The Effect of Temperature on Cold and Heat Resistance of Growing Plants: II. COLD RESISTANT SPECIES

The dynamics of cold and heat resistance in a number of coldresistant plant species (potato, meadow fescue, spring and winterwheat) exposed to temperatures from –13 °C to + 50°Chas been studied under controlled environmental conditions.The thermo-resistance of leaves was shown to be constant atcertain temperatures (a range of background temperatures), butit increased (ranges of heat and cold hardening) or decreased(ranges of heat and cold injury) at other temperatures. A gradationof temperatures with respect of ‘thermo-resistance’for these ranges is being proposed. The limits of the rangesvary depending on endogenous (species characteristics, phaseof development) and exogenous factors (environmental conditions).Thus, at gradually rising or falling temperatures the boundariesbetween the ranges of hardening and injury are markedly shiftedtowards more extreme temperatures. Generally, the data showuniformity of responses to extreme temperatures by cold resistantplants; the differences observed between species are quantitative. Key words: Temperature, Cold-resistant plants     

Effect of High-Pressure Gas Atmospheres and Anaesthetics on Chilling Injury of Plants

High pressures and anaesthetics were used to study chillinginjury in plants. Changes in membrane fluidity at low but nonfreezingtemperatures are thought to be involved in chilling injury-aphysiological disorder of many economically important plants,e.g. banana, cotton, cucumber, maize, rice, sorghum, and tomato.High-pressure helium and nitrogen atmospheres of 12 MPa increasedthe severity of chilling injury (i.e. rate of ion leakage) inexcised cucumber cotyledon discs, cucumber hypocotyl segmentsand tomato pericarp discs, and also increased the thresholdtemperature at which chilling occurred by 2° to 6°C.Exposure to vapours of the anaesthetics halothane and methoxyfluranereduced chilling injury in cucumber cotyledon discs, cucumberhypocotyl segments and tomato pericarp discs. The relative effectivenessof the two anaesthetics in reducing chilling injury was similarto their relative effectiveness in inducing anaesthesia in animalsand their relative lipid solubilities. The response of the tissuesto halothane and methoxyflurane, which increase membrane fluidity,and to high pressures, which reduce membrane fluidity, are consistentwith the hypothesis that cold-induced phase transition of membranescould be responsible for chilling injury. However, other cellularcomponents may also be affected, e.g. low temperatures, highpressures and anaesthetics can alter protein conformation, affection channels, depolymerize microtubules and cause the releaseof calcium from membrane lipids. Key words: Cucumber, Cucumis sativus, tomato, Lycopersicon esculentum, halothane, ion leakage, methoxyflurane     

Temperature dependence of delayed ehlorophyll fluorescence in intact leaves of higher plants. A rapid method for detecting the phase transition of thylakoid membrane lipids

The temperature dependence of the yield of in vivo prompt and delayed chiorophyll fluorescence was investigated in maize and barley leaves. In the chilling-sensitive maize, delayed fluorescence at steady-state level showed a maximum near the temperature at which thylakoid membrane lipids undergo a phase transition as revealed by differential scanning calorimetry measurements. In the chilling-resistant barley, no phase transition was detected above 0°C and the delayed light emission varied in a monotonic fashion. It was shown that measurements of delayed luminescence intensity in vivo can provide a rapid and sensitive method for detecting the phase change of membrane lipids in intact leaves of chilling-sensitive plant species such as tomato, cotton, cucumber, castor bean or avocado. In contrast, the use of steady-state prompt chlorophyll fluorescence as an indicator of membrane fluidity change was not successful.     

Temperature dependence of delayed chlorophyll fluorescence in intact leaves of higher plants. A rapid method for detecting the phase transition of thylakoid membrane lipids

The temperature dependence of the yield of in vivo prompt and delayed chlorophyll fluorescence was investigated in maize and barley leaves. In the chilling-sensitive maize, delayed fluorescence at steady-state level showed a maximum near the temperature at which thylakoid membrane lipids undergo a phase transition as revealed by differential scanning calorimetry measurements. In the chilling-resistant barley, no phase transition was detected above 0°C and the delayed light emission varied in a monotonic fashion. It was shown that measurements of delayed luminescence intensity in vivo can provide a rapid and sensitive method for detecting the phase change of membrane lipids in intact leaves of chilling-sensitive plant species such as tomato, cotton, cucumber, castor bean or avocado. In contrast, the use of steady-state prompt chlorophyll fluorescence as an indicator of membrane fluidity change was not successful.     

