Hydrogenases in Plants: Comparison
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Please note this is a comparison between Version 2 by Catherine Yang and Version 1 by Grace Russell.

Hydrogenases catalyze the reversible oxidation of H2, and are found in many organisms, including plants. One of the cellular effects of H2 is the selective removal of reactive oxygen species (ROS) and reactive nitrogen species (RNS), specifically hydroxyl radicals and peroxynitrite. Therefore, the function of hydrogenases and the action of H2 needs to be reviewed in the context of the signalling roles of a range of redox active compounds. Enzymes can be controlled by the covalent modification of thiol groups, and although motifs targeted by nitric oxide (NO) can be predicted in hydrogenases sequences it is likely that the metal prosthetic groups are the target of inhibition.

  • HYDROGENASES
  • PLANTS
  • REDOX
  • CHEMISTRY
  • MOLECULAR HYDROGEN

1. Introduction

Treatment with H

2 has been described as being beneficial for a range of human diseases [3,4], whilst in agriculture, application of H

has been described as being beneficial for a range of human diseases [1][2], whilst in agriculture, application of H

2 has been demonstrated to increase both crop health and yield [5], important factors that may prove beneficial for the arable and cattle-feed industries in particular. To illustrate, evidence shows that H

has been demonstrated to increase both crop health and yield [3], important factors that may prove beneficial for the arable and cattle-feed industries in particular. To illustrate, evidence shows that H

2 is able to mediate root development and stress responses in plants, in response to heavy metals [6] and drought [7] in particular. It can also be used for improving post-harvest storage of crops, for example with kiwifruits [8]. Therefore, how organisms such as plants can be exposed to H

is able to mediate root development and stress responses in plants, in response to heavy metals [4] and drought [5] in particular. It can also be used for improving post-harvest storage of crops, for example with kiwifruits [6]. Therefore, how organisms such as plants can be exposed to H

2

, and how they respond to it, is important to understand and may lead to better treatments and better yields in the future.

In light of ongoing research it is becoming clear that H

2

should be seen as part of a suite of small reactive molecules that can influence and control cellular function. It has long been known that reactive oxygen species (ROS), such as superoxide anion (O

2·−

), hydrogen peroxide (H

2

O

2

) and hydroxyl radicals (

·OH), are produced in cells and can impact activities in the intracellular and extracellular environs, during stress responses as an example [9]. Of further significance are the reactive nitrogen species (RNS), such as nitric oxide (

OH), are produced in cells and can impact activities in the intracellular and extracellular environs, during stress responses as an example [7]. Of further significance are the reactive nitrogen species (RNS), such as nitric oxide (

·

NO) and peroxynitrite (ONOO

−) [10]. Hydrogen sulfide (H

) [8]. Hydrogen sulfide (H

2S) too, is an important signalling molecule [11], often produced, along with ROS and RNS, during stress responses [12].

S) too, is an important signalling molecule [9], often produced, along with ROS and RNS, during stress responses [10].

As these molecules can be generated by plant cells concomitantly, both temporally and spatially, it is likely that there would be an interplay between them [13], and also, interactions with H

As these molecules can be generated by plant cells concomitantly, both temporally and spatially, it is likely that there would be an interplay between them [11], and also, interactions with H

2

. This crosstalk could, of course, be bidirectional wherein H

2

may interfere with NO signalling, for example. Alternatively ROS and NO may also modify H

2

metabolism. In either case, signalling events would be affected, and this would influence both short-term and long-term cellular activities.

H

2

is an extremely small (MW 2.016 g/mol) and relatively inert molecule. As a consequence, it is hard to envisage how it can be perceived by a classical receptor protein, or how it could partake in the control of proteins through covalent modifications, as has been found for NO effects, typically through

S-nitrosation [14]. However, H

-nitrosation [12]. However, H

2 has been shown to have effects through the selective removal of reactive oxygen species (ROS), in particular hydroxyl radicals [15], and the scavenging of RNS, in particular peroxynitrite. H

has been shown to have effects through the selective removal of reactive oxygen species (ROS), in particular hydroxyl radicals [13], and the scavenging of RNS, in particular peroxynitrite. H

2 is also known to have effects through action on haem oxygenase enzymes (e.g., HO-1) [16]. It has also been mooted that the physical properties of H

is also known to have effects through action on haem oxygenase enzymes (e.g., HO-1) [14]. It has also been mooted that the physical properties of H

2 may mediate some of the effects seen in higher plants and animals [17]. However, we are currently far from a full understanding of how H

may mediate some of the effects seen in higher plants and animals [15]. However, we are currently far from a full understanding of how H

2

interacts with cellular components and influences cellular activity, and a great deal of research into the molecular mechanisms of the interplay between molecular hydrogen and cellular systems will be required if we are to elucidate such complexities.

