ISSN 1021-4437, Russian Journal of Plant Physiology, 2016, Vol. 63, No. 3, pp. 409–416. © Pleiades Publishing, Ltd.

, 2016.
Original Russian Text © R.V. Malyshev, M.A. Shelyakin, T.K. Golovko, 2016, published in Fiziologiya Rastenii, 2016, Vol. 63, No. 3, pp. 434–442.

RESEARCH PAPERS

Bud Dormancy Breaking Affects Respiration and Energy Balance

of Bilberry Shoots in the Initial Stage of Growth
R. V. Malyshev, M. A. Shelyakin, and T. K. Golovko
Institute of Biology, Komi Scientific Center, Ural Branch, Russian Academy of Sciences,
ul. Kommunisticheskaya 28, Syktyvkar, 167982 Russia
e-mail: shelyakin@ib.komisc.ru
Received July 31, 2015

Abstract—Respiration and heat production in the shoots of bilberry (Vaccinium myrtillus L.) were studied at the
beginning of growth after breaking bud dormancy by means of transfer of the shoots to indoor conditions
(November–April) and upon natural sprouting in spring (May). The buds released from dormancy at the begin-
ning of winter sprouted slower and showed lower respiratory activity than the buds that started growing in May.
In May, cytochrome respiratory pathway in sprouting buds was 1.3 times more active than energetically ineffec-
tive alternative pathway, whereas activity of cytochrome pathway in December was 1.4 times lower as compared
with the alternative. In November–December, the rate of heat evolution by the buds was 3–5 times lower than
in April–May. In case of early breaking of bud dormancy, the share of respiration energy dissipated as heat was
30% on average. In the buds whose growth was induced later, the value of this parameter was twice as much. The
ratio between heat evolution and respiration depended on temperature. High temperature more intensely acti-
vated heat evolution than respiration, which caused a decrease in the level of metabolic energy available for
growth. In the temperature range of 5–15°C characteristic of the beginning of vegetation, the share of respira-
tion energy dissipated as heat was 2–3 times lower than at 20–30°C, which reflects a great adaptability of
V. myrtillus to climatic conditions of the region. Our data suggest that progression through a full cycle of winter
dormancy is physiologically important for shoot growth. Early dormancy release brought about changes in res-
piration and energy balance of the shoots in the initial stage of extra-bud growth.

Keywords: Vaccinium myrtillus, buds, dormancy breaking, growth, respiration, heat evolution, energy storage
DOI: 10.1134/S1021443716030092

INTRODUCTION There are three types of bud dormancy in woody

Bud is a primordial undeveloped shoot. Vegetative
bud consists of a meristematic embryonic axis ending
with an apical cone and primordial leaves of different
age located one over another on this axis [1]. In the
majority of plant species, outer leaves of the bud are
specialized bud scales that perform protective func-
tions.
Transformation of the bud into a shoot starts with
expansion of primordial leaves and growth of inter-
nodes. In temperate zone, the buds of woody plants
produce shoots in spring or in early summer; then new
overwintering buds with primordial shoots of the next
year are formed. The buds spend winter in a dormant
state. Reduction in photoperiod (extension of night)
and lower temperature are signals for the onset of dor-
mancy [2, 3].
Abbreviations: АОX—alternative oxidase; АP—alternative respi-
ratory pathway; CP—cytochrome respiratory pathway; EES—
efficiency of energy storage; q—rate of heat production; Valt,
Vcyt and Vres—activity of alternative, cytochrome, and residual
respiration, respectively; Vtotal—rate of total respiration
plants: relative, true, and exogenous. Relative dor-
mancy covers a period from the formation of new buds
in the axils to autumn fall of the leaves. True dormancy
lasts approximately to the middle of winter. It is also
called organic or physiological (endodormancy [4]),
since the buds contain many growth inhibitors in this
period (АBA, ethylene, phenolics, etc.). Exogenous
dormancy (ecodormancy) is easy to break, since it is
caused by adverse conditions (most often, by low tem-
peratures or water deficit).
Dormant buds lack exterior symptoms of growth
and are highly resistant to dehydration and adverse
environmental influences (first of all, to low below-
zero temperatures) [5]. This is favored by accumula-
tion of soluble carbohydrates and protective proteins
[6, 7]. Release of bud dormancy is accompanied by a
considerable activation of the processes associated
with mobilization of storage substances and energy
production. It was shown that expression of the genes
encoding glycolytic enzymes was activated, as were the
proteins participating in ROS quenching and protec-
tion of meristematic tissues against injury [8].