Photoinhibition at low temperature in chilling-sensitive and -resistant plants

Photoinhibition resulting from exposure at 7°C to a moderate photon flux density (300 micromoles per square meter per second, 400-700 nanometers) for 20 hours was measured in leaves of annual crops differing widely in chilling tolerance. The incidence of photoinhibition, determined as the decrease in the ratio of induced to total chlorophyll fluorescence emission at 693 nanometers (F_v/F_max) measured at 77 Kelvin, was not confined to chilling-sensitive species. The extent of photoinhibition in leaves of all chilling-resistant plants tested (barley [Hordeum vulgare L.], broad bean [Vicia faba L.], pea [Pisum sativum L.], and wheat [Triticum aestivum L.]) was about half of that measured in chilling-sensitive plants (bean [Phaseolus vulgaris L.], cucumber [Cucumis sativus L.], lablab [Lablab purpureus L.], maize [Zea mays L.], pearl millet [Pennisetum typhoides (Burm. f.) Stapf & Hubbard], pigeon pea [Cajanus cajun (L.) Millsp.], sesame [Sesamum indicum L.], sorghum [Sorghum bicolor L. Moench], and tomato [Lycopersicon esculentum Mill.]). Rice (Oryza sativa L.) leaves of the indica type were more susceptible to photoinhibition at 7°C than leaves of the japonica type. Photoinhibition was dependent both on temperature and light, increasing nonlinearly with decreasing temperature and linearly with increasing light intensity. In contrast to photoinhibition during chilling, large differences, up to 166-fold, were found in the relative susceptibility of the different species to chilling injury in the dark. It was concluded that chilling temperatures increased the likelihood of photoinhibition in leaves of both chilling-sensitive and -resistant plants. Further, while the photoinhibition during chilling generally occurred more rapidly in chilling-sensitive plants, this was not related directly to chilling sensitivity.     

Effect of High Temperature on Photosynthesis in Potatoes

The effect of high temperatures on the rate of photosynthesiswas studied in several potato varieties. Temperatures of upto 38 °C did not cause a reduction in the photosynthesisof plants that had been grown at these temperatures for longperiods prior to measurement. Higher temperatures of 40–42°C, or the transfer of plants from daytime temperature regimesof 22 °C to 32 °C, caused a reduction in net photosynthesis.This reduction was found to be essentially mesophyllic in origin.High temperature was found to be associated with a decreasein stomatal resistance, an increase in transpiration, and alarger difference between air and leaf temperatures. Dark respirationrates and compensation points for CO₂ concentration were alsogreater at the high temperatures. It was concluded that thepotato crop can be adopted to grow and have an adequate rateof photosynthesis even at relatively high temperatures. Source-sinkrelationships, which were modified by the later formation oftubers at higher temperatures, did not affect photosynthesisin this study. Varietal differences in resistance to heat stresswere observed, with the clone Cl-884 showing a more efficientcapacity for photosynthesis at temperatures up to 40 °Cthan many commonly grown varieties. High temperature, photosynthesis, potato, Solanum tuberosum L     

The effect of temperature of the rate of photosynthetic electron transfer in chloroplasts of chilling-sensitive and chilling-resistant plants

