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a Dep. of Crop and Soil Sciences, 3111 Miller Plant Sciences Bldg., Univ. of Georgia, Athens, GA 30602-7272 (current address: Dep. of Plant Agric., Univ. of Guelph, Guelph, ON N1G 2W1 Canada)
b USDA-ARS, Crop Protection and Manage. Res. Unit, Tifton, GA 31793
* Corresponding author (hjearl{at}uga.edu)
Received for publication June 18, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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II1200) for each plot. Crop dry matter accumulation was not linearly related to IPAR, due to decreased RUE in the water stress treatments. However, the linear relationship was restored when daily IPAR was multiplied by the current estimate of II1200, suggesting that II1200 can be used as an indicator of whole-crop RUE.
Abbreviations: APAR, absorbed PAR • DAP, days after planting • II, quantum efficiency of photosystem II • II1200, II at PPFD = 1200 µmol m-2 s-1 • HI, harvest index • IPAR, intercepted PAR • PAR, photosynthetically active radiation • PPFD, photosynthetic photon flux density • RUE, radiation use efficiency
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Decreased RUE is likely a major component of yield loss in maize under water deficit stress. Methods for measuring RUE of maize in the field, usually over periods of several weeks, are well established, and involve destructive measurements of aboveground crop dry matter combined with continuous (Tollenaar and Bruulsema, 1988; Tollenaar and Aguilera, 1992; Muchow and Sinclair, 1994) or periodic (Otegui et al., 1995; Westgate et al., 1997; Kiniry et al., 1998) measurements of canopy absorption of incident PAR. It is sometimes of interest to evaluate changes in RUE over short periods of time (hours or days), which precludes the direct measurement of changes in whole crop dry matter. The only way to make such short-term measurements at the whole canopy level is via measurement of net CO2 exchange, using either canopy enclosures (Jones at al., 1986) or micrometeorological techniques such as eddy flux covariance (Rochette et al., 1996); however, these techniques are generally unsuitable for small plot field experiments with many treatments. Since reductions in whole canopy RUE result from reduced RUE at the level of individual leaves, leaf gas exchange (net photosynthesis) measurements can provide a useful, semiquantitative indicator of short-term changes in crop RUE, given sufficient sampling of leaf positions within the canopy. Leaf gas exchange measurements of this type have led to an increased understanding of the short-term physiological responses of maize to water deficit and other stresses under field conditions (Ceulemans et al., 1988; Wolfe et al., 1988b; Dwyer et al., 1992). For C4 species such as maize, chlorophyll fluorometry may serve as a surrogate for leaf gas exchange measurements in assessing instantaneous leaf RUE under current PAR (Edwards and Baker, 1993; Earl and Tollenaar, 1998). Since each fluorescence measurement takes only a few seconds, hundreds of measurements can be made per day with a single instrument, thus greatly improving on the sampling resolution that can be achieved with leaf gas exchange techniques (Earl and Tollenaar, 1999).
Few studies have quantified the relative contributions of PAR absorption, RUE, and reduced HI to yield loss in maize exposed to water stress in the field. Thus, the first objective of the present work was to quantify the relative importance of these three factors in reducing maize yield under two different levels of drought stress. The second objective was to use chlorophyll fluorometry to characterize changes in leaf level RUE in maize under drought stress and on recovery from drought stress. Finally, we investigated how closely differences in leaf RUE among stress treatments, integrated over time, were correlated with treatment differences in whole crop RUE over the same time periods.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Irrigation was with pond water filtered through quartz sand using a swimming pool filter, and applied via surface drip tape with one tape per row and a 10-cm emitter spacing (Chapin Watermatics, Watertown, NY). System pressure was regulated between 70 and 80 kPa, and the resulting measured application rate was 0.42 cm h-1. The system design included a valve for each main plot, so that water application could be independently controlled for the purpose of applying the different irrigation treatments.
