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Effect of Temperature on the Thermoresistance and Respiration of Tomato Leaves (Lycopersicon esculentum MILL.)
Biochem. Physiol. Pflanzen 178, 601- 605 (1983)
Effect of Temperature on the Thermoresistance and Respiration of Tomato Leaves (Lycopersicon esculentum MILL.) V. V. TALANOVA, A. F. TITov, S. N. DROZDOV and T. V. AKBIOVA Institute of Biology, Karelian Branch of the USSR Academy of Sciences, Petrozavodsk, USSR Key Term Index: temperature, resista.nce, respiration; Lycopersicon esculenlum
Summary The effect of temperature in the 4-45 °C range on the thenrtoresistance and respiratory activity of tomato leaves was studied. It was shown that a change in temperature from 15 to 26 °0 (a. back-
ground range) does not affect the resistance of tomato leaves, temperatures from 6 to 14 °0 and
those from 27 to 42 °0 induce an increase in resistance to cold and heat, respectively; at temperatures below 5 °0 and above 43 °0 a. drop in thermoresistance is observed. Hardening was accompained by a change in the oxygen uptake (by a decrease - when hardened by cold and by an increase when hardened by heat), by a rise in the respiratory quotient (when hardened by cold), and by increase in dehydrogenase activity. Cold dehardening resulted in a sharp rise in respiratory activity (after 3 hat 25 °C). Upon dehardening (25 °C) the activity of oxygen uptake, the respiratory quotient, and dehydrogenase activity returned to the initial level after 5- 6 d. Injurious tem,peratures led to a. drop in respiratory activity and in dehydrogenase activity.
Introduction
One of the plants most thoroughly studied for its response to environmental temperature is the tomato. It is known, that at positive temperatures below 10 'C its growth is depressed (FRIEND and HELSON 1976; BENDIX and WENT 1956; BREIDENBACH and WARING 1977), the photosynthetic apparatus is disturbed (KANUIGA et al. 1978, 1979 S~lILLIE and NOT1' 1979; MICHALSKI and KANUIGA 1980), the content of hormones in tissues and organs (DAlE and CAMPBELL 1981), the activity of a nnmber of enzymes (GRAHAM et aI. 1979; KANUIGA et al. 1979), the permeability of intracellular membranes (LE\VIS and HORKMAN 1964), and the rate of cytoplasm streaming (PATTERSON et al. 1979) are altered. Because the analysis of physiological changes on temperature is not supported by the assessment of plant thermoresistance, it is not always possible to distinguish reactions associated with cold adaptation (hardening) from those which characterize low temperature injury. The effect of high temperatures is even less thoroughly studied. Therefore, the aim of this paper is to investigate the effect of temperature on the thermoresistanee and leaf respiration of tomato plants within their entire vital activity range. Abbreviations: CR, cold resistance; DA, dehydrogenase activity; HR, heat resistance; R.Q. respiratory quotient; RR, respiratory rate
602
V. V.
TALANOVA
et al.
Material and Methods Tomato plants, cv. Moskovsky osenny, were grown in climatic chambers (air temperature 25°C, its relative humidity 60-70%, illumination 10,000 lx, photoperiod 14 h), watered with nutrient solution, pH 6.5. The plants which reached the phase of three true leaves were exposed to a predetermined temperature for 1-3 d. The interval between the temperatures studied equalled 2_5°C. The other conditions were unchanged. In the course of the experiments the resistance to cold and hea.t was controlled daily. The dynamics of respiratory activity was studied at the optimal temperature (25 0 0), at hardening temperatures (8 and 40 °0) and at injurious temperatures (4 and 45 °0). Leaf cuttings were tested for resistance to cold -by freezing for 5- 40 min in a microrefrigerator (DROZDOV et at 1976). and resistance to heat by 5 min heating in Geplers thermostat (ALEXANDROV 1963). The number of living cells after the effect of temperature was determined with a light micros~ cope. Temperature inducing cytoplasm coagulation in half of the parenchyma cells of the cutting (LT5O' °0) was assumed to be the value of thermoresistance. The respiration rates were measured manometrically using Warburg equipment by maintaining the necessary temperature in a. thermo~ static bath. Dehydrogenase activity was deter mined by the reduction of 2.3.5.~triphenyl-tetrazolium chloride to formazane (PYL'NEV 1964). Replication was 3-6-fold within one variant. Each variant was replicated at least twice. Data. obtained were treated statistically.
