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Downstream Signalling from Molecular Hydrogen: History
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Subjects: Plant Sciences
Contributor: John Hancock , Grace Russell

Molecular hydrogen (H2) is now considered part of the suite of small molecules that can control cellular activity. As such, H2 has been suggested to be used in the therapy of diseases in humans and in plant science to enhance the growth and productivity of plants.

  • antioxidants
  • heme oxygenase
  • hydrogen gas
  • hydrogenase

1. Introduction

Molecular hydrogen (H2) is now recognized to have biochemical effects in both animals [1][2] and plants [3][4]. Although it is a relatively inert gas, H2 appears to have profound effects on cell activity, which can be harnessed to help plant growth, survival, and productivity [5][6][7][8].

Plants, particularly as they are sessile, have to endure and survive a wide range of stress challenges, both biotic and abiotic. These stresses include attack by pathogens [9] and insects [10], as well as heavy metals [11], extreme temperature [12], salt [13], and ultraviolet B light [14]. It has become apparent over many years of study that there are common molecular responses to such stresses, and these mechanisms often involve reactive oxygen species (ROS) [15] and reactive nitrogen species (RNS) [16]. These compounds include ROS such as superoxide anions (O2·−) and hydrogen peroxide (H2O2), the latter of which is a major focus of ROS signalling [17]. Importantly, ROS also include the hydroxyl radical (·OH). The most prominent RNS is nitric oxide (NO), which is known to be involved in plant cell signalling processes [18]. However, other RNS include peroxynitrite and nitrosoglutathione, both of which can act as signalling molecules [19][20]. It is also apparent that crosstalk occurs between ROS and RNS [21] as well as with other reactive signalling molecules such as hydrogen sulphide (H2S) [22][23].

H2 fits into this suite of reactive signalling molecules and was shown to increase the fitness of plants [24]. Suitable examples of recent papers on H2 effects on plants include mitigation of salinity effects in barley [25] and Arabidopsis [26], and increased tolerance to cadmium in alfalfa [27]. However, exactly how H2 interacts and has an effect is unclear. The metabolism of H2 in plants is not a novel idea [28] and some plants are known to be significant generators of H2, such as Chlamydomonas [29][30], whilst higher plants have been shown to produce H2 too. Plant H2 generation has been known for a long time [28][31], with more recent examples being reported using rice seedlings [32] and tomato plants [33]. The role of hydrogenase enzymes and the generation of H2 by plants was recently reviewed [7].

Molecular hydrogen, being a gas, is hard to use either in laboratory or environmental settings. It is extremely flammable [34], relatively insoluble [35][36], and will readily move to the gas phase. Despite this, treatment with H2 is often facilitated by the production of hydrogen-rich water (HRW), which can then be applied to the soil or directly onto the foliage. If using hydroponics, the HRW can be added directly to the feed solution.

2. Downstream Effects

For any molecule to be used in cell signalling, it needs to be perceived by cells and to initiate a response. For many molecules, this involves a receptor protein, which may be on the cell surface [37] or in an intracellular compartment, such as the cytoplasm [38] or nucleus [39]. Some signalling molecules are perceived by proteins not classed as receptors, such as the effect of NO on soluble guanylyl cyclase (sGC). Here, NO reacts with the iron in the heme group of the enzyme, thereby activating it [40], although the involvement of such mechanisms has been questioned in plants [41]. Alternatively, the reactive nature of ROS and RNS allows them to oxidize [42] and nitrosate [43] thiol groups on proteins, propagating the signalling needed. It is hard to envisage how H2, being so small and relatively inert, can be perceived by cells. Some of the mechanisms reported and mooted are discussed below.

2.1. Effects on Reactive Oxygen Species and Antioxidant Capacity

Stress responses in plants often involve ROS metabolism. There is often an increase in ROS accumulation, which, in some cases, can initiate programmed cell death (PCD) in plants [44]. ROS accumulate in the presence of heavy metals [45], such as cadmium [46], mercury, and copper [47]. ROS also accumulate in the presence of salt, extreme temperature, and pathogens [48]. Increases in the intracellular ROS under such stress conditions are often accompanied by an increase in antioxidant levels in cells, for example, in the presence of salt [49], heavy metals [50], and extreme temperature [51]. Therefore, the modulation of ROS metabolism is crucial for stress responses: increases in ROS lead to changes in cellular function, whilst antioxidants modulate and dampen that response.