Experimental Design and Crop Dry Matter Measurements
This work was performed as part of a study to investigate the interactive effects of lesion nematode (Pratylenchus zeae Graham) infection and water stress on corn yield. The design was a split-plot with six replications. The main-plot factor was one of three irrigation treatments (control, mild water stress, severe water stress), and the subplot factor was one of three Telone II (1,3-dichloro-1-propene) application rates in 2000 (0, 9.4, or 56.2 L ha-1) or one of two Telone II application rates in 2001 (0 or 56.2 L ha-1). Telone II was injected at a depth of 40 cm 9 d before planting. Each subplot consisted of four 10-m rows. There were an additional four buffer rows between main plots and along the lateral borders of the experiment. Lateral borders were irrigated on the same schedule as the adjacent main plot. For buffer areas between main plots, two of the rows were irrigated with one main plot, and the other two with the other main plot. For the control treatment, we attempted to maintain plots water replete at all times by using a water budget approach that incorporated local measurements of daily pan evaporation; this was sufficient to prevent midday wilting from occurring at any point during the growing season. The mild stress treatment was irrigated half as frequently as the control, and the severe stress treatment was not irrigated at all after the sixth leaf stage, except for a single 1.5-cm application each year during the silking period.
Two destructive harvests were taken from each subplot, one near midseason (2 to 5 d before silking; 55 DAP in 2000, and 59 DAP in 2001) and one at physiological maturity (approximately 50% black layer formation in control plots; 111 DAP in 2000, and 114 DAP in 2001). Harvests were confined to the center two rows of each subplot, with two meters harvested per row (approximately 25 plants per harvest), and harvest areas were buffered from one another and from row ends by 2 m. For the first harvest, fresh weight of the entire sample and also of a six-plant subsample was determined in the field, and then the subsample was dried to constant weight at 80°C in a forced air drier. Dry weight of the entire sample was calculated from the subsample dry weight/fresh weight ratio and the total sample fresh weight. For the second harvest, a subsample of six plants was divided into ears and stover and dried to constant weight. Ears from the remaining plants in the harvest area were also harvested and dried. All ears were shelled to determine grain dry weight, and total aboveground dry matter was calculated from the subsample grain dry weight to total dry weight ratio and the total sample grain dry weight.
Canopy Interception and Chlorophyll Fluorescence Measurements
Beginning 3 wk after planting, canopy interception of incident PAR was estimated for each subplot once every 7 to 10 d. In 2000, this was done by measuring PAR at the bottom of the canopy using a line quantum sensor (LI-191SA, LI-COR, Lincoln NE) simultaneously with PAR incident at the top of the canopy with a point sensor (LI-190SA, LI-COR). Four measurements were taken within each subplot, two with the line sensor centered on a row, and two with the sensor centered between the rows. The fraction of incident PAR intercepted by the canopy was calculated for each reading, and the mean was taken as the estimate for the subplot. In 2001, canopy interception was measured with a SunScan canopy analysis system (Delta-T Devices, Cambridge, UK), which includes a 1-m probe for measuring PAR at the bottom of the canopy, and another sensor (model BF2) located outside of the canopy for measurement of incident PAR. In 2001, eight estimates of interception were made per subplot and averaged together. In both years, measurements of canopy interception were made on days with <20% cloud cover, within 1.5 h of solar noon. Also, canopy interception was logged at 15-min intervals for two subplots on several days during each of the 2 yr. Two LI-191SA line sensors, each in a different subplot, and one LI-190SA point sensor, positioned above the canopy, were connected to a data logger. Every third or fourth day, the line sensors were moved to different randomly chosen subplots. These data were used to examine the relationship between canopy interception during the 30-min period around solar noon and mean daily canopy interception. The point sensor had been recently calibrated by the manufacturer (traceable to the US National Institute of Standards and Technology), and was in turn used to calibrate the line sensors. Daily incident short-wave radiation was recorded by a weather station located within 400 m of the experimental site. Over the course of the experiment, the average ratio of daily incident photons in the PAR, measured by the calibrated LI-190SA point sensor, and daily incident solar radiation measured by the weather station was 2.19 mol MJ-1 (data not shown); this is within 7% of the value reported by Meek et al. (1984). Daily incident PAR was taken as 0.5 x total short-wave radiation (Szeicz, 1974).