409
410 MALYSHEV et al.
In the zones of intense growth rich in meristems,
cell supply with energy and metabolites predominantly
depends on respiration. If the substrate is transformed
to biomass at a maximum efficiency, respiratory costs
of the synthesis of 1 g of vegetative biomass may range
from 0.33 to 0.43 g of glucose [9, 10]. In this case, only
a portion of energy derived from the oxidized substrate
is stored in newly synthesized biomass, and the rest of
it is inevitably dissipated in the environment as heat
[11]. Energy evolved as heat may be measured calori-
metrically. Metabolic heat evolution is a measure of
energy dissipation from the tissue to environment and
characterizes efficiency of energy utilization [12, 13].
The sprouting buds are a good model for the study
of the effect of internal and external factors on gener-
ation and dissipation of metabolic energy and effi-
ciency of its storage, which is important for under-
standing bioenergetics of living systems.
The aim of this work was to compare respiration,
the ratio between respiratory pathways, and heat pro-
duction in the shoots of Vaccinium myrtillus in the ini-
tial stage of extra-bud growth during the time of natu-
ral resumption of growth in spring and upon artificial
breaking of winter bud dormancy.
MATERIALS AND METHODS
Investigations were conducted with the plants of
bilberry (Vaccinium myrtillus L.)—a branchy decidu-
ous 15–30-cm-high dwarf shrub, family Ericaceaе.
Bilberry plays an important cenotic role in ground
cover of dark and light coniferous taiga. Bilberry over-
winters under snow. In the region of investigations
(subarea of middle taiga), its buds start bursting in the
first half of May when average daily air temperature
rises to 7–10°C. Bilberry blooms in June, and berries
ripen in late July–early August.
The experiments were conducted in 2013–2015.
The shoots were cut from 20–25 partial bushes grow-
ing in a bilberry haircap spruce forest near Syktyvkar
(61о40′ N, 50о49′ E). The samples were taken from
November to May. In November–April, the shoots
were transferred to indoor conditions and placed in
the vessels with water until complete budburst. Every
2–4 days, we recorded the number of unfolded vege-
tative buds and measured their length. The shoots with
broken buds sampled in May were preliminarily
adapted indoors for 24 h.
Respiratory rate was determined by О2 consumption
at 20°С polarographically using a Clark electrode (Oxy-
therm system, Hansatech Inst., United Kingdom) and
expressed in nmol О2/(g dry wt min). Fragments (15–
20 mg) of unfolded buds (4–6 pieces) were placed in a
3-mL reaction vessel containing 1.5 mL of Hepes-buf-
fer (Helicon, Russia) at a concentration of 50 mM,
pH 7.2. Measurements were taken at constant stirring.
All the measurements were repeated 4–6 times.
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
Activity of respiratory pathways was estimated by
means of specific inhibitors [14]. As an inhibitor of
alternative oxidase (AOX), we used benzhydroxamic
acid (Lancaster, United Kingdom) at a concentration
of 7 mM. Cytochrome oxidase activity was inhibited
with KCN (Sigma, United States) at a concentration
of 3 mM. Optimal concentrations of inhibitors of
mitochondrial oxidases were selected in preliminary
experiments. In order to detect nonspecific effect of
toxic substances on respiration, we employed a method
of direct titration adapted for plant tissues [15].
The rate of oxygen consumption was represented as
a sum of components:
Vtotal = Valt + Vcyt + Vres, (1)
where Vtotal is total respiration, Valt is alternative respi-
ration suppressed by AOX inhibitor, Vcyt is cyanide-
sensitive (cytochrome) respiration, and Vres is residual
respiration recorded in the presence of inhibitors of
alternative and cytochrome respiratory pathways.
The rate of metabolic heat evolution by the buds
was determined by the method of direct calorimetry at
20°C using a Biotest-2 apparatus (Institute for Biolog-
ical Instrumentation, Russian Academy of Sciences,
Pushchino, Russia). Biotest-2 differential isothermal
microcalorimeter is a specialized instrument designed
to study metabolic activity of plant tissues [16]. It is
equipped with eight aluminum calorimetric cells, each
1 сm3 in volume. Threshold of response in respect to
noise level is at least 2 μW, which corresponds to
0.00004°C. After replacement of a container (cell)
with the sample, measuring mode recovered in 30 min.
Each cell accommodated 2–3 completely unfolded
buds (fresh weight of 150–200 mg). The rate of respi-
ration was determined by heat effect of the reaction
between CO2 released by the object and 0.4 М NaOH
[12]. The advantage of this method consists in the fact
that heat evolution and respiration are measured in the
same sample by heat effect, which makes it possible to
estimate energy balance of the object under investiga-
tion [13].
The rates of heat evolution (q) and respiration (RCO2 )
were calculated according to the formulas (2) and (3),
respectively:
q = 0.022 ([( q 2 + q 4 ) 2] − [(Q1 + Q5 ) 2]) , (2)
RCO2 = [( 0.022q3 ) − q ] 108.5, (3)
where 0.022 is calibration coefficient of the instru-
ment, μW; 108.5 is heat effect of the reaction between
1 mole of СО2 and 0.4 М NaOH, μW/nmol; Q1 is heat
flow from the empty working container before the
measurement; Q5 is heat flow from the empty working
container after the measurement; q2 is heat flow from
the container with the object; q3 is total heat flow from
the object and reaction of СО2 released by the object
with 0.4 М NаОН; and q4 is heat flow from container
Vol. 63 No. 3 2016
 BUD DORMANCY BREAKING AFFECTS RESPIRATION 411

