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Int. J. Mol. Sci. 2012, 13, 15193-15208; doi:10.3390/ijms131115193
International Journal of
Molecular Sciences
ISSN 1422-0067
www.mdpi.com/journal/ijms
Review
Nitric Oxide-Dependent Posttranslational Modification in Plants:
An Update
Jeremy Astier and Christian Lindermayr
Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, Ingolstädter Landstr. 1,
85764 Neuherberg, Germany; E-Mails: jeremy.astier@helmholtz-muenchen.de (J.A.);
lindermayr@helmholtz-muenchen.de (C.L.); Tel.: +49-89-3187-2129 (J.A.);
+49-89-3187-2285 (C.L.); Fax: +49-89-3187-3383 (J.A.); +49-89-3187-3383 (C.L.)
Received: 6 September 2012; in revised form: 16 October 2012 / Accepted: 6 November 2012 /
Published: 16 November 2012
Abstract: Nitric oxide (NO) has been demonstrated as an essential regulator of several
physiological processes in plants. The understanding of the molecular mechanism
underlying its critical role constitutes a major field of research. NO can exert its biological
function through different ways, such as the modulation of gene expression, the
mobilization of second messengers, or interplays with protein kinases. Besides this
signaling events, NO can be responsible of the posttranslational modifications (PTM) of
target proteins. Several modifications have been identified so far, whereas metal
nitrosylation, the tyrosine nitration and the S-nitrosylation can be considered as the main
ones. Recent data demonstrate that these PTM are involved in the control of a wide range
of physiological processes in plants, such as the plant immune system. However, a great
deal of effort is still necessary to pinpoint the role of each PTM in plant physiology. Taken
together, these new advances in proteomic research provide a better comprehension of the
role of NO in plant signaling.
Keywords: metal nitrosylation; S-nitrosylation; tyrosine nitration; nitric oxide;
posttranslational modification; plants
1. Introduction
Nitric oxide (NO) is a ubiquitous diatomic gas that has been described as an important regulator of
a wide range of physiological processes in animal models [1]. NO production is not restricted to
OPEN ACCESS
Int. J. Mol. Sci. 2012, 13 15194
animal cells, and several studies have shown that it takes place in other kingdoms, such as plant
organisms [2]. Several lines of evidence indicate that NO can be synthesized in plants from nitrite,
polyamines and L-arginine, through nonenzymatic or enzymatic mechanisms [3,4]. However, with the
exception of nitrate reductase, the corresponding enzymes are yet to be identified, and understanding
NO generation in plants remains an important challenge [4,5]. Nevertheless, the functions of NO in
plants have been widely studied over the past decades and a significant amount of evidence
demonstrated the involvement of NO in the regulation of several biological processes, including
hormonal signaling, root growth, stomatal closing, iron homeostasis, germination, or pollen tube
growth. Moreover, NO participates in the establishment of adaptive responses against biotic and
abiotic stresses in plants [2,6–8].
Although the described NO functions in plants have been increasing over the last years, the precise
molecular mechanisms underlying its physiological roles are still poorly understood. Some works
about NO way of action in plants demonstrated that artificially generated as well as endogenously
produced NO can modulate several gene expressions, involved in stress responses, hormonal signaling
or primary metabolism [4,9–11]. In addition, NO has been demonstrated to impact cGMP, Ca2+,
protein kinase, ROS or phytohormones signaling in plants [2,12–14]. Moreover NO can directly
modify target proteins by posttranslational modification (PTM), three of them being the major
NO-dependent PTM. The first one concerns the interaction of NO moiety with metalloproteins in a
so-called metal nitrosylation. The second refers to the modification of tyrosine residues of proteins by
NO, resulting to the formation of 3-nitrotyrosine. The last one concerns the formation of a nitrosothiol
group on cysteine residues of target proteins, in a reaction called S-nitrosylation. Under distinct
conditions, other NO-dependent modifications, such as S-glutathionylation or formation of disulfide
bridges, are also observed [15–17]. However, these modifications will not be discussed in this review.