Beginning 4 wk after planting, chlorophyll fluorescence measurements were made in each subplot approximately once per week within 2 h of solar noon, using a Mini-PAM chlorophyll fluorometer equipped with a 2030-B leaf clip holder (Heinz Walz GmbH, Effeltrich, Germany). Sampling protocols and instrument settings were as described in Earl and Tollenaar (1999). On each measuring day, 10 (2000) or 15 (2001) measurements were made per subplot on leaf tissue that was directly sunlit. Sunlit leaf tissue was randomly chosen within the canopy, except that the upper four leaves were rarely sampled once plants attained their full height. Care was taken before and during the measurement not to alter the natural leaf orientation with respect to the sun, or to shade the tissue to be measured. The steady state fluorescence value, FS, was first recorded, and then a saturating pulse of light was applied to the tissue using the instrument's halogen source, to induce the maximum fluorescence value (F'M). A micro-quantum sensor recorded the photosynthetic photon flux density (PPFD) incident normal to the leaf during the FS determination. The quantum efficiency of photosystem II (II) was calculated according to Genty et al. (1989) as
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This value equates to the efficiency with which photons absorbed by the chlorophyll of photosystem II are used to carry out charge separation in the reaction center, and can be used to calculate the linear electron transport rate when the absorbed PPFD and fractional distribution of photons to photosystem II are known (Genty et al., 1989). Because of the relative absence of photorespiration in C4 species such as maize, the electron transport rate is closely correlated with the gross photosynthetic CO2 assimilation rate (Edwards and Baker, 1993; Earl and Tollenaar, 1998). Thus, at any given PPFD level, II is linearly related to gross CO2 assimilation in maize, and may therefore be considered a direct indicator of leaf instantaneous RUE.
On each day that chlorophyll fluorescence was measured, "SPAD values" were determined for 10 leaves per subplot using a SPAD 502 Chlorophyll Meter (Minolta Corporation, Ramsey, NJ). These leaves were chosen using the same criteria as for chlorophyll fluorescence measurements. SPAD readings are based on measurements of transmittance through the leaf of red and far red light, and in maize are strongly correlated with leaf absorptance of PAR (Earl and Tollenaar, 1997). The mean SPAD value for each subplot on each measuring day was used to estimate leaf absorptance of incident PPFD, using the method described by Earl and Tollenaar (1997).
Data Analyses
Telone treatments were found to have no significant effect on any of the measured parameters, with the exception of a 3.7% increase (p = 0.02) in early season IPAR for the high Telone rate vs. the control (averaged across watering treatments and years—data not shown). For the purposes of the present work, all data were averaged within a main plot and the experiment was analyzed as a simple randomized complete block design, using the PROC ANOVA procedure in SAS (SAS Inst., Cary, NC). Means separations for irrigation treatment effects were performed with protected LSD tests. Early season flooding caused severe stunting in two of the main plots of one replication of the experiment in 2001; all data from this replication were discarded.
Chlorophyll fluorescence measurements were made over a broad range of leaf-normal PPFD levels, resulting from the naturally occurring variation in incident PPFD and leaf angles. Data from each main plot on each day were combined, and the II value at a PPFD level of 1200 µmol m-2 s-1 (II1200) was determined by interpolation from linear regression (PROC REG procedure in SAS) (Fig. 1)
. The II1200 value was used as the representative II for each main plot on each measuring day. This value was chosen because 1200 µmol m-2 s-1 was close to the average PPFD recorded during fluorescence measurements, and because II1200 could be estimated for every main plot on every measuring day without extrapolating beyond the actual data range.
