High-Temperature Sensitivity and Its Acclimation for Photosynthetic Electron Transport Reactions of Desert Succulents' - Plant Physiology
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Plant Physiol. (1987) 84, 1063-1067
0032-0889/87/84/1063/05/$0 1.00/0
High-Temperature Sensitivity and Its Acclimation for
Photosynthetic Electron Transport Reactions of Desert
Succulents'
Received for publication November 21, 1986 and in revised form April 6, 1987
MAHADEV B. CHETTI2 AND PARK S. NOBEL*
Department ofBiology and Laboratory of Biomedical and Environmental Sciences, University of
California, Los Angeles, California 90024
ABSTRACT grown at day/night temperatures of 20°C/l 5C and treated for
10 min at 50°C, whole chain electron transport is reduced by
Photosynthetic electron transport reactions of succulent plants from about 65% (5). For chloroplasts isolated from Opuntia polyacan-
hot deserts are able to tolerate extremely high temperatures and to tha grown at moderate day/night temperatures (25°C/1 5°C), the
acclimate to seasonal increases in temperature. In this study, we report rates of the Hill reaction and NADP reduction decrease above
the influence of relatively long, in vivo, high-temperature treatments on about 40°C (8).
electron transport reactions for two desert succulents, Agave deserti and CAM succulents from hot deserts tolerate the highest tissue
Opuntia ficus-indica, species which can tolerate 60°C. Whole chain temperatures among the higher vascular plants (21, 26). Yet
electron transport averaged 3°C more sensitive to a 1-hour high-temper- high-temperature tolerances and their acclimation to increasing
ature treatment than did PSII (Photosystem II) which in turn averaged growth temperatures have not been systematically investigated
3°C more sensitive than did PSI. For plants maintained at day/night air for the photosynthetic electron transport reactions of such plants.
temperatures of 30°C/20°C, treatment at 50°C caused these reactions to Most previous studies on the susceptibility of electron transport
be inhibited an average of 39% during the first hour, an additional 31% reactions to high temperature have been done using isolated
during the next 4 hours, and 100% by 12 hours. Upon shifting the plants chloroplasts that were treated for relatively short periods (24, 25,
from 30°C/20°C to 45°C/35°C, the high temperatures where activity was 28, 30). Because chloroplasts once isolated can respond differ-
inhibited 50% increased 3°C to 8°C for the three electron transport ently to heating than when in the intact tissue (22), in the present
reactions, the half-times for acclimation averaging 5 days for A. deserti study the intact tissue was subjected to the high temperature
and 4 days for 0. ficus-indica. For the 45°C/35°C plants treated at 60°C before the chloroplasts were isolated. Moreover, the potential for
for 1 hour, PSI activity was reduced by 54% for A. deserti and 36% for the electron transport reactions to acclimate to higher growth
0. ficus-indica. Acclimation leads to a toleration of very high tempera- temperatures has received little attention and has not been
tures without substantial disruption of electron transport for these desert previously investigated for desert succulents. To test for accli-
succulents, facilitating their survival in hot deserts. Indeed, the electron mation, the plants were shifted from moderate air temperatures
transport reactions of these species tolerate longer periods at higher to high air temperatures and changes in PSI, PSII, and whole
temperatures than any other vascular plant so far reported. chain electron transport were measured for chloroplast mem-
branes. Both the temperatures leading to 50% inhibition of these
reactions and the kinetics of inhibition at 50°C were examined.
MATERIALS AND METHODS
Plant Material. Medium-sized plants of Agave deserti Engelm.
Tissue temperatures of desert succulents in their natural hab- (Agavaceae) and single mature cladodes (flattened ovoid stem
itats can be 10 to 22°C higher than ambient air temperatures (7, segments) of Opuntia ficus-indica (L.) Miller (Cactaceae) were
27). The highest nonlethal temperatures recorded are over 60°C planted in loamy sand and maintained in environmental growth
for various species of agaves (20, 21) and Opuntia (6, 16, 26), chambers at day/night air temperatures of 30°C/20°C or 45°C/
although most physiological processes are impaired when tissue 35°C. PAR from 400 to 700 nm (measured with a LI-COR LI-
temperatures of higher plants exceed 50°C (18). Moreover, the 190S quantum sensor) averaged 400 ,mol m-2 s-' in the planes
high temperatures tolerated by agaves and cacti increase in of the photosynthetic surfaces for a 12 h photoperiod. The
response to increasing growth temperatures (20, 21, 26). relative humidity averaged 40% during the daytime and 60% at
Electron transport reactions associated with thylakoid mem- night,. and the CO2 content of the air was 350 ql L'. The plants
branes are more sensitive to high temperature than are soluble were watered with one-tenth strength Hoagland solution No. 1
enzymes in chloroplasts (5, 25). As treatment temperatures are (12) so that the soil water potential in the root zone was -0.2 ±
increased substantially, the rate of electron transport mediated 0.2 MPa.
