Plant Physiol. (1999) 120: 821-826
Thermotolerance of Leaf Discs from Four Isoprene-Emitting Species
Is Not Enhanced by Exposure to Exogenous Isoprene1
Barry A. Logan2, * and
Russell K. Monson
Department of Environmental, Population, and Organismic Biology,
University of Colorado, Boulder, Colorado 80309-0334
 |
ABSTRACT |
The
effects of exogenously supplied isoprene on chlorophyll
fluorescence characteristics were examined in leaf discs of four isoprene-emitting plant species, kudzu (Pueraria lobata
[Willd.] Ohwi.), velvet bean (Mucuna
sp.), quaking aspen (Populus tremuloides Michx.), and pussy willow (Salix discolor Muhl).
Isoprene, supplied to the leaves at either 18 µL L
1 in
compressed air or 21 µL L1 in N2, had no
effect on the temperature at which minimal fluorescence exhibited an
upward inflection during controlled increases in leaf-disc temperature.
During exposure to 1008 µmol photons m2
s1 in an N2 atmosphere, 21 µL
L1 isoprene had no effect on the thermally induced
inflection of steady-state fluorescence. The maximum quantum efficiency
of photosystem II photochemistry decreased sharply as leaf-disc
temperature was increased; however, this decrease was unaffected by
exposure of leaf discs to 21 µL L1 isoprene. Therefore,
there were no discernible effects of isoprene on the occurrence
of symptoms of high-temperature damage to thylakoid membranes. Our data
do not support the hypothesis that isoprene enhances leaf
thermotolerance.
| |
INTRODUCTION |
More than 4 decades ago emission of isoprene
(2-methyl-1,3-butadiene) from leaves of higher plants was first
described (Sanadze, 1957
). Since that time understanding of the
biochemistry and environmental controls of isoprene emission has grown
considerably, along with an appreciation for the role that phytogenic
isoprene plays in critical oxidative atmospheric processes (for
reviews, see Sharkey et al., 1991; Sharkey, 1996; Lerdau et al., 1997).
However, a function for isoprene in leaves remained elusive until
Sharkey and Singsaas (1995) reported evidence from kudzu
(Pueraria lobata [Willd.] Ohwi.) that isoprene protected
thylakoid membranes against damage induced by high leaf temperatures.
Under conditions that suppressed endogenous isoprene synthesis,
isoprene supplied exogenously at physiologically realistic
concentrations resulted in an increase in the temperature at which
chlorophyll fluorescence emission exhibited a distinct upward
inflection (Sharkey and Singsaas, 1995; Singsaas et al., 1997).
Furthermore, it was reported that a linear relationship exists between
the concentration of supplied isoprene and the extent of its effect on
leaf thermotolerance (Singsaas et al., 1997). Subsequently, it was
reported that certain monoterpenes, another class of phytogenic
hydrocarbons, protect the photosynthetic apparatus of Quercus
ilex L. from thermal damage (Loreto et al., 1998).
High temperature-induced inflection of chlorophyll fluorescence has
been used widely as an indicator of thermal damage and correlates with
the temperature at which leaves experience significant tissue necrosis
(Bilger et al., 1984). Dislocation between the light-harvesting
complexes and PSII reaction centers due to excessive membrane fluidity
is thought to underlie this phenomenon (Armond et al., 1980), although
Yamane et al. (1997) suggested that denaturation of PSII reaction
center proteins may be involved as well.
Current understanding of leaf isoprene synthesis is largely consistent
with the hypothesis that isoprene protects thylakoids from thermal
damage. Isoprene is hydrophobic and presumably partitions into the
interior of membrane bilayers. The final step in isoprene formation is
catalyzed by isoprene synthase (Silver and Fall, 1995), an enzyme with
stromal and thylakoid-bound isoforms (Wildermuth and Fall, 1998). This
location for isoprene production would allow for its direct diffusion
into thylakoids. The capacity to synthesize isoprene is found only in
individuals acclimated to warm temperatures. In addition, isoprene
emission rate exhibits a strong positive temperature response (Sanadze
and Kursanov, 1966; Monson and Fall, 1989; Loreto and Sharkey, 1990).
In fact, a Q10 for leaf isoprene emission as high
as 8 has been reported (Sharkey and Loreto, 1993). High temperatures often occur simultaneously with
other environmental factors, such as water stress, which lead to
stomatal closure. Whereas the rate of isoprene emission is relatively
unaffected by stomatal conductance (Monson and Fall, 1989; Fall and
Monson, 1992), stomatal closure will increase isoprene concentrations inside the leaf at the time when enhanced thermotolerance is needed most. Isoprene concentrations inside leaves of a high isoprene-emitter such as kudzu can exceed 30 µL L1 (Singsaas
et al., 1997).