Results and Diseussion
The main results of the studies on the effect of temperature on the thermoresistance of tomato plants are summarized in Fig. 1. It was found that changes in the range of 15-26°C did not affect leaf resistance. Temperatures of 6-14 °C induce an increase in resistance to cold and those of 27-42 °C lead to an increa~ed resistance to heat. Temperatures below 5 and above 43 °C result in a drop in thermoresistanee and injury of plants which have not been prehardened. On the basis of these data it is logical to distinguish five zones in the given temperature range: background (15-26 °C), hardening by cold (6- 14 °C) and hardening by heat (27- 42 °C), injurious cold (below 5 °C) and injurious heat (above 43°C). The results of the studies on the dynamics of thermoresistance and respiratory activity of leaves when hardened or injured are shown in Figs. 2-4. An increase in the resistance to cold of plants was observed already after one day at a hardening temperature of 8°C (Fig. 2A). The value of the hardening effect rose to reach its maximum after 3-5 d exposure. After the plants were brought back to optimal growth conditions (25°C) their resistance to cold returned to the initiallevcl in 5 d. The respiratory rate of leaves altered simultaneously with resistance. In the process of hardening the activity of oxygen uptake descreased (Fig. 2B) and R.Q. increased (Fig. 2C). After-affect hardening resulted in enhanced respiratory rate which was dependent on the duration of the effect of the hardening temperature. Then the amount of the oxygen and R.Q. gradually declined to the initial level. In the course of the experiment dehydrogenaM activity changed parallel with the resistance to cold (Fig. 2A). In the case of hardening by heat (40° C) plants responded more rapidly: an increase in resistance to heat of the leaves was registered 12 h after the beginning of the temperature treatment, and the maximum hardening effect wa~ achieved on the first day
603
Thermoresistance of Tomato Leaves Temperature, tiC CR " " --':':: 8.02==;'-"-'--"-2::-:5:::.-8.4
..--, DA 0.9
-0
M
-6.8
a7
-6.0
0.6
RR ~~~~~~~~~~
#00 HR
300 200
z
56
100 R4.
1.2 50
8
16 24 32 Temperature,OC
1
40
#8
C
~
1.4
.~
/
1.0
02'
6
8
Time , da!ls
W
g
2
Fig. 1. Effect of temperature on the resistance to cold alld heat. Cold resistance (I) was estimated from the lethal temperatu re for parenchyma. cell s (LT50' °C) after 40 min freezing; heat resista.nce (2) was estimated from the lethal temperature for parenchyma cells (LT5O' °C) after 5 min heating. Fig. 2. Dynamics of resistance to cold and respiratory activity of tomato platlts !vhen hardened by cold
and
whe ~l
dehardened.
A) CR, cold resistance (LT50' °0 after 5 min freezing); HR, heat resistance (LT5O' °C afte r 5 min heating); DA, dehydrogenase activity (optical density unit); B) RR, respiratory ra.te (PI Ozlg fresh weight· h) wa.s measured at temperatures mentioned in figure; C) R-.Q., respiratory quotient.
(Fig. 3A). Dehardening tooks 5 d - the same figure a~ for the aforementioned decline in hardening to cold. Upon hardening the oxygen uptake increased (Fig. 3B); and upon dehardening it decreased and reached the initial level after 3- 4 d. Corresponding changes in dehydrogenase activity occurred simnltaneously with a rise or drop in resistance to heat (Fig. 3 A). The dynamics of thermoresistance, respiratory and dehydrogenase activity at injurious temperatures are shown in Fig. 4. A temperature of 4 °C led to decreased resistance to cold, dchydrogenase activity, oxygen uptake and ability of its reduction in leaves. R.Q. had a tendency to decline. At a high injurious temperatures the patterns of changes in the resistance to heat, in respiration and in dehydrogenase activity were similar. These effects were observed already after 12 h exposu re. Thus, the results of the experiments indicate that tem peratures differing in intensity also differ in their effect on the resistance to heat and cold and respiratory activity of to mato leaves. At the same time data obtained enable us to conclude t hat there is a close interrelation between the level of thermoresistance and that of respiratory
604
V. V.
Temperatwre,OC
HR
qO'
25'
A
57
TALANOVA
ct a1.
