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Plant Physiol. (1998) 117: 1501-1506
In Vivo Ubiquinone Reduction Levels during Thermogenesis in
Araceae1
Anneke M. Wagner*,
Marijke J. Wagner, and
Anthony L. Moore
Department of Molecular Cell Physiology, Vrije Universiteit, De
Boelelaan 1087, 1081 HV Amsterdam, The Netherlands (A.M.W.,
M.J.W.); and Department of Biochemistry, University of Sussex,
Falmer, Brighton BN1 9QG, United Kingdom (A.L.M.)
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ABSTRACT |
In vivo ubiquinone (UQ) reduction
levels were measured during the development of the inflorescences of
Arum maculatum and Amorphophallus
krausei. Thermogenesis in A. maculatum spadices appeared not to be confined to a single developmental stage, but occurred during various stages. The UQ pool in both A. maculatum and A. krausei appendices was
approximately 90% reduced during thermogenesis. Respiratory
characteristics of isolated appendix mitochondria did not change in the
period around thermogenesis. Apparently, synthesis of the required
enzyme capacity is regulated via a coarse control upon which a fine
control of metabolism that regulates the onset of thermogenesis is
imposed.
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INTRODUCTION |
UQ plays a central role in the mitochondrial respiratory chain in
plants. It is reduced by several dehydrogenases and can distribute
electrons to the Cyt pathway and the AOX. Consequently, in isolated
plant mitochondria, the UQ redox state can be varied by modulating the
activities of UQ-reducing and -oxidizing systems (Dry et al., 1989 ; Van
den Bergen et al., 1994). In a previous paper we reported that in
petunia cells the UQ pool is about 60% reduced throughout the whole
batch culture (Wagner and Wagner, 1995). These cells go through a cycle
of high supply of respiratory substrate at the beginning of the
culture, when the cells are diluted in fresh medium with excess Glc, to
the point of Glc starvation, but this variation in substrate supply
apparently does not influence the UQ reduction state. It was proposed
that AOX plays an important role in controlling these UQ-reduction
levels by acting as an overflow for excess reducing equivalents,
thereby preventing the production of reactive oxygen species by highly
reduced components of the respiratory chain (Purvis and Shewfelt, 1993;
Wagner and Krab, 1995; Purvis, 1997; Wagner and Moore, 1997).
Even when the Cyt pathway is inhibited by antimycin A, in vivo
UQ-reduction levels of about 60% are observed in petunia cells (measured after 2 d of culture in the presence of antimycin A), whereas the expression of AOX protein is increased and the kinetics of
succinate dehydrogenase are changed (Wagner and Wagner, 1997). Apparently, in these cells the relative amounts and kinetic parameters of the components of the respiratory chains are reorganized in such a
way that the reduction level of the UQ pool is not affected, whereas
O2 consumption continues at a high rate,
preventing the O2 concentration in the cells from
rising to high levels, which would also favor free radical formation
(Wagner and Moore, 1997). Respiration rates vary by at most a factor of
3 during batch culture of these cells.
A much more extreme situation with respect to differences in substrate
supply occurs during the development of the flowers of Arum
maculatum. The inflorescence consists of a central column (spadix)
wrapped by a modified bract (spathe). The base of the spathe forms the
floral chamber in which the female flowers and, above these, the male
flowers are located. The upper part of the spadix consists of a
club-shaped organ, the appendix. When the inflorescence emerges, the
spathe is tightly wrapped around the spadix, but at the time of
flowering the upper part of the spathe unfolds, exposing the appendix,
which undergoes a metabolic "explosion." Respiration, which
increases 100-fold, proceeds mainly via the alternative pathway, which
leads to a temperature rise in the appendix tissue that may be as high
as 15°C to 20°C above ambient temperature.
