ARTICLE IN PRESS

Journal of Plant Physiology 162 (2005) 281—289

www.elsevier.de/jplph

High temperature effects on photosynthetic

activity of two tomato cultivars with different
heat susceptibility
Daymi Camejoa, Pedro Rodrı́gueza, Ma% Angeles Moralesb,c,
José Miguel Dell’Amicoa, Arturo Torrecillasb,c,d, Juan José Alarcónb,c,

a
Instituto Nacional de Ciencias Agrı́colas (INCA), Gaveta Postal 1, 32700 San José de Las Lajas, La Habana, Cuba
b
Centro de Edafologı́a y Biologı́a Aplicada del Segura, CSIC, P.O. Box 164, E-30100 Murcia, Spain
c
Unidad Asociada al CSIC de Horticultura Sostenible en Zonas Àridas (UPCT-CEBAS)
d
Dpto. Producción Agraria, ETSIA, Universidad Politécnica de Cartagena (UPCT), Paseo Alfonso XIII s/n, E-30203
Cartagena, Murcia, Spain

Received 3 May 2004; accepted 15 July 2004

KEYWORDS Summary
Carotenoid;
The functional activities of the photosynthetic apparatus of two tomato cultivars of
Electron transport;
different thermotolerance were investigated after a short period of high temperature
Fluorescence;
treatment. Seedlings of two tomato genotypes, Lycopersicon esculentum var.
Photosynthesis;
Campbell-28 and the wild thermotolerant Nagcarlang, were grown under a
Rubisco;
photoperiod of 16 h at 25 1C and dark period of 8 h at 20 1C. At the fourth true
Stomata;
leaf stage, a group of plants was exposed to heat stress of 45 1C for 2 h. The heat
Thermo tolerance;
shock treatment caused important reductions of the net photosynthetic rate (Pn) of
Tomato
Campbell-28 plants due to non-stomatal components. These non-stomatal effects
were not evident in Nagcarlang-treated plants. This reduction in the CO2 assimilation
rate observed in Campbell-28 was generated by affections in the Calvin cycle
and also in the PSII functioning. No changes in these parameters were observed in
the thermotolerant genotype after the stress. Injury to the plasma membrane
because of the heat stress was evident only in the Campbell-28 genotype. Heat led to
a sun-type adaptation response of the photosynthesis pigment apparatus for the
Nagcarlang genotype, but not for Campbell-28, and thus an increase in chlorophyll a/b

Abbreviations: Ci, intercellular CO2 concentration; Fo, initial chlorophyll fluorescence; Fm, maximum chlorophyll fluorescence; Fv,
variable chlorophyll fluorescence; Fv/Fm, maximum photochemical efficiency of Photosystem II in dark adapted leaves; Pn, net
photosynthetic rate; PSII, photosystem II; FPSIIopen, efficiency of the open reaction centre in light; Jmax, maximum electron transport
rate contributing to Rubisco regeneration; LHCPs, light harvesting chlorophyll proteins; Vc, max, maximum carboxylation velocity of
Rubisco
Corresponding author. Centro de Edafologı́a y Biologı́a Aplicada del Segura, (CEBAS-CSIC), P.O. Box 164, Espinardo, Murcia E-30100,
Spain. Tel.: +34 968 396303; fax: +34 968 396213.
E-mail address: jalarcon@cebas.csic.es (J.J. Alarcón).

0176-1617/$ - see front matter & 2004 Elsevier GmbH. All rights reserved.
doi:10.1016/j.jplph.2004.07.014
 ARTICLE IN PRESS
282 D. Camejo et al.

ratio and a decrease in chlorophyll/carotenoid ratio were shown in Nagcarlang

stressed plants.
& 2004 Elsevier GmbH. All rights reserved.