DA 0.9
ae
55
CR
07
53
-6.4 52
06 Sf
DA
RR
-5.6 50
B
500
-4.8
RR
~(}()
300
A
c: CR
B
f.2
"
.
C
f50
2
q 6 Time, days
8
4'
0
3
L
D R.Q. 4°
" "45° •
50 0
as
O.f
4°
C
.
DA
0.3
250
R.q. f.O
HR
0
2
Time, days
f.O
0.8
06 2
4
Fig. 3. Dynamics of resistance to heat and respiratory activity of tomato plants when hardened by heat and when dehardened.
Explanation sec legend Fig. 2. Fig. 4. DYllamics of resistance to cold and heat and respiratory activity of lomato plant observed at injuried temperatures. Explanation see legend Fig. 2.
gas exchange in plants. In the course of hardening an increase in resistance was associated with a change in the oxygen uptake and R.Q. and an augmentation of dehydrogenase activity. The reorganization of respiratory processes observed seems to be a necessary element of adaptation, because the aquiring of increased resistance requ ired a certain amount of energy (LANGRIDGE 1963; SEMIKHATOVA 1980). Dehardening, the reversal process, is also accompanied by a change in the respiratory system. Injurious temperatures unlike hardening temperatures, result in the damaging functional activity of the respiratory system, which is only able to reduce in the case of short-time effects. References V. Y.: Cyto·physiologicaJ and cyto·ecological investigation of resistance of plant cells to the action of high and low temperatures. Acad. Sci. URSS, Acta. Series IV, 18, 234- 274 (1963). BENDIX, S., and WENT, F. W.: Some effects of temperature and photoperiod on the growth of tomato seedlings. Bot. Ga,. 117, 326-335 (1956). ALEXANDROV,
Thermoresistance of Tomato
I~eaves
60&
BREIDENBACH, R. W., and WARING, A. J.: Response to chilling of tomato seedlings and cells in suspension cultures. Plant Physiol. 60, 190- 192 (1977). DAlE, J., and CAMPBELL, W. F.: Response of tomato plants to stressful temperatures. Increase in abscisic acid concentrations. Plant Physiol. 67, 26-29 (1981). DROZDOV, S. N., KURETZ, V. K, BUDIKINA, N. P., and BALAGUROVA, N. 1.: Determination of plant resistance to frost. In: "Methods of estimation of resistance to unfavourable environmental condition (UDOVENKO, G. V., ed.), pp. 222- 229. Kolos, Leningrad 1976. FRIEND, D. J. C., and HELSON, V. A.: Thermoperiodic effects on the growth and photosynthesis of wheat and other crop plants. Bot. Gaz. 137, 75- 84 (1976). GRAIlAlf, D., HOCKLEY, D. G . , and PATTERSON, B. D.: Temperature effects on phosphoenol pyruvate carboxylase from chilling sensitive and chilling resistant plants. In: Low temperatu re stress in crop plants (GR.<\TlAM, D., and RAISON, J. K., eds.), pp. 453- 461. Academic Press, New York, London, Sydney, Toronto and San Francisco 1979. KANUIGA, Z., SOCHANOWICZ, B., ZABEK, J., and KRZYSTYNIAK, K.: Photosynthetic apparatus in chilling-sensitive plants. 1. Reactivation of Hill reaction activity inhibited on the cold and dark storage of detached leaves and intact plants. Planta 140, 121- 128 (1978). KANUIG .