1. Photochemical activities as a function of temperature have been compared in chloroplasts isolated from chilling-sensitive (below approximately 12 °C) and chilling-resistant plants.2. An Arrhenius plot of the photoreduction of NADP⁺ from water by chloroplasts isolated from tomato (Lycopersicon esculentum var. Gross Lisse), a chilling-sensitive plant, shows a change in slope at about 12 °C. Between 25 and 14 °C the activation energy for this reaction is 8.3 kcal·mole^?1. Between 11 and 3 °C the activation energy increases to 22 kcal·mole^?1. Photoreduction of NADP⁺ by chloroplasts from another chilling-sensitive plant, bean (Phaseolus vulgaris var. brown beauty), shows an increase in activation energy from 5.9 to 17.5 kcal·mole^?1 below about 12 °C.3. The photoreduction of NADP⁺ by chloroplasts isolated from two chilling-resistant plants, lettuce (Lactuca sativa var. winter lake) and pea (Pisum sativum var. greenfeast), shows constant activation energies of 5.4 and 8.0 kcal·mole^?1, respectively, over the temperature range 3–25 °C.4. The effect of temperature on photosynthetic electron transfer in the chloroplasts of chilling-sensitive plants is localized in Photosystem I region of photosynthesis. Both the photoreduction of NADP⁺ from reduced 2,6-dichlorophenol-indophenol and the ferredoxin-NADP⁺ reductase (EC 1.6.99.4) activity of choroplasts of chilling-sensitive plants show increases in activation energies at approximately 12 °C whereas Photosystem II activity of chloroplasts of chilling-sensitive plants shows a constant activation energy over the temperature range 3–25 °C. The photoreduction of Diquat (1,1′-ethylene-2,2′-dipyridylium dibromide) from water by bean chloroplasts, however, does not show a change in activation energy over the same temperature range. The activation energies of each of these reactions in chilling-resistant plants is constant between 3 and 25 °C.5. The effect of temperature on the activation energy of these reactions in chloroplasts from chilling-sensitive plants is reversible.6. In chilling-sensitive plants, the increased activation energies below approximately 12 °C, with consequent decreased rates of reaction for the photoreduction of NADP⁺, would result in impaired photosynthetic activity at chilling temperatures. This could explain the changes in chloroplast structure and function when chilling-sensitive plants are exposed to chilling temperatures.     

The Decreased Cold-Resistance of Chilling-Sensitive Plants Is Related to Suppressed CO2 Assimilation in Leaves and Sugar Accumulation in Roots

Tomato (Lycopersicon esculentum L., cv. Sibirskii skorospelyi) and cucumber (Cucumis sativus L., cv. Konkurent) plants were grown in a soil culture in a greenhouse at an average daily temperature of 20°C and ambient illumination until the development of five and eight true leaves, respectively. During the subsequent three days, some plants were kept in a climatic chamber at 6°C in the light, whereas other plants remained in a greenhouse (control). The cold-resistance of cucumber leaves and roots, as assayed from the electrolyte leakage, was reduced after cold exposure stronger than cold-resistance of tomato organs. The ratio photosynthesis/dark respiration was lower in cucumber than in tomato leaves at all measurement temperatures. The concentrations of sugars (sucrose + glucose + fructose) increased in chilled tomato roots but decreased in cucumber roots. Cold exposure changed the activities of various invertase forms (soluble and insoluble acidic and alkaline invertases). The total invertase activity and the ratio of mono- to disaccharides increased. The lower cucumber cold-resistance is related to the higher sensitivity of its photosynthetic apparatus to chilling and, as a consequence, insufficient root supply with sugars.     

Contribution of Oxidative Stress to the Development of Cold-Induced Damage to Leaves of Chilling-Sensitive Plants: 3. Injury of Cell Membranes by Chilling Temperatures

Changes in permeability of cell membranes (judged from electrolyte leakage) were examined on leaves of 7- to 11-day-old seedlings of maize (Zea mays L.), cucumber (Cucumis sativus L.), millet (Panicum miliaceum L.), and on etiolated shoots of potato (Solanum tuberosum L.) immediately after cooling plants for 1–24 h at 2°C and one day after a 24-h chilling treatment. A gradually increasing leakage of ions from the cells was observed upon prolongation of chilling exposure, with the maximum attained by the end of 24-h chilling treatment. The leakage of electrolyte was slightly reduced in the post-treatment period but it was still higher than the electrolyte leakage from the control samples (untreated plants). The cold treatment of chilling-sensitive plants (but not of potato) revealed a positive correlation between the rates of lipid peroxidation, indicative of chilling injury, and the electrolyte efflux (r = 0.61–0.96). The evaluation of plant susceptibility to injury showed that millet and potato plants recovered from the chilling damage in 24 h after the treatment, whereas maize and cucumber plants did not show such a recovery.     

Changes in Photosynthesis in Inbred Maize Lines with Different Degrees of Chilling Tolerance Grown at Optimum and Suboptimum Temperatures

The effects of growth temperature on changes in net photosynthetic rate (PN) and the chlorophyll fluorescence induction parameter Fv/Fm were investigated after cold stress in inbred maize lines with different degrees of cold tolerance. There was no significant difference between lines grown at optimum temperatures of 25/23 and 20/18 °C as regards PN and Fv/Fm determined at the growth temperature, but these parameters were lower for plants grown at a suboptimum temperature of 15/13 °C. After cold treatment, the decrease in PN was more pronounced in chilling-sensitive lines. The higher the growth temperature was, the more pronounced decrease occurred in PN and Fv/Fm. Thus at low growth temperature both damaging and adaptive processes occur.     