Introduction to obtain new varieties with high tolerance to these

Higher plants, being immobile, have a greater need
of protection against several stresses, including
high or low temperature, water stress, salinity,
metal toxicity, and others. One of the most studied
of these stresses is high temperature, which
provokes severe damage in the photosynthetic
apparatus. Photosynthesis is known to be one of
the most heat-sensitive processes and it can be
completely inhibited by high temperature before
other symptoms of the stress are detected (Berry
and Bjôrkman, 1980).
These photosynthesis decreases could result from
the inhibition of photosystem II (PSII) activity,
which has been shown to be the most thermally
labile component of the electron transport chain
(Quinn and Williams, 1985; Havaux et al., 1991;
Havaux and Tardy, 1996; Havaux et al., 1996). The
inhibition of PSII also leads to a decrease in the
variable chlorophyll fluorescence. Thus, in vivo
chlorophyll fluorescence has been showed to be a
sensitive and reliable method for detection and
quantification of temperature-induced changes in
the photosynthetic apparatus (Krause and Weis,
1991; Govindjee, 1995; Strasser, 1997).
It had been reported that Calvin cycle activity is
also sensitive to rapid heat-stress treatments
(Bilger et al., 1987). There is evidence that
inactivation of Rubisco is an early event in the
inhibition of photosynthesis by high temperature
(Weis, 1981a, b; Kobza and Edwards, 1987; Feller
et al., 1998) and that the inhibition of Rubisco
activase may be a key regulatory process affected
by high temperature-stress.
The inactivation of photosynthesis by high tem-
perature is also related to the damage of the
membrane. According to Blum and Ebercon (1981),
membrane disintegration is a primary symptom of
heat injury. In this sense, the conductivity test,
based on the thermostability of the plasmalemma,
has been proposed as a good indicator of thermo-
tolerance in plants (Shanahan et al., 1990; Ristic
et al., 1996).
The optimum temperatures for tomato cultiva-
tion are between 25 and 30 1C during the photo-
period and 20 1C during the dark period. However,
tomato cultivation is increasing in the tropics and
sub-tropics where high temperature often disturbs
plant establishment. For this reason, it is important
climatic conditions. In our opinion, the differences
in thermotolerance of tomato plants are due mainly
to cellular processes (inhibition of photosystem II
activity, effects of Calvin cycle activity, thermo-
stability of the plasmalemma, role of pigments in
protecting the membrane, etc.). In the present
study, the effects of high-temperature on these
physiological parameters of two tomato genotypes
(Lycopersicon esculentum c.v. Campbell-28 and the
wild thermotolerant type Nagcarlang ) were deter-
mined. Based on this physiological comparison,
insight into the mechanism responsible for differ-
ences in thermo tolerance should be possible.
Material and methods
Plant material and experimental conditions
Seedlings of two tomato genotypes, Lycopersicon
esculentum c.v. Campbell-28 and the wild thermo-
tolerant type Nagcarlang, were grown in pots filled
with silica sand and daily irrigated and fertilized
with half-strength Hoagland’s nutrient solution
(Hoagland and Arnon, 1950).
Plants were grown under a photoperiod of
16 h at 25 1C and a dark period of 8 h at 20 1C.
Irradiance was 350 mmol m
2 s
1 and relative
humidity was 60%.
At the stage of the fourth true leaf, a group of
plants were exposed to temperature stress at 45 1C
during 2 h (45 1C–2 h). Leaf temperature was about
40 1C during the stress in both genotypes. The
plants were light-adapted for 2 h before exposure
to heat stress. Another group, which was main-
tained untreated at 25 1C, served as a control.
Gas-exchange measurements
Gas-exchange measurements (photosynthesis and
stomatal conductance) were taken on the third leaf
using a portable LICOR Li-6200 (LI-COR Inc.,
Lincoln, NE, USA) at the end of heat stress.
Four leaf gas exchange measurements were
made per treatment at each sampling time. The
measurements were made under light conditions
(350 mmol m
2 s
1) at 25 1C immediately after the
stress period.
 ARTICLE IN PRESS
High temperature on tomato
A–Ci response curves
Curves of CO2 assimilation versus intercellular CO2
concentration (A–Ci) were made using a portable
LICOR Li-6400 (LI-COR Inc, Lincoln, NE, USA) and
following the protocol of Long and Bernacchi
(2003). Leaf temperature was fixed to 25 1C. The
intercellular CO2 concentration (Ci ) was varied in
nine steps from 100 to 1000 mmol mol
1, and net
photosynthesis under saturating irradiance
(1800 mmol m
2 s
1) was measured at each step.
At least four points were recorded at Ci p250 to
evaluate the maximum carboxylation velocity of
Rubisco (Vc,max). The maximum electron transport
rates contributing to RuP2 regeneration (Jmax) were
made by fitting a maximum likelihood regression
below and above the inflexion of the A=Ci response.
Fifteen minutes of equilibration were allowed
between changes in Ci before making a measure-
ment. Four curves were made immediately after
the stress period for each genotype and treatment.
Fluorescence measurements
Chlorophyll fluorescence measurements were taken
on the same leaves used for gas-exchange using a
portable fluorometer Opti-Sciences mod. OS 30
(Opti-Sciences Inc., Tyngsboro, MA, USA). Stressed
and control leaves were pre-darkened for 20 min
before starting the experiment. The saturation
pulse to determinate the emission of chlorophyll
fluorescence on the upper surface of the leaf was
2600 mmol m
2 s
1, according to the results ob-
tained previously in light response curves (A-Q).
The initial chlorophyll fluorescence yield, Fo, the
variable chlorophyll fluorescence yield, Fv, and the
maximum chlorophyll fluorescence yield, Fm, were
read in the fluorometer. The maximum photoche-
mical efficiency of PSII in dark-adapted leaves (Fv/
Fm) and nomenclature used were according Van
Kooten and Snel (1990). Efficiency of the open
reaction centre in light (FPSIIopen) was calculated
according to Bilger and Bjôrkman (1990).
Determination of pigment content
The procedure was carried out at 4 1C and dark. A
leaf sample (0.25 g) was mashed in a mortar and
pestle with 80% acetone (v/v), the extract was
filtered through two layers of nylon and centrifuged
in sealed tubes at 15000g for 5 min. The super-
natant was collected and read at 663 and 647 nm
for chlorophyll a and chlorophyll b, respectively,
and at 470 nm for carotenoid content. The con-
centrations for Chlorophyll a, Chlorophyll b, and
283
the sum of leaf carotenoids (xanthophylls and
carotenes) were given in mg ml
1 extract solution
according to the equations of Lichtenthaler and
Buschmann (2001):
Chlorophyll a ¼ 12:25A663
2:79 A647 ;
Chlorophyll b ¼ 21:50A647
5:10 A663 ;
Carotenoid ¼ ð1000 A470
1:82Chl a

