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Crop Science 42:1164-1172 (2002)
© 2002 Crop Science Society of America

CROP PHYSIOLOGY & METABOLISM

Response of Leaf Photosynthesis during the Grain-Filling Period of Maize to Duration of Cold Exposure, Acclimation, and Incident PPFD

J. Ying, E. A. Lee and M. Tollenaar*

Dep. of Plant Agriculture, Univ. of Guelph, Guelph, ON, N1G 2W1, Canada

* Corresponding author (mtollena{at}uoguelph.ca)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Maize (Zea mays L.) leaf photosynthesis during the grain-filling period is affected by low ({approx}4°C) night temperatures. Three factors that are potentially involved in this phenomenon were examined: (i) duration of cold exposure, (ii) acclimation prior to exposure to light, and (iii) level of incident photosynthetic photon flux density (PPFD) following cold exposure. Studies were carried out with plants grown hydroponically under both field and controlled-environment conditions. Three hybrids (‘Pride 5’, ‘Pioneer 3902’, and ‘Cargill 1877’) were used in the field experiments and Pioneer 3902 was used in controlled-environment experiments. Plants were exposed to 4°C in the dark for either 2 or 16 h and, subsequently, acclimated for either 0 or 1 h in the dark before exposure to high PPFD. Four incident PPFD levels (400, 650, 1200, and 2000 µmol m-2 s-1) after cold exposure were examined. Both duration of cold exposure and acclimation after cold exposure affected the reduction in leaf carbon exchange rate (CER). Leaf CER was reduced by 18.0% after a 2-h exposure and by 30.4% after a 16-h exposure to 4°C, and leaf CER was reduced by 20.4 and 28.0% for 1- and 0-h acclimation, respectively. Dark-adapted Fv/Fm (Fv = variable fluorescence; Fm = maximum chlorophyll fluorescence), that is, maximum quantum efficiency of Photosystem II, was 0.71 after cold exposure during the night compared with 0.81 for the control. The Fv/Fm was affected by duration of cold exposure (0.74 and 0.68 for 2- and 16-h exposure, respectively) but not by acclimation. Reduction in leaf photosynthesis after cold exposure was linearly related to the incident PPFD level. Results support the contention that the reduction in CER due to low night temperature is not associated with photoinhibition.

Abbreviations: CER, carbon exchange rate • LED, light-emitting diode • PPFD, photosynthetic photon flux density • PSII, Photosystem II


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
CROPS ORIGINATING FROM THE TROPICS AND SUBTROPICS are greatly influenced by low temperature when grown in temperate regions. Maize (Zea mays L.), which originated in the subtropics, is particularly sensitive to low temperature at all stages of development (Miedema, 1982; Hope et al., 1992; Hodges et al., 1997; Ying et al., 2000; Staebler, 2001). Leaf CER is often the first physiological process to be inhibited by low or suboptimal temperature (Öquist, 1983; Wise, 1995; Kratsch and Wise, 2000). Exposure of maize plants to low temperatures during the growing season results in a significant depression in leaf CER and quantum efficiency of PSII, measured as the ratio of variable (Fv) to maximum (Fm) chlorophyll fluorescence (Fv/Fm) (Smillie et al., 1988; Hallgren and Öquist, 1990; Aguilera et al., 1999; Ying et al., 2000). Genetic variation does exist for the severity of the response to low temperatures for several parameters such as leaf CER, quantum efficiency of PSII, rate of development, and rate of dry matter accumulation (Hetherington et al., 1983; Fracheboud et al., 1999; Ying et al., 2000; Staebler, 2001).

Several factors appear to play a role in the severity of the effect that low temperature has on leaf CER and Fv/Fm in maize. Reduction in leaf CER has been closely associated with the extent and duration of low temperature exposure. Decreases in CER ranging from 5 to 30% in maize grown for 24 h at a 8/4°C day/night temperature (Wolfe, 1991), to 40% following exposure to two consecutive nights <3°C (Fuentes and King, 1989) have been reported. High PPFD exacerbates the impact of low temperatures on leaf CER and Fv/Fm (Farage and Long, 1987; Andrews et al., 1995), perhaps through photoinhibition. Photoinhibition occurs when the light energy captured by chlorophyll is in excess of that which can be used in photochemistry or dissipated by other means. The excess energy often produces reactive oxygen species, which result in photo-oxidative damage to the photosynthetic apparatus (van Hasselt and van Berlo, 1980). Photosystem II is the most vulnerable part of the photosynthetic apparatus, with damage to PSII often the first result of stress (Maxwell and Johnson, 2000).