Here, we will highlight metal nitrosylation, tyrosine nitration, and S-nitrosylation, discuss their
importance and mechanisms of formation, and finally present recent examples of plant proteins
modified by NO.
2. Metal Nitrosylation in Plants
Because of its chemical properties, NO can interact with transition metals of metalloproteins
to form metal-nitrosyl complexes. More precisely, NO· binds iron, zinc or copper centers of
metalloproteins through coordination chemistry [18]. The bound NO group is then susceptible to
further nucleophilic or less frequently electrophilic attacks, depending on the protein bounded [18,19].
This reactivity explains the possible involvement of metal-nitrosyl complexes in the formation of
S-nitrosothiols groups [20]. The reversible formation of the metal-nitrosyl complex will induce
conformational changes that impact the reactivity or the activity of the concerned target
proteins [18,19]. This PTM has been highlighted through the use of different analytical techniques
such as infrared spectroscopy, electron paramagnetic resonance, or crystallography assays [21–23].
In animals, a well-described model for this kind of PTM is the activation of soluble guanylate
cyclase (sGC) after N-methyl-D-aspartate (NMDA) receptor activation in neurons. NO binds to the
six-coordinate complex heme of sGC, which rapidly is converted to a five-coordinate ferrous nitrosyl
complex. This reaction will cause the rupture of Fe-His bound in the heme, leading to conformational
Int. J. Mol. Sci. 2012, 13 15195
changes that activate sGC (for review see [24]). This activation results in the production of cyclic
guanosine 3',5' monophosphate (cGMP), a second messenger involved in different signaling
processes [25]. In plants, cGMP has also been linked to NO-dependent signaling [4] and response to
biotic and abiotic stresses, such as NaCl exposure or pathogen attack [26,27]. Although several sGC
have been characterized in plants, only one recent work identified a protein from Arabidopsis thaliana
exhibiting a sGC activity modulated by NO [28]. In this work, authors identified and characterized
AtNOGC1. This protein has been identified using in silico analysis searching for plant proteins
containing a heme-binding motif and a catalytic center of plant GC. Using recombinant protein and the
in vitro activity test, they have shown that AtNOGC1 displays an increased GC activity when treated
with NO. This work strengthens a direct link between NO and cGMP signaling, but the physiological
role of this protein and its regulation by NO remain to be determined in planta.
The best characterized plant protein undergoing metal nitrosylation is hemoglobin. In plants,
hemoglobins are separated in three groups based on their structural properties, namely class 1, 2 and
truncated hemoglobin class 3 [29–31]. Class-1 nonsymbiotic hemoglobins (nsHb) have a high affinity
for oxygen with a low KD and are therefore unlikely to function as oxygen transporters [29–31]. Over
the past decade, extensive work has shown that, in plants, oxygenated class 1 nsHbs can be oxidized
by NO, resulting in nitrate production [32–34]. This NO scavenging reaction is now accepted as a
general mechanism modulating NO bioavailability, participating in the regulation and detoxification
of NO in plants [2,29–31,35]. Some studies also reported similar processes for class-2 symbiotic
hemoglobins (sHb) that are able to interact with NO and to scavenge it [36–39]. Few data are available
for the third class of Hb and no roles of these proteins in NO signaling have yet been demonstrated
in plants.
Beside this NO scavenging role of Hb, recent data have demonstrated that both class-1 and class-2
nsHb could display a nitrite reductase activity, leading to the formation of nitric oxide in vitro during
hypoxia or anoxia [40,41]. These results reinforced the link between NO signaling and hemoglobins.
Nonetheless, complementary analysis must be performed to confirm such activity in vivo.
Few more studies report the inhibition of some target proteins through metal nitrosylation in plants
such as the ascorbate peroxidase, the cytochrome c oxidase, the lipoxygenase or the catalase [42–45].