95:15lChl bÞ=225:
Measurements of electrolyte leakage
Electrolyte leakage was determined by conductiv-
ity method according to Lafuente et al. (1991).
Leaf segments of uniform maturity were cut in discs
and washed three times with de-ionized water to
eliminate the external residues. Discs were placed
in Erlenmeyer flasks with 20 ml of de-ionized water
and maintained in repose for 20 h. Then, the
conductivity of the solution was read with a
conductivity meter Cyber Scan 200. After that,
the sample was boiled for 15 min in order to kill the
tissues and then the conductivity of this solution
was recorded. The percentage of electrolytes
originally diffused out was calculated as follows:
% electrolyte ¼ C1 =C2  100;
where C1 and C2 are the conductivities of the
solution before and after killing the tissues,
respectively.
Statistical analysis
The experiment was conducted in a completely
randomized design. Gas-exchange, fluorescence,
and electrolyte leakage results are the means of
four independents measurements on different
plants in each treatment. Pigment content results
are the means of six measurements per treatment.
The significance of differences between means
values was determined by one-way analysis of
variance. Duncan’s multiple range test was used
to compare the means when necessary.
Results
The CO2 assimilation rate measured immediately
after the high temperature period was significantly
reduced (50%) in treated plants of Campbell-28,
while tolerant Nagcarlang genotype plants showed
no such modifications after the stress (Fig. 1A).
Under this stress condition, there was no evidence
 ARTICLE IN PRESS
284 D. Camejo et al.

25 50
a A
20 40 Campbell-28
Photosynthesis

30
15 a a
b
20
10

10
5

Photosynthesis
0
0
50
1200
b B Nagcarlang
40
1000
Stomatal conductance

a a 30
800 a

600 20

400 10

200 0

0 200 400 600 800 1000

Campbell-28 Nagcarlang
Intercellular p(CO2)
Figure 1. (A and B) Net photosynthesis
Figure 2. The relationship between net photosynthesis
(mmol CO2 m
2 s
1) and stomatal conductance
(mmol CO2 m
2 s
1) and substomatal CO2 concentration
(mmol m
2 s
1) in leaves of control (white bars) and
(Ci, mmol m
1) in leaves of control (dark points) and
stressed plants (striped bars) of Campbell-28 and
stressed plants (white points) of Campbell-28 and
Nagcarlang. Bars represent the means7SE of four
Nagcarlang. Points represent the means7SE of four
replicates. Means for each genotype that do not have a
replicates.
common letter are significantly different by Duncan’s
test.