Low temperatures (i.e., <10°C) coinciding with bright mornings (i.e., high incident PPFD) occur frequently during the grain-filling period of maize grown in Ontario. Duration of the cold period and level of incident PPFD could influence the reduction in leaf CER. Decreases in leaf CER of field-grown maize after a minimum morning temperature of 9.6°C ranged from 18 to 30% (Dwyer and Tollenaar 1989). A similar reduction in leaf CER was shown in a more recent study after an exposure to 4°C for 16 h (Ying et al., 2000). The similarity in the responses of leaf CER in the two reports is surprising, because both the minimum night temperature was lower (i.e., 4 vs. 9.6°C) and the duration of the exposure was much longer in the latter study (Ying et al., 2000). In the Dwyer and Tollenaar (1989) study, the minimum temperature under field conditions probably occurred during only a short period before sunrise. The apparent discrepancies between the two studies may be attributable, in part, to differences in the duration of the low temperature stress as well as recovery time (acclimation) prior to exposure to high incident PPFD. In the more recent study (Ying et al., 2000), plants were acclimated at room temperature in the dark for 1 h before exposure to light, whereas plants in the Dwyer and Tollenaar (1989) study probably experienced the lowest temperature just before sunrise. The objective of the current study was to examine three potential extenuating factors that may contribute to decreases in leaf CER and Fv/Fm following exposure to low temperatures during the grain-filling period: (i) duration and timing of low temperature exposure, (ii) acclimation prior to exposure to light, and (iii) incident PPFD level following low temperature exposure.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Field Studies
Experiments were conducted in 2000 at the Cambridge Research Station, Cambridge, ON (43°39' N, 80°25' W and 376 m above sea level), using a hydroponic system in the field (Tollenaar and Migus, 1984; Ying et al., 2000). In short, the system consisted of an automatic pumping system, water supply system, nutrient injection system, and 22.5-L plastic pails filled with Turface baked montmorillonite clay (International Minerals and Chemical Corp., Blue Mountain, MS). Pails were watered three times a day using a nutrient solution as described by Tollenaar (1989). Application of nutrient solution to the pails was controlled by a timer. The duration of the application was set such that nutrient solution drained from the bottom of the pails. Once a week, pails were flushed with water to prevent salt accumulation. Three seeds were planted on 9 May 2000, and seedlings were thinned at the 3-leaf stage to two plants per pail. Pails were arranged at 0.35 m between pail centers within a row and 1.42 m between rows so that the plant density was 40 000 plants ha-1. Plants in the end pails of each row and one row at each side of the experimental area were used as border. Plants were allowed to open-pollinate and all measurements were taken on plants with a fertilized ear.

Treatments consisted of three short-season maize hybrids (Pride 5, Pioneer 3902, and Cargill 1877), two durations of cold exposure during the night (2 h and 16 h), and two acclimation periods in the dark at an ambient temperature similar to that in the field (0 h and 1 h) prior to transferring the plants to the field. The experimental design was a split-split-split-plot-in-time with three replications. The main factor was hybrids, subfactor was duration of cold exposure, sub-subfactor was acclimation, and the sub-sub-subfactor was measuring time (1100 and 1500 h). The experimental unit was one pail (i.e., two plants) per treatment in each replication. Cold stress was imposed on the plants by placing pails in a dark 4°C cold room during the night at silking, and at 1, 2, 3, and 5 wk after silking. Control plants remained in the field; previous work showed no significant differences between control plants left in the field and those moved into the building during the night (Ying et al., 2000). A computer-based portable temperature monitoring systems was installed to measure the air temperature in the cold room. Results of previous experiments (Ying et al., 2000) showed that leaf temperature declined to cold-room temperature within 6 min after placing the plants in the 4°C cold room and leaf temperature attained ambient air temperature within 20 to 25 min after plants were moved out of the cold room. Also, soil temperature declined at a rate of {approx}1°C h-1 at 0.2 m below soil surface after the plants were moved into the cold room, and soil temperature increased from 6°C at the end of the 16-h cold period, to 15°C after 3.5 h, and to 20°C after 6 h. In the present study, all pails that were used for leaf measurements were flushed with water immediately after transferal of the plants in the low-temperature treatment from the building to the field, and the temperature of the water was {approx}20°C. Plants that were acclimated, were placed in a dark room inside a building without temperature control, that is, ambient temperature was similar to that outside in the field, between 0900 and 1000 h and, subsequently, transferred to the field. Nonacclimated plants were transferred immediately from the cold room to the field at 0900h. The schedule in Fig. 1 was used for transferring plants.



