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. 2014 Jul 22;65(18):5331–5338. doi: 10.1093/jxb/eru294

Effect of exogenous methanol on glycolate oxidase and photorespiratory intermediates in cotton

Yan-Ru Bai 1, Ping Yang 1, Yuan-Yuan Su 1, Zong-Ling He 1, Xiao-Nan Ti 1,*
PMCID: PMC4400538  PMID: 25053644

Summary

Exogenous MeOH enhances cotton yield by inhibiting glycolate oxidase activity, which increases glyoxylate and decreases glycine, and suggests that there is another photorespiratory pathway in cotton.

Key words: Exogenous methanol, glycolate oxidase, photorespiratory pathway, photorespiratory intermediates, mechanism, cotton.

Abstract

Application of methanol (MeOH) inhibits photorespiration and enhances growth and yield in C3 plants. However, the underlying cellular and molecular mechanisms are not clear. In this study, we investigated the effects of foliar application of MeOH (30%, v/v) on glycolate oxidase (GO) activity and photorespiratory intermediates in cotton leaves in a field experiment. MeOH treatment significantly inhibited GO activity (by 30% compared with the controls). We also found that endogenous glyoxylate, a photorespiratory intermediate, increased and glycine decreased significantly in MeOH-treated plants. Serine increased significantly in MeOH-treated plants. These results thus demonstrated that exogenous MeOH can modulate GO activity and the production of photorespiratory intermediates, and sheds new lights on our current understanding of how exogenous MeOH inhibits photorespiration and enhances the growth and yield of C3 plants such as cotton.

Introduction

It was discovered 20 years ago that the application of methanol (MeOH) in arid environments increases the yield of C3 plants (Nonomura and Benson, 1992; Devlin et al., 1995; Salehi, 2013). However, the underlying mechanisms by which MeOH increases yields are not clear. It is believed that MeOH alleviates CO2 deficiency and inhibits photorespiration (Benson and Nonomura, 1992; Hemming et al., 1995; Fall and Benson, 1996; Gout et al., 2000). It is well known that photorespiration is an essential auxiliary metabolic pathway that allows photosynthesis to happen in oxygen-containing environments in terrestrial C3 plants (Wingler et al., 2000). It occurs because oxygen can substitute carbon dioxide in the first reaction of the photosynthetic carbon dioxide-fixation process and arrests the synthesis of 2-phosphoglycolate (2-PG) in the chloroplast. Therefore, 2-PG is considered as a by-product of photorespiration in the photorespiratory pathway. In this pathway, 2-PG is further converted to glycolate, glyoxylate, glycine (Gly), and serine (Ser), and is used to resynthesize glycerate in the chloroplast, peroxisome, and mitochondrion (Brem et al., 1983; Blackwell et al., 1990; Leegood et al., 1995). Although reports on MeOH production, emission, and its catabolism have been documented in vascular plants (Benson and Nonomura, 1992; Nemecek-Marshall et al., 1995; Fall and Benson, 1996; Gout et al., 2000; Galbally and Kirstine, 2002; Niinemets et al., 2004), little is known about its physiological role in plant growth and its relationship with the photorespiratory intermediates when MeOH is applied to C3 plants. Cotton, Gossypium hirsutum L., is a typical C3 plant, and has significantly higher photorespiration rates (Dong et al., 2000). In this study, we evaluated the physiological responses of cotton to MeOH foliar application under field conditions and report the effects of (i) exogenous MeOH on levels of photorespiratory major metabolites intermediates; (ii) mutation of key enzymes on the activity of photorespiration; and (iii) the mechanism of MeOH regulation of photorespiration in cotton.