of stomatal conductance influencing the inhibition
of CO2 assimilation in Campbell-28 plants (Fig 1B).
Analyses of the A–Ci curves show that Vc,max and
Jmax were similar in both genotypes when no
heating was applied, thus the values of Vc,max were
92.07 and 90.22 mmol m
2 s
1, and the values of
Jmax were 186.86 and 200.01 mmol m
2 s
1 in con-
trol plants of Campbell-28 and Nagcarlang, respec-
tively. However, the effects of heat stress on the
photosynthetic behaviour of both tomato geno-
types were different. The apparent Rubisco activity
and the maximum rate of electron transport were
reduced in Campbell-28 (V c;max ¼ 45:02 and
Jmax ¼ 71:16) and were maintained similar to the
non-stressed plants in Nagcarlang (V c;max ¼ 100:65
and Jmax ¼ 187:70). Considering the behaviour of
Campbell-28, the heat stress had a larger effect on
Jmax than Vc,max; this was reflected in a decrease in
the ratio of Jmax/Vc,max from 2.03 at control
treatment to around 1.58 at heat shock treatment
(see Fig. 2).
High temperature treatment also modified the
chlorophyll fluorescence emission in stressed
Campbell-28 plants. Thus, in this genotype, initial
fluorescence (Fo) values increased (Fig. 3A), while
the values of Fv were reduced in treated plants
(Fig. 3B) at the end of the heat-shock in relation to
the control treatment. Maximum photochemical
efficiency of PSII in dark-adapted leaves, expressed
as Fv/Fm (Fig. 4A), as well as the efficiency of
the open reaction centre of light, expressed as
FPSIIopen (FPSIIopen=Fv0 /Fm0 =(Fm0
Fo)/Fm0 ) (Fig. 4B),
were reduced in the stressed plants of Campbell-28
at the end of the heat shock. Nagcarlang plants
showed no modifications of any of the fluorescence
parameters during the heat-shock treatment (Figs.
3 and 4).
Heat stress altered the chlorophyll and carote-
noid contents in the thermo-tolerant genotype (Fig.
5). An increase in chlorophyll a/b was shown in
Nagcarlang stressed plants (Fig. 5A), which was
mainly caused by an increase in chlorophyll a
 ARTICLE IN PRESS
High temperature on tomato 285

600 1.0
a a
A a A
500 b b
0.8
a
400 a
a
0.6

Fv / Fm
300
Fo

0.4
200

100 0.2

0 0.0

1500 1.0
a a a B a
a B
1200 0.8
b a
b
900 0.6

ΦPSIIopen
Fv

600 0.4

300 0.2

0 0.0
Campbell Nagcarlang Campbell Nagcarlang

Figure 3. (A and B) Initial (Fo) and variable (Fv)
chlorophyll fluorescence yield in leaves of control (white
bars) and stressed plants (striped bars) of Campbell-28
and Nagcarlang. Bars represent the means7SE of four
replicates. Means for each genotype that do not have a
common letter are significantly different by Duncan’s
test.
content and a decrease in chlorophyll b content
(data not shown). The carotenoid content in-
creased during the stress in Nagcarlang, and thus
the chlorophyll/carotenoid ratio decreased signifi-
cantly in Nagcarlang-treated plants with respect to
the control treatment (Fig. 5B).
The functioning of the membrane was also
altered by heat stress. The efflux of electrolytes
significantly increased in the stressed Campbell-28
plants (Fig. 6). However, in Nagcarlang no mod-
ifications to membrane permeability were observed
after the heat-shock treatment (Fig. 6).
Discussion
According to von Caemmerer and Farquhar (1981),
changes in the net rate of CO2 assimilation reflect
alterations in both stomatal conductance and/or
mesophyll capacity for photosynthesis. In our case,
the decrease in CO2 assimilation observed in the
Figure 4. (A and B) Maximum photochemical efficiency
of PSII in dark adapted leaves (Fv/Fm) and efficiency of
the open reaction centre (FPSIIopen) in leaves of control
(white bars) and stressed plants (striped bars) of Camp-
bell-28 and Nagcarlang. Bars represent the means7SE of
four replicates. Means for each genotype that do not
have a common letter are significantly different by
Duncan’s test.
heat-treated Campbell-28 plants (Fig. 1A) was not
attributable to stomatal limitation; in fact, an
increase in stomatal conductance was observed in
stressed plants of this genotype relative to control
plants (Fig. 1B). Leaf transpiration and internal CO2
concentration also increased with high tempera-
ture treatment (data not shown). Leonardos et al.
(1996) and Law and Crafts-Brandner (1999) re-
ported a similar relationship between leaf tem-
perature and stomatal conductance working with
cotton and wheat. The increase in the stomatal
conductance observed in treated plants of Camp-
bell-28 indicated that the reduction in CO2 assim-
ilation during the stress was not limited by stomatal
closure, but by alterations on mesophyll capacity,
which depend on the activity of Rubisco and on the
capacity of photosynthetic electron transport to
regenerate Rubisco (Crafts-Brandner et al., 1997;
Eckardt and Portis, 1997; Feller et al., 1998).
The initial slope of the A–Ci curves, sometimes
called ‘‘carboxylation efficiency’’ (Ku and Edwards,
 ARTICLE IN PRESS
286 D. Camejo et al.