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  		Fig. 1. Schedule for 4°C exposure of maize plants in a dark cold room, acclimation after cold exposure in a dark room and ambient temperature, and transferral to the field.

 
Climate data were collected using a data logger (CR-10, Campbell Scientific Ltd., Logan, UT) {approx}20 m from the experimental area in the field. Accumulated daily photosynthetically active irradiation was measured with a pyranometer sensor (LI-200B, LI-COR, Inc., Lincoln, NE) located {approx}3 m above the soil. Type-T thermocouples (No. 22, Thermoelectronic Canada Ltd., Brampton, ON, Canada), positioned within a model 41004-5 gill multi-plate radiation shield (Campbell Scientific) {approx}2 m above the soil were used to record maximum and minimum temperatures.

Controlled-Environment Studies
Two experiments were conducted in controlled-environment growth cabinets (Model PGW36, Conviron, Winnipeg, MB, Canada). In each experiment, the maize hybrid Pioneer 3902 was grown in 22.5-L plastic pails filled with Turface. Plants were grown under a 26/16°C day/night temperature regime, 16 h photoperiod, 75% relative humidity, and 650 µmol m-2 s-1 incident PPFD at the top of the crop canopy that was supplied by a mixture of cool white fluorescent tubes and inside frost tungsten bulbs (Osram Sylvania, Drummondville, QC, Canada). Three seeds per pail were planted, and seedlings were thinned at the 3-leaf stage to one per pail. Pails were watered daily using a nutrient solution as described by Tollenaar (1989). Pails in the growth cabinet were rotated periodically to minimize position-induced plant-to-plant variability. Air temperature in each growth cabinet was continuously monitored with four thermocouples positioned close to the whorls of four plants. Plants were grown in growth cabinets until the 15-leaf stage, and then moved to a growth room for a period of {approx}2 wk. Conditions in the growth room were similar to those in the growth cabinets except that PPFD at the top of the canopy was 350 µmol m-2 s-1. Ears were pollinated at silking. Due to the height limitation of the growth cabinet, the tassel and two topmost leaves of all plants were removed when the plants were returned to the growth cabinets. Cold stress was imposed on the plants by placing pails in a 4°C cold room during a 16-h dark period, whereas the control plants remained in the growth cabinet programmed at the same photoperiod.

The first experiment was carried out at 3 wk after silking; treatments were a duration of cold exposure (2 and 16 h) and a duration of acclimation (0 and 1 h acclimation at 20°C in the dark). The experimental design was a split-split-plot-in time with three replications and one plant per replication. The main factor was duration of cold exposure, subfactor was acclimation period, and the sub-subfactor was measuring time. Timing and procedure of plant transfer were similar to those described for the field experiment. Plants were placed at 1000 h in a 26°C growth room under a microwave lamp (Model VBL-3400, Hutchins International, Mississauga, ON, Canada) that resulted in 2000 µmol m-2 s-1 PPFD at the top of the canopy. In the second experiment, treatments were three levels of PPFD (400, 650, and 1200 µmol m-2 s-1) that followed a 16-h cold exposure, and CER was measured at 1000, 1200, 1400, and 1500 h in the 26°C growth room. The experimental design was a split-plot-in-time with three replications. Incident PPFD level was treated as the main factor and measuring times as the subfactor with one plant per replication. Incident PPFD was controlled by adjusting the distance between the top of the canopy and the microwave lamp, and the light-emitting diode (LED) light source of the LI-6400 (see below) was set at the treatment PPFD when leaf CER measurements were made. Leaf temperature was controlled during CER measurements (see below), but leaf temperature between measurements may have differed among the three PPFD treatments, although differences were likely small because of the low heat output of the microwave lamp and a high fan speed in the room.