Materials and methods

Plant growth and treatment

To study the effects of methanol on photorespiratory intermediates and activity of enzymes, methanol was applied to fresh flower cover of cotton (Gossypium hirsutum L., varieties of “Huiyuan 710”) after topping in a field experiment. The experiment was in factorial format based on randomized complete block design with three replications. Every plot area was 25 m2 with intervals of more than 5 m between the plots, and was performed on San Ping internship farm of Xinjiang Agricultural University, which has a semi-arid climate. The experiment was performed in July and August 2013, located in 87º21’ east longitude and 43º56’ north latitude, where the average annual rainfall is 194mm, there is a large temperature difference between day and night in summer, and the average temperature is 28.4 °C in July and August. The treatments were: (i) sprayed with deionized water (control) and (ii) MeOH 30% (v/v). Foliar applications were performed between 11.30–12.00h (the local noon) on a bright sunny day (26 July). The plants were then sampled continuously over 20 days (from 27 July to 15 August); only leaves above the 2nd or 3rd leaf that formed on each plant was sampled, at 12.00h (noon) each day. From every plot five leaves of different individuals were taken, mixed randomly, and placed in a liquid nitrogen container immediately. The weather conditions of the sampling day were measured by a CIRAS-2 Portable Photosynthesis System. Results are shown in Table 1.

Table 1.

The weather conditions during the period of study

Days after treated* 1 2 3 4 5 6 7 8 9 10
Weather condition S S O R C S S S R O
Temperature (°C) 27.2 28.5 26.1 25.3 26.3 31.5 33.1 33.4 27.3 28.0
Light intensity
(µmol m–2 s–1)		 1799.2 1765.1 785.3 582.5 1121.7 1794.3 1856.6 1838.1 496.9 790.9
Days after treated* 11 12 13 14 15 16 17 18 19 20
Weather condition R S S S S S S S S S
Temperature (°C) 26.2 33.5 32.7 33.2 34.4 35.5 33.6 32.5 32.1 31.4
Light intensity
(µmol m–2 s–1)		 544.5 1955.8 1938.2 1968.4 1989.5 2077.1 1973.6 1831.7 1854.4 1817.3
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* Continuous sampling 20 days from 27 July to 15 August after MeOH-treated (on 26 July, 2013); S, sunny day; O, overcast day; C, cloudy day; R, rainy day. Temperature and light intensity were measured by CIRAS-2 Portable Photosynthesis System.

Determination of glycolate oxidase (GO) activities

Glycolate oxidase (GO; EC 1.1.3.1) was assayed as described by Booker et al. (1997), with modifications. The cotton leaf samples were removed from the liquid nitrogen container, ground into fine powder with liquid nitrogen in an ice-water bath, and 0.5g of the homogenized samples was then homogenized with 5ml 50 mmol Tris-HCl buffer (mixed with 0.01% Triton X-100, 5 mmol l–1 DTT, (pH 7.8) in an ice bath. The extracts were clarified by centrifugation at 5000g for 15min at 4 °C. The supernatants were pooled and collected for GO analysis. A 2ml volume of assay mixture containing 50 mmol Tris-HCl buffer (pH 7.8), 0.009% (v/v) Triton X-100, 3.3 mmol phenylhydrazine HCl (pH 6.8), 50 µl of plant extract, and 5 mmol glycolate (neutralized to pH 7.0 with KOH) was used to start the reaction at 25 °C. GO activity was determined by following the formation of glyoxylate phenylhydrazone (extinction coefficient of 17mmol–1 cm–1) at 324nm in the UV-vis spectrophotometer (UV-1700, Nikon) for 2min after an initial lag phase of 1min.

Testing of glyoxylate contents

The cotton leaf samples were removed from the liquid nitrogen container, ground into fine powder with liquid nitrogen in an ice-water bath, and 1.0g of the homogenized sample was added to 15ml of hot water (Rojano-Delgado et al., 2010). The leaf contents were then extracted for 40min in a water bath at 80 °C. Activated carbon (0.25g) was added to the extraction to remove impurities, and the samples were centrifuged for 10min at 5000g, 4 °C. Finally, the supernatant was collected for glyoxylate detection. 1.0ml extract was mixed with 1.0ml sodium acetate solution and 1.0ml hydroxylamine hydrochloride in a 10ml colorimetric tube. The tube was heated at 80 °C in a water bath for 20min and the volume was kept constant with distilled water after cooling. The scanning wavelength range was 200–800nm; the known maximum absorption wavelength of glyoxylate is 215nm (Dong et al., 2005). The absorbance of the samples was then detected at 570nm in a UV-vis spectrophotometer (UV-1700, Nikon).