5 1977), indicates limitations on RuP2 carboxylase

A activity. Several authors have derived equations to
b predict that the initial slopes of the A–Ci curves,
Chlorophyll a / Chlorophyll b

4
and thus the coefficient Vc,max calculated from the
a curve to low intercellular p(CO2), describe the rate
3 a a of carboxylation limited by RuP2 activation. In our
case, Vc,max was reduced in Campbell-28 stressed
2 plants but it was not altered by the heat shock in
Nagcarlang (Fig. 2).
The coefficient Jmax, which is calculated from the
1
curve to high p(CO2) and describes the rate of
carboxylation limited by capacity of photosynthetic
0 electron transport to regenerate RuP2, was also
8
reduced by high temperature in Campbell-28
a a although it was not significantly modified by the
a B
7 heat stress in Nagcarlang (Fig. 2).
All of these results confirm that PSII and Calvin
Chlorophyll / Carotenoid

6
b
cycle activities were affected by heat temperature
5 in Campbell-28 genotype, while in Nagcarlang they
4
were not modified. It is noted that the modifica-
tions on photochemical reactions were more severe
3 than those found on the RuP2 carboxylase activity,
2
however it is not easy to quantify the effects of
both modifications on the total photosynthetic
1 capacity. Usually, about half of the PSII complex
0
must be inactivated before photosynthetic capacity
Campbell Nagcarlang becomes limited (Heber et al., 1988; Öquist and
Malmber, 1989; How-Yeon et al., 1999). However,
Figure 5. (A and B) Chlorophyll a/b ratio and chlor- previous reports have documented that a slight
ophyll/carotenoid ratio in leaves of control (white bars)
inactivation of the Rubisco is closely correlated
and stressed plants (striped bars) of Campbell-28 and
Nagcarlang. Bars represent the means7SE of four
with temperature-induced changes in the CO2
replicates. Means for each genotype that do not have a assimilation rate (Feller et al., 1998; Law and
common letter are significantly different by Duncan’s Crafts-Brandner, 1999).
test. The effects provoked by heat stress on the
photosynthetic apparatus of Campbell-28 plants
were also evidenced through analysis of chlorophyll
fluorescence. Functional and structural damages on
60
PSII were achieved in heat-stressed plants of
b
Campbell-28, thus the increase of Fo value ob-
50
served in treated plants (Fig. 3A) was presumably
Electrolyte leakage (%)

