0.8-cm discs (2.0 cm2; 28 mg fresh weight) were cut with a sharp punch in near darkness from a single leaf from plants grown in high CO2. The discs were transferred to microfuge tubes that were quickly placed in liquid N2 and then stored at –70°C. Four samples at a time were thawed in an ice bath for the GO assays. A small amount of washed sand was placed in each tube, and 0.8 mL of cold extraction buffer was added (0.05 M potassium phosphate buffer, pH 8.0, containing 1 mM mercaptoethanol). The leaf discs were ground with a plastic pestle and the tubes centrifuged under refrigeration at 16,000g for 10 min. The supernatant was used for the enzyme assays.
The reactions were carried out in 12- x 100-mm test tubes on samples from four plants at a time. For each sample, two separate tubes were used, one without glycolate and the other containing the complete reaction mixture. Each tube had 100 µL of extraction buffer, 100 µL cold (freshly prepared) 1.6% phenylhydrazine hydrochloride, 100 µL freshly prepared FMN (4.8 mg 10 mL–1), 300 µL of leaf extract, and water to make the final volume 1.5 mL. The tubes were shaken at 30°C for 10 min, then at 1-min intervals, 50 µL 0.1 M potassium glycolate was added to every other tube and the reaction continued for 20 min. The reaction was stopped by the addition of 500 µL 12 N HCl. Color development of the glyoxylate phenylhydrazone was induced by the addition of 100 µL 8% potassium ferricyanide to each tube (Jameel et al., 1984
Genomic DNA from leaves was prepared according to Dellaporta (1993)
Radioactive calcium [1-14C]glycolate was obtained from American Radiolabeled Chemicals. It was dissolved in water and first passed through a column of Dowex 50 (H+ form, Bio-Rad) and eluted with water. Potassium glycolate (0.1 M) was added to make the final concentration 40 mM. A portion was added to a column of Dowex 1 X8, 100 to 200 mesh, anion-exchange resin (Bio-Rad) 0.7 cm in diameter and 6 cm in height. The column was eluted with 10 mL of water, then with 4 mL of 4 N acetic acid, and these fractions were discarded. Glycolic acid was eluted by collection of the next 10 mL of 4 N acetic acid (Zelitch, 1972 For metabolic experiments, 12 0.8-cm leaf discs (6.0 cm2) were cut with a punch from a leaf obtained from plants growing in high CO2 and previously identified as having wild-type, intermediate, or low GO activity. The discs were floated on water and transferred to 50-mL Erlenmeyer flasks containing center wells. Potassium [1-14C]glycolate (1.0 mL, 40 mM, 2.41 x 106 dpm) was added to each flask, and a control flask omitting leaf discs was used in every experiment. A paper wick moistened with 5 M ethanolamine was placed in the centerwell to trap 14CO2. The flasks were covered with aluminum foil, closed with a rubber serum stopper, and shaken for 2 h at 20°C. The paper wicks were removed to scintillation vials and the radioactivity determined by scintillation spectrometry. Experiments on the metabolism of [1-14C]Gly, 7.1 x 106 dpm, were carried out in a similar manner as those with [1-14C]glycolate. At the end of the experiments, the 14CO2 was determined as before. The flask was filled with water to dilute the radioactive substrate, and the leaf discs were killed by placing them in a Ten Broeck homogenizer containing 5 mL of boiling 20% ethanol and kept in a boiling water bath for 5 min. The leaf tissue was ground in the homogenizer, centrifuged, the residue washed with water and centrifuged again, and the combined supernatants further analyzed for radioactive metabolites. A portion of each sample was placed on a Dowex-1 acetate column, and the neutral and basic compounds, including Gly and Ser, were eluted with water. A 1.0-mL portion of each sample was concentrated to 400 µL in a rotary evaporator under vacuum, and 50-µL samples were placed on a HPLC cation exchange Na+ column (PRP x 200, 4.2 x 250 mm, Hamilton) and eluted at 30°C with 25% [NaCl:HCl 0.05 m] and 75% water. Ser and Gly eluted separately in this system. Eluates containing each compound were collected in scintillation vials and their radioactivity determined by scintillation spectrometry.
All measurements were conducted using a computer-controlled, dual channel flow-through apparatus previously described (Peterson et al., 2001
Plants were grown in high CO2 under temperature- and light-controlled conditions as described above. Plants were kept in normal air in darkness for 1 h. Leaf segments were cut from a leaf (zero time), and the same light and temperature conditions were then maintained for the plants as before but in normal air. Successive segments (2–6 cm2) were cut from the same leaf during the time course, and the segments were placed in microfuge tubes and plunged into liquid nitrogen. The tubes were stored at –70°C. Leaf tissue was extracted in boiling 20% ethanol as described above. The samples were ground and the suspension centrifuged for 10 min at 15,000g under refrigeration. The residue was suspended in water and centrifuged again. The combined supernatants were added to columns of Dowex-1 X8 acetate, 100 to 200 mesh, anion-exchange resin (Bio-Rad) 0.8 cm in diameter and 6.0 cm in height. The columns were washed with water, elution continued with 4 mL of 4 N acetic acid that was discarded, and the glycolic acid fraction (also known to contain glyceric acid in leaf extracts) was eluted by addition of 10 mL 4 N acetic acid (Zelitch, 1972
We thank Martin P.N. Gent for the HPLC analyses, Regan Huntley and Carol Clark for technical assistance, and Gary Brudvig for helpful comments. We also thank Linda Rymarquis who initially characterized go1 mutant families. Received August 26, 2008; accepted September 16, 2008; published September 19, 2008.
1 This work was supported by the Hatch Fund (grant no. CONH00246 to R.B.P.) and by the National Science Foundation (grant no. DBI–0076892) to T.P.B.  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Israel Zelitch (israel.zelitch{at}po.state.ct.us).
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.128439 * Corresponding author; e-mail israel.zelitch{at}po.state.ct.us.
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ABSTRACT
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-hydroxysulfonate, and found that glycolate accumulation was 10% as great in maize as in tobacco (Nicotiana tabacum; C3). Because no mechanism for the metabolism of glycolate is known without its first being converted to glyoxylate, this demonstrated that the rate of CO2 production by photorespiration was no more than 5% of the net CO2 assimilation rate (A) in C4 photosynthesis. Additional studies that monitored 18O2 and 13CO2 exchange and estimates from electron transport suggested a similar photorespiratory rate in maize of 2% to 7% of A (Volk and Jackson, 1972
2 = 0.23; P = 0.63). DNA-blot analysis was used to identify an Ac-containing, 3.2-kb EcoRI fragment that cosegregated with the mutant phenotype (data not shown). Approximately 800 bp of DNA flanking this sequence was recovered using an inverse PCR technique as described in "Materials and Methods." To recover additional sequences flanking the Ac insertion, we exploited the somatic instability of the active Ac insertion to selectively amplify Ac junction fragments that were generated through local insertions. This method, known as Ac casting (Singh et al., 2003
