karpets2015

ISSN 1021 4437, Russian Journal of Plant Physiology, 2015, Vol. 62, No. 1, pp. 65–70. © Pleiades Publishing, Ltd., 2015.
Original Russian Text © Yu.V. Karpets, Yu.E. Kolupaev, A.A. Vayner, 2015, published in Fiziologiya Rastenii, 2015, Vol. 62, No. 1, pp. 72–78.
65
INTRODUCTION
The plant cell physiological responses to stressors
are known to occur with the involvement of signaling
messengers, calcium ions, cAMP, phosphatidic acid,
ROS, nitric oxide (NO), etc. [1, 2]. There are some
indications that hydrogen peroxide and nitric oxide
play an important role on temperature signal trans
duction in plant cells.
Hydrogen peroxide accumulation was observed at
plant treatment with low above zero temperatures [3,
4]. It is reasonable to suppose that ROS accumulation
is associated with the development of defense
responses to hypo and hyperthermia and other abi
otic stressors. Thus, it was shown for maize seedlings
that their 4 h long exposure to 1°C with subsequent
6 h plant keeping at 26°C induced a transitional accu
mulation of hydrogen peroxide in tissues and
improved plant resistance to long term action of low
temperatures [5]. A short term increase in the hydro
gen peroxide content was also demonstrated after
wheat seeling treatment with the high hardening tem
perature [6, 7]. Plant pretreatment with antioxidants
ionol and dimethylthiourea (DMTU) and also with
imidazole, the inhibitor of NADPH oxidase, pre
vented the development of plant heat resistance and
the activation of antioxidant enzymes. In maize leaves,
H2O2 accumulation preceded the increase in the
ABA content and subsequent activation of the antioxi
dant system [8]. In this connection, it may be supposed
that ROS are messengers required for the induction of
reactions determining plant resistance development to
stress temperatures and water deficiency.
There are some data about the changes in the con
tent of endogenous NO in plants under the influence of
abiotic stressors. Enhanced NO synthesis in response to
hyperthermia was observed in cultured tobacco cells [9]
and sugarcane callus culture [10]. Similar effects were
observed in arabidopsis plants under the influence of
high and low temperatures [11, 12]. At the same time, a
possible relation between NO formation and resistance
development is poorly studied. Song et al. [13] showed
that 2 h long exposure of rice plants to hardening tem
perature (38°C) increased the content of NO in their
leaves. Plant treatment with PTIO (2 phenyl
4,4,5,5 tetramethylimidazoline 1 oxyl 3 oxide), the
scavenger of nitric oxide, prevented the development
of their heat resistance. However, it is not clear whether
NO is involved in the induction of plant resistance at the
short term action of high temperatures [7].
RESEARCH PAPERS
Functional Interaction between Nitric Oxide and Hydrogen Peroxide
during Formation of Wheat Seedling Induced Heat Resistance
Yu. V. Karpets, Yu. E. Kolupaev, and A. A. Vayner
Dokuchev Kharkov National Agrarian University, Kommunist 1, Kharkov, 62483 Ukraine;
e mail: plant_biology@mail.ru
Received March 27, 2014
Abstract—The involvement of nitric oxide (NO) and hydrogen peroxide (H2O2) in the formation of heat
resistance induced by 1 min long treatment with a temperature of 42°C in 3 day old seedlings of winter soft
wheat (Triticum aestivum L., cv. Elegiya) was studied. The content of NO in the roots was increased within
2 h after seedling hardening heating. The content of H2O2 was increased within 30 min after heating. This
effect was neutralized when seedlings were treated with the nitric oxide scavenger PTIO (2 phenyl
4,4,5,5 tetramethylimidazoline 1 oxyl 3 oxide) and the inhibitor of NO synthase L NAME (NG
nitro
L arginine methyl ester). Seedling treatment with the antioxidants ionol and dimethylthiourea (DMTU)
reduced the hardening induced nitric oxide accumulation in tissues. When seedlings were treated with the
NO donor sodium nitroprusside (SNP), the amount of endogenous NO and H2O2 in them increased; exog
enous hydrogen peroxide affected similarly. Hardening heating and treatment with SNP and hydrogen per
oxide increased seedling resistance to damaging heating, whereas NO antagonists (PTIO and L NAME) and
antioxidants (ionol and DMTU) prevented the development of seedling heat resistance after hardening heat
ing. It is concluded that, during the induction of wheat seedling heat resistance by the hardening heating,
functional interaction between NO and H2O2 as signaling messengers occurs.