with the object after the removal of the vessel with the 5
alkali. 3
One work cycle with a sample lasted for approxi-
mately 2 h. At one time, we could investigate seven 4 1
samples. Found values of q and RCO 2 were divided by 2

dry weight of the object under consideration and
expressed in μW/mg dry wt and nmol/(mg dry wt s),
respectively.
In order to reveal the effect of temperature on
metabolism of the shoots sprouting in spring, we mea-
sured the rate of heat evolution at 5, 10, 15, 20, 25, 30,
and 35°C. At each temperature, we used freshly col-
lected samples of unfolded buds. Measurements were
repeated four or five times.
Statistical treatment. The data were statistically
treated using Statistica v. 6.1 software (StatSoft,
United States). Normality of distribution was esti-
mated using the Shapiro-Wilk’s test. The means were
compared using ANOVA variance analysis (Duncan’s
test). The results were treated using Pearson’s correla-
tion analysis. All the calculations were done at the
given level of significance P ≤ 0.05. Figures and tables
show the means and their standard errors.
RESULTS
Duration of the period before the beginning of
budburst varied depending on the time of sampling.
When dormancy was broken in November, the buds on
the shoots sprouted 18 days after the transfer to indoor
conditions, whereas they unfolded on the third to
fourth day in April (Fig. 1). It is interesting that the
length of vegetative buds considerably increased
during winter dormancy. If average length of buds was
a little larger than 1 mm in November, it amounted to
2.5 mm in April.
The rate of bud respiration depended on the time of
dormancy release (Table 1). The rate of О2 consump-
tion in unfolded buds of the shoots sampled in Decem-
ber–February was 1.5–1.8 times lower than in April–
May. Cytochrome respiration (CP) changed in parallel
with the rate of total respiration. In December–March,
the rate of respiration along the main pathway was, on
average, 1000 nmol О2/(g dry wt min), and it amounted
Length, mm
3
2
1
0 5 10 15 20
Time, days
Fig. 1. Length and time of vegetative buds, unfolding on the
shoots of V. myrtillus cut in (1) November, (2) February, and
(3) April. Arrows indicate the beginning of bud sprouting
after transfer of the shoots to indoor conditions. The means
and their standard errors are shown (n = 30–40).
to 1900 nmol О2/(g dry wt min) in April–May. At the
same time, the contribution of CP to total О2 consump-
tion varied from 35 to 40% rising to 50% in May. The
rate of cyanide-resistant respiration maintained with
the participation of AOX was comparable, and it was
even above the rate of energetically efficient CP in
December. Contribution of alternative respiratory
pathway (AP) to total respiration in December was 50%
and it decreased to 38% in May. Elevation of total res-
piration of buds in April depended on activation of AP
to a greater extent than of CP. The share of residual res-
piration resistant to inhibitors was 12–15% on average
of total О2 consumption.
Calorimetric determination of respiration showed
that the rate of СО2 evolution by unfolded buds changed
depending on the time of sampling (Table 2). The low-
est figures were recorded in November and the greatest
in May. In December–April, the rate of СО2 evolution
varied from 0.03 to 0.04 nmol/(mg dry wt s), which is
equivalent to 1800–2400 nmol О2/(g dry wt min).