Recently, Gupta and colleagues [46] have shown that NO produced during hypoxia inhibits the
aconitase, resulting in an increased level of citrate in A. thaliana. Therefore, the precise mechanisms of
inactivation of this protein remain to be determined.
3. Tyrosine Nitration in Plants
Tyrosine (Tyr) nitration is the reaction of a nitrating agent with a tyrosine residue of a target protein
that lead to the addition of a nitro group (NO2) in the ortho position of the phenolic hydroxyl group,
resulting in the formation of 3-nitrotyrosine [47]. The NO2 group originates mainly from peroxynitrite
(ONOO−), a powerful oxidative agent resulting from the reaction between NO and the superoxide
anion. Under physiological condition, ONOO− can react with CO2 and be further decomposed in CO3•−
and NO2, a powerful nitrating agent. Moreover, Tyr nitration can result from the reaction of nitric
oxide with tyrosyl radicals [48].
Int. J. Mol. Sci. 2012, 13 15196
Tyr nitration is restricted to specific target tyrosine residues [49,50] and can promote
conformational changes that lead to the activation or the inhibition of the target proteins. Although this
modification was first thought to be irreversible, a growing body of evidence tends to demonstrate that
denitration processes may occur, both in enzymatic or nonenzymatic ways [51,52]. Moreover, even if
this PTM is associated with protein degradation in animals [51], it has not been proved in plants.
Furthermore, some proteomics analyses done in A. thaliana challenged by a pathogen have
demonstrated that the increase in nitrated proteins is a transient phenomenon, suggesting that it is a
reversible mechanism [53,54].
The study of this PTM has been mainly based on two methods. The first one is the use of specific
antibodies raised against 3-nitrotyrosine residues, allowing the immuno-purification of the modified
proteins or their detection in western blotting experiments [55]. The other is the use of chemical
analysis techniques such as chromatography purification before mass spectrometry analysis [56–58].
Moreover, some techniques resulting in the specific fluorescent labeling of the 3-nitrotyrosine residues
have been recently developed [59].
The biological significance of this PTM is not well established in plants. It is likely that Tyr
nitration interferes with signaling based on phosphorylation/dephosphorylation, especially if both
modifications involve the same Tyr residues. However, no published data is yet available for such
mechanism in plants [52].
Only few works have been done so far to determine Tyr nitrated proteins in plants. Early
approaches reporting evidence for the occurrence of Tyr nitration in plants concerned tobacco cells
invalidated for the expression of nitrate reductase [60] or treated by an elicitor [61], leaves of
salt-stressed olive plants [62] and A. thaliana challenged by an avirulent strain of Pseudomonas
syringae [54].
More recent studies aimed in identifying the proteins undergoing this PTM. The first work was
carried out on A. thaliana infected by P. syringae [53]. In this work, authors identified eleven proteins
that are undergoing Tyr nitration during the development of the hypersensitive response (HR), a form
of programmed cell death (PCD) triggered by plant cells at the sites of pathogen infection. The
proteins identified are related to primary metabolism, such as nitrogen assimilation, ATP synthesis,
Calvin cycle and glycolysis and photosynthesis. Interestingly, another group pointed out the
importance of Tyr nitration as a significant PTM for the proteins involved in the photosynthetic
apparatus [63,64].
Using anti-nitrotyrosine antibodies immuno-purification coupled with mass spectrometry analysis,
Chaki and colleagues [65] identified 21 nitrated proteins in total extracts from hypocotyls of untreated
sunflowers plants. These proteins are involved in several processes, such as the primary metabolism
(photo- and ATP synthesis, carbohydrate and nitrogen metabolism), the proteasome pathway and cell
signaling and antioxidant machinery. A further work done on sunflower hypocotyl submitted to high
temperatures allowed the identification of these 21 proteins plus a new one, a carbonic anhydrase [65].
