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Methane protects against polyethylene glycol-induced osmotic stress in maize by improving sugar and ascorbic acid metabolism

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ABSTRACT

Although aerobic methane (CH4) release from plants leads to an intense scientific and public controversy in the recent years, the potential functions of endogenous CH4 production in plants are still largely unknown. Here, we reported that polyethylene glycol (PEG)-induced osmotic stress significantly increased CH4 production and soluble sugar contents in maize (Zea mays L.) root tissues. These enhancements were more pronounced in the drought stress-tolerant cultivar Zhengdan 958 (ZD958) than in the drought stress-sensitive cultivar Zhongjiangyu No.1 (ZJY1). Exogenously applied 0.65 mM CH4 not only increased endogenous CH4 production, but also decreased the contents of thiobarbituric acid reactive substances. PEG-induced water deficit symptoms, such as decreased biomass and relative water contents in both root and shoot tissues, were also alleviated. These beneficial responses paralleled the increases in the contents of soluble sugar and the reduced ascorbic acid (AsA), and the ratio of AsA/dehydroascorbate (DHA). Further comparison of transcript profiles of some key enzymes in sugar and AsA metabolism suggested that CH4 might participate in sugar signaling, which in turn increased AsA production and recycling. Together, these results suggested that CH4 might function as a gaseous molecule that enhances osmotic stress tolerance in maize by modulating sugar and AsA metabolism.

No MeSH data available.


Regulation of transcripts related to ascorbic acid metabolism.5-d-old maize seedlings of ZD958 and ZJY1 were preincubated in the solution containing 0.65 mM CH4 for 1 d, and then transferred to half-strength Hoagland solutions with or without 20% PEG-6000 for 2 d. Relative gene expression of GDP-L-galactose phosphorylase (GGP; DT943063), L-galactono-1,4-lactone dehydrogenase (GalLDH; DT943591), ascorbate peroxidase 1 (APX1; NM_001177011), ascorbate peroxidase 3 (APX3; NM_001159274), ascorbate peroxidase 6 (APX6; NM_001139033), dehydroascorbate reductase (DHAR; DR807318), and monodehydroascorbate reductase (MDHAR; CO461725) in root tissues were analyzed55. Control seedlings were incubated in Hoagland solution alone. Data are presented as means ± SE (5 root parts per experiment performed three times). Bars with different letters denote significant differences according to multiple comparisons (P < 0.05).
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f7: Regulation of transcripts related to ascorbic acid metabolism.5-d-old maize seedlings of ZD958 and ZJY1 were preincubated in the solution containing 0.65 mM CH4 for 1 d, and then transferred to half-strength Hoagland solutions with or without 20% PEG-6000 for 2 d. Relative gene expression of GDP-L-galactose phosphorylase (GGP; DT943063), L-galactono-1,4-lactone dehydrogenase (GalLDH; DT943591), ascorbate peroxidase 1 (APX1; NM_001177011), ascorbate peroxidase 3 (APX3; NM_001159274), ascorbate peroxidase 6 (APX6; NM_001139033), dehydroascorbate reductase (DHAR; DR807318), and monodehydroascorbate reductase (MDHAR; CO461725) in root tissues were analyzed55. Control seedlings were incubated in Hoagland solution alone. Data are presented as means ± SE (5 root parts per experiment performed three times). Bars with different letters denote significant differences according to multiple comparisons (P < 0.05).

Mentions: In order to investigate the relationship between CH4 and AsA metabolism, the transcriptional profiles of some key genes in AsA production and recycling (Supplementary Fig. S1) were analyzed. As shown in Fig. 7, CH4 pretreatment alone brought about much higher transcript levels of GDP-L-galactose phosphorylase (GGP), L-galactono-1,4-lactone dehydrogenase (GalLDH), ascorbate peroxidase 1/3/6 (APX1/3/6), dehydroascorbate reductase (DHAR), and monodehydroascorbate reductase (MDHAR) in ZD958; no such significant increases were observed in ZJY1 except for the gene expression of MDHAR. Compared with the control conditions, PEG treatment significantly decreased the transcript levels of GGP and APX3 in both ZD958 and ZJY1, but increased the expression of APX6. Except for APX1 and APX6 in ZJY1, higher transcript levels of all the tested genes were observed in CH4 pretreatment alone than those in only PEG-6000 stress. After CH4 pretreatment followed by PEG stress, there were significant increases in the levels of GalLDH, APX1/3, and MDHAR mRNA in the root tissues of ZD958 (in particular) and ZJY1 compared to PEG alone, all of which were consistent with the decreased H2O2 concentration and high level of AsA/DHA ratio (Fig. 6a,d).