Keywords: Triticum aestivum, nitric oxide, hydrogen peroxide, heat hardening, heat resistance
DOI: 10.1134/S1021443714060090
Abbreviations: DMTU—dimethylthiourea; L NAME—inhibi
tor of NO synthase (NG
nitro L arginine methyl ester); PTIO—
NO scavenger (2 phenyl 4,4,5,5 tetramethylimidazoline 1 oxyl
3 oxide); SNP—sodium nitroprusside.

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RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 62 No. 1 2015
KARPETS et al.
The interrelation between NO and ROS as signal
ing messengers at such treatments is also poorly stud
ied. At the same time, some experimental data are
obtained about ROS involvement in the realisation of
NO physiological effects and vice versa [14]. Thus, at
the treatment of Hypericum perforatum plants with
H2O2, the NO production was enhanced, whereas
under the influence of exogenous NO donor, sodium
nitroprusside (SNP), the content of endogenous H2O2
increased [15]. In ginseng root culture [16] and in iso
lated wheat coleoptiles [17], the NO donor enhanced
the generation of superoxide anion radical. In H. per
foratum plants, heat shock increased the content of
hydrogen peroxide, and this process was partially sup
pressed by the NO scavenger PTIO [15]. At the same
time, catalase did not suppress the effect of NO treat
ment of beans as the agent inducing stoma closure; this
effect was manifested independently of the ROS con
tent [18]. Treatment of detached maize leaves with
SNP did not result in the accumulation of hydrogen
peroxide in them, although treatment with hydrogen
peroxide enhanced NO generation [19].
The objective of this work was to study a possible
functional interaction of nitric oxide and hydrogen
peroxide during the induction of heat resistance of
wheat seedlings by the short term treatment with high
temperature. To this end, the dynamics of endogenous
H2O2 and NO and the effects of antagonists of these
signaling messengers on their contents in the roots of
intact seedlings after treatment with hardening tem
perature and also on the development of seedling heat
resistance were studied.
MATERIALS AND METHODS
Experiments were performed with etiolated seed
lings of soft winter wheat (Triticum aestivum L., cv.
Elegiya) grown on purified tap water at 22°C. The
roots of intact three day old seedlings were kept for
24 h in the solutions of NO scavenger PTIO convert
ing NO into nitrite [20], the inhibitor of NO synthase
L NAME, antioxidants ionol (butylhydroxytoluene)
or DMTU (dimethylthiourea). Control seedlings
were kept for 24 h in water.
The applied concentrations of these compounds
(100 µM PTIO, 2 mM L NAME, 50 µM ionol, and
150 µM DMTU), which noticeably reduced the posi
tive effect of hardening heating on seedling heat resis
tance, were chosen in preliminary experiments.
After treatment with tested compounds, some
seedlings in cheesecloth bags were subjected to hard
ening heating at 42.0 ± 0.1°C for 1 min; the procedure
was performed in broad glass bakers with water placed
in the water ultrathermostat [6, 7]. Then plant mate
rial of corresponding treatments was transferred again
into the solutions of tested effectors and kept for 24 h
until the potentially lethal heating. Control samples
were kept in water all the time.
As it has been established earlier, the highest seed
ling heat resistance was developed in 24 h after their
hardening heating [7]. In this moment, their heat
resistance was determined by seedling lethal heating at
46.0 ± 0.1°C for 10 min in the water ultrathermostat.
In 4 days after damaging heating, the relative number
of survived seedlings was determined [7].
In some series of experiments, the effects of
NO donor, sodium nitroprusside (2 mM SNP) or
hydrogen peroxide (10 mM) on seedling heat resis
tance were studied. In this case, the roots of intact
seedlings were kept in these solutions for 24 h and then
seedling heat resistance was determined as described
above.
The roots of intact seedlings were used for bio
chemical analyses. It is known that the roots of wheat
seedlings are more sensitive to heating than shoots;
therefore, they are a convenient model for the inhibi
tory analysis [7].