Detection of amino acid contents

The cotton leaf samples were removed from the liquid nitrogen container, ground into fine powder with liquid nitrogen in an ice-water bath, and 1.0g of the homogenized sample was mixed with 10mL 80 % (v/v) ethanol at 80 °C for 40min. The extracts were added to 0.25g of activated carbon to remove impurity by centrifugation at 5000g for 10min at 4 °C. Pellets were extracted three times with 80% ethanol and the supernatants were pooled and collected for amino acid analysis (Bialczk et al., 2005). Precolumn derivatization was carried out. Extracts were filtered through a 0.45 µm filter membrane. A 500 µl extract was added into a 2.0ml centrifuge tube, mixed with 400 µl pH 10.0 borate buffer solution and 100 µl derivative agents, and incubated at 25 °C for exactly 20min. The reaction mixture was immediately used for HPLC analysis (LC-20AB-UV, Shimadzu). The derivatization solution was freshly prepared every day as following: 5mg of o-phthaldialdehyde (OPA) was dissolved in 0.05ml methanol, followed by addition of 25 µl of β-mercaptoethanol. Gly and Ser were purchased from Sigma. The detailed analysis parameters have been described in Alcázar et al. (2007).

Unless otherwise noted, all preparation procedures were conducted in a cold room (4–5 °C) or in an ice-water bath.

Results

To determine enzyme activity and the production of photorespiration intermediates, we sprayed cotton leaf slices with 30% (v/v) MeOH during flowering stages and monitored the changes of glycolate oxidase activity and the contents of glyoxylate, Gly, and Ser for 20 days. Twice there were rainy days (rainy, overcast, or cloudy days (collectively referred to as “rainy days”), in days 3–5 and days 9–11) during the period of study (Table 1). The sampling temperature and light intensity were measured by a CIRAS-2 Portable Photosynthesis System, and are shown in Table 1.

Effects of exogenous methanol on glycolate oxidase activities

Glycolate oxidase (GO; EC 1.1.3.15), located in the peroxisome, is a key enzyme that controls an essential step in the oxidative photorespiratory cycle (Frederick et al., 1973; Barak et al., 2001). It oxidizes glycolate and converts it into glyoxylate in C3 plants. Transamination of glyoxylate generates Gly, which, subsequently, is converted to Ser and CO2 in the mitochondrion. Ser gives rise to glycerate, which is ultimately converted to 3-phosphoglycerate in the chloroplast (Zelitch et al., 2009). The mitochondrial glycolate oxidation activity contributes to photorespiration in vascular plants (Niessen et al., 2007). Therefore, GO activity has a direct influence on photorespiration rate (Esquivel, 1998; Xu et al., 2006).

We found that the effect of MeOH on the activity of GO is related to photorespiration metabolism in cotton leaves. In control leaves, the GO activities were lower in rainy days than in sunny days, and were decreased as the temperature increased (>30 °C) during the growing period (Fig. 1). These results are also in line with the report by Downton and Slatyer (1972). However, the magnitude of these changes was significantly higher in MeOH-treated plants than that seen in the controls. MeOH treatment resulted in a 30% decrease in GO activity as compared with the controls. The GO activity decreased further with rainy conditions, approximately 1.10 µmol g–1 min–1 (Fig. 1). The reaction catalysed by GO is the only known route for the conversion of glycolate to glyoxylate (Niessen et al., 2007). Our result that GO activities were lower in MeOH-treated plants than that in control plants suggests that exogenous MeOH inhibits GO activity.

Fig. 1.

Fig. 1.

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Effect of exogenous methanol on glycolate oxidase (GO) activity in cotton leaves during flowering and boll stages for 20 days. The treatments were: (i) sprayed with deionized water (control) and (ii) MeOH 30% (v/v). Leaves of five different individuals were harvested from the control and MeOH-treated cotton plants after topping, and GO activity was analysed by the method of Booker et al. (1997). The data are means±SD (n=3) of activity of GO in control (open bars) and MeOH-treated (grey bars) samples. Standard error bars are included. Data were analysed by one-Way ANOVA, Student-Newman-Keuls with SPSS 17.0 software. “**” indicates a significant difference P<0.01; “*” indicates difference P<0.05; No symbol indicates no difference (P>0.05) (between the control and MeOH-treated). The weather condition is show in X axis below (S, sunny day; O, overcast day; C, cloud day; R, rainy day).