-\, Z., ZABEK, J., and MICHALSKI, W. P.: Photosynthetic a.pparatus in chilling-sensitive plants. VI. Cold and dark induced changes in chloroplast superoxide dismutase activity in relation to loosely-bound manganese content.: Planta 140, 145- 150 (1979). LANGRIDGE, J.: Biochemical aspects of temperature response. Ann. Rev. Plant Physiol. 14, 441-462 (1963). LEWIS, T. L., and WORKMAN, M.: The effect of low temperature on phosphate esterification and ccll membrane permeability in tomato fruit and cabbadge leaf tissue. Aust. BioI. Sci. 17, 141- 152 (1964). MICHALSKI, W. P., and KANUIGA, Z.: Photosynthetic apparatus in chilling sensitive plants. VII. Comparison of the effect of ga.lactolipase treatment of chloroplast and co ld-da.rk storage of leaves on photosynthetic electron flow. Biochem. Biophys. Acta aSS, 84- 99 (1980). PATTERSON, B. D., GRAHAM, D., and PAULL, R.: Adaptation to chilling: survival, germination, respiration and proplasmic dynamics. In: Low temperature stress in crop plants (GRAHAM, D., and RAISON, I. K., cds.) pp. 23- 35. Academic Press, New York, London, Sydney, Toronto and San Francisco 1979. PYL'NEV, V. M.: A vacuum-infiltration micromethod for assay of dehydrogena.se activity in liver tissues. Bioehemistry 29, 837 ~ 840 (1964). SEMIKIIATOVA, O. A.: Energetic aspects of integration of physiological processes in the plant. Sov. Plant Physiol. 27, 1005 ~1017 (1980). SMILLIE, R. }'I.; and NOTT, R: Assa.y of chilling injury in wild and domestic tomatoes based on photosystem activity of the chilled leaves. Plant Physiol. 796 ~801 (1979).
Received August 15, 1982; accepted February 10, 1983 Authors' address: V. V. TALANOVA, A. F. TITOV, S. N. DROZDOV and T. V. AKIMOVA, Institute of Biology, Karelian Branch of the USSR Academy of Sciences, Petrozavodsk, 185610, USSR.
Effect of Temperature on the Thermoresistance and Respiration of Tomato Leaves (Lycopersicon esculentum MILL.) V. V. TALANOVA, A. F. TITov, S. N. DROZDOV and T. V. AKBIOVA Institute of Biology, Karelian Branch of the USSR Academy of Sciences, Petrozavodsk, USSR Key Term Index: temperature, resista.nce, respiration; Lycopersicon esculenlum
Summary The effect of temperature in the 4-45 °C range on the thenrtoresistance and respiratory activity of tomato leaves was studied. It was shown that a change in temperature from 15 to 26 °0 (a. back-
ground range) does not affect the resistance of tomato leaves, temperatures from 6 to 14 °0 and
those from 27 to 42 °0 induce an increase in resistance to cold and heat, respectively; at temperatures below 5 °0 and above 43 °0 a. drop in thermoresistance is observed. Hardening was accompained by a change in the oxygen uptake (by a decrease - when hardened by cold and by an increase when hardened by heat), by a rise in the respiratory quotient (when hardened by cold), and by increase in dehydrogenase activity. Cold dehardening resulted in a sharp rise in respiratory activity (after 3 hat 25 °C). Upon dehardening (25 °C) the activity of oxygen uptake, the respiratory quotient, and dehydrogenase activity returned to the initial level after 5- 6 d. Injurious tem,peratures led to a. drop in respiratory activity and in dehydrogenase activity.