Temperature effects on the reactive oxygen species formation and antioxidant defence in roots of two cucurbit species with contrasting root zone temperature optima

Suboptimal root zone temperature (14°C) was imposed on chilling-sensitive cucumber (Cucumis sativus L.) and chilling-tolerant figleaf gourd (Cucurbita ficifolia Bouché) plants. Exposure of roots to low temperature for up to 10 days caused a strong growth inhibition in cucumber compared with figleaf gourd. Physiological analysis showed that generation of reactive oxygen species (ROS) such as hydrogen peroxide and superoxide anion was significantly induced in cucumber plants as fast as 1 day after low root zone temperature treatment. In addition to the significant induction of antioxidant superoxide dismutase activity, low root zone temperature also increased the mitochondrial electron transport allocated to alternative pathway while decreased cytochrome pathway salicylhydroxamic acid-resistant respiration. However, these defense responses could not compensate for the ROS production, resulting in membrane lipid peroxidation and loss of root cell viability in the low root zone temperature treated cucumber roots. In contrast, 14°C root zone temperature had no significant effects on figleaf gourd plant growth, antioxidant enzymes, ROS levels and alternative respiratory pathway. Hence, difference in ROS metabolism would be associated with the remarkable difference in adaptability of cucumber and figleaf gourd plants in response to suboptimal root zone temperature condition.     

A Comparison of the Effects of Chilling on Thylakoid Electron Transfer in Pea (Pisum sativum L.) and Cucumber (Cucumis sativus L.)

Experiments comparing the photosynthetic responses of a chilling-resistant species (Pisum sativum L. cv Alaska) and a chilling-sensitive species (Cucumis sativus L. cv Ashley) have shown that cucumber photosynthesis is adversely affected by chilling temperatures in the light, while pea photosynthesis is not inhibited by chilling in the light. To further investigate the site of the differential response of these two species to chilling stress, thylakoid membranes were isolated under various conditions and rates of photosynthetic electron transfer were determined. Preliminary experiments revealed that the integrity of cucumber thylakoids from 25°C-grown plants was affected by the isolation temperature; cucumber thylakoids isolated at 5°C in 400 millimolar NaCl were uncoupled, while thylakoids isolated at room temperature in 400 millimolar NaCl were coupled, as determined by addition of gramicidin. The concentration of NaCl in the homogenization buffer was found to be a critical factor in the uncoupling of cucumber thylakoids at 5°C. In contrast, pea thylakoid membranes were not influenced by isolation temperatures or NaCl concentrations. In a second set of experiments, thylakoid membranes were isolated from pea and cucumber plants at successive intervals during a whole-plant light period chilling stress (5°C). During wholeplant chilling, thylakoids isolated from cucumber plants chilled in the light were uncoupled even when the membranes were isolated at warm temperatures. Pea thylakoids were not uncoupled by the whole-plant chilling treatment. The difference in integrity of thylakoid membrane coupling following chilling in the light demonstrates a fundamental difference in photosynthetic function between these two species that may have some bearing on why pea is a chilling-resistant plant and cucumber is a chilling-sensitive plant.     

The mitigating role of environmental factors in seedling injury and chill-dependent depression of catalase activity in maize leaves

In pot experiments performed on maize seedlings chilled at 5 °C, leaf injury was diminished by the application of elevated temperature (1 or 5 h at 15 or 20°C, “warm breaks” treatment) in a dose-dependent manner. The lower the injury count, the higher the catalase (CAT) activity. In a separate experiment, the application of 100 % relative humidity also protected the plants from chilling injury and water loss, increased their gas exchange and variable to maximum chlorophyll fluorescence ratio (F_v/F_m), but did not influence CAT activity. Another protective environmental factor, elevated atmospheric CO₂ concentration [700 μmol(CO₂) mol⁻¹(air)] diminished CAT activity inhibition, but only in plants of chilling-resistant cultivar. The positive impact of specific environmental factors accompanying chilling is not obviously related to the suppression of the inhibition of CAT activity, although the enzyme is considered as chilling-sensitive.     