related to alterations in the capacity to trap energy

40
(Havaux, 1993). These alterations were also
30
noticed through the Fv reduced values (Fig. 3B),
a indicating a reduction in the number of open PSII
20 a units (Björkman, 1987; Snel et al., 1991), which are
a presumably generated by a slow reoxydation of the
10 electron transfer chain intermediates.
High temperature reduced the Fv/Fm ratio (Fig. 4A)
0 and FPSIIopen (Fig. 4B), indicating that an important
Campbell Nagcarlang portion of the PSII reaction centre was damaged.
Figure 6. Electrolyte leakage (%) in leaves of control
These damages are associated with structural mod-
(white bars) and stressed plants (striped bars) of Camp- ifications on PSII, especially in D1 protein, which in
bell-28 and Nagcarlang. Bars represent the means7SE of conditions of heat stress is phosphorylated and
six replicates. Means for each genotype that do not have degraded afterwards (Asada et al., 1998).
a common letter are significantly different by Duncan’s The increase of the chlorophyll a/b ratio and the
test. decrease of the chlorophyll/carotenoid ratio in
 ARTICLE IN PRESS
High temperature on tomato
stressed Nagcarlang plants (Figs. 5A and 5B) suggest
that these relationships could be used as an indicator
of tolerance and physiological status of the plants
under these stress conditions. Increases in the ratio Chl
a/b are always associated with a change in pigment
composition of the photosynthesis apparatus towards a
more sun-type like chloroplast which possesses less
light harvesting chlorophyll proteins (LHCPs). The
decrease in the light absorption cross section of
chloroplasts by decreasing the LHCPs amounts is an
essential protection mechanism of chloroplasts, leaves
and plants, which allows them to survive unfavourable
conditions. This high-light response is given, not only
by changes in the irradiation under which the
plants are grown, but also by diverse chemicals or
stressors, such as heat and water stress, that are
often associated with long-term high-light stress
(Lichtenthaler et al., 2000). Sun-type and high-light
chloroplasts are known to also posses a higher
carotenoid content on a chlorophyll basis than
medium-light or low-light chloroplasts, which is
indicated by lower values for the ration of chlorophylls
(a þ b) to carotenoids (x þ c) (Lichtenthaler et al.,
1981, 1982). In this experiment, heat led to a sun-type
adaptation response of the photosynthesis pigment
apparatus for the Nagcarlang genotype but not for
Campbell-28 (Fig. 5). Nagcarlang plants, grown at a
medium irradiance, responded to heat stress by a
decrease in their LHCPs amounts, which is a protection
mechanism to avoid photooxidation and photoinhibi-
tion (Licthenthaler and Burkart, 1999). In addition, it is
well documented that carotenoids, which increased in
the heat-treated Nagcarlang plants, not only play a
role as accessory light-harvesting pigments but they
also protect photosynthetic systems against reactive
oxygen species (Young, 1991; Asada et al., 1998;
Loggini et al., 1999).
We also were interested in knowing whether the
structural integrity of the membrane was affected
by high temperature and whether it was related to
thermo-tolerance. An increase in electrolyte leak-
age was observed in stressed Campbell-28 plants
(Fig. 6), indicating alterations in the permeability
of the membranes and a reduction in their ability to
retain solutes and water due to high temperature.
However, in the tolerant genotype Nagcarlang, the
permeability of the membrane was not modified by
heat-shock treatment (Fig. 6), indicating the
maintenance of its functioning. The leakage of
electrolytes through the plasmalemma has been
often related to photosynthetic and mitochondrial
activity reductions in plant cells (Shanahan et al.,
1990; Ristic et al., 1996). Inefficient functioning of
the membranes have been found in different
species and under several stress condition (Cheng-
kun et al., 1996; Dı́az et al., 1996; Schmidty and
287
González, 1998; Karim et al., 1999). In our
experiment the loss of integrity of the membranes
was associated with the sensitivity of the genotype
to high temperatures.
In summary, the comparison of two tomato
genotypes of different heat susceptibility per-
mitted determining that the tolerance or sensitivity
to heat was clearly manifested throughout the
photosynthetic activity. The short exposure to heat
stress provoked important reductions in photo-
synthesis in Campbell-28, while Nagcarlang was