Cells may be exposed to H

2

from both endogenous and exogenous sources. Exogenous sources, such as the arrival of H

2

from the environment, are important to consider, especially as this may be the way H

2 is used as a medication or agricultural treatment. However, many organisms are known to contain discrete hydrogenase enzymes responsible for the reversible oxidation of molecular hydrogen. Such enzymes are typically classified on the basis of their metal chelation properties e.g., Fe, FeFe, and NiFe [18], which may either generate or remove molecular hydrogen in cellular systems. In animals, the gut microflora is also an important source of H

is used as a medication or agricultural treatment. However, many organisms are known to contain discrete hydrogenase enzymes responsible for the reversible oxidation of molecular hydrogen. Such enzymes are typically classified on the basis of their metal chelation properties e.g., Fe, FeFe, and NiFe [16], which may either generate or remove molecular hydrogen in cellular systems. In animals, the gut microflora is also an important source of H

2 [19]; however, non-gut bacteria may also contribute to accumulation of H

[17]; however, non-gut bacteria may also contribute to accumulation of H

2 in biological systems [20].

in biological systems [18].

2. Hydrogenases of Higher Plants

It has been known for a long time that hydrogen is metabolized by higher plants and that (FeFe)-hydrogenases exist in eukaryotic species, including plants [45]. These metallo-protein complexes appear to be able to catalyze both forward and backwards reactions, effectively removing or generating H

It has been known for a long time that hydrogen is metabolized by higher plants and that (FeFe)-hydrogenases exist in eukaryotic species, including plants [19]. These metallo-protein complexes appear to be able to catalyze both forward and backwards reactions, effectively removing or generating H

2

. They also seem to be involved in the appropriate biosynthesis of (Fe-S) clusters and the sensitivity to O

2. Knockouts of encoding genes leads to poor plant development, with these enzymes appearing to be involved in the control of the cell cycle and sugar metabolism [46], as well as transcription control and in stress responses [47]. Eukaryotic hydrogenases are often referred to as NAR (nuclear architecture related) or GOLLUM (different oxygen levels influences morphogenesis) proteins. For example, in plants there is GOLLUM1 in

. Knockouts of encoding genes leads to poor plant development, with these enzymes appearing to be involved in the control of the cell cycle and sugar metabolism [20], as well as transcription control and in stress responses [21]. Eukaryotic hydrogenases are often referred to as NAR (nuclear architecture related) or GOLLUM (different oxygen levels influences morphogenesis) proteins. For example, in plants there is GOLLUM1 in

Medicago truncatula [48] and AtNAR1 in

[22] and AtNAR1 in

Arabidopsis [49], although currently such naming appears to be interchangeable.

[23], although currently such naming appears to be interchangeable.

It is tempting, as with the hydrogenases in

C. reinhardtii

, to suggest that redox signalling molecules may have an impact on the action of higher plant hydrogenases. As with the HYDA1 and HYDA2 sequences above, if such enzymes are controlled by the presence of ROS, NO, or H

2S, then thiol side groups may be the targets for modification. This may, for example, be for covalent modification with ROS or NO, but neither polypeptide sequence contains any –SNO motifs ((IL)-X-C-X-X-(DE) [37]) suggesting that control by NO by this means is unlikely. A brief analysis of the Arabidopsis AtNar1 sequence (Accession number: NM_117739) shows 13 cysteine residues. When aligned with the ferredoxin hydrogenase from

S, then thiol side groups may be the targets for modification. This may, for example, be for covalent modification with ROS or NO, but neither polypeptide sequence contains any –SNO motifs ((IL)-X-C-X-X-(DE) [24]) suggesting that control by NO by this means is unlikely. A brief analysis of the Arabidopsis AtNar1 sequence (Accession number: NM_117739) shows 13 cysteine residues. When aligned with the ferredoxin hydrogenase from

Artemisia annua

(sweet wormwood or qinghao: Accession number: PWA71961) there is 69% identity in the sequence. Interestingly, all but one of the cysteine residues is conserved, thereby evolution would suggest that they are retained for a reason.