by PSI can increase while that mediated by PSII decreases (1, 4, High Temperature Treatment and Chloroplast Isolation. The
22, 28). For chloroplasts isolated from leaves of Nerium oleander sensitivity of photosynthetic electron transport reactions to high
temperature was routinely measured by immersing mature shoot
'Supported by the Ecological Research Division of the Department pieces (sealed in plastic bags) in water baths maintained at
of Energy, Contract DE-AC03-76-SFOO012. particular temperatures ±+1C for 1 h before isolating the chlo-
2 Supported by a postdoctoral fellowship from the Ministry of Educa- roplasts. Chloroplasts were isolated at 0°C employing procedures
tion and Culture, Government of India. similar to those previously used for cacti (8).
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Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.[0~ W
1064 CHETTI AND NOBEL Plant Physiol. Vol. 84, 1987
Chlorenchyma tissue was removed using a sharp razor blade chain electron transport activity was inhibited by 20% at 40°C
and cut into small pieces while immersed in isolation medium for 30°C/20°C plants, no inhibition occurring for 45°C/35°C
(50 mm Tricine-KOH [pH 8.1], 400 mm sorbitol, 10 mm KCl, 5 plants at that temperature (Fig. IC). Greater inhibitions in the
mM EDTA, 5 mM MgC92, 2 mM Na-ascorbate, and 0.5 mg/ml activities of PSI, PSII, and WC electron transport were observed
BSA; all chemicals were obtained from Sigma). Approximately at treatment temperatures above 40°C for 30°C/20°C plants
15 ml of isolation medium was used per gram of chlorenchyma compared with 45°C/35°C plants; for example, 60°C treatment
tissue. To maximize chloroplast stability (11), the isolation me- resulted in 70% inhibition of PSI for 30°C/20°C plants compared
dium was vacuum-infiltrated into the cut pieces, which were with 54% inhibition for 45°C/35°C plants. The half-inactivation
then homogenized in a Waring blender for 20 s (A. deserti) or temperatures were 49°C for WC electron transport, 5 1°C for
15 s (O. ficus-indica). The homogenate was squeezed through six PSII, and 54°C for PSI for 30°C/20°C plants, increasing to 52,
layers of muslin cloth, the filtrate was centrifuged at IOOOg for 56, and 59°C, respectively, for 45°C/35°C plants. About 14% of
15 s to remove whole cells and starch, and the supernatant fluid PSI activity was still present after treating pieces of 45°C/35°C
was centrifuged at 3000g for 5 min (all centrifugations were plants for 1 h at 70°C (Fig. IA).
performed using a Sorvall RC-5B refrigerated superspeed centri- For Opuntiaficus-indica, the rates of all the electron transport
fuge with an SS-34 rotor). The resulting pellet was resuspended reactions were about 20% higher than for A. deserti, but the
in distilled water (with 1 mg/ml of BSA) to rupture the chloro- relative patterns of temperature responses were similar (Fig. 2).
plasts. The Chl concentration (2) was about 2 mg/ml. Chloroplast PSI was again least sensitive to high temperatures, PSII was
membranes prepared in this manner did not differ in their intermediate, and WC electron transport was most sensitive. The
capacity for electron transport for at least 2 h, within which time 45°C/35°C plants were less sensitive to temperatures above 40°C
all measurements were completed. The data presented are rep- than 30°C/20°C plants (averages of 60°C versus 54°C for 50%
resentative of at least two separate experiments that gave results inhibition of the three electron transport reactions); for instance,
within 0.4C of each other for the 50% inhibition temperatures. inhibition of PSI and PSII activities was clearly evident at 50°C
Measurement of Photosynthetic Electron Transport. PSI activ- for 30°C/20°C plants but not for 45°C/35°C plants (Fig. 2, A and
ity was determined as oxygen uptake with the Na ascorbate- B). 0. ficus-indica was more tolerant of high temperatures than
DCPIP3 couple as the electron donor and MV as the electron A. deserti, with very little inhibition occurring at 50°C and with
acceptor, basically as described previously (24). 02 was measured PSI retaining 23% of its maximal activity at 70C for 45°C/35°C
polarographically with a Yellow Springs Instrument Clark-type plants (Fig. 2A).