Moreover the exposition of the sunflowers plants to a high temperature induced a stronger Tyr
nitration of some of the previously identified nitrated proteins, whereas none of them displayed a
reduced level of nitration.
A recent extensive identification of nitrated proteins in plants has been carried out on crude protein
extracts from A. thaliana seedlings using immuno-purification followed by mass spectrometry
Int. J. Mol. Sci. 2012, 13 15197
analysis. In this study, Lozano-Juste [66] identified 127 proteins that are putatively Tyr nitrated in
A. thaliana. Among them, 35% have homologs that were previously reported to be nitrated in other
organisms, supporting the relevance of these results. Remarkably, here again more than 60% of the
identified proteins are involved in the primary metabolism.
More recently, Tanou and colleagues [58] assayed the Tyr nitration content of citrus plants, both in
leaves and roots, after salt stress or chemical treatment with NO or H2O2. Out of these analyses, they
were able to identify 88 and 86 putative candidates in leaves and roots, respectively. Remarkably, 23%
of the candidate proteins in leaves are involved in photosynthesis.
If all these recent studies provided putative candidates for Tyr nitration, only few studies
characterized a single protein with the determination of the nitrated residue(s). These more detailed
characterizations are essential to confirm the potential candidates obtained by the broad proteomic
analyses presented above, and to confirm the biological impact of this PTM.
In their study of high temperature treated sunflowers, Chaki and colleagues [67] demonstrated that
the ferredoxin-NADP oxidoreductase (FNR), an enzyme mediating the final step of photosynthetic
electron flow in chloroplasts, was inhibited after SIN-1 (a peroxynitrite generator) treatment in vitro
and after high-temperature treatment in vivo. Nevertheless, the precise Tyr residue involved in this
mechanism remains to be determined.
Àlvarez and collegues [68] recently reported the inhibition of O-acetylserine(thiol)lyase A1
(OASA1) by Tyr nitration in A. thaliana. They have demonstrated that this protein undergoes Tyr
nitration selectively on its Tyr302 residue in vivo after a treatment with SIN-1. The authors explained
that inactivation of this enzyme could avoid an extra production of cysteine and/or glutathione,
preventing locally the scavenging of reactive oxygen and nitrogen species, further needed in
downstream signaling events for an efficient stress response.
Using the symbiotic model involving root nodule formation between Medicago truncatula and
Sinorhizobium meliloti, Melo and collegues [69] have shown that one of the guanylate cyclase
(MtGS1a) is modified by Tyr nitration. The nitration of the Tyr167 residue of this protein results in a
loss of its activity and occurs in vivo in response to an impaired nitrogen fixation, modulating the
MtGS1a activity in accordance with the cell requirement in ammonia assimilation.
4. S-Nitrosylation in Plants
S-nitrosylation, also known as S-nitrosation, constitutes the most studied and described
NO-dependent PTM in plants. It refers to the reversible covalent binding of an NO moiety to the thiol
group of a cysteinyl residue (Cys) of a target protein, leading to the formation of an S-nitrosothiol
(SNO; [70]). Depending on the target protein concerned, this PTM will lead to a modification of its
enzymatic activity or its protein function.
NO can exist in three different reactive states—nitrosonium cation (NO+), nitric oxide radical
(NO•), and nitroxyl anion (NO−)—which show different reactivities with thiol groups. While NO· do
not directly interact with thiols, NO+ confers strong electrophilicity and reactivity towards most
biological R-SH species. However, besides the direct S-nitrosylation activity of NO, this molecule
mainly functions as a precursor for several higher nitrogen oxides, which effectively mediate
S-nitrosylation of proteins. Additionally, S-nitrosylation can also be achieved through the exchange of
Int. J. Mol. Sci. 2012, 13 15198
the NO moiety from an S-nitrosylated protein in a so-called transnitrosylation reaction [71,72]. Besides
the possibility of the existence of other proteins with suspected transnitrosylases activity in
animals [20], GSNO appears to be one of the major actors of the transnitrosylase activity in plants,
modulating the total SNO content [72–75].