Introduction
One of the plants most thoroughly studied for its response to environmental temperature is the tomato. It is known, that at positive temperatures below 10 'C its growth is depressed (FRIEND and HELSON 1976; BENDIX and WENT 1956; BREIDENBACH and WARING 1977), the photosynthetic apparatus is disturbed (KANUIGA et al. 1978, 1979 S~lILLIE and NOT1' 1979; MICHALSKI and KANUIGA 1980), the content of hormones in tissues and organs (DAlE and CAMPBELL 1981), the activity of a nnmber of enzymes (GRAHAM et aI. 1979; KANUIGA et al. 1979), the permeability of intracellular membranes (LE\VIS and HORKMAN 1964), and the rate of cytoplasm streaming (PATTERSON et al. 1979) are altered. Because the analysis of physiological changes on temperature is not supported by the assessment of plant thermoresistance, it is not always possible to distinguish reactions associated with cold adaptation (hardening) from those which characterize low temperature injury. The effect of high temperatures is even less thoroughly studied. Therefore, the aim of this paper is to investigate the effect of temperature on the thermoresistanee and leaf respiration of tomato plants within their entire vital activity range. Abbreviations: CR, cold resistance; DA, dehydrogenase activity; HR, heat resistance; R.Q. respiratory quotient; RR, respiratory rate
602
V. V.
TALANOVA
et al.
Material and Methods Tomato plants, cv. Moskovsky osenny, were grown in climatic chambers (air temperature 25°C, its relative humidity 60-70%, illumination 10,000 lx, photoperiod 14 h), watered with nutrient solution, pH 6.5. The plants which reached the phase of three true leaves were exposed to a predetermined temperature for 1-3 d. The interval between the temperatures studied equalled 2_5°C. The other conditions were unchanged. In the course of the experiments the resistance to cold and hea.t was controlled daily. The dynamics of respiratory activity was studied at the optimal temperature (25 0 0), at hardening temperatures (8 and 40 °0) and at injurious temperatures (4 and 45 °0). Leaf cuttings were tested for resistance to cold -by freezing for 5- 40 min in a microrefrigerator (DROZDOV et at 1976). and resistance to heat by 5 min heating in Geplers thermostat (ALEXANDROV 1963). The number of living cells after the effect of temperature was determined with a light micros~ cope. Temperature inducing cytoplasm coagulation in half of the parenchyma cells of the cutting (LT5O' °0) was assumed to be the value of thermoresistance. The respiration rates were measured manometrically using Warburg equipment by maintaining the necessary temperature in a. thermo~ static bath. Dehydrogenase activity was deter mined by the reduction of 2.3.5.~triphenyl-tetrazolium chloride to formazane (PYL'NEV 1964). Replication was 3-6-fold within one variant. Each variant was replicated at least twice. Data. obtained were treated statistically.
Results and Diseussion
The main results of the studies on the effect of temperature on the thermoresistance of tomato plants are summarized in Fig. 1. It was found that changes in the range of 15-26°C did not affect leaf resistance. Temperatures of 6-14 °C induce an increase in resistance to cold and those of 27-42 °C lead to an increa~ed resistance to heat. Temperatures below 5 and above 43 °C result in a drop in thermoresistanee and injury of plants which have not been prehardened. On the basis of these data it is logical to distinguish five zones in the given temperature range: background (15-26 °C), hardening by cold (6- 14 °C) and hardening by heat (27- 42 °C), injurious cold (below 5 °C) and injurious heat (above 43°C). The results of the studies on the dynamics of thermoresistance and respiratory activity of leaves when hardened or injured are shown in Figs. 2-4. An increase in the resistance to cold of plants was observed already after one day at a hardening temperature of 8°C (Fig. 2A). The value of the hardening effect rose to reach its maximum after 3-5 d exposure. After the plants were brought back to optimal growth conditions (25°C) their resistance to cold returned to the initiallevcl in 5 d. The respiratory rate of leaves altered simultaneously with resistance. In the process of hardening the activity of oxygen uptake descreased (Fig. 2B) and R.Q. increased (Fig. 2C). After-affect hardening resulted in enhanced respiratory rate which was dependent on the duration of the effect of the hardening temperature. Then the amount of the oxygen and R.Q. gradually declined to the initial level. In the course of the experiment dehydrogenaM activity changed parallel with the resistance to cold (Fig. 2A). In the case of hardening by heat (40° C) plants responded more rapidly: an increase in resistance to heat of the leaves was registered 12 h after the beginning of the temperature treatment, and the maximum hardening effect wa~ achieved on the first day
603
Thermoresistance of Tomato Leaves Temperature, tiC CR " " --':':: 8.02==;'-"-'--"-2::-:5:::.-8.4