electrode. The assay mixture contained 50 mm Tricine-KOH Upon changing growth temperatures from 30°C/20°C to 45°C/
(pH 8.1), 5 mM MgCl2, 5 mm KCI, 3 mM NaHCO3, 5 mM Na- 35°C, full acclimation was completed within 15 d for all three
ascorbate, 0.1 mm DCPIP, 0.01 mM DCMU, 0.5 mM MV, 1 mM electron transport reactions for both species (Fig. 3). The half-
sodium azide (prepared daily), 3000 units of superoxide dismu-
tase from bovine liver, and chloroplast membranes equivalent to
40 ,g Chl in 4.0 ml. The suspension was illuminated with a 300- 2!o A Agavme deserti
W, cool-beam, incandescent light filtered through 20 cm of 0.1% .-
CuS04 solution to remove infrared and ultraviolet. The PAR on a) I
the reaction vessel with a 1-cm light path length was 1200 Mmol - V 81 |0
== >dS ~~~~PSI
m -2 s- , which was saturating for PSI activity. The initial steady 0. bv"45/ 35
rate of 02 uptake at 25°C was recorded using a Perkin-Elmer 165 NE
recorder. .5
4PO 30/2\
The rate of photoreduction of DCPIP was used to measure 1
PSII activity under the same temperature and PAR conditions 'a
as for PSI. The assay mixture contained 40 mm Tricine-KOH w -
(pH 8.1), 5 mM MgCl2, 2 mM K2HPO4, 10 mM KCI, 30 Mm 61
DCPIP, and chloroplast membranes equivalent to 7 Mug Chl in Q) PSI[
1.0 ml. The decrease in DCPIP absorbance at 590 nm upon bu 7
4 12
illumination of the chloroplast membrane suspension for 30 s
was measured with a Beckman DU-7 spectrophotometer. A -E
molar extinction coefficient of 15,960 M-' cm-' at 590 nm for 0 -
DCPIP was used to calculate the activity (22). 0.
a)
E
Electron transport from water to MV, here designated WC
electron transport, was measured similarly to previous studies
(1). The assay medium contained 50 mM Tricine-KOH (pH 8.1), 6;o -C
5 mM MgCl2, 6 mm NH4CI, 1 mm sodium azide (prepared daily), .-
:E
1 mm MV, and chloroplast membranes; the volume, Chl level, cav I
-- hole c ha in
temperature, and PAR were the same as for the PSI assay. The 0 T=
_
E
oxidation of MV was measured as the initial steady rate of 02 OL
uptake with the Clark-type 02 electrode. 2
RESULTS E
z
OW. 1 X I_
For Agave deserti, whole chain electron transport was more 10 20 30 40 50 60 70 80
sensitive to high temperatures than was PSII, which in turn was
more sensitive than PSI (Fig. 1). PSI and PSII activities were Treatment temperature (OC)
actually similar for treatment temperatures from 10 to 40°C for FIG. 1. Effect of temperature treatment in vivo for 1 h on (A) PSI
both 30°C/20°C and 45°C/35°C plants (Fig. 1, A and B). Whole (DCPIPH2 -+ MV), (B) PSII (H20 DCPIP), and (C) WC (H20
-* -*
MV) electron transport reactions of chloroplasts isolated from A. deserti
3 Abbreviations: DCPIP, 2,6-dichlorophenol indophenol; MV, methyl maintained for at least 2 weeks under day/night air temperatures of
viologen; WC, whole chain. 30°C/20°C (0-O) or 45'C/35°C (A -- A). -
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Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.HIGH-TEMPERATURE SENSITIVITY OF ELECTRON TRANSPORT REACTIONS 1065
160
-c
C)
0
0. 0'
U
a r- 0
E
_ C
c
E
.0
E I..
0-
6. _
c
-~ G')
al - 0.
CI
U) _ a.
