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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 sugar metabolism and signaling pathways by CH4.5-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 sucrose synthase 1 (SH1; X02400), sucrose synthase 2 (SUS1; L22296), soluble acid invertase 1 (IVR1; AF171874), soluble acid invertase 2 (IVR2; U31451), hexokinase 1/3/9 (HXK1/3/9; NM_001158821/XM_008676343/XM_008658658), UDP-glucose dehydrogenase (UDPGDH; EU961705) in root tissues were analyzed. 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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f5: Regulation of transcripts related to sugar metabolism and signaling pathways by CH4.5-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 sucrose synthase 1 (SH1; X02400), sucrose synthase 2 (SUS1; L22296), soluble acid invertase 1 (IVR1; AF171874), soluble acid invertase 2 (IVR2; U31451), hexokinase 1/3/9 (HXK1/3/9; NM_001158821/XM_008676343/XM_008658658), UDP-glucose dehydrogenase (UDPGDH; EU961705) in root tissues were analyzed. 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: To further establish the relationship between CH4 and sugar metabolism under PEG treatment, we analyzed the transcriptional profiles of some key genes in sugar metabolism and signaling pathways (Supplementary Fig. S1). Similar to the previous reports2728, PEG treatment significantly increased the transcript levels of sucrose synthase 1 (SH1) and UDP-glucose dehydrogenase (UDPGDH), while decreased the gene expression of soluble acid invertase 2 (IVR2) and hexokinase 3 (HXK3) in root tissues of two maize cultivars (Fig. 5). Compared with PEG alone, the transcript levels of sucrose synthase 2 (SUS1), soluble acid invertase 1 (IVR1), and hexokinase 1/9 (HXK1/9), were dramatically enhanced by CH4 pretreatment in ZD958, a tolerant cultivar. However, no such striking differences were observed in root tissues of ZJY1 (a sensitive cultivar), showing no significant changes or weak induction in these three transcripts. These results indicated that CH4 conferred plant tolerance against osmotic stress by improving sugar metabolism.


Methane protects against polyethylene glycol-induced osmotic stress in maize by improving sugar and ascorbic acid metabolism
Regulation of transcripts related to sugar metabolism and signaling pathways by CH4.5-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 sucrose synthase 1 (SH1; X02400), sucrose synthase 2 (SUS1; L22296), soluble acid invertase 1 (IVR1; AF171874), soluble acid invertase 2 (IVR2; U31451), hexokinase 1/3/9 (HXK1/3/9; NM_001158821/XM_008676343/XM_008658658), UDP-glucose dehydrogenase (UDPGDH; EU961705) in root tissues were analyzed. 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).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC5384014&req=5

f5: Regulation of transcripts related to sugar metabolism and signaling pathways by CH4.5-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 sucrose synthase 1 (SH1; X02400), sucrose synthase 2 (SUS1; L22296), soluble acid invertase 1 (IVR1; AF171874), soluble acid invertase 2 (IVR2; U31451), hexokinase 1/3/9 (HXK1/3/9; NM_001158821/XM_008676343/XM_008658658), UDP-glucose dehydrogenase (UDPGDH; EU961705) in root tissues were analyzed. 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: To further establish the relationship between CH4 and sugar metabolism under PEG treatment, we analyzed the transcriptional profiles of some key genes in sugar metabolism and signaling pathways (Supplementary Fig. S1). Similar to the previous reports2728, PEG treatment significantly increased the transcript levels of sucrose synthase 1 (SH1) and UDP-glucose dehydrogenase (UDPGDH), while decreased the gene expression of soluble acid invertase 2 (IVR2) and hexokinase 3 (HXK3) in root tissues of two maize cultivars (Fig. 5). Compared with PEG alone, the transcript levels of sucrose synthase 2 (SUS1), soluble acid invertase 1 (IVR1), and hexokinase 1/9 (HXK1/9), were dramatically enhanced by CH4 pretreatment in ZD958, a tolerant cultivar. However, no such striking differences were observed in root tissues of ZJY1 (a sensitive cultivar), showing no significant changes or weak induction in these three transcripts. These results indicated that CH4 conferred plant tolerance against osmotic stress by improving sugar metabolism.

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.