In an attempt to determine if the UQ-reduction levels vary during the
development of the inflorescence of A. maculatum, we have
measured in vivo UQ concentrations and reduction states and the
temperature of the appendix at various developmental stages. Since
there appeared to be dramatic differences in UQ reduction during the
period of thermogenesis compared with pre- or postthermogenic tissues,
we also studied the characteristics of mitochondria isolated from
thermogenic appendices and compared them with those of nonthermogenic but otherwise morphologically indistinguishable appendices.
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MATERIALS AND METHODS |
Plant Materials
Inflorescences of Arum maculatum were collected
from plants growing at various sites on the campus of the University of
Sussex (Brighton, UK). A flowering Amorphophallus krausei
was obtained from the Rijksherbarium/Hortus Botanicus of the
Rijksuniversiteit Leiden (The Netherlands).
Temperature Measurements
Appendices of A. maculatum were collected during
various times of the day and left at room temperature (varying between
20°C and 22°C) in a shaded area for 15 min, after which time the
appendix temperature was measured with a thermocouple (Electronic
Thermometer model 1604, Comarck Electronics Ltd., Hertfordshire,
UK) at about 1 cm below the appendix surface. For continuous
temperature measurements, the upper half of the spathe of an intact
plant in situ was removed to reveal the appendix, and a thermocouple
connected to a recorder was inserted.
Measurements of in Vivo UQ Reduction
Pieces of appendix tissue of 0.5 to 1 g were cut and
immediately dropped in liquid N2, ground to a
fine powder with a mortar and pestle, and 10 mL of 0.2 M
HClO4 in methanol (0°C) was added. The mixture
was transferred to a tube with 10 mL of petroleum ether (boiling point
40°C-60°C) and vortexed for 1 min. After the mixture was
centrifuged at 1500g for 2 min, the upper petroleum ether
phase was removed, transferred to a test tube, and evaporated to
dryness under a flow of N2. Another 10 mL of
petroleum ether was added to the lower phase, and the vortex and
centrifugation steps were repeated. The upper phase was added to the
one previously obtained. After evaporation, extracts could be stored
for at least 1 d under N2 at  20°C.
Immediately before use, the extracted UQ was resuspended with a glass
rod in 100 µL of N2-purged ethanol, and
analyzed by HPLC at the Vrije Universiteit in Amsterdam with a pump
system (Gilson, Villiers le Bel, France) and detector (model 811, Perkin-Elmer), and at the University of Sussex with an absorbance system (model 160, Beckman), a solvent-delivery module (model 110B,
Beckman), and a reverse-phase column (model 10-RP 18 Lichrosorb, Chrompack, Bergen op Zoom, The Netherlands; 4.6 × 250 mm in size). The
column was equilibrated with N2-purged
ethanol-methanol (3:2, v/v) and this mixture was used as the mobile
phase. Detection of UQ was performed at
A290. The amounts of UQ10 and
UQH210 were calibrated from the peak areas (as
determined by weighing).
Isolation of Mitochondria and Measurements of Mitochondrial
Respiration
Mitochondria from A. maculatum appendices were isolated
and purified on Percoll gradients as described by Moore et al. (1993). O2 consumption was measured at 20°C in 2 mL of
reaction medium containing 0.3 M mannitol, 1 mM
MgCl2, 5 mM
KH2PO4, 10 mM
KCl, and 20 mM Mops, pH 7.2, in a glass vessel housing a
Rank O2 electrode. Succinate (20 mM)
or NADH (2 mM) in the absence or presence of 5 mM pyruvate were added as substrates. State 3 measurements
were performed in the presence of 0.15 mM ADP. KCN (0.1 mM) was added to inhibit respiration via the Cyt pathway,
and 2 µM octyl gallate was added to inhibit AOX.
Mitochondrial protein was determined by the method of Bradford (1976),
using BSA for calibration.