The content of NO in the roots and shoots was
determined by the modified method of Zhou et al. [21].
This method is based on the conversion of endogenous
NO into nitrite and quantification of nitrite by the
Griess reaction. The sample of freshly collected plant
material was homogenized on ice in 50 mM acetate
buffer (pH 3.6) supplemented with 2% zinc acetate.
The homogenate was centrifuged at a temperature not
above 4°C at 8000 g for 15 min; than 250 mg of wood
charcoal was added to 10 mL of the supernatant. The
mixture was filtered through the paper filter and 2 mL
of the filtrate was mixed with 1 mL of 1% Griess
reagent in 12% acetic acid. In 30 min, absorption at
530 nm was measured. The solutions of sodium nitrite
were used as standards.
The content of hydrogen peroxide was determined
by ferric thiocyanate method after H2O2 extraction
from the roots homogenized in the cold with 5% TCA.
The samples were centrifuged at a temperature not
exceeding 4°C for 10 min at 8000 g; the H2O2 concen
tration was determined in the supernatant using the
Mohr salt and ammonium thiocyanate [22]. Hydro
gen peroxide solutions were used as standards.
Experiments were performed in three replicates
with three recordings each. Figures present mean val
ues and their standard deviations. Differences are con
sidered as significant at p ≤ 0.05, except where specifi
cally noted.
RESULTS
The content of nitric oxide in the control seedling
roots was not almost changed during 24 h of experi
ment. Hardening heating increased significantly the
content of NO already after 15 min (Fig. 1a). The
amount of NO in root tissues remained increased by
25–35% during first two hours after hardening; the
highest effect was observed after 0.5–1.0 h. In 4 h the
effect of heating reduced markedly, and by 24 h the

FUNCTIONAL INTERACTION BETWEEN NITRIC OXIDE AND HYDROGEN PEROXIDE 67
content of NO in the roots of control and hardened
seedlings was almost similar.
The content of hydrogen peroxide in the control
seedling roots was essentially unchanged (Fig. 1b). At
the same time, already in 5 min after hardening heating
the content of H2O2 in seedling roots was transiently
increased, and this increase was observed for 30 min.
Taking into account the observed dynamics of NO
and H2O2 contents in seedling roots, in further experi
ments these parameters were assayed in 15 min, 30 min,
1 h, and 24 h after hardening heating.
To elucidate a possible relationship between NO
and hydrogen peroxide as signaling messengers during
hardening, the effects of NO antagonists (PTIO and
L NAME) on the content of H2O2 and antioxidants
(ionol and DMTU) on the content of NO in seedling
roots after hardening heating were studied.
PTIO and L NAME reduced the content of hydro
gen peroxide in seedling roots insignificantly (Table 1).
At the same time, both the scavenger of NO (PTIO)
and the inhibitor of NO synthase (L NAME) neutral
ized the effect of hydrogen peroxide accumulation
observed in 15–30 min after hardening heating. Later
(in 1 and 24 h after hardening heating) differences
between treatments became less obvious (Table 1).
On the other hand, antioxidants ionol and DMTU
suppressed the NO accumulation in the roots induced
by hardening with a maximum in 0.5–1.0 h after hard
ening heating (Table 2). In 24 h after the start of obser
vations, there were no substantial differences between
treatments.
We can assume that both nitric oxide and hydrogen
peroxide are involved in the development of seedling
heat resistance induced by hardening heating. Thus, the
effects of hardening were similarly neutralized by both
NO antagonists (PTIO and L NAME) and antioxi
dants (ionol and DMTU) (Fig. 2). However, NO scav
enger and NO synthase inhibitor themselves induced a
slight increase in the seedling resistance to hyperther
mia. Antioxidants ionol and DMTU exerted similar
effects. At the same time, these effects of NO antago
nists and antioxidants on heat resistance were much less
substantial than the effect of hardening (Fig. 2).
Seedling heat resistance was induced by treat
ments with SNP and H2O2 (Fig. 3). The content of
NO in the roots was increased under the influence of
70
0
40
60
50
1 2 3 4 24
1
2
(а)
NOcontent,nmol/gfrwt
200
0
80
160
120
1 2 3 4 24
1
2
(b)
H2O2content,nmol/gfrwt
180
140
100
Time, hTime, h
Fig. 1. Dynamics of NO (a) and H2O2 (b) contents in the wheat seedling roots after 1 min hardening heating at 42°C.