not affected. This reduction in the CO2 assimilation
rate observed in Campbell-28 was generated by
affections in the Calvin cycle and also in the PSII
functioning. We propose that the pigments content
of the light harvesting complex is an important
aspect related to the tolerance of tomato plants to
high temperatures. The loss of integrity of the
membranes was also associated with the thermo-
tolerance of tomato plants.
Acknowledgements
This work was supported by ‘‘Convenio de Coopera-
ción Cientı́fica Hispano-Cubano del CSIC-CITMA’’
(2001CU0015).
References
Asada K, Endo T, Mano J, Miyake C. Molecular mechanism
for relaxation of and protection from light stress.
Saton K, Murata N editors. Stress responses of
photosynthetic organisms. Amsterdam: Elsevier;
1998. p. 37–52.
Berry J, Björkman O. Photosynthetic response and
adaptation to temperature in higher plants. Annu
Rev Plant Physiol 1980;31:491–543.
Bilger W, Björkman O. Role of the xanthophylls cycle in
photoprotection elucidated by measurements of light-
induced absorbance changes, fluorescence and photo-
synthesis in leaves of Hedera canariensis. Photosynth
Res 1990;25:173–86.
Bilger W, Schreiber U, Lange OL. Chlorophyll fluorescence
as an indicator of heat induced limitation of photo-
synthesis Arbutus unedo L. In: Tenhunen JD, Catarino
FM, Lange OL editors. Plant Response to Stress. Berlin:
Springer; 1987. p. 391–9.
Björkman O. Low temperature chlorophyll fluorescence
in leaves and its relationship to photon yield of
photosynthesis in photoinhibition. In: Kyle DJ, Osmond
CB, Arntzen CJ editors. Photoinhibition. Amsterdam:
Elsevier; 1987. p. 123–34.
Blum A, Ebercon A. Cell membrane stability as a measure
of drought and heat tolerance in wheat. Crop Sci 1981;
21:43–7.
 ARTICLE IN PRESS
288
Crafts-Brandner SJ, van de Loo FJ, Salvucci ME. The
two forms of ribulose-1,5-bisphosphate carboxylase/
oxygenase activase differ in sensitivity to elevated
temperature. Plant Physiol 1997;114:439–44.
Chengkun H, Suzhi G, Jiasen L. Effects of drought stress
on activated oxygen metabolism in tomato. J Fujian
Agr Univ 1996;25(3):307–11.
Dı́az P, Rodrı́guez M, Cornide MT, Coto O, Ruiz A, Niubo E,
Mitchel E, Maribona RH, Barquie O, Leonard H,
Sánchez C. Indicadores fisiológicos y bioquı́micos para
la evaluación de la osmotolerancia en caña de azùcar.
In: Resùmenes X Seminario Cientı́fico. INCA. Cultivos
Tropicales 1996;17(3):125.
Eckardt NA, Portis Jr. AR. Heat denaturation profiles of
ribulose-1,5-bisphosphate carboxylase/oxidase (Ru-
bisco) and Rubisco activase and the inability of
Rubisco activase to restore activity of heat-denatured
Rubisco. Plant Physiol 1997;113:243–8.
Feller U, Crafts-Brandner SJ, Salvucci ME. Moderately
high temperature inhibits ribulose-1,5-bisphosphate
carboxylase/oxygenase (Rubisco) activase-mediated
activation of Rubisco. Plant Physiol 1998;116:
539–46.
Govindjee. Sixty-three years since Kautsky: chlorophyll
a fluorescence. Aust J Plant Physiol 1995;22:
131–60.
Havaux M. Characterization of thermal damage to the
photosynthetic electron transport system in potato
leaves. Plant Sci 1993;94:19–33.
Havaux M, Greppin H, Strasser R. Functioning of photo-
system I and II in pea leaves exposed to heat stress in
the presence or absence of light. Analysis using in vivo
fluorescence, absorbance, oxygen and photoacoustic
measurements. Planta 1991;186:88–98.
Havaux M, Tardy F. Temperature-dependent adjustment
of the thermal stability of photosystem II in vivo:
possible involvement of xanthophylls content. Plant
Cell Environ 1996;19:1359–68.
Havaux M, Tardy F, Rayenel J, Chanu D, Parot P. Thylakoid
membrane stability to heat stress by flash spectro-
scopic measurements of the electrochromic shift in
intact potato leaves: Influence of the xanthophyll
content. Plant Cell Environ 1996;19:1359–68.
Heber U, Neimanis S, Dietz KJ. Fractional control of
photosynthesis by the QB protein, the cytochrome f/b6
complex and other components of the photosynthetic
apparatus. Planta 1988;173:267–74.
Hoagland DR, Arnon DI. The water-culture method for
growing plants without soil. Univ Calif Agric Exp Stat
Circ 1950;347
How-Yeon L, Wah Soon C, Young-Nam H. Photoinactiva-
tion of photysystem II in leaves of Capsicum annuum.
Physiol Plant 1999;105:377–84.
Karim MA, Fracheboud Y, Stamp P. Photosynthetic activity
of developing leaves of Zea mays is less affected by
heat stress than that of development leaves. Physiol
Plant 1999;105:685–93.
Kobza J, Edwards GE. Influences of leaf temperature on