0' 0
n E
-o - cl
C U
E
L. .
-5 5 10
c E Time at 450C/35°C (days)
FIG. 3. Time course of high temperature acclimation for PSI (5-
0), PSII (A - - - A), and whole chain (O.... 0) electron transport
(V reactions of chloroplasts isolated from A. deserti (A) or 0. ficus-indica
o-*-_E (B). The high temperatures leading to 50% inhibition of these reactions
relative to controls treated at 35°C (Figs. 1 and 2) were determined at
various times after transferring to 45°C/35°C plants that had been main-
;j tained for at least 2 weeks at 30°C/20°C.
Treatment temperature ('IC)
FIG. 2. Effect of temperature treatment in vivo for 1 h on (A) PSI,
(B) PSII, and (C) WC electron transport reactions of chloroplasts isolated
from 0. ficus-indica maintained for at least 2 weeks under day/night air
temperatures of 30°C/20°C (O-O) or 45°C/35'C (A - -- A).
times for the shifts in the temperatures for 50% inhibition of
PSI, PSII, and whole chain electron transport were 4, 5, and 6 d,
respectively, for A. deserti and 3, 3, and 5d, respectively, for 0.
ficus-indica (Fig. 3). The half-times for the lowering of the high
temperature for 50% inhibition of the electron transport reac- o 40 A
tions were similar when the plants were shifted from 45°C/35°C
to 30°C/20°C (data not shown). Specifically, for PSI, PSII, and
WC electron transport, the half-times were 4, 5, and 5d, respec- C) 20 -
4 8/S
tively, for A. deserti and 4 d for all three reactions for 0. ficus-
indica.
The kinetics of temperature inhibition at a treatment temper-
ature of 50°C were also studied for the three electron transport
o v~~~~~~~~~~~~~o
reactions for 30°C/20°C plants (Fig. 4). The rate of inhibition 60 .
was highest during the first hour, averaging 44% for A. deserti
and 34% for 0. ficus-indica. During the next 4 h, the additional
inhibition averaged 32% for A. deserti and 30% for 0. ficus-
indica (Fig. 4). After 12 h at 50°C, 100% inhibition of PSI, PSII,
and WC electron transport occurred for both species. imecouse or he nhiitin o PS (ficu-indPico
FIG.4. (A-
DISCUSSION 20 l-I
A
The temperature sensitivity varied with the electron transport O 2 3 4 5
reactions considered, PSI being more tolerant of high tempera-
tures than PSII which in turn was more tolerant than WC Time at 50° C (h)
electron transport. The optimal temperatures for PSI, PSII, and FIG. 4. Time course for the inhibition of PSI (E-O), PSII (A - -
WC electron transport averaged about 30°C for Agave deserti (O.... 0) electron transport reactions. Tissue pieces from
- A), and WC
and Opuntia ficus-indica maintained at day/night air tempera- plants maintained at 30°C/20°C for at least 2 weeks were treated at 50'C
tures of 30°C/20°C. For both species, this optimum shifted for specified times before the isolation of chloroplasts. Percent inhibition
upward to about 40°C when the growth temperatures were was determined relative to controls treated at 30°C (Figs. 1 and 2).
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Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.1066 CHETTI AND NOBEL Plant Physiol. Vol. 84, 1987
increased to 45°C/35°C. Of the three activities tested, WC elec- species, the half-inactivation temperatures increased an average
tron transport began to decline first at treatment temperatures
above 40°C for 45°C/35°C plants, indicating that a portion of
6°C
of for PSI and PS1I and 4°C for WC electron transport. Half-
times were similar for increases or decreases in growth tempera-
the WC between PSI and PSII was most sensitive to high tem- ture, averaging 5 d for A. deserti and 4 d for 0. ficus-indica.
peratures. For tissue from 45°C/35°C plants maintained for 1 h Half-times averaged 4 d for PSI and PSII and 5 d for WC electron
at 600C, PSI still had 46% activity for A. deserti and 64% for 0. transport. The half-times for shifts in the high temperature
ficus-indica. For 45°C/35°C plants, half-inactivation tempera- inactivation of the uptake of a vital stain are 3 d for A. deserti
tures for the two species averaged 61°C for PSI, 58°C for PSII, (21) and various cacti (26). All of these acclimations are thus
and 54°C for WC electron transport. rapid enough to respond to seasonal changes in ambient temper-
The sensitivity of electron transport reactions to high temper- ature. Moreover, for most desert succulents, maximum high-
atures has also been investigated for other species. For instance, temperature tolerance is well correlated with the ability to accli-
treating leaves of Nerium oleander at various high temperatures mate to high temperatures, suggesting that species with highest
for 10 min indicated that 50% inhibition in whole chain electron temperature tolerances achieve them via this acclimation ability
transport activity occurred at 49°C and 25% inhibition of PSI (21, 26).