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Grain yield losses attributable to different components (IPAR, RUE, and HI) were estimated using a simple path model. That is, component yield losses were assumed to occur in a specific order, consistent with a simple mechanistic model of yield formation (reduced IPAR acts first, followed by reduced RUE and finally by reduced HI). First, yield loss associated with reduced IPAR was estimated as:
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Table 2 shows the estimated component grain yield losses attributable to reductions in IPAR, RUE, and HI for the two stress treatments in each year. Reduced IPAR was always the smallest yield loss component, except under the mild stress treatment in 2001, when yield losses due to reduced HI were similarly small. In 2000, HI was the largest yield loss component under mild stress, while RUE was the largest yield loss component under severe stress.
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II1200 (Fig. 4)
. In 2000, there was a stress-induced reduction observed on one date in the early season, an extended period of severely reduced II1200 at midseason, and another period of reduced II1200 near the end of the season. In 2001, treatment effects on II1200 were mostly confined to the midseason, and were less severe than those observed in 2000. The pattern of II1200 in 2000 suggests that the control treatment may have suffered from some stress at midseason. In both years, II1200 of stressed plots recovered to near the level of control plots on rewatering; that is, there was little evidence of lasting damage to leaf photosynthetic capacity.
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The analysis presented in Fig. 5
illustrates the relationship between whole canopy RUE and II1200. During Period 1, the three treatments had similar whole canopy RUE, but during Period 2 whole canopy RUE differed between the treatments; that is, the points do not fall on a common line through the origin when dry matter accumulation is plotted against cumulative IPAR (left side of Fig. 5). To incorporate the effect of leaf level RUE into this analysis, the estimated value of IPAR for each plot on each day was multiplied by the estimated value of II1200 for that plot on that day, derived from the interpolation/extrapolation shown in Fig. 4. Thus, for each day, IPAR was adjusted for the estimated efficiency with which individual leaves could utilize the intercepted radiation. The product of IPAR and II1200 integrated over time was strongly linearly related to whole canopy dry matter accumulation during the latter half of the season (Period 2) (Fig. 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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II indicated severe reductions in leaf photosynthesis in the period immediately after silking (Fig. 4), the most sensitive period for kernel set. There have been few attempts to quantify the importance of IPAR as a yield loss component in maize under different levels of water deficit stress. Wolfe et al. (1988a) recorded green leaf area duration under irrigated and nonirrigated conditions, but did not measure IPAR. Stone et al. (2001) reported that reduced radiation interception was an important yield loss component for sweet corn exposed to a range of water stress treatments, although in that study radiation interception was calculated from leaf area measurements rather than measured directly. In the present work, early season water stress was too mild to produce large differences in leaf area expansion, and so all three treatments had similar PAR interception values on those days when leaf rolling did not occur in the stress treatments (Fig. 4). The IPAR might have been a more important yield loss component if severe and lasting water stress had occurred earlier in the season.
The method used to arrive at the estimates of yield loss components presented in Table 2 (calculations described in Materials and Methods) is useful for quantifying the relative magnitude of the three different yield-limiting factors in final analysis only—it should not be used in a predictive manner. That is, it should not be assumed that circumventing one of the yield loss components would have restored exactly the amount of yield associated with that component in Table 2. The three yield loss components are physiologically interdependent; eliminating one may affect the others either positively or negatively. For example, if IPAR had been greater in the stress treatments and this resulted in greater whole canopy water use, RUE may have been lower because of greater water stress at the leaf level. As another example, if RUE had been higher, HI might also have increased if the resulting extra photosynthate helped to prevent kernel abortion and therefore sink limitation during the grain-filling period.