Temperature-dependent phase behavior of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants

Seven major lipid classes were isolated from leaves of chilling-sensitive and chilling-resistant plants, and the temperature-dependent phase behaviors of their aqueous dispersions were studied by a fluorescence polarization method using trans-parinaric acid and its methyl ester. Phosphatidylglycerols from the chilling-sensitive plants went from the liquid crystalline state into the phase separation state at about 30°C in 100 mm NaCl and at about 40°C in 5 mm MgCl₂. In contrast, phosphatidylglycerols from the chilling-resistant plants went into the phase separation state at a much lower temperature. The other classes of lipids remained in the liquid crystalline state at all temperatures between 5°C and 40°C regardless of the chilling sensitivity of the plants, except sulfoquinovosyl diacylglycerol from sponge cucumber in which phase separation seemed to begin at about 15°C. Compositions and positional distributions of fatty acids of the lipids suggest that the phosphatidylglycerols from the chilling-sensitive plants, but no other lipids, contained large proportions of molecular species which undergo phase transition at room temperature or above. The thermotropic phase behaviors and the fatty acid compositions suggest that, among the major lipid classes from leaves of the chilling-sensitive plants, only phosphatidylglycerol can induce a phase transition. Since a major part of this lipid in leaves originates from the chloroplasts, phase transition probably occurs in the chloroplast membranes.     

Temperature-induced Changes in Hill Activity of Chloroplasts Isolated from Chilling-sensitive and Chilling-resistant Plants

The effect of temperature on Hill activity has been compared in chilling-sensitive and chilling-resistant plants. The Arrhenius activation energy (Ea) for the photoreduction of 2,6-dichlorophenolindophenol by chloroplasts isolated from two chilling-sensitive plants, mung bean (Vigna radiata L. var. Mungo) and maize (Zea mays L. cv. PX 616), increased at low temperatures, below 17 C for mung bean and below 11 C for maize. However, the Ea for this reaction in pea (Pisum sativum L. cv. Massay Gem), a chilling-resistant plant, likewise increased at temperatures below 14 C. A second change in Ea occurred at higher temperatures. The Ea decreased above about 28 C for mung bean, 30 C for maize, and 25 C for pea. At temperatures approaching 40 C, thermal inactivation of Hill activity occurred. These results, when taken together with previous results obtained with the chilling-resistant plant barley, indicate that chloroplasts from both chilling-sensitive and chilling-resistant plants can undergo a change in chloroplast membrane activity at low temperatures above freezing and that the presence of such a change in chloroplast membranes is not necessarily correlated with chilling sensitivity.     

Contribution of Oxidative Stress to the Development of Cold-Induced Damage to Leaves of Chilling-Sensitive Plants: 2. The Activity of Antioxidant Enzymes during Plant Chilling

Changes in the activities of cytosolic superoxide dismutase, ascorbate peroxidase, and catalase were studied in 7–11-day-old seedlings of maize (Zea mays L.), cucumber (Cucumis sativus L.), millet (Panicum miliaceum L.), and etiolated potato (Solanum tuberosum L.) sprouts. The assays were performed immediately after chilling at 2°C for 1–24 h and one day after 24-h chilling. During the first 1–2 h of chilling, enzyme activities were substantially reduced in chilling-sensitive plants (cucumber and maize). Further chilling resulted in a gradual increase in the enzyme activities to a degree dependent on plant species. One day after the plants were returned to a high temperature, the enzyme activities were restored to an initial level or exceeded it (excluding maize superoxide dismutase). In the potato (cold-resistant species), we did not observe any regular changes in the activities of antioxidant enzymes. On the whole, the activities of these enzymes inversely depended on species cold-resistance. The conclusion is that one of the cold-resistance factors is the capacity of antioxidant enzymes to maintain their activities during chilling and restore them relatively rapidly after plant transfer to warm conditions.     