In the present study we surveyed the effect of isoprene on the
thermotolerance of four isoprene-emitting plant species, kudzu, velvet
bean (Mucuna sp.), quaking aspen (Populus
tremuloides Michx.), and pussy willow (Salix discolor
Muhl.). We used experimental methods analogous to those of Bilger et
al. (1984) and Singsaas et al. (1997) to determine the inflection
temperature of chlorophyll fluorescence from leaf discs in the presence
or absence of 18 to 21 µL L1 exogenously
supplied isoprene. In addition, we measured the effect of exogenous
isoprene on maximum quantum efficiency of PSII photochemistry (Fv/Fm)
in kudzu during an increase in leaf-disc temperature.
| |
MATERIALS AND METHODS |
Kudzu (Pueraria lobata [Willd.] Ohwi.) and velvet
bean (Mucuna sp.; J.L. Hudson, La Honda, CA) seeds were
germinated on moist paper towels and transferred to 19-L pots filled
with 3:1 Growing Mix no. 2 (Farfard, Agawam, MA):perlite. Plants were
grown in a greenhouse exposed to direct full sunlight, watered daily,
and fertilized with a complete nutrient medium three to four times weekly. Quaking aspen (Populus tremuloides Michx.; 1.5 m) and pussy willow (Salix discolor Muhl.; 2 m) trees
were purchased at local nurseries. Trees were grown outdoors, exposed
to direct full sunlight for a portion of the day, watered daily, and
fertilized with Osmocote nutrient pellets (Scotts-Sierra, Marysville,
OH) mixed into the soil medium. Leaf discs from mature, fully developed leaves were used for all of the experiments. During illumination in
room air leaf discs of kudzu, velvet bean, and aspen emitted isoprene
(data not shown; emission from leaf discs of pussy willow was not
determined).
Determination of the TC
The TC, measured as the
temperature at which Fo exhibited an
upward inflection, was determined using a modification of the method
described by Bilger et al. (1984). Whole leaves were collected during
midmorning and adapted to very low light (2 µmol
m2 s1) for between 1 and 6 h on moist paper towels in an unsealed plastic chamber. The
duration of low-light adaptation had no effect on TC (data not shown). Chlorophyll
fluorescence emission was monitored from 2.54-cm2
leaf discs in an LD-2 chamber (Hansatech, King's Lynn, Norfolk, UK)
using a PAM 101 chlorophyll fluorometer (Walz, Effeltrich, Germany;
settings: intensity = 8, gain = 7, damping = 7, and
measuring beam frequency = 1.6 kHz). The fluorescence signal was
recorded with a strip-chart recorder. A port on the leaf chamber was
modified to bring the end of the fiber optics closer to the leaf disc. A nonfunctional platinum/silver electrode covered with Teflon tape was
inserted in the chamber to maintain its seal. The foam spacer commonly
located between metal screens in the chamber during measurements of
O2 evolution was replaced with wadded glass wool to minimize the reaction of isoprene with materials in the chamber. Leaf-disc temperature was controlled by a circulating water bath.
Prior to collecting fluorescence measurements we derived a reproducible
linear relationship between water-bath and leaf-disc temperatures
during increases from 32°C to 56°C. This relationship is described
by the following equation: Leaf temperature = (0.867 × water-bath temperature) + 3.63 (r2 = 0.999; the relationship was derived
from four independent temperature increases). During fluorescence
measurements the rate of leaf-disc temperature increase was
approximately 1.7°C min1. Leaf discs were
exposed to very-low-intensity far-red illumination (less than 1 µmol
m2 s1) from a Hansatech
LS-2 light source with the appropriate filters during measurements to
maintain PSII in the oxidized state (Bilger et al., 1984). Immediately
prior to a measurement, a leaf disc was removed from a
low-light-adapted leaf and placed in the chamber under measuring
conditions (30°C and low-intensity far-red illumination under the
appropriate gas) for 5 min before the temperature increase was
initiated.