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RESULTS AND DISCUSSION |
Classification of the Developmental Stages of A. maculatum Inflorescences
James and Beevers (1950) described six stages during the
development of the A. maculatum inflorescence: the
 -stage, in which the inflorescence is just emerging and the spathe
is tightly folded; the  -stage, in which the spathe is still tightly
folded; the  -stage, in which the spathe is loosening from the
appendix; the  -stage, in which the spathe is half-open; the
 -stage, in which the spathe is fully open and the pollen is shed;
and the  -stage, in which the spadix withers after the female flowers
are pollinated and the pollen of the male flowers is shed. It was
reported that respiration reached the highest rates in the -stage
and the -stage. ap Rees et al. (1977) reported that
thermogenesis takes place late in the -stage, although it was noted
that the extent and timing of thermogenesis varied considerably.
Other literature describes the onset of thermogenesis to occur at the
time of opening of the spathe (Prime, 1960), or even when the spathe is
partly unfolded (Bermadinger-Stabentheiner and Stabentheiner, 1995),
which would suggest that thermogenesis occurs in the -stage, when
the spathe is half-open. In the present study we measured appendix
temperatures from A. maculatum inflorescences at various
developmental stages. We classified the inflorescences according to the
stages through as defined by James and Beevers (1950), with the
exception that we also distinguished between fully open inflorescences
before ( ) and after
(+) pollen is shed.
Appendix Temperature and Developmental Stage
Figure 1 shows appendix temperatures
in a total of 101 inflorescences of A. maculatum. With the
exception of the inflorescences in which pollen was shed (stage
+) the average temperature of the appendix was
higher than the ambient temperature, with the highest
temperatures found in the -stage. In this stage, as in the
-stage, the -stage, and, to a lesser
extent, the -stage, a large variation in appendix temperature was
observed, including appendix temperatures that did not differ from
ambient temperatures, and temperatures below ambient temperatures,
which may be caused by the high transpiration rates in the spadix
(Skubatz et al., 1990; Bermadinger-Stabentheiner and Stabentheiner,
1995). Inflorescences at all stages could be found irrespective of the
time of day, and no correlation was found between time of harvesting
and appendix temperature at any stage (data not shown).
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| Figure 1.
Appendix temperatures during the various stages of
development of Arum lily inflorescences. Appendices were collected
during various times of the day and left at ambient temperature
(varying between 20°C and 22°C, shaded area) for 15 min, after
which time the appendix temperature was measured with a thermocouple at
about 1 cm below the appendix surface. For definitions of the
developmental stages, see ``Materials and Methods''.
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Temporal Dynamics of the Development of Thermogenesis
The observed large variation in appendix temperature at each
developmental stage of A. maculatum inflorescences could be
explained either by a large variation in the timing of thermogenesis
(not related to a certain degree of spathe opening), to variations in
the final temperature the appendix achieves, or to the length of the
thermogenic period. With respect to the temporal dynamics of spadix
development, Prime (1960) reported that there is no definite time of
day that all plants open, and that the sequence and timing of events
varies considerably with the site of the plant and the weather at the
time of flowering. It was reported that if the spathe is sheltered and
the weather is cool, the pollen may not be shed until the 3rd d after
opening of the spathe, and in cold periods the spathe may not even
fully unfold. When A. maculatum was observed growing at
various sites on the campus of the University of Sussex, a large
variation in timing of the opening process was found and one particular
specimen even remained half-open (-stage) for more than 2 d.
To estimate the variation in length of the thermogenic period and the
variation in maximal temperatures reached, the temperatures in three
appendices of A. maculatum plants were continuously
recorded. They were measured in situ on different days at ambient
temperatures varying from 12°C to 19°C. The upper half of the
spathe was removed to reveal the appendix, and a thermocouple connected
to a recorder was inserted. Table I shows
that the onset of the thermogenic period was not confined to a certain
time of day, but that the total length of the thermogenic process and
the maximal temperatures reached were not markedly different in the
three plants. It would therefore appear that it is mainly the variation
in timing of the onset of thermogenesis that causes the large variation
in appendix temperature at each developmental stage.
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Table I.
Characteristics of the thermogenic period in A. maculatum appendices
Time of day at which the temperature started to rise, duration of the
thermogenic period, and the maximal temperatures of three intact plants
measured in situ.