photosynthetic carbon metabolism in wheat. Plant
Physiol 1987;83:69–74.
D. Camejo et al.
Krause G, Weis E. Chlorophyll fluorescence and photo-
synthesis: The basics. Annu Rev Plant Physiol Plant Mol
Biol 1991;42:313–49.
Ku S, Edwards G. Oxygen inhibition of photosynthesis. II.
Kinetic characteristics as affected by temperature.
Plant Physiol 1977;59:991–9.
Lafuente MT, Belver A, Guye MG, Salveit ME. Effect of
temperature conditioning on chilling injury of cucum-
ber cotyledons–posible role of abscisic acid and heat-
shock proteins. Plant Physiol 1991;95:443–9.
Law RD, Crafts-Brandner SJ. Inhibition and acclimation of
photosynthesis to heat stress is closely correlated with
activation of ribulose-1,5-bisphosphate carboxylase/
oxygenase. Plant Physiol 1999;120:173–81.
Leonardos ED, Tsujita MJ, Grodzinski B. The effect of
source or sink temperature on photosynthesis and 14C
partitioning in and export from a source leaf of
Alstroemeria. Physiol Plant 1996;97:563–75.
Lichtenthaler HK, Babani F, Langsdorf G, Bushcmann C.
Measurement of differences in red chlorophyll fluor-
escence and photosynthetic activity between sun and
shade leaves by fluorescence imaging. Photosyntheti-
ca 2000;38(4):521–9.
Licthenthaler HK, Burkart S. Photosynthesis and high light
stress. Bulg J Plant Physiol 1999;25(3-4):3–16.
Lichtenthaler HK, Buschmann C. Chlorophylls and
carotenoids–Measurement and characterization by
UV-VIS. In: Lichtenthaler HK editor. Current Protocols
in Food Analyticial Chemistry (CPFA), (Supplement 1).
New York: Wiley; 2001.
Lichtenthaler HK, Buschmann C, Döll M, Fietz HJ, Bach T,
Kozel U, Meier D, Rahmsdorf U. Photosynthetic
activity, choroplast ultrastructure, and leaf charac-
teristics of high-light and low-light plants and of sun
and shade leaves. Photosynth Res 1981;2:115–41.
Lichthenthaler HK, Kuhn G, Prenzel U, Buschmann C,
Meier D. Adaptation of chloroplast-ultrastructure and
of chlorophyll-protein levels to high-light and low-light
growth conditions. Z Naturforsch 1982;37:464–75.
Loggini B, Scartazza A, Brugnoli E, Navari-Izzo F.
Antioxidant defecnse system, pigment composition
and photosynthetic efficiency in two wheat cultivars
subjected to drought. Plant Physiol 1999;119:1091–9.
Long SP, Bernacchi J. Gas exchange measurements, what
can they tell us about the underlying limitations to
photosynthesis? Procedures and sources of error. J Exp
Bot 2003;54:2393–401.
Öquist G, Malmber G. Light and temperature dependent
inhibition of photosynthesis in frost-hardened and un-
hardened seedlings of Pine. Photosynth Res 1989;20:
261–77.
Quinn PJ, Williams WP. Environmentally induced changes
in thylakoid membranes and their effect on photo-
synthetic function. In: Barber J, Baker NR editors.
Photosynthetic Mechanisms and the Environment.
Amsterdam: Elsevier; 1985. p. 1–47.
Ristic Z, Williams G, Yang G, Martin B, Fullerton S.
Dehydration, damage to cellular membranes, and
heat-shock proteins in maize hybrids from different
climates. J Plant Physiol 1996;149:424–32.
 ARTICLE IN PRESS
High temperature on tomato
Schmidty A, González V. Medición de conductividad
eléctrica en discos de hojas y estudio morfológico de
callos de cuatro variedades de caña de azùcar
(Saccharum spp.) bajo condiciones de estrés salino.
In: Resùmenes II Encuentro Latinoamericano de
Biotecnologı́a Vegetal. Redbio ’98, 1998. p. 345.
Shanahan JF, Edwards IB, Quick JS, Fenwick JR. Mem-
brane thermostability and heat tolerance of spring
wheat. Crop Sci 1990;30:247–51.
Snel JFH, van Kooten O, van Hove LWA. Assessment of
stress in plants by analysis of photosynthetic perfor-
mance. Trac-Trends Anal Chem 1991;10:26–30.
Strasser BJ. Donor side capacity of photosynthesis II
probed by chlorophyll a fluorescence transients.
Photosynth Res 1997;52:147–55.
289
Van Kooten O, Snel FH. The use of chlorophyll fluores-
cence nomenclature in plant stress physiology. Photo-
synth Res 1990;25:147–50.
Von Caemmerer S, Farquhar GD. Some relationships
between the biochemistry of photosynthesis and the
gas exchange of leaves. Planta 1981;153:376–87.
Young A. The photoprotective role of carotenoids in
higher plants. Physiol Plant 1991;83:702–8.
Weis E. Reversible heat-inactivation of the Calvin cycle: a
possible mechanism of the temperature regulation of
photosynthesis. Planta 1981a;151:33–9.
Weis E. The temperature sensitivity of dark-inactivation
and light-activation of the ribulose-1,5-bisphosphate
carboxylase in spinach chloroplasts. FEBS Lett 1981b;
129:197–200.