Aligning these plant sequences with the sequence for the human cytosolic iron-sulfur assembly component 3 isoform 1 (Accession number: NP_071938.1), using

Clustal Omega [50], there are still nine conserved cysteine residues. Surprisingly, Cys 380 is conserved in Arabidopsis AtNAR1 but not in the Artemisia sequence, yet it is contained in the human sequence (Figure 1). The human sequence also contains three cysteine residues not found in the plant sequences, but still they do not fall in a –SNO conserved region. However, putting the sequence through the iSNO-PseAAC prediction tool [35] gives the data shown in Table 1. Four conserved cysteine residues in the three sequences investigated were predicted to be modified by NO. Using the Arabidopsis sequence numbers, these were Cys24, Cys177, Cys233, and Cys362. Interestingly, two of these are conversed also in the human sequence: Cys177 and Cys233 (Table 1 and Figure 1). Such conservation across a wide range of species suggests that they have a possible significant role and it may be that they are there for control through NO signalling. This is, of course, with the caveat that it has been suggested that the three-dimensional orientation of the amino acids is more important than the sequence in the region [36]. Furthermore, as discussed above, it is likely that the metal prosthetic groups are the target for NO, rather than the amino acid thiol side chains [38].

[25], there are still nine conserved cysteine residues. Surprisingly, Cys 380 is conserved in Arabidopsis AtNAR1 but not in the Artemisia sequence, yet it is contained in the human sequence (Figure 1). The human sequence also contains three cysteine residues not found in the plant sequences, but still they do not fall in a –SNO conserved region. However, putting the sequence through the iSNO-PseAAC prediction tool [26] gives the data shown in Table 1. Four conserved cysteine residues in the three sequences investigated were predicted to be modified by NO. Using the Arabidopsis sequence numbers, these were Cys24, Cys177, Cys233, and Cys362. Interestingly, two of these are conversed also in the human sequence: Cys177 and Cys233 (Table 1 and Figure 1). Such conservation across a wide range of species suggests that they have a possible significant role and it may be that they are there for control through NO signalling. This is, of course, with the caveat that it has been suggested that the three-dimensional orientation of the amino acids is more important than the sequence in the region [27]. Furthermore, as discussed above, it is likely that the metal prosthetic groups are the target for NO, rather than the amino acid thiol side chains [28].

Figure 1.

Amino acid sequence alignments of hydrogenases.

Clustal Omega

[50] was used to align three hydrogenase sequences: human cytosolic iron-sulfur assembly component 3 isoform 1(Accession number: NP_071938.1); AtNar1 (Accession number: NP_567496.4); ferredoxin hydrogenase from

Artemisia annua (Accession number: PWA71961). C: Common to all sequences; C: common to just plant species; C: Common to human and Arabidopsis; C: unique to human; and Y: tyrosine residues. Sequences predicted to become –SNO using the iSNO-PseAAC prediction tool [35] are underlined and in bold. –SNO: nitrosated thiol.

(Accession number: PWA71961). C: Common to all sequences; C: common to just plant species; C: Common to human and Arabidopsis; C: unique to human; and Y: tyrosine residues. Sequences predicted to become –SNO using the iSNO-PseAAC prediction tool [26] are underlined and in bold. –SNO: nitrosated thiol.

Table 1. S

-nitrosation sites in four hydrogenase proteins predicted using the iSNO-PseAAC prediction tool (http://app.aporc.org/iSNO-PseAAC/) [35]. Arabidopsis: ferredoxin hydrogenase (

Arabidopsis thaliana

) NP_567496.4; Medicago: protein NAR1 (

Medicago truncatula)

XP_003606579.2; Artemisia: ferredoxin hydrogenase (

Artemisia annua

) PWA71961.1; Human: cytosolic iron-sulfur assembly component 3 isoform 1 (

Homo sapiens

) NP_071938.1. Alignment table signifies that the regions are aligned in the amino acid sequences (highlighted in Figure 1). Target cysteine residues which may become –SNO are highlighted here in red. –SNO: nitrosated thiol.

Arabidopsis

Medicago

Artemisia

Human

Position of -SNO

Sequence

Position of -SNO

Sequence

Position of -SNO

Sequence

Position of -SNO

Sequence

24

LNDFIAPSQA

CVISLKDSKPI

24

VNDFIVPSQA

C

TVSLKERRLK

24

LNDYIAPSQG

C

VVSMKSGSDR

 

 

64

VKISLKDCLA

CSGCITSAETV

 

 

68

VKISLKDCLA

C

SGCITSAETV

 

 

 

 

 

 

 

 

179

FVRRFRGQAD

C

RQALPLLASA

177

QSPLPVLSSA

CPGWICYAEKQ

176

KSSLPMISSA

C

PGLICYAEKS

181

TSSLPMISSA

C

PGWICYAEKT

190

RQALPLLASA

C

PGWICYAEKT

182

VLSSACPGWI

CYAEKQLGSYV

 

 