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In Vivo UQ Reductions and Developmental Stages
The temperature measurements at the various developmental stages
show that the onset of thermogenesis in A. maculatum is not necessarily confined to a certain morphological stage. Consequently, when inflorescences are collected by morphological stage only, a mixed
population of prethermogenic, thermogenic, and postthermogenic inflorescences will be present. We therefore measured in vivo UQ
reductions in appendices for which the temperature was determined individually. The spathe was removed, the temperature was measured, and
close to the point where temperature was measured, a piece of tissue
was cut from the appendix and UQ was extracted. HPLC traces showed that
UQ9 and UQ10 were both present in the appendix tissue, with UQ10 being
the major UQ present at every stage. Expressed on a fresh-weight basis,
UQ10 concentration increased from 0.26 ± 0.07 nmol/g fresh weight
(n = 6) at the -stage to 0.72 ± 0.18 nmol/g
fresh weight (n = 12) at the -stage. This may have
been due to an increase in mitochondrial protein during development. Indeed, this appears to be the case, since when UQ amounts were measured in isolated mitochondria from the - and -stages, the difference between these two stages expressed on the basis of mitochondrial protein was less than that expressed on a fresh-weight basis (1.74 ± 0.45 to 2.48 ± 0.68 nmol/mg protein;
n = 6). The amount of UQ9 also increased during
development of the inflorescence, but to a somewhat larger extent than
UQ10, and the UQ9:UQ10 ratio changed from 1:11 to 1:7 (data not shown).
In accordance with previous results (Ribas-Carbo et al., 1995), it was
found that UQ9 and UQ10 had the same reduction level under the various
conditions investigated. Since both UQ9 and UQ10 showed similar
variations in reduction levels, all further results are expressed in
UQ10 reduction levels only.
Figure 2 shows the levels of in vivo UQ10
reduction of 31 appendices at various developmental stages. In contrast
to all tissues measured previously (petunia [Wagner and Wagner, 1995,
1997] and bean roots, potato, and potato callus [A.M. Wagner,
unpublished data]), in vivo UQ reductions in A. maculatum
did not remain constant, but varied from 40% to almost 100%. The
highest UQ10 reduction levels were generally observed in the - and
-stages, although the UQ10 pool in one spadix from a -stage plant
was approximately 90% reduced.
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| Figure 2.
In vivo UQ10 reduction expressed as UQ reduced
(UQred) and as the percentage of total UQ
(UQtot) in the appendix during the various stages
of development of A. maculatum inflorescences. For
definitions of the developmental stages, see ``Materials and Methods''.
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In Figure 3 the relationship between
appendix temperature and UQ10 reduction is plotted. At temperatures
above 25°C, the level of UQ10 reduction was always around 90%. In
the temperature region between 20°C and 25°C, the extent of UQ10
reduction was highly variable, probably representing a mixture of
appendices that were either warming up or cooling down. The very high
reduction levels found at high appendix temperatures can be explained
in two ways: (a) the input of substrate into the respiratory chains may
exceed the electron transport capacity of the oxidizing pathways, or (b) O2 may become a limiting factor.
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| Figure 3.
Relationship between appendix temperatures and
UQ10 reduction (UQred) levels as a percentage of total UQ
(UQtot) at the various stages of development of
A. maculatum inflorescences. For details of temperature
measurements, see legend to Figure 1. For definitions of the
developmental stages, see ``Materials and Methods''.
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James and Beevers (1950) reported that respiration of the appendix of
A. maculatum, measured both in tissue slices and in a
cell-free extract, was not saturated at 100% O2.
Likewise, Wedding et al. (1973) described a
Km for O2 of appendix
slices of 1.3 µM, whereas the
Km in isolated appendix mitochondria was
0.3 µM. Therefore, it is possible that with the extremely
high respiratory rates found in thermogenic tissues,
O2 diffusion becomes limiting, especially within
the massive structure of the A. maculatum appendix.