To determine the effect of exogenous isoprene on
TC, leaf discs collected from opposite
sides of the leaf midvein were exposed to either a control gas
(compressed air [Singsaas et al., 1997] or
N2) or isoprene in compressed air (18 µL
L1) or N2 (21 µL1)
during measurement. Gases were humidified by passage through a ceramic
diffuser in a flask of distilled water and flowed through the leaf
chamber at a rate of 50 cm3
min1 (chamber volume was approximately 5.5 cm3). All of the tubing used to direct gas from
the cylinders to the measuring chamber was Teflon or glass, with the
exception of two short connecting pieces. Potential effects of temporal artifacts on TC were eliminated by
conducting control and isoprene treatments immediately after one
another and alternating (from leaf to leaf) between conducting the
control or isoprene treatment first. The gas exiting the chamber was
directed into a Fast Isoprene Sensor (Hills Scientific, Boulder, CO;
described by Hills et al., 1991) to verify that the desired isoprene
concentration had been achieved during the experimental treatment. The
Fast Isoprene Sensor was also used to verify that control leaf discs
exhibited no endogenous isoprene production. The "degree of
thermoprotection" is defined as: TC
(isoprene exposure) 
TC (control). Paired
Student's t tests were used determine whether isoprene had
a statistically significant effect on
TC.
Determination of the Thermal Breakpoint of Steady-State
Fluorescence during Exposure to Actinic Light
The temperature at which steady-state fluorescence exhibited an
inflection, defined as the "thermal breakpoint," was measured from
leaf discs of kudzu and velvet bean. Measurements of the thermal
breakpoint were made in N2, in the presence and
absence of 21 µL L1 isoprene, to suppress the
endogenous production of isoprene (Singsaas et al., 1997). The absence
of endogenous isoprene production from control leaf discs in the
presence of pure N2 was confirmed by directing
gas from the chamber outlet into the Fast Isoprene Sensor. Measurements
were made as described above, except that leaf discs received no period
of adaptation to the measurement conditions, measurements were made in
1008 µmol photons m2
s1, and the gas flow rate was reduced
somewhat in the middle of the temperature induction.
Determination of
Fv/Fm
Changes
Fv/Fm
during an increase in leaf-disc temperature, in the presence and
absence of exogenous isoprene, were assessed in kudzu under the
conditions described for the determination of
TC. To measure
Fm, a flashlamp (model KL1500, Walz)
was used to direct a saturating pulse of light (approximately 2500 µmol photons m2 s1)
through the fiber optics to the leaf disc.
| |
RESULTS |
A representative trace of FO
during an increase in leaf-disc temperature from 32°C to 56°C is
presented in Figure 1A. This trace was
measured under conditions defined by Bilger et al. (1984), i.e.
low-light adaptation prior to measurement and weak far-red illumination
during measurement, and allowed for the unambiguous determination of
the TC (Fig. 1A). No leaf isoprene
emission was detected under these conditions (data not shown).
Exogenously supplied isoprene, either 18 µL
L1 in compressed air or 21 µL
L1 in N2, had no
significant effect on the TC of kudzu,
velvet bean, quaking aspen, or pussy willow, all of which are isoprene
emitters (Tables I and
II). The degree of thermoprotection,
TC (isoprene) TC (control), did not differ significantly from
zero in any of the four species (Tables I and II). Therefore,
exogenously supplied isoprene had no measured effect on thermotolerance
under these conditions.
View larger version (15K):
[in this window]
[in a new window]
| Figure 1.
Representative traces of the response of
chlorophyll fluorescence emission to increasing leaf temperature. A,
The response of Fo during exposure to
compressed air (Fo traces during exposure to
N2 as well as room air looked similar). B, The response of
steady-state fluorescence during illumination with 1008 µmol photons
m2 s1 and exposure to N2. The
rate of leaf temperature increase was 1.7°C min1. Both
traces are from kudzu; however, the responses of the other species were
similar. Methods for determining TC and the
thermal breakpoint are exemplified.
|
|
View this table:
[in this window]
[in a new window]
|
Table I.
Tc from leaf discs of four
isoprene-emitting species exposed to compressed air or 18 µL
L1 isoprene in compressed air
Tc was measured as the temperature at which
Fo exhibited an upward inflection (see Fig. 1).
Leaf discs for each replicate measured in compressed air, with and
without isoprene, were collected from opposite sides of the midvein of
the same leaf. Paired Student's t tests examined if the
degree of thermoprotection was different from zero. iso, Isoprene.
SDs are given.
|
|
View this table:
[in this window]
[in a new window]
|
Table II.
Tc from leaf discs of four
isoprene-emitting species exposed to N2, or 21 µL
L1 isoprene in N2
Tc was measured as the temperature at which
Fo exhibited an upward inflection (see Fig. 1).