186

MISSACPGWI

C

YAEKTLGSYV

195

LLASACPGWI

C

YAEKTHGSFI

233

HEVYHVTVMP

CYDKKLEAARD

232

EEVYHVTVMP

C

YDKKLEASRD

237

GDIYHVTVMP

C

YDKKLEASRD

246

DKIYHVTVMP

C

YDKKLEASRP

 

 

 

 

 

 

270

NQEHQTRDVD

C

VLTTGEVFRL

362

EGKTVLKFAL

CYGFQNLQNIV

366

DGETVLKFAL

C

YGFSNLQKNI

365

EGKTVLKFAL

C

YGFRNLQNVV

 

 

380

NIVRRVKTRK

CDYQYVEIMAC

 

 

 

 

385

NLVQRLKRGR

C

PYHYVEVMAC

394

YVEIMACPAG

CLNGGGQIKPK

 

 

 

 

 

 

 

 

 

 

 

 

453

THWLQGTDSE

C

AGRLLHTQYH

The three-dimensional orientation of amino acids may be important for S-persulfidation of these proteins as well [40], although there appears to be no evidence in the literature of hydrogenases being covalently modified in this way. This being said, it is known that hydrogenases are inhibited by H

The three-dimensional orientation of amino acids may be important for S-persulfidation of these proteins as well [29], although there appears to be no evidence in the literature of hydrogenases being covalently modified in this way. This being said, it is known that hydrogenases are inhibited by H

2S [51], perhaps by attack on the metal center, as suggested for NO [38].

S [30], perhaps by attack on the metal center, as suggested for NO [28].

All three sequences (Human,

Arabidopsis

, and

Artemisia

:

Figure 1) have eight conserved tyrosine residues. It is possible that they may be used for nitro-tyrosine formation, but there is no evidence of the conserved region used by Urmey and Zondlo [41]. In a similar way, looking for the cysteine residues which may be glutathionylated [43], there is no evidence of this sequence being in the hydrogenase amino acid sequences investigated here (Figure 1). From what can be considered a rather naïve point of view, using bioinformatics, it is therefore possible that hydrogenases in higher organisms are inhibited by NO through thiol modification, and possibly by ROS, but as yet there is little evidence that such control is significant.

Figure 1) have eight conserved tyrosine residues. It is possible that they may be used for nitro-tyrosine formation, but there is no evidence of the conserved region used by Urmey and Zondlo [31]. In a similar way, looking for the cysteine residues which may be glutathionylated [32], there is no evidence of this sequence being in the hydrogenase amino acid sequences investigated here (Figure 1). From what can be considered a rather naïve point of view, using bioinformatics, it is therefore possible that hydrogenases in higher organisms are inhibited by NO through thiol modification, and possibly by ROS, but as yet there is little evidence that such control is significant.

3. Conclusions and Perspectives

There is a growing body of evidence that molecular hydrogen is perceived by organisms and has beneficial effects. Lower plants such as

C. reinhardtii

are known to produce substantial quantities of H

2

, so much so that their use as a source of H

2 to be used as a biofuel has been suggested [30,31]. Higher plants also contain hydrogenases, which catalyze the reversible oxidation of H

to be used as a biofuel has been suggested [33][34]. Higher plants also contain hydrogenases, which catalyze the reversible oxidation of H

2

. H

2

is likely to be present in cells spatially and temporally with other reactive molecules used in cell signalling, such as ROS, NO, and H

2

S. Therefore, the interplay between H

2

enzymes and metabolism will need to take this into account in future enquiries. Spatial and temporal measurements of all the reactive molecules involved in signalling need to be undertaken, probably requiring new fluorescent probes. Only by knowing where and when all relevant players in the regulatory orchestra are accumulated, will a full understanding of the manner in which they give a coordinated response be gained.

Hydrogenase enzymes are known to be inhibited by NO [32]. Even though –SNO formation sites can be predicted in hydrogenase sequences using algorithms such as iSNO-PseAAC [32], there is little, if any, experimental evidence that they are used in such a way, rather that the metal centres are likely targets [38]. Similarly, hydrogenases are known to be inhibited by H

Hydrogenase enzymes are known to be inhibited by NO [35]. Even though –SNO formation sites can be predicted in hydrogenase sequences using algorithms such as iSNO-PseAAC [35], there is little, if any, experimental evidence that they are used in such a way, rather that the metal centres are likely targets [28]. Similarly, hydrogenases are known to be inhibited by H

2S [52], but again there is little evidence of such proteins being

S [36], but again there is little evidence of such proteins being

S

-persulfidated. Future experimental work should be focused on clarifying if there are any effects of NO, ROS, and H

2

S on the accumulation of H

2

in plant cells.