Effects of exogenous methanol on glyoxylate contents

Next, we determined the contents of glyoxylate in response to MeOH treatment. Endogenous glyoxylate increased significantly in MeOH-treated samples compared with the control samples (Fig. 2). Moreover, a correlation between the contents of glyoxylate and weather condition was observed: compared with the controls, when the light intensity and temperature were low in rainy days (d 3–5 and 9–11 after the treatment, Fig. 2), the increase in the contents of glyoxylate was negligible (2.88%). However, when the light and temperature were high in sunny days (days 1–2, 6–8, and 12–20 after the treatment, Fig. 2), the increase of glyoxylate contents was marked (18.86%). Furthermore, the magnitudes of glyoxylate fluctuation were always higher in MeOH-treated samples than that in control samples (control 23.11 vs. treatment 25.67 µmol gFW–1) (Fig. 2). As hot, dry, and sunny days are the favourable weather conditions for the photorespiration of C3 plants such as cotton (Downton and Slatyer, 1972; Buchanan, 1980; Dong et al., 2000), this result suggested that the photorespiratory pathway is enhanced by exogenous MeOH, most likely by stimulating, rather than inhibiting, GO activity (Fig. 1), because the contents of glyoxylate, a product of glycolate in photorespiratory pathway, were influenced by the fluctuations of light and temperature (Ouver and Zelitch, 1977; Buchanan, 1980; Peterson, 1980; Créach and Stewart, 1982) (Fig. 1).

Fig. 2.

Fig. 2.

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Effect of exogenous methanol on glyoxylate exchange content in cotton leaves during flowering and boll stages for 20 days. The treatments were: (i) sprayed with deionized water (control) and (ii) MeOH 30% (v/v). A pool of leaves from five different individuals was sampled from control and MeOH-treated cotton plants after topping and glyoxylate content analysed by the methods of Dong et al. (2005) and Rojano-Delgado et al. (2010). Data represent means±SD of three biological replicates. Standard error bars are included. Data were analysed by one-Way ANOVA, Student-Newman-Keuls with SPSS 17.0 software. “**” indicates significant difference of P<0.01; “*” indicates a difference of P<0.05; no symbol indicates no difference (P>0.05) (between the control and MeOH-treated). The weather condition is show in X axis (S, sunny day; O, overcast day; C, cloud day; R, rainy day).

Effects of exogenous methanol on glycine and serine contents

Gly, a two-carbon compound, is produced during photorespiration from the transmutation of glyoxylate (Day and Wiskich, 1981; Brem et al., 1983; Engel et al., 2007). As shown in Figure 3, the Gly content changes with the weather condition. Gly contents in MeOH-treated samples were not higher, but lower, than that in controls (control 0.64 vs. treatment 0.57 µmol gFW–1), and even lower in rainy days (0.36 µmol gFW–1). Glyoxylate is a precursor of Gly in the photorespiratory pathway (Timm et al., 2012). In general, an increase in the amount of substrate results in a corresponding increase of the product. However, in our MeOH-treated samples, changes of Gly contents were smaller than the control samples, especially in the rainy days, although the glyoxylate contents were significantly higher in MeOH-treated samples. There is a photorespiratory nitrogen cycle in which glyoxylate is converted to Gly, using glutamate (Glu) as an amino donor (Douce and Neuburger, 1999). We checked the flux of contents of Glu, but there was no significant difference between the control and MeOH-treated plants (Supplementary Fig. S1 is available at JXB online). Accordingly, we hypothesize that this glyoxylate increase could be a potential regulatory mechanism responsible for partial inhibition of GO.

Fig. 3.

Fig. 3.

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Effect of exogenous methanol on Gly contents in cotton leaves during flowering and boll stages for 20 days. The treatments were: (i) sprayed with deionized water (control) and (ii) MeOH 30% (v/v). Leaves of five different individuals were harvested from control and MeOH-treated cotton plants after topping and Gly contents were analysed by methods of Bialczk et al. (2005) and Alcázar et al. (2007) in a HPLC device. Data represent means±SD of three biological replicates. Standard error bars are included. Data were analysed by one-Way ANOVA, Student-Newman-Keuls with SPSS 17.0 software. “**” indicates a significant difference of P<0.01; “*” indicates a difference of P<0.05; no symbol indicates no difference (P>0.05) (between the control and MeOH-treated). The weather condition is shown in the X axis (S, sunny day; O, overcast day; C, cloud day; R, rainy day).