Despite the fact that Cys is present in the majority of plant proteins, S-nitrosylation is restricted to
specific Cys residues. This specificity seems to be driven by the presence of surrounding acidic and
basic amino acids in the vicinity of the considered Cys, and the presence of this residue in an
hydrophobic pocket that can favor the concentration of nitrosylating agents [20]. Moreover, allosteric
and conformational mechanisms that increase the nucleophilicity of the Cys residue favor the
S-nitrosylation, as well as a colocalization of the production of nitrosylating agents with their target
proteins [76]. However, the specificity of S-nitrosylation is still up for discussion. A recent analysis
of 55 known S-nitrosylated proteins containing 70 NO-Cys sites revealed that proximal
acid–base motif, Cys pKa, sulfur atom exposure, and Cys conservation or hydrophobicity in the
vicinity of the modified Cys, do not define the specificity of S-nitrosylation. Instead, this analysis revealed
a revised acid–base motif, which is located more distantly to the Cys and has its charged groups
exposed [77].
As a major PTM, S-nitrosylation is a reversible and dynamic mechanism. Nonenzymatic and
enzymatic ways have been proposed to promote denitrosylation of target proteins and tightly regulate
this Cys modification [17,70,78,79].
The study of the S-nitrosylated proteins has been mainly based on the use of the biotin switch, a
pioneer technique developed by Jaffrey and colleagues [80]. This technique refers to the labeling of
S-nitrosylated proteins, allowing in a three step reaction the replacement of the SNO group by a
biotin tag. This specific labeling allows the further purification and/or detection of S-nitrosylated
proteins using affinity chromatography or antibodies detection techniques, and can be coupled with
mass spectrometry analysis for further identification [70,81]. Based on this specific labeling of
S-nitrosylated proteins, several other proteomic-based approaches have been recently developed (for
review see [20,70]).
Study of S-nitrosylation in plants is a recent topic of interest, but over the last seven years, an
increasing amount of analyses and characterizations provided evidences that it is a major PTM in
plants. The first analyses were based on proteome wide-scale analysis in order to identify potential
candidate proteins undergoing S-nitrosylation in plants. Analyses were done on A. thaliana plants
untreated or after a brief salt stress [81], A. thaliana seedlings exposed to NO gas [82], to P. syringae
pv. tomato [83], in the medicinal plant Kalanchoe pinnata after GSNO treatment of protein extracts [84]
and in Brassica juncea exposed to low temperature [85], in citrus exposed to salinity, H2O2 or GSNO
treatments [58,86] and more recently in rice noe1 (nitric oxide excess1) mutant [87] and in tobacco cell
suspensions exposed to the oomycete elicitor cryptogein [88]. Protein S-nitrosylation was also
investigated in organelles, such as purified mitochondria of A. thaliana [89] and peroxisomes of pea
plants exposed to abiotic stress [90]. All these analysis provide a list of over 200 putatively
S-nitrosylated plant proteins. However, for the most part of them, S-nitrosylation were obtained using
pharmacological NO donors. Moreover, the S-nitrosylation of these candidates needs confirmation
by a candidate-specific approach, to ensure a mechanistic and biological comprehension of the impact
of the S-nitrosylation in plants.
Int. J. Mol. Sci. 2012, 13 15199
Apart from these general proteomic approaches, around 20 different candidate proteins have
been more tightly characterized [17,33,54,84,88,89,91–99]. The functional significance of the
S-nitrosylation of these candidates has been recently reviewed for the most part of them [70,75,100].