H2 has been shown to be able to help plant cells mitigate stress challenge. H2 can help reduce salt stress [52][53], and reduce stress due to aluminium [54][55], cadmium [56], and mercury [57]. H2 also can help mitigate against drought stress [58][59] and paraquat induced oxidative stress [60].

As can be seen from the discussion above, both stress responses and the effects of H2 can be linked to ROS metabolism and antioxidant levels in cells. Therefore, it is particularly pertinent that H2 has been posited to be an antioxidant [61]. Although this study discusses the effects in H2 in a clinical setting, the redox chemistry would be the same in plants cells. In an animal setting, a study showed that H2 is an antioxidant against the hydroxyl radical (·OH) but has no effects against other ROS [62]. This is most significant, as it is usually hydrogen peroxide (H2O2) that is deemed to be the primary inter- and intracellular signal [17][63]. Of importance, the specificity of H2 to scavenge ·OH has been disputed, as an in vitro study showed that H2 can scavenge H2O2. However, H2 could not scavenge superoxide anions [53]. In an experiment looking at the radiolysis of water, a negligible effect on the formation or consumption of H2O2 was seen when molecular hydrogen was added [64].

The application of H2 has mitigating influences during stress, and therefore if the effects of H2 are mediated by the removal of ·OH, then it might be expected that ·OH radicals would need to be produced during these stress responses, assuming H2 is working in these cases as a ·OH scavenger. It is in fact the case that ·OH can be found in these circumstances. For example, hydroxyl radicals increase during metal ion challenge [65], a cellular challenge in which H2 has been shown to have a beneficial effect [54][55][56][57]. In a similar manner ·OH is produced during paraquat treatment of plants [66], another situation mitigated by H2 [60]. During chilling stress and drought stress, increases in free iron and H2O2 have been recorded, and this implicates hydroxyl radical generation in downstream cellular responses [67]. Once again, H2 has beneficial effects under drought conditions [58][59], as well as chilling stress [68]. ·OH and H2 also have similar actions in heat stress [69][70]. Therefore, it can be seen that there are many stress conditions which elicit accumulation of ·OH and are also relieved by the presence of H2, suggesting that the ·OH scavenging activity of H2 is potentially responsible for the changes in cellular activity seen. This of course does not consider any spatial-temporal differences in ·OH accumulation during different stresses, or plant species variations, but the correlation of ·OH action and H2 effects may be pointing to a possible mechanism.

Certainly, to support the notion that ·OH removal by H2 could be biologically significant, a look at other ·OH scavengers may be useful. Such scavenging has been suggested to be useful for animal health [71], whilst in plants, mannitol has been suggested to be protective through this mechanism [67]. Sugars such as sucralose has been studied for its ·OH scavenging effects in Arabidopsis [72], whilst β-carboline alkaloids [73] and more novel compounds have been used in animal systems [74]. Such studies show that there is merit in modulating ·OH in cells, and therefore support the notion that such action by H2 may be significant.

On the other hand, and importantly, it has been suggested that the reaction of H2 with ·OH is too slow to be of physiological relevance [75], although the authors were discussing clinical settings. In this paper the rate constant for the reaction of H2 with ·OH producing H2O and H· is only 4.2 × 107 M−1 s−1 (from [76][77]). The rate constant for other radical reactions was quoted as 109 M−1 s−1. It was suggested [75] that the ·OH would react with other biomolecules before reacting with the H2, rendering the presence of H2 as being irrelevant. Others have doubted whether H2 has its effects through scavenging ·OH, although this is from a human health perspective [78]. Assuming this is correct, the correlation of ·OH production and H2 effects during stress responses would also be irrelevant, begging the question, if ·OH scavenging is not the mechanism, what is?