Methane protects against polyethylene glycol-induced osmotic stress in maize by improving sugar and ascorbic acid metabolism
Regulation of transcripts related to ascorbic acid metabolism.5-d-old maize seedlings of ZD958 and ZJY1 were preincubated in the solution containing 0.65 mM CH4 for 1 d, and then transferred to half-strength Hoagland solutions with or without 20% PEG-6000 for 2 d. Relative gene expression of GDP-L-galactose phosphorylase (GGP; DT943063), L-galactono-1,4-lactone dehydrogenase (GalLDH; DT943591), ascorbate peroxidase 1 (APX1; NM_001177011), ascorbate peroxidase 3 (APX3; NM_001159274), ascorbate peroxidase 6 (APX6; NM_001139033), dehydroascorbate reductase (DHAR; DR807318), and monodehydroascorbate reductase (MDHAR; CO461725) in root tissues were analyzed55. Control seedlings were incubated in Hoagland solution alone. Data are presented as means ± SE (5 root parts per experiment performed three times). Bars with different letters denote significant differences according to multiple comparisons (P < 0.05).
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Related In: Results  -  Collection

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f7: Regulation of transcripts related to ascorbic acid metabolism.5-d-old maize seedlings of ZD958 and ZJY1 were preincubated in the solution containing 0.65 mM CH4 for 1 d, and then transferred to half-strength Hoagland solutions with or without 20% PEG-6000 for 2 d. Relative gene expression of GDP-L-galactose phosphorylase (GGP; DT943063), L-galactono-1,4-lactone dehydrogenase (GalLDH; DT943591), ascorbate peroxidase 1 (APX1; NM_001177011), ascorbate peroxidase 3 (APX3; NM_001159274), ascorbate peroxidase 6 (APX6; NM_001139033), dehydroascorbate reductase (DHAR; DR807318), and monodehydroascorbate reductase (MDHAR; CO461725) in root tissues were analyzed55. Control seedlings were incubated in Hoagland solution alone. Data are presented as means ± SE (5 root parts per experiment performed three times). Bars with different letters denote significant differences according to multiple comparisons (P < 0.05).
Mentions: In order to investigate the relationship between CH4 and AsA metabolism, the transcriptional profiles of some key genes in AsA production and recycling (Supplementary Fig. S1) were analyzed. As shown in Fig. 7, CH4 pretreatment alone brought about much higher transcript levels of GDP-L-galactose phosphorylase (GGP), L-galactono-1,4-lactone dehydrogenase (GalLDH), ascorbate peroxidase 1/3/6 (APX1/3/6), dehydroascorbate reductase (DHAR), and monodehydroascorbate reductase (MDHAR) in ZD958; no such significant increases were observed in ZJY1 except for the gene expression of MDHAR. Compared with the control conditions, PEG treatment significantly decreased the transcript levels of GGP and APX3 in both ZD958 and ZJY1, but increased the expression of APX6. Except for APX1 and APX6 in ZJY1, higher transcript levels of all the tested genes were observed in CH4 pretreatment alone than those in only PEG-6000 stress. After CH4 pretreatment followed by PEG stress, there were significant increases in the levels of GalLDH, APX1/3, and MDHAR mRNA in the root tissues of ZD958 (in particular) and ZJY1 compared to PEG alone, all of which were consistent with the decreased H2O2 concentration and high level of AsA/DHA ratio (Fig. 6a,d).

View Article: PubMed Central - PubMed

ABSTRACT

Although aerobic methane (CH4) release from plants leads to an intense scientific and public controversy in the recent years, the potential functions of endogenous CH4 production in plants are still largely unknown. Here, we reported that polyethylene glycol (PEG)-induced osmotic stress significantly increased CH4 production and soluble sugar contents in maize (Zea mays L.) root tissues. These enhancements were more pronounced in the drought stress-tolerant cultivar Zhengdan 958 (ZD958) than in the drought stress-sensitive cultivar Zhongjiangyu No.1 (ZJY1). Exogenously applied 0.65&thinsp;mM CH4 not only increased endogenous CH4 production, but also decreased the contents of thiobarbituric acid reactive substances. PEG-induced water deficit symptoms, such as decreased biomass and relative water contents in both root and shoot tissues, were also alleviated. These beneficial responses paralleled the increases in the contents of soluble sugar and the reduced ascorbic acid (AsA), and the ratio of AsA/dehydroascorbate (DHA). Further comparison of transcript profiles of some key enzymes in sugar and AsA metabolism suggested that CH4 might participate in sugar signaling, which in turn increased AsA production and recycling. Together, these results suggested that CH4 might function as a gaseous molecule that enhances osmotic stress tolerance in maize by modulating sugar and AsA metabolism.

No MeSH data available.