Prior temperature exposure affects subsequent chilling sensitivity

The chilling sensitivity of small discs or segments of tissue excised from chillingsensitive species was significantly altered by prior temperature exposure subsequent to holding the tissue at chilling temperatures as measured by a number of physiological processes sensitive to chilling. This temperature conditioning was reversible by an additional temperature exposure before chilling, and mature-green and red-ripe tomato tissue exhibit similar chilling sensitivities. Exposing pericarp discs excised from tomato fruit (Lycopersicon esculentum Mill. cv. Castelmart), a chilling-sensitive species, to temperatures from 0 to 37°C for 6 h before chilling the discs at 2.5°C for 4 days significantly altered the rate of ion leakage from the discs, but had no effect on the rate of ion leakage before chilling and only a minimal effect on discs held at a non-chilling temperature of 12°C. Exposing chillingsensitive tissue to temperatures below that required to induce heat-shock proteins but above 20°C significantly increased chilling sensitivity as compared to tissue exposed to temperatures between 10 and 20°C. Rates of ion leakage after 4 days of chilling at 2.5°C were higher from fruit and vegetative tissue of chilling-sensitive species (Cucumis sativus L. cv. Poinsett 76, and Cucurbita pepo L. cv. Young Beauty) that were previously exposed for 6 h to 32°C than from similar tissue exposed to 12°C. Exposure to 32 and 12°C had no effect on the rate of ion leakage from fruit tissue of chilling tolerant species (Malus domestica Borkh. cv. Golden Delicious, Pyrus communis L. cv. Bartlett). Ethylene and CO₂ production were higher and lycopene synthesis was lower in chilled tomato pericarp discs that were previously exposed for 6 h to 32°C than the values from tissue exposed to 12°C for 6 h before chilling. Increased chilling sensitivity induced by a 6 h exposure to 32°C could be reversed by subsequent exposure to 12°C for 6 h.     

Combined NMR-observation of cold denaturation in supercooled water and heat denaturation enables accurate measurement of ΔC p of protein unfolding

Cold and heat denaturation of the double mutant Arg 3→Glu/Leu 66→Glu of cold shock protein Csp of Bacillus caldolyticus was monitored using 1D ¹H NMR spectroscopy in the temperature range from −12°C in supercooled water up to +70°C. The fraction of unfolded protein, f _u, was determined as a function of the temperature. The data characterizing the unfolding transitions could be consistently interpreted in the framework of two-state models: cold and heat denaturation temperatures were determined to be −11°C and 39°C, respectively. A joint fit to both cold and heat transition data enabled the accurate spectroscopic determination of the heat capacity difference between native and denatured state, ΔC _p of unfolding. The approach described in this letter, or a variant thereof, is generally applicable and promises to be of value for routine studies of protein folding.     

Phase Transition Temperatures Determined for Chloroplast Thylakoid Membranes and for Liposomes Prepared from Charged Lipids Extracted from Thylakoid Membranes of Higher Plants

Lipid phase separation temperatures of intact thylakoid membranesfrom a number of chilling sensitive plants were measured usingchlorophyll a as the intrinsic fluorescent probe. The phospho-and sulfolipids were extracted from the thylakoid lamellae ofthese plants and purified by silicic acid column and thin layerchromatographies. These separated lipids were eluted and recombinedto give a total charged anionic thylakoid lipid fraction thatwas used to prepare liposomes containing purified chlorophylla as the fluorescent probe. The phase separation temperaturesof these liposomes were compared to phase separation temperaturesin intact thylakoid membranes isolated from the same plants. The chilling-sensitive plants—corn, pepper, tomato andwater hyacinth — showed phase separation temperaturesranging from 9 to 19°C for both the liposomes and the thylakoidmembranes. In addition, low temperature phase separations wereseen from –21 to –27°C. Mimulus, which is notas chilling sensitive as the former plants, had a phase separationtemperature near 0 to 2.5°C and at –27°C. In general,there was a good agreement between the phase separation temperaturesof intact thylakoids and the purified anionic lipid fractionextracted from these thylakoids. Similar results were obtained using either trans-parinaric acidor chlorophyll a as the fluorescent probe in liposomes madefrom anionic thylakoid lipids or in liposomes prepared frompure dimyristoyl phosphatidyl choline, distearoyl phosphatidylcholine, or mixtures of equal amounts of these phospholipids. ¹ CIW-DPB Publication # 728. ³ Present address: Laboratory of Experimental Physics, Departmentof Biophysics, State University of Utrecht, Princetonplein 5,Utrecht, The Netherlands. (Received January 18, 1981; Accepted July 2, 1981)     

Low Temperature Effects on Early Vegetative Growth, Leaf Gas Exchange and Water Potential of Chilling-sensitive and Chilling-tolerant Crop Species

Two chilling-sensitive (Phaseolus vulgaris L., Zea mays L.)and two chilling-tolerant (Pisum sativum L., Spinacia oleraceaL.) species were raised in growth chambers under warm (28/18°Cday/night cycle) and cool (18/12°C) temperature regimes.Growth analysis techniques were used to evaluate leaf area andbiomass partitioning during early autotrophic growth. Plantsacclimated to both temperatures were measured for leaf gas exchangeand water potential (