Table 1. Rate of total respiration (Vtotal) and activities of cytochrome (Vcyt) and alternative (Valt) pathways and residual res-
piration (Vres) in unfolded buds of V. myrtillus depending on the time of dormancy release (nmol О2/(g dry wt min))
Month Vtotal Vcyt Valt Vres
Dec. 2629 ± 175a 925 ± 98a 1320 ± 142a 383 ± 45ab
Feb. 2675 ± 216a 1130 ± 90a 1230 ± 123a 315 ± 66a
Mar. 3045 ± 145ab 1110 ± 82ab 1448 ± 134a 486 ± 48ab
Apr. 4843 ± 347c 1901 ± 319b 2190 ± 198b 753 ± 55c
May 3967 ± 273b 1942 ± 163b 1504 ± 82a 521 ± 71b
The means and their standard errors are shown (n = 4–6). Measurements were taken at 20°C. Different superscripts designate reliability
of changes in the parameter depending on the time of dormancy release (ANOVA, Duncan’s test, Р ≤ 0.05).

RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 63 No. 3 2016

412 MALYSHEV et al.

(а) (b)
0.15 50

0.10 40
Evolution of CO2 (RCO2),
nmol/(mg dry wt s)

Heat evolution (q),

0.05

μW/mg dry wt
30

0 20
5 10 15 20 25 30 35
–0.05 10

–0.10 0
5 10 15 20 25 30 35
–0.15 –10
Temperature, °С

Fig. 2. Temperature dependence of the rate of (а) respiration and (b) heat evolution in the buds of V. myrtillus unfolded in May.
The means and their standard errors for 2–3 series of independent experiments are shown (n = 10–15).

In November, the buds released from dormancy
were notable for a very low rate of heat generation (q)
(Table 2). In December, q value in the buds noticeably
increased. A considerable rise in this parameter was
observed in February. In February–April, q value was
five times greater than in November and 2.5 times
greater than in December. In May, sprouting buds of
bilberry produced heat at the same rate as the buds
artificially released from dormancy in the period from
February to April.
Investigations conducted with the buds that
unfolded in spring showed a dependence of heat evo-
lution and respiration on temperature (Fig. 2). Both
parameters increased when the temperature rose from
5 to 30°C. At 35°C, respiration and the processes asso-
ciated with heat production were suppressed. Analysis
Table 2. Rate of heat production (q) and respiration (RCO2 )
in unfolded buds of V. myrtillus depending on the time of
dormancy release
RCO2 , nmol/(mg dry
Month q, μW/mg dry wt
Nov. 2.6 ± 1.2a
Dec. 5.0 ± 1.0a
Feb. 13.3 ± 1.6b
Mar. 10.0 ± 0.7b
Apr. 13.0 ± 1.5b
May 14.2 ± 1.2b
The means and their standard errors for two or three series of
independent determinations are shown (n = 7–10). Measure-
ments were taken at 20°C. Different superscripts designate reli-
ability of changes in the parameter depending on the time of dor-
mancy release (ANOVA, Duncan’s test, Р ≤ 0.05).
of temperature dependence has shown that the great-
est increase in СО2 evolution occurred when tempera-
ture rose from 15 to 25°C. The magnitude of coeffi-
cient Q10 for respiration within the ranges of 5–15°C
and 20–30°C was much lower than in the ranges of
10–20°C and 15–25°C (Table 3). As to heat evolution
by the buds, Q10 value for this parameter was higher
than for respiration. The most significant increase in
the rate of heat evolution in sprouting buds was
observed when temperature rose from 10 to 20°C.
DISCUSSION
Transition to deep dormancy enables plants not
only to survive critical periods but it is also a stage nec-
essary for changes preparing plants for rapid growth
when favorable period comes. Low-temperature expo-
sure of a certain duration is necessary for the buds of
woody plants in the temperate zone. It prevents early
initiation of growth in spring and shoot injury in case
of return of cold weather [17]. Our investigations
showed that a disturbance of biological rhythm of
development as a result of artificial breaking of bud
wt s) dormancy exerted a profound influence on the initial
stage of extra-bud growth of bilberry shoots. The ear-
0.020 ± 0.002a
lier the shoots were transferred to indoor conditions,
0.030 ± 0.004ab the longer time interval before budbreak (Fig. 1). Sim-
0.040 ± 0.005b ilar results were obtained for Betula pendula, Alnus glu-
0.040 ± 0.003b tinosa, and Prunus padus [17]. On the branches of
A. glutinosa placed in a controlled-climate chamber in
0.040 ± 0.004b
November, the buds unfolded in 60 days, in March,
0.060 ± 0.004c they unfolded as early as in 10 days; the buds of
P. padus opened in 25 and 5 days, respectively.
The buds of bilberry released from dormancy
before the proper time did not reach the level of meta-
bolic activity characteristic of unfolded buds that nat-

RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 63 No. 3 2016

 BUD DORMANCY BREAKING AFFECTS RESPIRATION
urally resumed growing in May. This showed in a
lower rate of respiration and heat production
(Tables 1, 2). In April–May, О2 consumption charac-
teristic of mitochondrial respiration was much higher;
in addition, the ratio between cytochrome and alter-
native pathways changed. In December, Vcyt/Valt ratio
was 0.7 and it rose to 1.3 in May. When the share of
ineffective respiration decreased, sprouting buds could
more efficiently utilize respiratory substrate for pro-
duction of metabolic energy.
According to literature data, bud respiration of
deciduous woody plants goes down by autumn and
greatly rises in spring upon dormancy release [17–21].
For instance, respiration rate of B. pendula buds in
October–February remained very low and it grew
more than ten times amounting in April to 1400 μL
О2/(g dry wt h) [17]. For comparison, in May the rate
of respiration of sprouting bilberry buds was approxi-
mately 4000 nmol О2/(g dry wt min) at 20°C (Table 1)
or 5400 μL О2/(g dry wt h). Under natural conditions,
average daily air temperature in the first ten-day-
period of May was 7–10°C. Therefore, the rate of res-
piration of sprouting buds of V. myrtillus was 2–3 times
lower.
The data about activity and the ratio between respi-
ratory pathways in the buds of woody plants are scanty.
In bilberry, contribution of AP to bud respiration upon
dormancy breaking in December amounted to 50%,
whereas it was 38% in May in completely unfolded
buds. The data we obtained agree with the results of not
numerous investigations of the buds of other plant spe-
cies. For instance, respiration of flower buds of peach
tree before and during the dormant period was more
intensely suppressed by AOX inhibitor salicylhy-
droxamic acid than by KCN that inhibits cytochrome
oxidase [22]. Upon bud dormancy release, the extent of
suppression of respiration with AOX inhibitor
decreased. In the course of dormancy induction in
peach tree buds caused by shortening of photoperiod,
CP activity decreased, whereas ability to transfer elec-
trons along AP became greater [23]. In the dormant
period, contribution of AP to total respiration of buds in
aquatic plants varied in a wide range (50–90%) [24].
It is interesting that respiratory activity of bilberry
shoots in the initial stage of extra-bud growth was
approximately the same as in the objects notable for
active respiration, such as wheat seedlings [25] or young
arabidopsis plants [26]. As to the ratio between respira-
tory pathways, sprouting shoots of bilberry also did not
differ from young organs of other plants [27–29].
Heat evolution by plant cells is an integral charac-
teristic of the whole metabolism [30]. Calorimetric
measurements showed that heat production in bilberry
buds greatly depended on the time when sprouting was
initiated. In May, the magnitude of q in unfolded buds
amounted to 14 μW/mg dry wt (at 20°C) being five
times greater than in the buds that were released from
dormancy in November. Data about heat production
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 63
413
Heat evolution (q), μW/mg dry wt
16
12
8
4
r = 0.75
0
0.01 0.02 0.03 0.04 0.05 0.06 0.07
Evolution of СО2 (RCO2), nmol/(mg dry wt s)
Fig. 3. Rate of heat evolution (q) as a function of respira-
tion (RCO 2 ) of unfolded buds of V. myrtillus (r is Pearson’s
correlation coefficient at the given significance level P ≤
0.05).
in the buds of woody plants are not numerous. We
showed earlier that the rate of heat evolution in the
sprouting shoots of Syringa josikaea and S. vulgaris was
25–30 μW/mg dry wt (at 20°C) [31]. The value of this
parameter in the apical flower buds of Malus domestica
treated before opening with bud breaking agents varied
from 10 to 12 μW/mg dry wt (at 25°C) [32].
We revealed a strong correlation (r = 0.75 at P =
0.01) between the rate of heat evolution and respira-
tion of unfolded buds measured calorimetrically
(Fig. 3). This makes it possible to regard q as a func-
tion of the rate of СО2 evolution RCO2 and agrees with
the notions that the bulk (up to 90%) of evolved heat
in young actively growing organs and tissues is
accounted for by their respiration [13]. It is known that
the bulk of СО2 is produced within Krebs cycle as a
result of oxidative decarboxylation of organic acids
and other compounds (lipids and proteins).
Correlation between q and consumption of О2 (Vtotal)
reflecting activity of mitochondrial pathways of respi-
ration was weak (r = 0.56 at P = 0.33) (Fig. 4a). It
could be caused by changes in the ratio between the
main (cytochrome, CP) and energy dissipating alter-
native respiratory pathway (AP). As was already noted,
the ratio Vcyt/Valt in the buds sprouting in May changed
in favor of cytochrome respiratory pathway, which
Table 3. Q10 coefficient of respiration (RCO2 ) and heat pro-
duction (q) of the shoots of bilberry V. myrtillus in the begin-
ning of extra-bud growth under natural conditions
Q5–15 Q10–20 Q15–25 Q20–30 Q25–35
Parameter
RCO2 1.6 2.0 2.3 1.6 –0.5
q 2.4 4.3 2.1 2.7 0.2
No. 3 2016
414 MALYSHEV et al.

