Hydrogen Metabolism in Higher Plants

Renwick, G.; Giumarro, C.; Siegel, S. M.

doi:10.1104/pp.39.3.303

Cited by 91 publications

(44 citation statements)

References 8 publications

(3 reference statements)

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“…Along with these studies, endogenous H 2 release was found in barley (Hordeum vulgare), rice, alfalfa (Medicago sativa), and Arabidopsis (Renwick et al, 1964;Xie et al, 2012;Jin et al, 2013;Zeng et al, 2013). The increasing significance of the physiological role of H 2 was reported in higher plants, in contrast with the limited knowledge about its biosynthesis.…”

Section: Gork Acts As the Downstream Target Of Hrw Signalingmentioning

confidence: 94%

“…It was previously found that a hydrogenase system could generate H 2 in bacteria and green algae (Meyer, 2007;Esquível et al, 2011). Although some earlier studies discovered the evolution of H 2 in several higher plant species (Renwick et al, 1964;Torres et al, 1984), it was also proposed that the eukaryotic hydrogenase-like protein does not metabolize H 2 (Cavazza et al, 2008;Mondy et al, 2014). Since the explosion limit of H 2 gas is about 4% to 72.4% (v/v, in the air), the direct application of H 2 gas in experiments is flammable and dangerous.…”

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confidence: 99%

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Reactive Oxygen Species-Dependent Nitric Oxide Production Contributes to Hydrogen-Promoted Stomatal Closure in Arabidopsis

et al. 2014

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The signaling role of hydrogen gas (H 2 ) has attracted increasing attention from animals to plants. However, the physiological significance and molecular mechanism of H 2 in drought tolerance are still largely unexplored. In this article, we report that abscisic acid (ABA) induced stomatal closure in Arabidopsis (Arabidopsis thaliana) by triggering intracellular signaling events involving H 2 , reactive oxygen species (ROS), nitric oxide (NO), and the guard cell outward-rectifying K + channel (GORK). ABA elicited a rapid and sustained H 2 release and production in Arabidopsis. Exogenous hydrogen-rich water (HRW) effectively led to an increase of intracellular H 2 production, a reduction in the stomatal aperture, and enhanced drought tolerance. Subsequent results revealed that HRW stimulated significant inductions of NO and ROS synthesis associated with stomatal closure in the wild type, which were individually abolished in the nitric reductase mutant nitrate reductase1/2 (nia1/2) or the NADPH oxidasedeficient mutant rbohF (for respiratory burst oxidase homolog). Furthermore, we demonstrate that the HRW-promoted NO generation is dependent on ROS production. The rbohF mutant had impaired NO synthesis and stomatal closure in response to HRW, while these changes were rescued by exogenous application of NO. In addition, both HRW and hydrogen peroxide failed to induce NO production or stomatal closure in the nia1/2 mutant, while HRW-promoted ROS accumulation was not impaired. In the GORK-null mutant, stomatal closure induced by ABA, HRW, NO, or hydrogen peroxide was partially suppressed. Together, these results define a main branch of H 2 -regulated stomatal movement involved in the ABA signaling cascade in which RbohF-dependent ROS and nitric reductase-associated NO production, and subsequent GORK activation, were causally involved.

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Section: Gork Acts As the Downstream Target Of Hrw Signalingmentioning

confidence: 94%

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confidence: 99%

Reactive Oxygen Species-Dependent Nitric Oxide Production Contributes to Hydrogen-Promoted Stomatal Closure in Arabidopsis

et al. 2014

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“…Sulphuric acid was added to digest plant material, which was adopted in the determination of carbon monoxide and hydrogen gas production4546. The GC was calibrated using a secondary standard CH 4 mixture (2.0 ppm CH 4 in N 2 ; Nanjing Special Gas Co., China).…”

Section: Methodsmentioning

confidence: 99%

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

Han

Duan

Wang

et al. 2017

Sci Rep

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Although aerobic methane (CH 4 ) release from plants leads to an intense scientific and public controversy in the recent years, the potential functions of endogenous CH 4 production in plants are still largely unknown. Here, we reported that polyethylene glycol (PEG)-induced osmotic stress significantly increased CH 4 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 CH 4 not only increased endogenous CH 4 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 CH 4 might participate in sugar signaling, which in turn increased AsA production and recycling. Together, these results suggested that CH 4 might function as a gaseous molecule that enhances osmotic stress tolerance in maize by modulating sugar and AsA metabolism.Methane (CH 4 ) is the most abundant reduced organic compound in the atmosphere, and also the second important greenhouse gas after carbon dioxide 1,2 . It was previously considered as a degradation product of organic substance by microbes under anoxic conditions 3 . Keppler et al. 4 further reported a surprising discovery that terrestrial plants can produce CH 4 under aerobic conditions. Although much controversy and debate followed this original work, a number of researchers have attempted to provide alternate explanations of the aerobic CH 4 formation from plants using different scales of measurement 5 . In fact, the non-microbial CH 4 production from plants constitutes a significant fraction of the global CH 4 sources 2,6 . A comprehensive understanding of CH 4 in plants is that the living plants and fungi can not only emit CH 4 to the atmosphere 7 , but also produce CH 4 in plants in vivo 8 . Interestingly, this phenomenon was observed in the researches of nitric oxide 9 , carbon monoxide 10 , as well as hydrogen gas 11 . In some plant species, several chemical compounds, such as lignin, cellulose, leaf surface wax, ascorbic acid (AsA), the methyl groups of sulphur-containing amino acid methionine (Met), were suggested to be the potential precursors of CH 4 2,5,12,13 .