Interestingly, most of the characterized proteins are linked or potentially linked to the plant
immunity. Peroxiredoxin II E (PrxII E) belongs to the peroxiredoxin family that detoxifies a large set
of peroxide substrate and participates in redox signaling in plants. Among them, PrxII E displays an
ONOO− reductase activity [54] that is inhibited through the S-nitrosylation of its Cys121 residue in
A. thaliana challenged with P. syringae bacteria [54,83]. This phenomenon is proposed by the authors
as a mechanism allowing a fine tuning of the NO signaling, avoiding damaging and signaling effect of
ONOO− notably through Tyr nitration.
Another plant signaling pathway leading to defense responses and impacted by NO through
S-nitrosylation involves the nonexpressor of pathogenesis-related gene 1 (NPR1)/Transcription factor
TGA1 system. In plants, NPR1 is a key regulator of salicylic acid (SA)-dependent signaling that
promotes defense responses in plants. Following oxidative changes triggered by SA, NPR1 hexamers
dissociate through the reduction of intermolecular disulfide bounds into monomers, and is translocated
into the nucleus where it interacts with TGA factor including TGA1, allowing the expression of
defense related genes [101]. Therefore, the oligomer/monomer switch and the NPR1/TGA interaction
are critical for triggering plant defense responses. Despite the existence of contradictory data,
S-nitrosylation of these proteins has been shown to be crucial in the regulation of theses processes (for
review see [70,75,100]). Another protein linked to SA signaling pathway has also been characterized:
the salicylic acid binding protein 3 (SABP3). SABP3 possesses carbonic anhydrase (CA) activity and
SA binding properties and is involved in the development of the HR in tobacco [102]. In A. thaliana
challenged by an avirulent P. syringae strain, SABP3 undergoes S-nitrosylation on its Cys280 residue
that leads to the decrease of the CA activity and SA binding properties of the protein [97]. All these data
highlight the connection between SA and NO signaling in the establishment of plant defense responses.
One recent important work allowing a better comprehension of the NO signaling in plants and
involving S-nitrosylation concerns the NADPH oxidase [98]. AtRBOHD is a NAPDH oxidase that is
responsible for reactive oxygen species (ROS) synthesis in responses to several pathogen attacks [103].
After P. syringae infection of A. thaliana plants, Yun and colleagues [98] reported the
S-nitrosylation of AtRBOHD on its Cys890 residue. This PTM avoid the fixation of one cofactor of the
enzyme, resulting in a decreased activity of the protein. Therefore, regulating AtRBOHD by
S-nitrosylation NO might modulate the ROS production after a pathogen attack, which impacts the
development of HR after pathogen infection.
Another recent work identified physiologically S-nitrosylated candidates in a plant defense context.
Indeed, the S-nitrosylation of eleven proteins has been reported subsequently to the recognition of
the oomycete elicitor cryptogein [88], known to trigger a fast and transient NO production in
tobacco leaves and cell suspensions [104–106]. Among these proteins, NtCDC48 has been further
characterized. CDC48 (cell division cycle 48) is a hexameric AAA+ ATPases (ATPases associated
with various cellular activities) involved in multiple cellular pathways, including growth, development,
cell division and differentiation, protein degradation and disease resistance [107–110]. NtCDC48 has
been shown to be S-nitrosylated on its Cys526 residue, which is required for the full activity of the
protein in vitro. NO donor treatments of the recombinant protein resulted in subtle conformational
Int. J. Mol. Sci. 2012, 13 15200
changes and a decrease of the activity of NtCDC48 in vitro. Nevertheless, further investigation must
be carried out to decipher the impact of NtCDC48 S-nitrosylation in plant defense reaction triggered
by cryptogein in planta.