(а) Our data suggest that, in actively growing tissues and

16 organs, thermal dissipation of energy covers not only
losses associated with involvement of AP. According to
Heat evolution (q),

calculations done in [11], approximately 90% of

12
μW/mg dry wt

energy contained in the respiration substrate may be

lost in the stage of ATP formation. Approximately as
8 much energy is inevitably dissipated in the processes of
biomass production (growth).
4 r = 0.56 Thermodynamic model [12, 13, 34] makes it possi-
ble to mathematically describe growth in terms of
0 energy storage and estimate its efficiency. Growth rate
1000 2000 3000 4000 5000 6000 is proportional to the difference between two charac-
Consumption of О2 (Vtotal), nmol O2/(g dry wt min) teristics—the rate of respiration and heat evolution:
(b) Δ H BR SG = 455RCO2 − q, (4)
16
where ∆HBRSG is growth rate (μW/mg dry wt), 455 is
changes in enthalpy per nmol of oxygen used for oxi-
Heat evolution (q),

12 dation of organic compounds (μW/nmol), Rсо2 is rate

μW/mg dry wt

of СО2 evolution (nmol/(mg dry wt s)), and q is rate of

metabolic heat evolution (μW/mg dry wt).
8
r = 0.73 The given equation is relevant to young plants or
apical parts of mature plants where the bulk of energy
4 produced in the course of respiration is spent on for-
mation of new structures. According to this model, the
0 ratio q 455RCO2 is a measure of efficiency of energy
500 1000 1500 2000 2500 storage (EES). This ratio may take on values above or
Consumption of О2 (Vcyt), nmol O2/(g dry wt min) below unity. Values less than unity point to energy
(c) storage by a plant: the lower this ratio, the more energy
16
is stored. At q 455RCO2 ≥ 1, storage of energy (growth)
ceases [34, 35].
Heat evolution (q),