Leaf discs for each replicate measured in N2, with and
without isoprene, were collected from opposite sides of the midvein of
the same leaf. Paired Student's t tests examined if the
degree of thermoprotection was different from zero. iso, Isoprene.
SDs are given.
|
|
In the studies by Sharkey and Singsaas (1995) and Singsaas et al.
(1997), the most profound effect of exogenous isoprene on chlorophyll
fluorescence was observed during exposure to saturating actinic light
(1000 µmol photons m2
s1). Therefore, we measured the temperature
response of steady-state fluorescence from leaf discs illuminated with
1008 µmol photons m2
s1. These measurements were conducted during
exposure to N2 to suppress endogenous isoprene
production (Monson and Fall, 1989; Sharkey and Singsaas, 1995; Singsaas
et al., 1997). Under these conditions fluorescence inflections were
less apparent and somewhat difficult to interpret (Fig. 1B). During
exposure to approximately one-half full sunlight in
N2, the effect of increasing temperature on
chlorophyll fluorescence cannot be attributed to thylakoid membrane
stability alone; temperature effects on photochemistry, xanthophyll
cycle-dependent energy dissipation, and zeaxanthin-mediated changes in
membrane stability (Havaux, 1998) could also influence the observed
fluorescence traces. In addition, QA is likely to
be highly reduced during exposure to these experimental conditions, and
Bilger et al. (1984) noted the importance of maintaining
QA in the oxidized state during determinations of
TC. Because of these concerns, we
chose to define the temperature of fluorescence inflection measured
under 1008 µmol photons m2
s1 in an N2 atmosphere as
the "thermal breakpoint", as opposed to TC, since the conditions for the
determination of TC were not satisfied. The thermal breakpoint and
TC of kudzu and velvet bean were
similar (Tables II and III). Isoprene
supplied exogenously at 21 µL L1 had no
effect on the thermal breakpoints of these two plant species and
therefore offered no statistically significant enhancement of
thermotolerance (Table III).
View this table:
[in this window]
[in a new window]
|
Table III.
The thermal breakpoint of leaf discs of kudzu and
velvet bean illuminated with 1008 µmol photons m2
s1 and exposed to N2 or 21 µL
L1 isoprene in N2
Thermal breakpoint is defined as the temperature at which steady-state
fluorescence exhibited an upward inflection (see Fig. 1). Leaf discs
for each replicate, with and without isoprene, were collected from
opposite sides of the midvein of the same leaf. Paired Student's
t tests examined if the degree of thermoprotection, defined
here as the (thermal breakpoint in 21 µL L1 isoprene in
N2-thermal breakpoint in N2), was different
from zero. SDs are given.
|
|
Decreases in the
Fv/Fm
of low-light-adapted leaves traditionally have been thought to reflect
damage to the photosynthetic apparatus (Tyystjärvi et al., 1992;
Aro et al., 1994; Osmond, 1994). However, it was recently suggested
that persistent xanthophyll cycle-dependent energy dissipation may also
be involved (Demmig-Adams et al., 1998). Increasing leaf-disc
temperatures resulted in a profound decrease in
Fv/Fm
between 42°C and 50°C (Fig. 2).
Exogenous isoprene at 21 µL L1 had no effect on this
decrease in
Fv/Fm
in kudzu (Fig. 2).
View larger version (36K):
[in this window]
[in a new window]
| Figure 2.
Changes in the
Fv/Fm during an
increase in the temperature of kudzu leaves exposed to N2
(black bars) or 21 µL L1 isoprene in N2
(white bars). The rate of leaf temperature increase was 1.7°C
min1. Error bars represent SD;
n = 3.
|
|
| |
DISCUSSION |
Isoprene supplied exogenously at physiologically realistic
concentrations had no effect on the temperature at which symptoms of
thermal damage to thylakoids appeared (Tables I-III) or on decreases in
Fv/Fm
(Fig. 2) of leaf discs from four isoprene-emitting species subjected to
controlled increases in leaf temperature. Therefore, our observations
do not support the hypothesis that isoprene increases the
thermotolerance of isoprene-emitting plant species.