Leaf Photosynthesis Measurements and Statistical Analyses
Leaf CER was measured using a portable, open-flow gas exchange system LI-6400 (LI-COR) at 2000 µmol m-2 s-1 PPFD at the leaf surface using 6400-02 LED light source (LI-COR) for all experiments except the second experiment in the controlled-environment studies. Measurements were taken on the first leaf above the topmost ear that was usually sun-lit in the field. Cloudless days were selected for taking the measurements because incident PPFD prior to measurement can influence leaf CER (Earl and Tollenaar, 1998). Leaf CER was measured for a 6-cm2 area of the leaf blade, which did not include the midrib. The flow rate of air through the chamber and sample side IRGA was set to 500 µmol s-1 in order to minimize the system response time to a change in CER. The CO2 concentration of the intake air was maintained at 350 µL L-1 using the 6400-01 CO2 injector (LI-COR). Leaf temperature was maintained at 28 ± 1°C by the LI-6400's Peltier thermoelectric coolers. Leaf CER, leaf conductance, and leaf internal CO2 was calculated by the LI-6400's operating software, which follows the method of von Caemmerer and Farquhar (1981). Leaf conductance is the inverse of the sum of the stomatal and boundary layer resistances.

The ratio of variable to maximum chlorophyll fluorescence (Fv/Fm) of dark-adapted leaves provides a means for quantifying maximum quantum efficiency. Chlorophyll fluorescence was measured using a Photosynthesis Yield Analyzer Mini-PAM (Heinz Walz GmbH, Effeltrich, Germany). The measuring light modulation frequency was set at 20 kHz for field conditions and at 0.6 kHz for indoor use to avoid signal noise. The gain, damping, and measuring light intensity were set in levels of 4, 2, and 12, respectively. The saturation pulse of light used to induce the maximum fluorescence level of the sample was 0.8 s in duration, and provided a PPFD of {approx}10 000 µmol m-2 s-1 at the leaf surface (Ying et al., 2000). Measurements were taken on the 1st leaf above the topmost ear. Measurements were taken before plants were moved out of the cold room in the morning and 1.5 h after being returned to the field. All measurements in the field were taken after the leaves were darkened for {approx}30 min using leaf clips (King Lynn, Norfolk, UK). Measurements were taken 2 to 3 s after the fiber probe was inserted in the leaf clip.

Data of the field experiment and the first experiment in the controlled-environment study were analyzed using the general linear models (PROC GLM) procedure of SAS (SAS Institute, 1996). A repeated-measures analysis of variance was used for the second experiment in the controlled-environment study. Data were analyzed using PROC MIXED in SAS according to the split-plot-in-time approach. Photosynthetic photon flux density level was treated as the main factor and measuring time was treated as in time subfactor. Carbon exchange rate was analyzed both as percentage reduction from the control and as an absolute value, while only measured values were analyzed for Fv/Fm.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Leaf Photosynthesis of Field-Grown Control Plants during the Grain-Filling Period
Variations in maximum and minimum temperature were large, with temperatures <10°C frequently observed during the grain-filling period (Fig. 2) . The average maximum air temperature was 24.6°C in August and 20.6°C in September, while the average minimum temperature was 12.8°C in August and 8.4°C in September. In August, the lowest temperature was 4.9°C and the minimum temperature was <10°C during seven of the 31 nights. In September, the lowest temperature was -1.4°C and the minimum temperature was <10°C during 22 of 30 nights. The number of days with a minimum temperature <10°C was similar to that observed in 1999 at the Cambridge Research Station (Ying et al., 2000), and nearly identical to the average for the period from 1986 to 1998 at the nearby Elora Experimental Station (i.e., 7 d in August, 18 d in September).



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  		Fig. 2. Daily maximum (top line) and minimum (bottom line) temperatures from 1 May to 30 Sept. 2000 at the Cambridge Research Station, Cambridge, ON, Canada.