12 Having applied the model to our data, we examined

μW/mg dry wt

the effect of artificial breaking of bud dormancy on the

8
r = 0.33
4 energy. It is interesting that, when bud sprouting was
0 times greater. These results apply to the temperature of
500 1000 1500 2000 2500
Consumption of О2 (Valt), nmol O2/(g dry wt min)
Fig. 4. Rate of heat evolution (q) as a function of (а) total
respiration (Vtotal), (b) cytochrome (Vcyt), and (c) alterna-
tive (Valt) pathways in unfolded buds of V. myrtillus (r is
Pearson’s correlation coefficient at the given significance
level Р ≤ 0.05).
agrees with the idea of a greater contribution of CP to
the growth respiration and alternative pathway to
maintenance respiration [26]. In sprouting buds of bil-
berry, q value correlated with the activity of energeti-
cally efficient CP (r = 0.73 at P = 0.02) (Fig. 4b) but
not with the activity of energy dissipating AP (r = 0.33
at P = 0.42) (Fig. 4c), as was shown in ageing sections
of potato or in cucumber leaves after cold stress [33].
ratio q 455RCO2 . First of all, one should note that
q 455RCO 2 value was below unity (Fig. 5), which
pointed to a potential ability of unfolded buds to store
induced in November–December, it was almost two
20°C, whereas average daily temperature in the first
half of May in natural conditions when the shoots of
bilberry resumed growing did not exceed 10°C. Since
the rate of heat production, as well as respiration,
depends on temperature (Fig. 2), changes in external
temperature also affect q 455RCO 2 . Figure 6 shows
that, at 5–15°C, the value of q 455RCO 2 ratio was, on
average, approximately 0.3 and increased 1.7 times
when temperature rose to 20–25°C. Heating of
unfolded buds to 30°C more intensely activated heat
production than respiration (Fig. 2). As a result, value
of q 455RCO 2 increased more than 1.5 times and
amounted to 0.84. In other words, temperature of
30°C is almost critical to shoot growth in the begin-
ning of vegetation, because of elevated dissipation of
energy. Complete upsetting of energy balance was
observed when sprouting shoots were exposed to a
temperature of 35°C. It was shown that response of

RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 63 No. 3 2016


1.0
Efficiency of energy storage,
0.8
q/455 RCO2
0.6
a observed in the range of temperatures characteristic of
a the period when natural sprouting of V. myrtillus
0.4
0.2
1 2
Fig. 5. Efficiency of energy storage (q/455Rco2) in the
buds of V. myrtillus depending on the time of unfolding.
Figures under columns correspond to the months:
(1) November, (2) December, (3) February, (4) March,
(5) April, (6) May. Different symbols above the columns
designate reliability of changes depending on the time of
bud dormancy release (ANOVA, Duncan’s test, Р ≤ 0.05).
5.0
~ 921.
~
Efficiency of energy storage,
1.0
0.8
q/455RCO2
0.6
0.4
0.2
0 peratures, Usp. Sovrem. Biol., 2001, vol. 121, pp. 3–22.
5 10 15 20 25
Temperature, °С
Fig. 6. Effect of temperature on efficiency of energy stor-
age ( q 455RCO 2 ) in the buds of V. myrtillus unfolded in
May. The means and their standard errors for 2–3 series of
independent determinations (n = 7–10) are shown.
plants’ respiration to temperature in many respects
determines their geographic distribution [34].
Thus, we ascertained the mechanisms of changes
in respiration, ratio between respiratory pathways, and
heat evolution in the shoots of bilberry in the initial
stage of extra-bud growth. It was shown that breaking
of buds’ dormancy affects their bioenergetics. The
buds prematurely released from winter dormancy
sprouted slower and were notable for a low metabolic
activity. The ratio between cytochrome and alternative
respiration in December was 1.9 times lower than in
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
BUD DORMANCY BREAKING AFFECTS RESPIRATION 415
May. Efficiency of energy storage in sprouting buds
depended on temperature. High temperatures more
intensely activated processes associated with heat pro-
b b duction than respiration. This brought about a rise in
b the share of energy dissipated as heat and a decrease in
the share of metabolic energy stored in the course of
b
growth. The most efficient storage of energy was
shoots starts. On the whole, the obtained data broaden
the notions about functional biology and bioenergetics
of sprouting buds.
3 4 5 6
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Translated by N. Balakshina
Vol. 63 No. 3 2016