The inflorescence of A. krausei, another member of the
Araceae, has a hollow appendix and the thermogenic tissue consists of a
layer of less than 0.5 cm. Therefore, it was important to measure in
vivo UQ-reduction status during the thermogenic period of this plant.
In the appendix of A. krausei, UQ10, the main UQ present,
became completely reduced during thermogenesis (91% ± 8%; mean
value ± SD of four samples from the same plant, taken when temperature had reached a stable level of 38°C). When the temperature had returned to room temperature, the UQ pool became more
oxidized (65% ± 8%; mean value of three samples from the same
plant ± SD). Although O2 will
diffuse more rapidly into the hollow spadix of A. krausei
than into the massive spadix of A. maculatum, it is still
possible that with the very high respiration rates during
thermogenesis, O2 diffusion also becomes a
limiting step in the A. krausei appendix. The regulation and
control of O2 consumption and UQ reduction in
thermogenic tissues will be the subject of further studies.
Mitochondrial Characteristics of Thermogenic and Nonthermogenic
Appendices in the -Stage
Since very different in vivo metabolic conditions can occur within
one developmental stage, the question arises whether mitochondria isolated from thermogenic appendices differ from those present in
nonthermogenic appendices at the same developmental stage. Appendices
in the -stage were therefore collected and divided into two groups,
one with appendix temperatures below 24°C (which may have been either
pre- or postthermogenic), and one with appendix temperatures higher
than 26°C. Table II shows the
mitochondrial parameters of these two groups. In both preparations,
NADH was respired at a faster rate than succinate, and in both samples respiration was entirely CN resistant, with the CN-resistance rate
being stimulated by pyruvate only when NADH was the substrate. This
stimulation was only about 20%, which is low compared with other
tissues, a phenomenon previously observed in Araceae (Leach et al.,
1996; Umbach and Siedow, 1996).
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Table II.
Characteristics of A. maculatum mitochondria
isolated from appendix tissue of inflorescences in the -stage with
an appendix temperature of >26°C or <24°C
Succinate (20 mM) or NADH (2 mM) were given as
respiratory substrates in the absence or presence of 0.15 mM ADP. CN-resistant respiration (+ 0.1 mM CN)
was measured in the absence or presence of 5 mM pyruvate.
Cyt pathway activity was measured in the presence of 2 µM
octyl gallate (OG). Data are mean values ± SD of
triplicate (O2 uptake) or single (UQ10 reduction)
measurements of one mitochondrial isolation.
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The severe inhibition of O2 uptake upon addition
of octyl gallate indicates that in both preparations the Cyt pathway
activity is low. Leach et al. (1996) reported that no significant
changes occur with respect to the characteristics of the Cyt pathway
during the development of the inflorescence of A. maculatum,
but found that AOX became more active at low UQ-reduction levels when
the inflorescence developed from the - and -stages to the
-stage. Our results show that once the inflorescence has reached the
-stage, no further changes take place with respect to AOX kinetics.
Independent of whether a -stage inflorescence is actually
thermogenic, O2 uptake rates under various
conditions and accompanying UQ reductions are the same, indicating that
kinetic parameters of UQ-reducing (dehydrogenases) and UQ-oxidizing
(Cyt pathway and AOX) enzymes were similar in the two mitochondrial
preparations (Wagner and Krab, 1995). This suggests that in the period
around thermogenesis, the mitochondrial "machinery" in A. maculatum does not change anymore.
This is in good agreement with what has been found for the capacities
of glycolytic enzymes such as phosphofructokinase (ap Rees et al.,
1976), which increase during the early developmental stages, but are
the same in prethermogenic and thermogenic appendices. Conversely, the
situation in A. maculatum appears to be different from what
has been described for Sauromatum guttatum, in which a
marked decrease is observed in the amount of Cyt oxidase protein and
activity as the appendix reaches "D-Day" (Elthon et al.,
1989). In S. guttatum, these changes in Cyt oxidase activity
are correlated more with the onset of thermogenesis than the increase
in AOX protein, which occurs well before thermogenesis sets in. Also, in A. maculatum increasing amounts of AOX protein, and
especially the appearance of a 35- to 36-kD polypeptide, are already
seen at the -stage and the early -stages, which may be several
days away from thermogenesis (Leach et al., 1996).