..--, DA 0.9
-0
M
-6.8
a7
-6.0
0.6
RR ~~~~~~~~~~
#00 HR
300 200
z
56
100 R4.
1.2 50
8
16 24 32 Temperature,OC
1
40
#8
C
~
1.4
.~
/
1.0
02'
6
8
Time , da!ls
W
g
2
Fig. 1. Effect of temperature on the resistance to cold alld heat. Cold resistance (I) was estimated from the lethal temperatu re for parenchyma. cell s (LT50' °C) after 40 min freezing; heat resista.nce (2) was estimated from the lethal temperature for parenchyma cells (LT5O' °C) after 5 min heating. Fig. 2. Dynamics of resistance to cold and respiratory activity of tomato platlts !vhen hardened by cold
and
whe ~l
dehardened.
A) CR, cold resistance (LT50' °0 after 5 min freezing); HR, heat resistance (LT5O' °C afte r 5 min heating); DA, dehydrogenase activity (optical density unit); B) RR, respiratory ra.te (PI Ozlg fresh weight· h) wa.s measured at temperatures mentioned in figure; C) R-.Q., respiratory quotient.
(Fig. 3A). Dehardening tooks 5 d - the same figure a~ for the aforementioned decline in hardening to cold. Upon hardening the oxygen uptake increased (Fig. 3B); and upon dehardening it decreased and reached the initial level after 3- 4 d. Corresponding changes in dehydrogenase activity occurred simnltaneously with a rise or drop in resistance to heat (Fig. 3 A). The dynamics of thermoresistance, respiratory and dehydrogenase activity at injurious temperatures are shown in Fig. 4. A temperature of 4 °C led to decreased resistance to cold, dchydrogenase activity, oxygen uptake and ability of its reduction in leaves. R.Q. had a tendency to decline. At a high injurious temperatures the patterns of changes in the resistance to heat, in respiration and in dehydrogenase activity were similar. These effects were observed already after 12 h exposu re. Thus, the results of the experiments indicate that tem peratures differing in intensity also differ in their effect on the resistance to heat and cold and respiratory activity of to mato leaves. At the same time data obtained enable us to conclude t hat there is a close interrelation between the level of thermoresistance and that of respiratory
604
V. V.
Temperatwre,OC
HR
qO'
25'
A
57
TALANOVA
ct a1.
DA 0.9
ae
55
CR
07
53
-6.4 52
06 Sf
DA
RR
-5.6 50
B
500
-4.8
RR
~(}()
300
A
c: CR
B
f.2
"
.
C
f50
2
q 6 Time, days
8
4'
0
3
L
D R.Q. 4°
" "45° •
50 0
as
O.f
4°
C
.
DA
0.3
250
R.q. f.O
HR
0
2
Time, days
f.O
0.8
06 2
4
Fig. 3. Dynamics of resistance to heat and respiratory activity of tomato plants when hardened by heat and when dehardened.
Explanation sec legend Fig. 2. Fig. 4. DYllamics of resistance to cold and heat and respiratory activity of lomato plant observed at injuried temperatures. Explanation see legend Fig. 2.