Our findings differ from those reported by Sharkey and Singsaas (1995)
and Singsaas et al. (1997). We have no certain explanation for this
discrepancy, although there were several differences in the
experimental approaches used that should be noted. Perhaps the most
important difference is that we used leaf discs, whereas detached
intact leaves were used primarily by Sharkey and Singsaas (1995) and
Singsaas et al. (1997). It is possible that a difference in the
physiological effect of a wound resulting from leaf-disc excision
versus leaf detachment underlies the contrasting observations. Wounding
of adjacent leaves has been shown to affect foliar isoprene emission
rate, although that effect included both increases and decreases in
isoprene emission rate, depending on conditions (Loreto and Sharkey,
1993). A second difference was that plants in our study were exposed to
warmer growth temperatures than those of Singsaas et al. (1997; growth
temperatures were not reported by Sharkey and Singsaas, 1995). Our
plants were grown either inside or beside a greenhouse in Boulder,
Colorado, during summer and regularly experienced midday temperatures
above 35°C, whereas maximum air temperatures experienced by the
plants of Singsaas et al. (1997) did not exceed 26°C. Whereas this
may have influenced our results, the need for enhanced thermotolerance
would be greater in warm-grown plants and perhaps should have biased
our results in favor of observing a thermotolerance effect of isoprene.
However, it should be noted that acclimation to warmer growth
temperatures has been shown to lead to lasting biochemical differences,
such as increases in the degree membrane lipid saturation (Pearcy, 1978), which presumably also protect membranes against high temperature damage. Such differences may explain why the fluorescence inflection temperatures we observed were slightly higher than those reported by
Sharkey and Singsaas (1995) and Singsaas et al. (1997). Finally, we
used a rate of leaf temperature increase of 1.7°C
min1, whereas a rate of 1.0°C
min1 was used by Singsaas et al. (1997; rate of
leaf temperature increase was not reported by Sharkey and Singsaas,
1995). As was noted by Sharkey (1996), the volatile nature of isoprene
makes it an ideal molecule to respond to the rapid, almost 10°C
fluctuations in temperature experienced by canopy leaves under some
conditions (Sharkey and Singsaas, 1995). If isoprene emission evolved
to aid plants coping with rapid temperature fluctuations, then our faster rate of leaf temperature increase better approximates relevant environmental conditions and should have also biased our results in
favor of observing a thermotolerance effect of isoprene.
Although the function, if one exists, for isoprene in leaves remains an
open question, we wish to emphasize that the data presented here do not
disprove the thermotolerance hypothesis. They merely serve to weaken
the current experimental evidence for thermotolerance. As was stated in
the introduction, the thermotolerance hypothesis remains quite
compelling because of its ability to explain the subcellular
localization of isoprene synthesis, as well many of the short- and
long-term responses of isoprene emission to the environment. It is
possible that exogenously supplied isoprene, under the conditions
imposed here, does not adequately approximate the effects of endogenous
isoprene production and therefore does not allow for a clear
demonstration of isoprene's role in leaves. Alternative means of
investigating a function for isoprene production could shed light on
this phenomenon.
| |
FOOTNOTES |
1
This study was supported by National Research
Initiative Competitive Grants Program/U.S. Department of Agriculture
award no. 97-35100-4418 and National Science Foundation award no.
DBI9413218.
2
Present address: Department of Biology, Bowdoin
College, Brunswick, ME 04011.
*
Corresponding author; e-mail blogan{at}polar.bowdoin.edu; fax
1-207-725-3405.
Received January 8, 1999;
accepted April 2, 1999.
| |
ABBREVIATIONS |
Abbreviations:
Fo, minimal
chlorophyll fluorescence.
Fv/Fm, ratio of
variable to maximal fluorescence giving the maximum quantum efficiency
of PSII photochemistry .
QA, primary and secondary electron
accepting plastoquinones of PSII.
TC, critical temperature for leaf damage.
| |
ACKNOWLEDGMENTS |
We thank Dr. Peter Harley (Atmospheric Chemistry Division,
National Center for Atmospheric Research) for preparing and quantifying our cylinders of diluted isoprene and Daniel Borchert (North Carolina State University, Raleigh), for providing kudzu seed. This study was improved by valuable discussions with Drs. Barbara Demmig-Adams, Ray Fall, Peter Harley, Manuel Lerdau, Eric Singsaas, and L. Andrew Staehelin.
| |
LITERATURE CITED |
Armond PA,
Björkman O,
Staehelin LA
(1980)
Dissociation of supramolecular complexes in chloroplast membranes: a manifestation of heat damage to the photosynthetic apparatus.
Biochim Biophys Acta
601:
433-442
[Medline]
Aro E-M,
McCaffrey S,
Anderson JM
(1994)
Recovery from photoinhibition in peas (Pisum sativum L.) acclimated to varying growth irradiances.