(1) Control; (2) hardening.
Table 1. Effects of the scavenger of NO (PTIO) and the inhibitor of animal NOS like enzyme (L NAME) on the content
of H2O2 (nmol/g fr wt) in the wheat seedling roots after 1 min hardening heating at 42°C
Treatment Before heating
Time after hardening heating
15 min 30 min 1 h 24 h
Control 126 ± 4 – – 129 ± 5 131 ± 4
Hardening – 167 ± 6 139 ± 5 136 ± 4 121 ± 3
PTIO, 100 µM 116 ± 6 – – 118 ± 3 113 ± 5
Hardening + PTIO, 100 µM – 133 ± 5 124 ± 4 128 ± 5 117 ± 4
L NAME, 2 mM 117 ± 7 – – 122 ± 3 125 ± 4
Hardening + L NAME, 2 mM – 138 ± 5 122 ± 4 118 ± 5 128 ± 6
Treatments with PTIO and L NAME are described in detail in the Materials and Methods section. A dash designates the absence of mea
surements.

68
KARPETS et al.
both NO donor and hydrogen peroxide. On the other
hand, treatment of intact seedling roots with H2O2
increased not only endogenous content of peroxide
but also the amount of nitric oxide in tissues (Fig. 3).
DISCUSSION
Under the influence of short term hardening heat
ing of wheat seedlings, a transient increase in the con
tents of nitric oxide and hydrogen peroxide occurred
(Fig. 1). An increased NO content in the roots was per
sisted for a longer time than the increased H2O2 con
tent, and the maximum of its content was manifested
later than the maximum of hydrogen peroxide content.
In this connection it is possible to suppose that hydro
gen peroxide is positioned upstream of nitric oxide in
the chain of transduction of signal induced by high
temperature hardening. However, the inhibitory analy
sis does not confirm this assumption. Thus, seedling
treatments with the scavenger of NO PTIO and the
inhibitor of the enzyme similar to animal NO synthase
L NAME prevented the heating induced increase in
the content of hydrogen peroxide (Table 1). On the
other hand, treatments with antioxidants ionol and
DMTU suppressed the increase in the hardening heat
ing induced increase in the content of nitric oxide
(Table 2).
As it was noted above, there are reports in the liter
ature that plant treatment with NO donors can
increase the content of ROS in tissues and vice versa
treatment with hydrogen peroxide can increase the
content of nitric oxide in the cells [15, 23]. We
observed similar effects in our experiments using treat
ments with SNP and H2O2: seedling treatment with
NO donor increased the content of hydrogen peroxide
in the roots, and the content of NO was increased
under the influence of treatment with hydrogen perox
ide (Fig. 3).
It can be assumed that very close functional inter
relations occur between nitric oxide and hydrogen
peroxide as signaling messengers. To explain possible
mechanisms of such interrelations is so far difficult.
There are some data in the literature that NO can
affect both ROS generating enzymes, NADPH oxi
dase in particular [16], and antioxidant enzymes [24],
and thus it is involved in the complex regulation of
ROS signals. The effects of ROS on the activities of
enzymes generating NO are less studied, although the
enhancement of NO generation under the influence of
treatment with H2O2 was demonstrated for various
plant materials [15, 19].
Along with discussed interaction between ROS and
NO mediated by enzymes, direct ROS and NO inter
action is also possible. Thus, the reaction between NO
and produces toxic peroxynitrite (ONOO–
),
which can oxidize the thiol residues and nitrate the
proteins on tyrosine [25]. On the other hand, under
definite conditions NO can evidently function as an
antioxidant. Thus, it was shown that low concentra
tions of exogenous NO suppressed lipid peroxidation
O2
−i
Table 2. Effects of antioxidants ionol and demethylthiourea on the content of NO (nmol/g fr wt) ) in the wheat seedling
roots after 1 min hardening heating at 42°C
Treatment Before heating
Time after hardening heating
15 min 30 min 1 h 24 h
Control 53.5 ± 1.6 – – 51.5 ± 2.2 53.0 ± 1.9
Hardening – 64.4 ± 2.6 71.0 ± 2.1 73.2 ± 1.8 51.3 ± 2.2
Ionol, 50 µM 47.4 ± 2.3 – – 48.8 ± 1.6 53.5 ± 2.5
Hardening + ionol, 50 µM – 51.6 ± 2.3 55.0 ± 2.6 54.1 ± 2.1 50.9 ± 2.0
DMTU, 150 µM 49.0 ± 1.8 – – 46.4 ± 1.7 51.0 ± 1.8
Hardening + DMTU, 150 µM – 52.3 ± 2.1 57.4 ± 1.8 58.6 ± 1.9 52.7 ± 2.3
Treatments with ionol and DMTU are described in detail in the Materials and Methods section. A dash designates the absence of mea
surements.