activity occurred at 55°C (3). The length of time that plants are Changes in membrane fatty acid saturation or composition
exposed to high temperatures is important, because the high can be involved in acclimation to high temperatures (23, 29).
temperature damage increases rapidly with time. The 1-h expo- However, the acquisition of high-temperature tolerance was not
sure time chosen here is appropriate for desert succulents in the accompanied by marked changes in overall fatty acid saturation
field, where maximum tissue temperatures generally occur for or composition for all desert succulents (14), although small
such periods (6, 26). Also, temperature treatment of whole organs changes for fatty acids in specific membranes may occur. High-
is more relevant to field situations than such treatment of isolated temperature tolerance of photosynthetic light reactions has been
chloroplasts, which are more heat sensitive than when they are attributed to the heat-induced appearance of polar lipids with
in intact tissue ( 17). For instance, a high temperature treatment more saturated fatty acids in the thylakoid membranes, which
of 46°C for 6 min caused almost as much reduction in PSII can cause an upward shift of the temperature for inactivation of
activity of isolated chloroplasts as did a 25 min treatment of the PSII (4, 29).
intact leaf before chloroplast isolation for Atriplex lentiformis When tissue from 30°C/20°C plants was treated at 50°C, the
(22). When Opuntia monoacantha cells were subjected to various average rate of inhibition of all three electron transport reactions
high temperatures for 8 min, 420C led to 50% inhibition of PSII during the first hour was over 4-fold greater than during the next
activity (9). Because of the heat inactivation of the 02 evolving 4 h. The greater inhibition during the first hour may indicate
system, ferricyanide-Hill activity of Euglena chloroplasts is abol- initial disruption of the three-dimensional architecture of the
ished by 5 min at 40°C (13). For isolated spinach chloroplasts, thylakoid membranes or perhaps loss of certain labile membrane
50% inhibition of PSII-dependent DCPIP reduction occurred for components. Heat shock proteins can also be induced by treating
only 3 min at 400C (25) and a 60% inhibition of ferricyanide desert succulents at 50°C, but generally 3 or more days are
reduction occurred for 5 min at 45°C (19). Although further necessary to obtain major changes in relative protein abundance
work with intact tissue is needed, the electron transport reactions (15). These kinetics are similar to those for thehigh-temperature
of A. deserti and 0. ficus-indica are apparently less sensitive to acclimation of all three electron transport reactions observed
high temperatures than are those of the other species that have here for both species. Such acclimation permitted the tolerance
been investigated. of temperatures in excess of 60°C, especially for PSI of 0. ficus-
The decline in the rates of electron transport reactions at indica, and may be an important aspect of the adaptation of
higher temperatures could be due to heat-induced damage to desert succulents to high ambient temperatures in their native
electron transport components as well as direct damage to the environments.
pigment systems (1). The site of inhibition of WC electron
transport under saturating light conditions may be prior to the LIERATURE CITED
site of electron donation by reduced DCPIP (1). Electron trans- 1. ARMOND PA, U SCHREIBER, 0 BJORKMAN 1978 Photosynthetic acclimation to
port in heat-damaged chloroplasts may be blocked by a lesion in temperature in the desert shrub, Larrea divaricata. II. Light-harvesting
the electron transport that removes electrons from water and efficiency and electron transport. Plant Physiol 61: 411-415
2. ARNON DI 1949 Copper enzymes in isolated chloroplasts. Polyphenoloxidase
transfers them to the reaction center of PSII, such as could occur in Beta vulgaris. Plant Physiol 24: 1-15
by the denaturation of a protein (4). Heat treatment may disso- 3. BADGER MR, 0 BJORKMAN, PA ARMOND 1982 An analysis of photosynthetic
ciate this protein from the membrane, or it may cause a lique- response and adaptation to temperature in higher plants: temperature accli-
fying of the membrane lipids, permitting them or other compo- mation in the desert evergreen Nerium oleander L. Plant Cell Environ 5:
85-99
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Populus deltoides. Plant Phys-
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