It is possible that H2 has indirect effects on antioxidant levels. There are several reports of antioxidant levels in plant cells altering on H2 treatment. For example, this was reported in a study using black barley (Hordeum distichum L.) [79]. Antioxidant enzymes such as catalase and SOD were increased in maize [80] with similar effects in Chinese cabbage [81]. HRW was also found to maintain the intracellular redox status of plant cells through alterations the levels of reduced and oxidized glutathione (GSH and GSSG) [56]. However, the direct targets of H2 have not been identified in such studies. Therefore, it may be that H2 is having effects on the cells’ antioxidant capacity, which can be measured, but it may not be a direct effect on the ROS themselves.

2.2. Impact on Reactive Nitrogen Species Metabolism

RNS, such as the nitric oxide radical (NO), have been known to have important effects in plant cells for over forty years [82], although there is still some controversy of their endogenous production and action [41]. NO, like ROS are well known to be involved in plant stress responses [83], many of which are ameliorated by H2 treatment, as discussed above. Therefore, the relationship between H2 presence and altered RNS metabolism is worth exploring.

H2 has been shown to have effects in nitrogen fixation [84], although this is only one facet of this complex process. Nitrogen fixation relies on many factors including nutrient availability, the soil-plant interactions, and community facilitation as exemplified by the work carried out with the alpine shrub Salix herbacea [85][86][87]. H2 has also been shown to alter NO synthesis during auxin-mediated root growth [33]. Li et al. [88] reported that NO was involved in H2-induced root growth, whilst Zhu et al. [89] also link H2 and NO, reporting that H2 promoted NO accumulation through increases in the activities of possible synthesizing enzymes: NO synthase-like enzymes and nitrate reductase. Additionally, HRW increased NO accumulation in a study on stomatal closure [90]. On the other hand, HRW decreased NO accumulation in alfalfa [55].

It is likely that during a stress response NO and ROS are produced temporally and spatially together, and they can interact to produce downstream products. Superoxide anions and NO together can lead to the generation of the ·OH radical [91], and as discussed above this have been mooted as a potential mechanism of H2 action. However, superoxide anions and NO can react to produce peroxynitrite (ONOO−) [91], which can act as a signalling molecule in its own right [92][93], possibility through alterations of amino acids [94], with tyrosine nitration being a major covalent change seen [92] which could have important downstream effects [95].

2.3. Stress, Heme Oxygenase and H2

An enzyme mechanism that has been found to be important for H2 effects in cells involves the heme oxygenase enzyme (HO-1). For example, this was shown to be involved in root development in cucumber on treatment with HRW [96]. Hydrogen-mediated tolerance to paraquat was also shown to involve heme oxygenase [60]. Similar data can be found in studies of animal systems, for example, in mice [97].

HO-1 has been shown to be involved in a range of abiotic stress responses in plants, including salt, heavy metals, UV light, and drought. Responses to stresses such as drought are complex, involving the result of many genes being expressed and the effects of gene polymorphisms, as seen with Phaseolus vulgaris L. [98][99][100][101], with wild types showing tolerance differences [102][103]. Resistance and tolerance to extreme temperatures are also important and involve complicated cellular responses [104][105][106][107]. Such responses are often associated with the accumulation of cellular ROS and RNS [106]. The catalytic action of HO-1 is the breakdown of heme. This is an oxygen-dependent reaction that uses NADPH as a cofactor and generates biliverdin, carbon monoxide (CO), and iron [107][108].

2.4. Paramagnetic Properties and Possible Cellular Effects

The above discussion throws doubt onto many biochemical and reactive aspects of H2 effects in cells. However, the physical properties of H2 may also be important. Hydrogen can exist with two nuclear spin states (ortho- and parahydrogen) [109][110]. It is the interconversion between these states that may be relevant here [111]. One of the interactions discussed was with NO, which could potentially alter NO signalling. There is also the possibility of interactions with transition metals [112]. This could have a potentially significant effect on cell signalling pathways, as many enzymes involved in signal transduction have metal prosthetic groups, including guanylyl cyclase (at least in animals), SOD, and many respiratory and photosynthetic components. Many of the aforementioned enzymes may be involved in ROS and RNS metabolism, which are important in plant responses to many stresses, with such conditions being mitigated by H2, as discussed above. It is conceivable that H2 may interact with the haem during the catalytic cycle of HO-1, accounting for the effects mediated by this enzyme.

This entry is adapted from the peer-reviewed paper 10.3390/plants10020367

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