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“…The production of hydrogen gas (H 2 ) in higher plants was discovered in 1964 (Renwick et al, 1964), and hydrogenaselike genes have been reported (Cavazza et al, 2008;Zeng et al, 2013). In animals, the antioxidant property of H 2 was first described in 2007 owing to its ability to react directly with ROS (Ohsawa et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Thus, enhanced antioxidant enzyme activities have been shown to be closely associated with plant tolerance of excess B (e.g. Ardıc et al, 2009;Aftab et al, 2010).The production of hydrogen gas (H 2 ) in higher plants was discovered in 1964 (Renwick et al, 1964), and hydrogenaselike genes have been reported (Cavazza et al, 2008;Zeng et al, 2013). In animals, the antioxidant property of H 2 was first described in 2007 owing to its ability to react directly with ROS (Ohsawa et al, 2007).…”

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confidence: 99%

Linking hydrogen-mediated boron toxicity tolerance with improvement of root elongation, water status and reactive oxygen species balance: a case study for rice

Wang

Duan

et al. 2016

Ann Bot

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Background and aims Boron is essential for plant growth but hazardous when present in excess. As the antioxidant properties of hydrogen gas (H 2 ) were recently described in plants, oxidative stress induced by excess boron was investigated along with other biological responses during rice (Oryza sativa) seed germination to study the beneficial role of H 2 .Methods Rice seeds were pretreated with exogenous H 2 . Using physiological, pharmacological and molecular approaches, the production of endogenous H 2 , growth status, reactive oxygen species (ROS) balance and relative gene expression in rice were measured under boron stress to investigate mechanisms of H 2 -mediated boron toxicity tolerance.Key Results In our test, boron-inhibited seed germination and seedling growth, and endogenous H 2 production, were obviously blocked by exogenously applying H 2 . The re-establishment of ROS balance was confirmed by reduced lipid peroxidation and ROS accumulation. Meanwhile, activities of catalase (CAT) and peroxidase (POX) were increased. Suppression of pectin methylesterase (PME) activity and downregulation of PME transcripts by H 2 were consistent with the alleviation of root growth inhibition caused by boron. Water status was improved as well. This result was confirmed by the upregulation of genes encoding specific aquaporins (AQPs), the maintenance of low osmotic potential and high content of soluble sugar. Increased transcription of representative AQP genes (PIP2;7 in particular) and BOR2 along with decreased BOR1 mRNA may contribute to lowering boron accumulation.Conclusions Hydrogen provides boron toxicity tolerance mainly by improving root elongation, water status and ROS balance.Key words: Oryza sativa, boron toxicity, seed germination, root elongation, hydrogen gas, ROS balance, water status, aquaporins. INTRODUCTIONAlthough boron (B) is an essential micronutrient for plant growth, an excessive concentration of B due to arid and saline soils, as well as low rainfall and poor irrigation, usually produces toxicity in plants, including inhibition of seed germination and seedling growth and reduction of crop yield (e.g. Reid et al., 2004;Roessner et al., 2006;Miwa et al., 2007). The inhibition of root elongation has been found to be one of the most distinct symptoms among all the responses to B toxicity in plants (e.g. Chio et al., 2007;Tanaka and Fujiwara, 2008), and it has been reported that pectin methylesterase (PME) and osmotic potential are involved in this process (Chio et al., 2007;Tanaka and Fujiwara, 2008). Due to the excess B normally occurring in arid and semiarid areas, water stress is another serious problem (e.g. Ben-Gal and Shani, 2003;Reid et al., 2009;Pandey and Archana, 2013). Several genes encoding B transporters have been identified to play roles in B absorption or providing tolerance to B toxicity, including PIP2;4, PIP2;7 (Kumar et al., 2014), TIP5;1 (Pang et al., 2010) and BOR1 (Nakagawa et al., 2007), as well as Bot1 in barley (Sutton et al., 2007) and BOR4 in Arabidopsis . Excess of B coul...

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Hydrogen Metabolism in Higher Plants

Cited by 91 publications

References 8 publications

Reactive Oxygen Species-Dependent Nitric Oxide Production Contributes to Hydrogen-Promoted Stomatal Closure in Arabidopsis

Reactive Oxygen Species-Dependent Nitric Oxide Production Contributes to Hydrogen-Promoted Stomatal Closure in Arabidopsis

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

Linking hydrogen-mediated boron toxicity tolerance with improvement of root elongation, water status and reactive oxygen species balance: a case study for rice

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