The bioavailability of H

2

for a plant will also be influenced by the environment, perhaps by associated organisms. However, it is now well known that climate change-induced abiotic stress events such as droughts, floods, or soil infertility in particular are exerting a negative influence on agricultural yields. With the frequency of such challenging situations increasing, there is an inescapable need to search for yield enhancing strategies to meet the target of food security for feeding the growing human population. Another aspect that favours the utilization of non-toxic substances such as molecular hydrogen, is the current and continued usage of chemical fertilizers for enhancing yields. These practices are not sustainable when considering long-term future plans as the chemicals used in these products are recognized as being environmentally destructive, on land and in aqueous regions, where there is a threat to life caused by noxious chemicals leaching from surrounding farm lands. Figure 2 gives a brief synopsis of how molecular hydrogen can effectively increase the quality, yields, and longevity of produce whilst reducing both production and environmental costs.

Figure 2.

Possible mechanisms by which H

2

acts in as a protective agent within plant systems. Several ways are shown by which H

2

may act, whilst highlighting the benefits for both agricultural and environmental sustainability. ONOO: peroxynitrite; OH: hydroxyl radical; CAT: catalase; HO-1; haem oxygenase-1; and SOD: superoxide dismutase.

Of particular interest to plant science is how the application of H

2 can be carried out in a commercial setting [20], and how this may be made sustainable and safe, considering hydrogen is highly inflammable. Spray treatments with HRW are probably the most convenient, cost-effective, and practical methods, where delivery can theoretically be applied either onto the soil or directly onto the foliage. In light of this, and with future vertical farming in mind, future inquiry should also include the application of H

can be carried out in a commercial setting [18], and how this may be made sustainable and safe, considering hydrogen is highly inflammable. Spray treatments with HRW are probably the most convenient, cost-effective, and practical methods, where delivery can theoretically be applied either onto the soil or directly onto the foliage. In light of this, and with future vertical farming in mind, future inquiry should also include the application of H

2

within hydroponic cultures.

It is extremely unlikely that plant cells perceive the presence of molecular hydrogen in a truly classical manner, by utilizing a cell receptor protein. Effects of H

2 application have been seen on the levels of some reactive signalling molecules, particularly hydroxyl radicals and peroxynitrite, with other ROS and RNS being relatively unaffected [14]. Effects have also been reported on haem-oxygenase activity [76], whilst it has been postulated that the physical properties of H

application have been seen on the levels of some reactive signalling molecules, particularly hydroxyl radicals and peroxynitrite, with other ROS and RNS being relatively unaffected [12]. Effects have also been reported on haem-oxygenase activity [37], whilst it has been postulated that the physical properties of H

2 may be important in mediating HO-1 activity [16]. Certainly, much more work needs to be carried out to ascertain how H

may be important in mediating HO-1 activity [14]. Certainly, much more work needs to be carried out to ascertain how H

2

has effects on the biochemical processes inside cells. Many enzymes and regulatory proteins are redox sensitive, and the manner in which H

2

interacts with the intracellular redox environment will need to be explored. Therefore, future work may also need to focus on exploring how H

2

alters gene expression and the complement of proteins in cells. This may, of course, be different in distinct plant tissues, so work would need to be carried out on roots and leaves, for example, as well as using specialist cells within those tissues, such as guard cells.

It is reasonably well established that H

2

has profound effects on plants, and can promote plant growth and development, and help to alleviate stress responses. Unlike ROS, NO, and H

2S, which are all extremely toxic, (despite being used as signalling molecules) [13,86], molecular hydrogen, either as a gas or dissolved in water (HRW), is thought to be biologically safe [85]. Therefore, manipulation of the availability of molecular hydrogen to plants, and a full appreciation of the effects it elicits, along with an understanding of the underpinning mechanisms of action of H2, should be a priority in future plant science endeavours for such work is likely to enhance plant growth and crop yields in the future.

[1][2][3][4]

S, which are all extremely toxic, (despite being used as signalling molecules)

[5][6][7][8][9][10][11]

, molecular hydrogen, either as a gas or dissolved in water (HRW), is thought to be biologically safe

[12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][33][34][29][30][31][32][35][36][37][38][39][40][41][42][43][44][45][46][47][48][49][50][51][52][53][54][55][56][57][58][59][60][61][62][63][64][65][66][67][68][69][70][71][72][73][74][75][76][77][78][79][80][81][82]

 

. Therefore, manipulation of the availability of molecular hydrogen to plants, and a full appreciation of the effects it elicits, along with an understanding of the underpinning mechanisms of action of H2, should be a priority in future plant science endeavours for such work is likely to enhance plant growth and crop yields in the future.

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