Radiation use efficiency in the present study was calculated on an IPAR basis, as opposed to the more rigorous absorbed PAR (APAR) basis, which also requires the measurement of canopy reflectance and soil reflectance. It is difficult to directly compare data between studies that use these two different methods (Bonhomme, 2000), but the RUE values observed under well watered conditions are similar to those reported by others using the IPAR method for maize. Our early season RUE estimates for control plots (2.83 g MJ-1 on average) were lower than the average (3.5 g MJ-1) of 12 studies reviewed by Kiniry et al. (1989). This may be attributable to differences in the estimation of PAR from measurements of total solar radiation; we assumed 50% of solar radiation was PAR (Szeicz, 1974), but for comparison with some other work a value of 45% may be appropriate (Meek et al., 1984). On that basis, our average early season RUE for control plots is 3.14 g MJ-1, well within the range of estimates reported by Kiniry et al. (1989). Westgate et al. (1997) used the 50% conversion factor and reported RUE values very similar to those in the present study. Estimates of RUE can be strongly influenced by minor differences in experimental protocols (Gallo et al., 1993). Maize RUE is also affected by factors such as crop variety (Tollenaar and Aguilera, 1992; Westgate et al., 1997), population density (Major et al., 1991), soil water availability (present work; Jones et al., 1986; Stone et al., 2001), fertility (Muchow and Sinclair, 1994), and cool night temperatures (McGinn and King, 1990; Major et al., 1991). Since the canopy photosynthetic response to incident PAR is nonlinear (Rochette et al., 1996), experiments conducted in regions with higher average PAR during the growing season should generally yield lower RUE estimates. Late-season RUE for maize is often lower than early season RUE (e.g., Otegui et al., 1995), which is consistent with the progressive loss of leaf photosynthetic capacity during the latter half of the season (Fig. 4; also, Earl and Tollenaar, 1999). However, crop RUE sometimes remains relatively stable (Muchow and Sinclair, 1994) or even increases (Tollenaar and Aguilera, 1992) during the grain filling stage. Comparisons between early season and late-season RUE will be affected by seasonal variation in environmental factors, as discussed above, and also by the timing of the final dry matter harvest relative to the progression of leaf senescence. In the present work, the final harvest occurred at 50% black layer formation, and early and late season RUE for control plots were very similar (Table 1), despite an apparent decline in leaf photosynthetic activity (Fig. 4).
Because the stress treatments sometimes had lower leaf absorptances than the control (Fig. 4), canopy reflectance of intercepted light may also have been higher in the stress treatments. This would bias the estimate of whole canopy RUE toward artificially low numbers in the stress treatments, since RUE was calculated using intercepted rather than absorbed PAR. However, based on the typical 5% reflectance of unstressed maize canopies (Tollenaar and Bruulsema, 1988; Tollenaar and Aguilera, 1992), and assuming that (i) changes in canopy reflectance are proportional to changes in leaf reflectance, and (ii) leaf reflectance accounts for about two-thirds of total light scattering by maize leaves (Earl and Tollenaar, 1997), we estimate that canopy reflectance of the control and severe stress treatments would differ by approximately 2% of IPAR (calculations not shown) on those days when treatment differences in leaf absorptance were at their maximum (i.e., the middle and end of the 2000 growing season in Fig. 4). Therefore, the bias in RUE estimates mentioned above would be something <2%, which is small relative to the Period 2 treatment differences in RUE reported in Table 1.
Leaf-level RUE in control plots, quantified as II1200, displayed a clear late-season decline in 2001 (Fig. 4), which is consistent with the observations of Earl and Tollenaar (1999). This characteristic pattern was not as obvious in 2000, perhaps because fluorescence measurements were terminated earlier in the season, but also because a midseason decline and subsequent recovery of II1200 in the control treatment obscured the overall trend in this parameter. The reason for this midseason decline in control plots in 2000 is not known, but it is unlikely that soil water limitations were the only cause, since in several cases fluorescence measurements during that period were made the day following irrigation. Extremely high daytime temperatures during the midseason in 2000 (Fig. 2) may have played a role in suppressing leaf photosynthetic rates.