Ser, a three-carbon compound, is converted from two molecules of Gly. Although no obvious increase of Gly contents was observed, (Figs 3 and 5A, B), the accumulation of Ser was increased significantly in MeOH-treated samples, especially during the rainy days (Figs 4 and 5C, D). As a result, the ratio of Gly to Ser, a parameter widely used for assessing the rate of photorespiration (Novitskaya et al., 2002), was decreased in MeOH-treated samples regardless of sunny or rainy conditions (Fig. 5E, F; Gly/Ser ratio: 1.38<control (1.55) on sunny days and 0.94<control (1.32) on rainy days). Thus, our results suggest that MeOH treatment can reduce the rate of photorespiration.

Fig. 5.

Fig. 5.

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Comparison of Gly and Ser data between sunny days and rainy days during the monitored period. (A, B) The average contents of Gly in sunny days; (C, D) the average contents of Ser in sunny days and in rainy days; (E, F) the Gly/Ser ratio in sunny days and in rainy days. Open bars indicate the mean for the control samples and the black bars the mean for the MeOH-treated samples. Standard error bars are included. Data were analysed by one-Way ANOVA, Student-Newman-Keuls with SPSS 17.0 software. “**” indicates a significant difference of P<0.01; “*” indicates a difference of P<0.05; no symbol indicates no difference (P>0.05) (between the control and MeOH-treated).

Fig. 4.

Fig. 4.

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Effect of exogenous methanol on Ser contents in cotton leaves during flowering and boll stages for 20 days. The treatments were: (i) sprayed with deionized water (control) and (ii) MeOH 30% (v/v). Leaves of five different individuals were harvested from control and MeOH-treated cotton plants after topping and Ser contents analysed by the same methods as Fig. 3. Data represent means±SD of three biological replicates. Standard error bars are included. Data were analysed by one-Way ANOVA, Student-Newman-Keuls with SPSS 17.0 software. “**” indicates a significant difference of P<0.01; “*” indicates a difference of P<0.05; no symbol indicates no difference (P>0.05) (between the control and MeOH-treated). The weather condition is show in the X axis (S, sunny day; O, overcast day; C, cloud day; R, rainy day).

Studies have shown that Ser may play an important role in the photorespiration pathway. Ser is a principal product of exogenous MeOH metabolism (Gout et al., 2000). Timm et al. (2013) showed that Ser acts as a metabolic signal for the transcriptional control of photorespiration-related genes, particularly those involved in the Gly-to-Ser interconversion. Ser can also inhibit the activity of GO (Timm et al., 2013). Our data that MeOH treatment increased Ser production suggests that a part of Ser may come from exogenous MeOH. It also suggests that the Ser contents may have other sources when the GO activity is partially inhibited by MeOH treatment in cotton leaves. Together, our data suggest that (i) MeOH serves as an elicitor molecule in cotton leaves for conversion of Ser and inhibits the activity of GO, and (ii) the decrease of Gly contents is due to the synthesis of Ser, which leads to the inhibition of photorespiration.

Discussion

This study aimed to understand the cellular mechanisms by which exogenous MeOH regulates photorespiration, focusing on the activities of GO and the contents of photorespiratory intermediates. We found that MeOH can influence the production of photorespiratory intermediates (Figs 3 and 4). These findings help explain why Ser contents increase and how Gly contents decrease, which lead to a reduction in the rate of photorespiration. Our data suggest that cellular contents of Ser or glyoxylate play an important role in the regulation of GO activities. However, questions remain; for example, how exogenous MeOH increases the accumulation of glyoxylate.