 
The three hybrids used in this study did not vary greatly in either their leaf CER rates at silking (Fig. 3) or in their silking dates. Silking dates were 31 July for Pride 5, 3 August for Pioneer 3902, and 2 August for Cargill 1877. Differences between the hybrids began to appear {approx}1 wk after silking. Leaf CER declined from 1 wk after silking to 5 wk after silking for all three hybrids. The linear rate of decline in CER during this period was significantly different for all three hybrids. Leaf CER of Pride 5 declined from 38.2 µmol CO2 m-2 s-1 at 1 wk after silking to 15.9 µmol CO2 m-2 s-1 5 wk after silking, resulting in a linear rate of decline of 4.4 ± 0.80 µmol CO2 m-2 s-1 per wk. Leaf CER in Pioneer 3902 and Cargill 1877 exhibited a similar pattern of developmental progression: from 41.9 to 24.8 µmol CO2 m-2 s-1 for Pioneer 3902, with a linear rate of decline of 3.3 ± 0.78 µmol CO2 m-2 s-1 wk-1; and from 38.2 to 26.4 µmol CO2 m-2 s-1 for Cargill 1877, with a linear rate of decline of 2.6 ± 0.62 µmol CO2 m-2 s-1 wk-1. Leaf CER declined linearly after silking and the rate of decline was 70% greater in Pride 5 than in Cargill 1877 (Fig. 3). A decline in maize leaf CER after silking has been reported in several studies (Dwyer and Tollenaar, 1989; Dwyer et al., 1989; Ying et al., 2000).



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  		Fig. 3. Leaf carbon exchange rate (CER) and the reduction in leaf CER from silking to 5 wk after silking of maize hybrids ‘Pride 5’, ‘Pioneer 3902’, and ‘Cargill 1877’. Data shown are means of three replications of two plants at 1100 h on day following 16-h cold exposure in the dark and 1 h acclimation in the dark.

 
Exposure to low temperature significantly reduced leaf CER (Table 1) and maximum quantum efficiency of PSII (Table 2), measured as dark-adapted chlorophyll fluorescence (Fv/Fm). The reduction in leaf CER across all treatments and stages of development due to cold treatments was greater at 1100 than at 1500 h (26.5 vs. 21.9%). The reduction in leaf CER across all treatments and stages of development was greater in Pride 5 (32.3%) than in Pioneer 3902 (21.6%) and Cargill 1877 (18.6%). Maximum quantum efficiency of PSII after plants were exposed to high PPFD following cold exposure differed from that of the control across all treatments and stages of development (0.71 vs. 0.81), but there were no differences in maximum quantum efficiency of PSII among the hybrids in the response to cold exposure.


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  		Table 1. Reductions in leaf carbon exchange rate (CER) of three maize hybrids during the grain-filling period. Plants were either acclimated for 1 h in the building (dark) or directly moved to the field after exposure to 4°C in cold room for either 2 or 16 h during the previous night. Data are the means of leaf CER measurements taken at 1100 and 1500 h.

 

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  		Table 2. The ratio of variable to maximum chlorophyll fluorescence (Fv/Fm) of dark-adapted leaves of three hybrids that were exposed to a low night temperature during the grain-filling period. Plants were acclimated for either 1 h in the building (dark) or directly moved to the field after exposure to 4°C in cold room for either 2 or 16 h during the previous night. Measurements were taken after leaves were dark adapted at 1100 h for 30 min using leaf clips. The dark-adapted Fv/Fm of control plants was 0.81.*§

 
Effect of the Duration of Cold Exposure on Leaf CER and Dark-Adapted Chlorophyll Fluorescence
The impact of low night temperature treatment on CER was influenced by the duration of cold exposure (Table 1). Across all treatments and stages of development, the reduction in CER was greater for the 16-h cold exposure compared with the 2-h cold exposure (30.4 vs. 18.0%), and there was no interaction between time of measurement and duration of cold exposure (i.e., difference between the two treatments was 12.8% in the morning and 12.0% in the afternoon; P < 0.50). Pioneer 3902 grown under controlled-environment conditions showed a reduction in leaf CER following low temperature exposure comparable with that observed in the field experiment (Table 3) and the response of leaf CER to the 16-h and 2-h cold exposure was similar to that in the field study (i.e., 30.8 vs. 16.4%).


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  		Table 3. Reductions in leaf carbon exchange rate (CER) due to cold exposure in the hybrid ‘Pioneer 3902’ relative to control plants grown under controlled-environment condition at silking. Plants were acclimated for either 0 to 1 h after exposure to 4°C for 2 or 16 h in the previous night. Data are the means of leaf CER measurements made at 1100 and 1500 h. Leaf CER of control plants was 43.2 µmol CO2 m-2 s-1.