The drought stress treatments produced large, easily measurable differences in II1200 in these experiments, which were used to infer comparable differences in gross CO2 assimilation. This is based on the model that, under realistic drought stress conditions, the primary limitation to maize photosynthesis is reduced leaf internal CO2 concentration (ci) due to stomatal closure (Saccardy et al., 1996). Since the quantum efficiencies of PSII and gross CO2 assimilation remain almost directly proportional across a broad range of ci in maize (Genty et al., 1989; Edwards and Baker, 1993; but see also Lal and Edwards, 1996), CO2 assimilation at any given PPFD should vary in direct proportion with II. It should be noted that II in this work was estimated on an incident, rather than an absorbed PPFD basis (Fig. 1). Leaf absorptance estimated from SPAD readings was sometimes as much as 5% higher in the control than in the severe stress treatment (Fig. 4); thus, if II1200 had been determined on an absorbed PPFD basis, treatment differences would have been larger than shown in Fig. 4.
The observed midseason loss and then recovery of leaf absorptance (Fig. 4) was unexpected. The indirect method used to estimate leaf absorptance (based on SPAD readings) has not been evaluated for reliability across different levels of leaf water status, so the observed fluctuations in leaf absorptance may be in part artifactual. However, maize leaf chlorophyll content has previously been observed to decline during drought stress, and then recover again on rewatering (Sanchez et al., 1983).
An important question for crop modeling and irrigation management is whether drought stress leading to severe reductions in leaf photosynthesis has any effect on subsequent leaf photosynthetic capacity following restoration of soil water content. There are few field data available that directly address this question. Using plants grown indoors under very low PPFD, Hao et al. (1999) found that electron transport capacity in maize was directly inhibited by even moderate water stress, and that it did not recover on rewatering. Working with maize plants grown under controlled environment conditions and moderate PPFD, Lal and Edwards (1996) reported that photosynthetic rates recovered completely 2 to 4 d after rewatering, following a water stress that was sufficient to reduce CO2 assimilation to approximately 5% of that of unstressed plants. Sanchez et al. (1983) worked with maize plants growing in the field in sand/nutrient solution culture and found that a water stress that reduced net CO2 assimilation rates to zero for 5 d did not result in any residual effect on leaf photosynthesis, even 1 d after rewatering. Results of the present study (Fig. 4) support the conclusion that complete (2001) or nearly complete (2000) recovery of leaf photosynthetic capacity can occur with rewatering, even following extended periods of severe water stress.
As expected, water stress caused reductions in late-season crop RUE in both years of this study (Table 1; Fig. 5); this was quantified as a reduction in mean dry matter accumulation per unit IPAR during a period of approximately 55 d. Measurements of leaf photosynthetic activity should be diagnostic of changes in crop RUE over much shorter periods of time. However, whether such measurements are based on leaf gas exchange or on chlorophyll fluorescence measurements, they can only be considered semiquantitative indicators of crop RUE, since they do not provide an estimate of photosynthetic activity that is fully integrated either spatially (across all leaf area) or temporally. As such, it is not obvious how a parameter such as II1200 should be quantitatively related to whole crop RUE. When daily intercepted PAR was adjusted for daily II1200 and summed over Period 2, it was strongly linearly related with the change in crop dry matter (Fig. 5). This result suggests that II1200 may be a useful indicator of current crop RUE; that is, that it can be used to adjust intercepted PAR measurements for differences in current leaf-level RUE. A similar approach was used by Earl and Tollenaar (1999) to show that thylakoid electron transport rates at a PPFD level of 1200 µmol m-2 s-1 were well correlated with differences in crop growth rates between three different maize hybrids. Also, Dwyer et al. (1991) reported a linear relationship between crop growth rates of four maize hybrids and leaf net CO2 exchange rates at high PPFD (2000 µmol m-2 s-1).
In summary, reduction of whole crop RUE was an important limitation to yield in field-grown maize subjected to drought stress, even when HI was also strongly reduced. At the single leaf level, effects of drought stress on radiation use efficiency were detectable as changes in the efficiency of photosystem II measured using a simple chlorophyll fluorescence technique. The parameter II1200, derived from chlorophyll fluorescence measurements made at many sunlit leaf positions within the canopy, appears to be a useful indicator of drought stress effects on whole crop RUE.
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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