The results found for A. maculatum suggest that the
mitochondrial "equipment" is put in readiness for the thermogenic
respiratory burst via a coarse control. We can still only speculate
about the exact nature of the fine control signal(s) that initiates and
regulates the metabolic "explosion" in A. maculatum. In
the appendix of S. guttatum, synthesis of SA has been
suggested to play a role, since concentrations of SA increase 100-fold
and reach final levels of over 1 µg/g fresh weight on the day before flowering (Raskin et al., 1987, 1989). High levels of SA have also been
found in thermogenic tissues of several other Araceae species from the
genera Arum and Amorphophallus (Raskin et al., 1990). It has been reported that SA can induce AOX protein expression in nonthermogenic tissues (Kapulnik et al., 1992; Rhoads and McIntosh, 1993; Lennon et al., 1997); however, the extreme rise in concentration of SA in S. guttatum occurs only shortly before
thermogenesis, when the amount of AOX protein has already increased.
Concluding Remarks
In petunia cell suspensions, in vivo UQ-reduction levels are
maintained at a stable level of about 60%, and we have argued that
this may be part of a strategy by the plant cell to prevent free
radical formation, which is likely to occur during high reduction states of the respiratory chain, particularly with respect to UQ
(Wagner and Wagner, 1995, 1997). In this paper, however, we show that
during development of the inflorescence of A. maculatum, the
UQ pool in the appendix tissue becomes reduced to very high levels in
vivo. Apparently, the regulatory mechanisms that normally control or
buffer the redox levels of the UQ pool do not function in the
thermogenic appendix. The reason for this may be related to the
specialized function of the appendix tissue compared with normal,
growing cells. The sole function of the appendix is to produce heat to
attract insects for pollination. A highly reduced UQ pool will give
maximal activity of the heat-producing AOX (Leach et al., 1996).
Following pollination, the appendix tissue senesces, so the need to
protect the appendix against free radical damage, which would occur at
such high reduction levels of the respiratory chain components, is
removed.
Thermogenesis in the appendix is characterized by high respiratory
activity and loss of control of redox regulation, which may result in
the formation of reactive oxygen species, increased SA concentrations,
and, finally, the death of the appendix tissue. This is similar to the
description of programmed cell death (apoptosis), as occurs in the
hypersensitive response in plant-pathogen interactions (Greenberg,
1997). The order of events and the nature of the signal molecules in
the program that causes apoptosis in plants are unclear at present.
There is agreement that an oxidative burst precedes cell death, but the
role of SA is still under debate (Lamb and Dixon, 1997). Therefore,
more insight into the signals triggering both the onset of
thermogenesis and programmed cell death is required before we can
decide whether thermogenesis in the Arum lily spadix can indeed be
regarded as an apoptotic event.
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FOOTNOTES |
1
The work described in this paper was supported
in part by a grant from the British Council and the Netherlands
Organization for Scientific Research.
*
Corresponding author; e-mail amwagner{at}bio.vu.nl; fax
31-20-444-7229.
Received January 29, 1998;
accepted May 15, 1998.
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ABBREVIATIONS |
Abbreviations:
AOX, alternative oxidase.
SA, salicylic acid.
UQ, ubiquinone.
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ACKNOWLEDGMENTS |
The authors acknowledge W.L.A. Hetterscheid and A.P.T.M. Vogel
of the Rijksherbarium/Hortus Botanicus (Rijksuniversiteit Leiden, The
Netherlands) for the generous supply of a flowering A. krausei. The authors also gratefully acknowledge Mr. Robin Albert
of Beckman Instruments, Inc. (High Wycombe, UK) for lending HPLC
equipment to A.L.M.
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Abstract
Introduction