Recently, it was demonstrated that the transport inhibitor response 1 (TIR1) protein of A. thaliana
undergoes S-nitrosylation in vitro [96]. TIR1 is a receptor subunit for auxin, part of an E3-ubiquitin
ligase complex involved in the degradation of transcriptional repressors called Auxin/indole-3acetic
proteins (Aux/IAA). This degradation results in the transcription of genes and participates to the auxin
signaling, involved in plant development. Interestingly, S-nitrosylation of TIR1 promotes its interaction
with Aux/IAA proteins, facilitating their degradation, and therefore taking part in the auxin-dependent
signaling pathway [96]. This example illustrates the involvement of the S-nitrosylation, not only in
plant defense, but also in plant development.
5. Conclusions
NO-triggered PTMs constitute today a major field of investigation in order to better understand the
NO-dependent signalization in plants (Table 1, Figure 1). To date, metal nitrosylation reports in plants
are scarce, and the main purpose of this PTM is assumed to be a scavenging and detoxification
process. More effort must be put on determining the involvement of this PTM in the induction of
further signaling events, such as the production of cGMP by putative NO-dependent sGC. On the
contrary, Tyr nitration has begun to be recognized over the last years as an emerging and important
PTM in plants. Nevertheless, a lot of work remains, such as by using more physiological approaches to
decipher the real biological role of this PTM in general plant physiology, thus allowing for a better
understanding of the impact of NO. S-nitrosylation is the best characterized NO-dependent PTM and a
general picture of the involvement of this PTM is emerging in different processes, especially in plant
defense mechanisms against biotic and abiotic stresses. Here again, several efforts are needed to better
understand the relevance of this PTM in physiological contexts.
Table 1. Examples of nitric oxide target proteins in plants.
Posttranslational modification Target protein References
Metal nitrosylation NO-dependant Gunylate cyclase 1 (AtNOGC1) [24]
Hemoglobins [25–37]
Aconitase [42]
Tyrosine nitration Ferredoxin-NADP oxidoreductase (FNR) [63]
O-acetylserine(thiol)lyase A1 (OASA1) [64]
Guanylate cyclase [65]
S-nitrosylation Peroxiredoxin II E (PrxII E) [50]
Nonexpressor of pathogenesis-related gene 1 (NPR1) [75,90]
Transcription factor TGA1 [90]
Salicylic acid binding protein 3 (SABP3) [93]
Respiratory burst oxidase homologue D (RBOHD) [94]
Cell division cycle 48 (CDC48) [84]
Transport inhibitor response 1 (TIR1) [92]
Int. J. Mol. Sci. 2012, 13 15201
Figure 1. Schematic illustration of NO dependent PTM in plants. To date, all the analyses
of NO-modified proteins in plants followed an NO production induced by (a)biotic stress
or NO donors treatment. The NO radical can react with transition metals (M) of
metalloproteins. This process is called metal nitrosylation and can affect notably
(non)-symbiotic hemoglobins (nsHb and sHb) and an Arabidopsis thaliana NO-dependent
guanylate cyclase (AtNOGC1). The Tyr nitration depends on the formation of NO
derivatives, particularly peroxynitrite formed in the presence of the superoxide anion
(O2•−). Nitration occurs on one of the two carbon equivalent (C3) of the aromatic ring of
tyrosine residues to form a 3-nitrotyrosine. This reaction has been demonstrated in plants
for the ferredoxin-NADP oxidoreductase (FNR), the guanylate cyclase of Medicago
truncatula (MtGS1a) or the of O-acetylserine(thiol)lyase A1 (OASA1). Protein
S-nitrosylation is the electrophilic attack of nitrosonium cation (NO+, resulting from the
oxidation of NO) on a thiolate group of a cysteine residue of a target protein. Among
numerous proteins, this posttranslational modification affect for example peroxyredoxin II
E (PrxII E), salicylic acid binding protein 3 (SABP3), nonexpressor of pathogenesis-related
gene 1 (NPR1), transcription factor TGA1, respiratory burst oxidase homologue D
(RBOHD) or cell division cycle 48 (CDC48). All these modifications will participate to
the change of the plant cell physiology depending on the stimulus applied.
Int. J. Mol. Sci. 2012, 13 15202
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