 
The maximum quantum efficiency of PSII (Fv/Fm) was significantly affected by duration of cold exposure during the night (Tables 2 and 4). Dark-adapted Fv/Fm was influenced by low temperature both at the end of the period of cold exposure and after a 1-h exposure to high PPFD following cold exposure. The observed reduction in maximum quantum efficiency of PSII in cold-exposed plants prior to exposure to incident PPFD is in contrast to numerous reports in the literature that showed that maximum quantum efficiency of PSII is rarely compromised immediately after exposure to low temperatures in the dark (Allen and Ort, 2001). Even more surprising was that Fv/Fm readings obtained immediately before transfer of plants out of the cold room and before exposure to incident PPFD were not different from those obtained following a 1-h exposure to high incident PPFD levels (Table 4). Our results indicate that the reduction in maximum quantum efficiency of PSII was not caused by photoinhibition.


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  		Table 4. Dark-adapted chlorophyll fluorescence (Fv/Fm) at the end of the cold exposure and after a 1-h exposure to light of plants exposed to 4°C during either a 2- or a 16-h period. Means of three hybrids across four stages of development.

 
There was a significant hybrid x duration interaction for the reduction leaf CER at four out of five stages of development (Table 1), and for Fv/Fm at two out of four stages of development (Table 2). The hybrid x duration interactions were not due to changes in rank of the hybrids between the 16- and 2-h cold exposure, but because differences in leaf CER reductions among hybrids were greater after a 16-h cold exposure then after a 2-h cold exposure (Fig. 4a) . Chlorophyll fluorescence showed a similar response (Fig. 4b). Genotypic differences in CER response to low temperatures and the lack of genotypic differences in the Fv/Fm response to low temperature that were observed in this study are consistent with those reported in Ying et al. (2000).



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  		Fig. 4. (a) Leaf carbon exchange rate (CER) of three hybrids after a 4°C exposure in the dark for either 16 or 2 h and field control across five stages of development during the grain-filling period, and (b) the ratio of variable to maximum chlorophyll fluorescence (Fv/Fm) of dark-adapted leaves of three hybrids after a 4°C exposure in the dark for either 2 or 16 h across two stages of development (i.e., 1 and 3 wk after silking). Measurements were taken after 1-h exposure to high photosynthetic photon flux density following cold exposure.

 
Effect of Acclimation on Leaf Carbon Exchange Rate and Dark-Adapted Chlorophyll Fluorescence
The impact of low temperature during the night on leaf CER was affected by acclimation in the dark at a temperature similar to that of the control, before exposure to high PPFD (Tables 1 and 3). Across all stages of development in field-grown plants, the reduction in CER was 28.0% for 0-h acclimation and 20.4% for 1-h acclimation. The difference in the reduction in leaf CER between 0- and 1-h acclimation was 8.9% in the morning and 6.3% in the afternoon across stages of development, hybrids, and duration of cold exposure, and this interaction was significant at P < 0.07. For plants grown under controlled-environment conditions, the reduction in leaf CER was 27.4% for no acclimation and 19.9% for 1-h acclimation in the dark (Table 3). The Fv/Fm was affected by acclimation only at one stage of development, that is, 1 wk after silking (Table 2). Results show that leaf CER recovers due to acclimation, but the recovery does not appear to be associated with differences in maximum efficiency of PSII.

Effect of Duration of Cold Exposure and Acclimation on Leaf Conductance and Internal CO2 Concentration
The reductions in leaf conductance and internal CO2 concentration due to a 16-h cold exposure, that is, 30 and 29%, respectively (Table 5), were similar to the reduction in leaf CER due to a 16-h cold exposure, or 31%. The concentration of CO2 in the stomatal cavity, that is, the internal CO2 concentration, is a result of the difference between the influx of CO2 via the stomata and the efflux of CO2 via uptake by the dark reactions of photosynthesis. In general, neither duration of cold exposure in the dark nor acclimation significantly influenced the reduction in leaf conductance and leaf internal CO2 after cold exposure. Leaf conductance of the hybrid Cargill 1877 was higher than that of the hybrid Pride 5 in both control and treatment plants, indicating greater influx of CO2 in the hybrid Cargill 1877. Leaf internal CO2 concentration was also greater in Cargill 1877 than in Pride 5; however, leaf internal CO2 concentration after cold exposure was lower in Cargill 1877 than Pride 5 in the 16-h cold-exposure treatments, indicating a greater uptake of CO2 in the dark reactions of photosynthesis in Cargill 1877. Hence, the higher tolerance of leaf CER to low night temperature in Cargill 1877 compared with Pride 5 (Table 1) appeared to be the result of a greater tolerance of both leaf conductance and dark reactions of photosynthesis.