gas exchange in plants. In the course of hardening an increase in resistance was associated with a change in the oxygen uptake and R.Q. and an augmentation of dehydrogenase activity. The reorganization of respiratory processes observed seems to be a necessary element of adaptation, because the aquiring of increased resistance requ ired a certain amount of energy (LANGRIDGE 1963; SEMIKHATOVA 1980). Dehardening, the reversal process, is also accompanied by a change in the respiratory system. Injurious temperatures unlike hardening temperatures, result in the damaging functional activity of the respiratory system, which is only able to reduce in the case of short-time effects. References V. Y.: Cyto·physiologicaJ and cyto·ecological investigation of resistance of plant cells to the action of high and low temperatures. Acad. Sci. URSS, Acta. Series IV, 18, 234- 274 (1963). BENDIX, S., and WENT, F. W.: Some effects of temperature and photoperiod on the growth of tomato seedlings. Bot. Ga,. 117, 326-335 (1956). ALEXANDROV,
Thermoresistance of Tomato
I~eaves
60&
BREIDENBACH, R. W., and WARING, A. J.: Response to chilling of tomato seedlings and cells in suspension cultures. Plant Physiol. 60, 190- 192 (1977). DAlE, J., and CAMPBELL, W. F.: Response of tomato plants to stressful temperatures. Increase in abscisic acid concentrations. Plant Physiol. 67, 26-29 (1981). DROZDOV, S. N., KURETZ, V. K, BUDIKINA, N. P., and BALAGUROVA, N. 1.: Determination of plant resistance to frost. In: "Methods of estimation of resistance to unfavourable environmental condition (UDOVENKO, G. V., ed.), pp. 222- 229. Kolos, Leningrad 1976. FRIEND, D. J. C., and HELSON, V. A.: Thermoperiodic effects on the growth and photosynthesis of wheat and other crop plants. Bot. Gaz. 137, 75- 84 (1976). GRAIlAlf, D., HOCKLEY, D. G . , and PATTERSON, B. D.: Temperature effects on phosphoenol pyruvate carboxylase from chilling sensitive and chilling resistant plants. In: Low temperatu re stress in crop plants (GR.<\TlAM, D., and RAISON, J. K., eds.), pp. 453- 461. Academic Press, New York, London, Sydney, Toronto and San Francisco 1979. KANUIGA, Z., SOCHANOWICZ, B., ZABEK, J., and KRZYSTYNIAK, K.: Photosynthetic apparatus in chilling-sensitive plants. 1. Reactivation of Hill reaction activity inhibited on the cold and dark storage of detached leaves and intact plants. Planta 140, 121- 128 (1978). KANUIG .-\, Z., ZABEK, J., and MICHALSKI, W. P.: Photosynthetic a.pparatus in chilling-sensitive plants. VI. Cold and dark induced changes in chloroplast superoxide dismutase activity in relation to loosely-bound manganese content.: Planta 140, 145- 150 (1979). LANGRIDGE, J.: Biochemical aspects of temperature response. Ann. Rev. Plant Physiol. 14, 441-462 (1963). LEWIS, T. L., and WORKMAN, M.: The effect of low temperature on phosphate esterification and ccll membrane permeability in tomato fruit and cabbadge leaf tissue. Aust. BioI. Sci. 17, 141- 152 (1964). MICHALSKI, W. P., and KANUIGA, Z.: Photosynthetic apparatus in chilling sensitive plants. VII. Comparison of the effect of ga.lactolipase treatment of chloroplast and co ld-da.rk storage of leaves on photosynthetic electron flow. Biochem. Biophys. Acta aSS, 84- 99 (1980). PATTERSON, B. D., GRAHAM, D., and PAULL, R.: Adaptation to chilling: survival, germination, respiration and proplasmic dynamics. In: Low temperature stress in crop plants (GRAHAM, D., and RAISON, I. K., cds.) pp. 23- 35. Academic Press, New York, London, Sydney, Toronto and San Francisco 1979. PYL'NEV, V. M.: A vacuum-infiltration micromethod for assay of dehydrogena.se activity in liver tissues. Bioehemistry 29, 837 ~ 840 (1964). SEMIKIIATOVA, O. A.: Energetic aspects of integration of physiological processes in the plant. Sov. Plant Physiol. 27, 1005 ~1017 (1980). SMILLIE, R. }'I.; and NOTT, R: Assa.y of chilling injury in wild and domestic tomatoes based on photosystem activity of the chilled leaves. Plant Physiol. 796 ~801 (1979).
Received August 15, 1982; accepted February 10, 1983 Authors' address: V. V. TALANOVA, A. F. TITOV, S. N. DROZDOV and T. V. AKIMOVA, Institute of Biology, Karelian Branch of the USSR Academy of Sciences, Petrozavodsk, 185610, USSR.