90
40
60
50
1 2 3 4
70
80
5 6 7 8 9 10
Treatment
Survival,%
Fig. 2. Wheat seedling survival after 10 min heating at
46°C.
(1) Control; (2) hardening; (3) PTIO, 100 µM; (4) hard
ening + PTIO; (5) L NAME, 2 mM; (6) hardening +
L NAME; (7) ionol, 50 µM; (8) hardening + ionol;
(9) DMTU, 150 µM; (10) hardening + DMTU. Treat
ment conditions are described in detail in the Materials
and Methods section.

FUNCTIONAL INTERACTION BETWEEN NITRIC OXIDE AND HYDROGEN PEROXIDE 69
and DNA fragmentation induced by plant treatment
with high H2O2 concentrations [26].
On the basis of the results obtained, it may be
assumed that heat resistance of wheat seedlings
induced by hardening heating may occur with the
simultaneous participation and functional interaction
between nitric oxide and hydrogen peroxide. Thus,
both nitric oxide antagonists and antioxidants sup
pressed the development of induced wheat seedling
heat resistance (Fig. 2). At the same time, plant treat
ments with NO donor (SNP) and hydrogen peroxide
increased seedling heat resistance (Fig. 3).
It is not excluded that heating activates essentially
simultaneously both the systems of ROS generation and
nitric oxide synthesis. It is also possible that the activa
tion of these systems and/or interaction between NO
and ROS depend on the fluctuations in the concentra
tions of other signaling messengers, calcium ions pri
marily. It is known that both the plant enzyme close to
the NO synthase of animals and NADPH oxidase are
activated with the involvement of calcium [27, 28]. This
assumption is in agreement with the results obtained in
the work [29] that the increase in the cytosolic calcium
concentration in the cells of wheat seedlings occurred
already after 1–2 min after heating at 37°C. However, a
conclusion about the role of calcium homeostasis in the
interaction between NO and ROS observed in our
experiments demands special additional investigations.
The interaction between ROS and nitric oxide can
also be mediated by their influence on activities of
antioxidant enzymes. For example, it is shown that
both an increase in the nitric oxide content in plant
cells after treatment with NO donor or its decrease
after treatment with its antagonist can lead to antioxi
dant enzyme activation [24]. The authors suggested
that NO can participate not only into “switching on”
but also in “switching off” antioxidant defense, modi
fication of ROS signal, and plant cell switching from
one stress protective mechanisms to other. It is of
interest that in our experiments NO antagonists and
antioxidants reduced a positive effect of hardening
heating on wheat seedling heat resistance, but them
selves they slightly increased such resistance (Fig. 2).
When in the case of antioxidants, an increase in the
seedling heat resistance might be determined by their
direct defensive action on cell components, similar
effects of nitric oxide scavenger and the inhibitor of the
enzyme catalyzing NO synthesis are difficult to
explain without special studies. It might be that the
exclusion from the signaling system of such messenger
as NO is itself a stress factor activating some plant
defensive systems, in particular antioxidant one [24].
Naturally, this assumption requires experimental vali
dation.
All in all, the results indicate a close functional
interaction between ROS and nitric oxide in the devel
opment of induced wheat seedling heat resistance.
A transient increases in the contents of NO and H2O2
in tissues after hardening heating are interdependent.
The investigations of endogenous contents of these
mediators in tissues in real time by nondestructive
methods could contribute to the understanding of this
interaction.
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Treatment
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Survival,%
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(1) Control; (2) SNP, 2 mM; (3) H2O2, 10 mM. Treatment conditions are described in detail in the Materials and Methods section.

70
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