Plant Physiol
104:
1033-1041
[Abstract]
Bilger H-W,
Schreiber U,
Lange OL
(1984)
Determination of leaf heat resistance: comparative investigation of chlorophyll fluorescence changes and tissue necrosis methods.
Oecologia
63:
256-262
Demmig-Adams B,
Moeller DL,
Logan BA,
Adams WW III
(1998)
Planta
205:
367-374
[CrossRef]
Fall R,
Monson RK
(1992)
Isoprene emission rate in relation to stomatal distribution and stomatal conductance.
Plant Physiol
100:
987-992
[Abstract/Free Full Text]
Havaux M
(1998)
Carotenoids as membrane stabilizers in chloroplasts.
Trends Plant Sci
3:
147-151
Hills AJ,
Fall R,
Monson RK
(1991)
Methods for the analysis of isoprene emission from leaves.
In
H Liskin,
J Jackson,
eds, Modern Methods of Plant Analysis, New Series, Vol 13: Plant Toxin Analysis.
Springer-Verlag, Berlin, pp 297-315
Lerdau M,
Guenther A,
Monson R
(1997)
Plant production and emission of volatile organic compounds.
Bioscience
47:
373-383
[CrossRef]
Loreto F,
Förster A,
Dürr M,
Csiky O,
Seufert G
(1998)
On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex L. fumigated with selected monoterpenes.
Plant Cell Environ
21:
101-107
[CrossRef]
Loreto F,
Sharkey TD
(1990)
A gas-exchange study of photosynthesis and isoprene emission in Quercus rubra L.
Planta
182:
523-531
Loreto F,
Sharkey TD
(1993)
Isoprene emission by plants is affected by transmissible wound signals.
Plant Cell Environ
16:
563-570
Monson RK,
Fall R
(1989)
Isoprene emission from aspen leaves. Influence of environment in relation to photosynthesis and photorespiration.
Plant Physiol
90:
267-274
[Abstract/Free Full Text]
Osmond CB
(1994)
What is photoinhibition? Some insights from comparisons of shade and sun plants.
In
N Baker,
J Boyer,
eds, Photoinhibition of Photosynthesis from Molecular Mechanisms to the Field.
Bios Scientific Publishers, Oxford, UK, pp 1-24
Pearcy RW
(1978)
Effect of growth temperature on the fatty acid composition of leaf lipids in Atriplex lentiformis (Torr.) Wats.
Plant Physiol
61:
484-486
[Abstract/Free Full Text]
Sanadze GA
(1957)
Emission of organic matters by leaves of Robinia pseudaecia L.
Soobsh Acad Nauk GSSR
19:
83
Sanadze GA,
Kursanov AL
(1966)
On certain conditions of the evolution of the diene C5H8 from poplar leaves.
Sov Plant Physiol
13:
184-189
Sharkey TD
(1996)
Emission of low molecular mass hydrocarbons from plants.
Trends Plant Sci
1:
78-82
Sharkey TD, Holland EA, Mooney HA, eds (1991) Trace Gas Emissions
by Plants. Academic Press, San Diego, CA
Sharkey TD,
Loreto F
(1993)
Water stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves.
Oecologia
95:
328-333
[CrossRef]
Sharkey TD,
Singsaas EL
(1995)
Why plants emit isoprene.
Nature
374:
769
Silver GM,
Fall R
(1995)
Characterization of aspen isoprene synthase, an enzyme responsible for leaf isoprene emission to the atmosphere.
J Biol Chem
270:
13010-13016
[Abstract/Free Full Text]
Singsaas EL,
Lerdau M,
Winter K,
Sharkey TD
(1997)
Isoprene increases thermotolerance of isoprene-emitting species.
Plant Physiol
115:
1413-1420
[Abstract]
Tyystjärvi E,
Ali-Yrkkö K,
Kettunen R,
Aro E-M
(1992)
Slow degradation of the D1 protein is related to the susceptibility of low-light grown pumpkin plants to photoinhibition.
Plant Physiol
100:
1310-1317
[Abstract/Free Full Text]
Wildermuth MC,
Fall R
(1998)
Biochemical characterization of stromal and thylakoid-bound isoforms of isoprene synthase in willow leaves.
Plant Physiol
116:
1111-1123
[Abstract/Free Full Text]
Yamane Y,
Kashino Y,
Koike H,
Satoh K
(1997)
Increases in the fluorescence Fo level and reversible inhibition of photosystem II reaction center by high-temperature treatments in higher plants.
Photosynth Res
52:
57-64
Top
Abstract
Introduction