Photorespiratory intermediate contents change in response to exogenous MeOH treatment

It is known that the cascade of photorespiration follows the sequence of glycolate → glyoxylate → Gly → Ser → light-dependent CO2 release in vascular plants (for review, and see Foyer et al., 2009). In this pathway or cycle, any changes in the contents of intermediates would alter the whole photorespiration pathway (Zelitch, 1972; Peterson, 1982). Our data reveal that cotton leaves treated with MeOH can effectively increase the contents of glyoxylate and Ser (Figs 2 and 4) and inhibit GO activity or, in other words, decrease the rate of photorespiration (by 30%, Fig. 1). This occurs even under conditions of significant Gly deficit (Fig. 3). It would be interesting to know why the contents of glyoxylate, a product of glycolate catalysed by GO, is higher in MeOH-treated plants than that in controls. Recent studies have also found an accumulation of glyoxylate when GO activity was inhibited in rice (Xu et al., 2009b ; Lu et al., 2014), suggesting that there are other ways to produce glyoxylate.

Exogenous MeOH may activate the glycerate pathway in cotton

MeOH is known as a deleterious by-product derived from pectin demethylation during the cell wall reconstruction process in vascular plants. The effects of MeOH on plant growth have been studied intensively in terrestrial plants (Ramberg et al., 2002; Kang et al., 2011). Although the effects of MeOH on plant physiology and gene expression have been investigated (McGiffen and Manthey, 1996; Gout et al., 2000; Hanson and Roje, 2001; Downie et al., 2004; Jin et al., 2011; Wu et al., 2013), its signal transduction mechanism has not been elucidated. Furthermore, most studies reported focus on vascular plants. MeOH is the simplest monohydric alcohol and exists commonly in nature (Benson et al., 2009; Fall and Benson, 1996; Xu et al., 2009a ). Not only that, MeOH, Gly, and Ser may have played an important role in the origin of life during the primordial soup geological period, and may have been involved in the evolution of photorespiration (Mouillon et al., 1999). Hence, on one hand, MeOH may have existed on Earth in its early years (Hanson and Hanson, 1996). Alternatively, the photorespiratory pathway could be an ancillary metabolic process that is essential for photosynthesis to occur in an O2-containing environment. It is also possible that MeOH co-evolved with oxygenic photosynthesis in cyanobacteria that lived 3.8–2.5 billion years ago in the near O2-free environment of the Precambrian ocean (Bauwe et al., 2010). Recent studies show that MeOH affects many aspects of vascular plants (Shen and Yeh, 2010; Kang et al., 2011; Peterhansel and Maurino, 2011; Peterhansel et al., 2013; Wu et al., 2013). Additionally, we observed various changes in the production of photorespiratory intermediates after MeOH treatment (Figs 2–4). The increase of glyoxylate is especially important in MeOH-treated samples (Fig. 2). It is most likely that a part of the glycolate pathway is inhibited in mitochondria but the glycerate pathway is activated in the chloroplast by exogenous MeOH. There are two different enzymes that can convert glycolate into glyoxylate in two different pathways (Zelitch, 1992; Bari et al., 2004; Stabenau and Winkler, 2005; Hackenberg et al., 2011; Bar-Even et al., 2012; Raven et al., 2012). Our recent study showed that activity of GO is inhibited by MeOH treatment in the cotton leaf (Su et al., 2012), and present data showed that the glyoxylate contents remain elevated even when GO activity is partially inhibited. The reason could be the activation of the glycolate dehydrogenase (GlcDH; EC 1.1.99.14) in the chloroplasts (Frederick et al., 1973; Eckardt, 2005; Eisenhut et al., 2006; Kebeish et al., 2007; Eisenhut et al., 2008; Kern et al., 2011; Zarzycki et al., 2013; Esser et al., 2014). In addition, our recent studies also showed that exogenous MeOH can improve the carboxylation activity in Rubisco, increasing the net photosynthesis in cotton (He et al., 2013). Consequently, these results suggested that vascular plants may also have the glycerate pathway, but this photorespiratory pathway is not active owing to complex evolution of plants in the terrestrial environment (Williams et al., 2013). Further studies on how exogenous MeOH activates the glycerate pathway are currently underway in our laboratory.

Supplementary data

Supplementary data are available at JXB online

Figure S1. Effect of exogenous methanol on Glu content in cotton leaves during flowering and boll stages for 20 days.

Supplementary Data
supp_65_18_5331__index.html (945B, html)

Acknowledgments

We gratefully acknowledge to Ju-Song Zhang for lending us the CIRAS-2 Portable Photosynthesis System. This work was supported by The National Science Foundation of China (No. 31160258).

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