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  		Table 5. Leaf conductance to water vapor and leaf internal CO2 concentration of three maize hybrids after a 4°C exposure in the dark across five stages of development during the grain-filling period.{dagger} Plants were acclimated for 1 h in the building room or directly moved to the field after cold exposure during either 2 or 16 h in the previous night. Means of two measurements during the day (1100 and 1500 h).

 
Effect of Incident Photosynthetic Photon Flux Density Levels on Leaf CER
Reduction in leaf CER after cold exposure during the night was positively correlated with an incident PPFD level following the low temperature exposure. Reductions in leaf CER after cold exposure in Pioneer 3902 grown under controlled-environment conditions were 18.7% at 400 µmol m-2 s-1, 21.3% at 650 µmol m-2 s-1, and 27.2% at 1200 µmol m-2 s-1. Leaf CER of the control plants increased from 14 µmol CO2 m-2 s-1 at 400 µmol m-2 s-1 PPFD to 40 µmol CO2 m-2 s-1 at 2000 µmol m-2 s-1 PPFD. The mean reduction of leaf CER after cold exposure in the hybrid Pioneer 3902 grown in the field was 30.4% when incident PPFD levels were 2000 µmol m-2 s-1. When taken together, results show a significant linear relationship between the reduction in leaf CER after cold exposure and incident PPFD (Fig. 5) . Consequently, it appears that cold-exposed plants are less capable of utilizing incident PPFD at high than at low levels of incident PPFD.



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  		Fig. 5. Relationship between reduction in leaf carbon exchange rate (CER) after a 16-h exposure to 4°C in the dark and incident photosynthetic photon flux density (PPFD) following cold exposure without acclimation in ‘Pioneer 3902’. In the growth-room study, plants were moved to PPFD levels of either 400, 650, or 1200 mmol m-2 s-1 at 0900 h, and depicted values are means derived from measurements made at 1000, 1200, 1400, and 1600 h. In the field study, plants were moved to the field at 1000 h, and the depicted value at 2000 µmol m-2 s-1 is a mean derived from measurements taken at 1100 and 1500 h across five stages of development (cf., Table 1).

 

   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
Reduction in leaf CER during the grain-filling period following low temperature exposure during the night was affected by duration of cold exposure in the dark, acclimation in the dark, and incident PPFD level following exposure. The effects of acclimation and incident PPFD on leaf CER implicate photoinhibition as a causal factor behind the reduction in leaf photosynthesis. The response of maximum quantum efficiency of PSII (Fv/Fm) to duration of low temperature exposure is similar to that observed for CER. However, other aspects regarding the effect on the maximum quantum efficiency of PSII due to cold exposure do not support the contention that photoinhibition is the causal factor behind the reduction in leaf photosynthesis. Surprisingly, the maximum quantum efficiency of PSII (Fv/Fm) was reduced in cold-exposed plants prior to exposure to incident PPFD and Fv/Fm measured at the end of the period of cold exposure was not different from that measured after 1-h exposure to high PPFD. By definition, photoinhibition is damage to PSII caused by exposure to high incident PPFD levels. Yet, our results show that the maximum quantum efficiency of PSII is reduced prior to exposure to high incident PPFD levels. Furthermore, recovery in photosynthesis (i.e., acclimation) was observed without a corresponding recovery in maximum quantum efficiency of PSII (Fv/Fm). Our results show that low temperature during the grain-filling period affects leaf photosynthesis partially through processes other than maximum quantum efficiency of PSII.


   ACKNOWLEDGMENTS
 
We are grateful for technical assistance by A. Aguilera and helpful comments on the manuscript by H.J. Earl, Univ. of Georgia. Financial support, in part, by the Ontario Ministry of Agriculture, Food, and Rural Affairs; the Ontario Corn Producers' Association; Pioneer Hi-Bred Ltd.; and Syngenta Seeds Canada, Inc., is gratefully acknowledged.

Received for publication June 6, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 


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