RESEARCH
Leaf Transpiration Efficiency of Sweet Corn Varieties from Three Eras of Breeding James A. Bunce*
ABSTRACT When measured under midday field conditions, modern varieties of maize (Zea mays L.) often have substomatal carbon dioxide concentration (Ci) values in excess of those required to saturate the photosynthetic carbon dioxide assimilation rate (A). This results in lower leaf transpiration efficiency (TE), the ratio of photosynthesis to transpiration, than potentially achievable for a given rate of photosynthesis. In some other crops, breeding has indirectly resulted in a large increase in stomatal conductance (gs), which would decrease TE. I tested whether this occurred in sweet corn by comparing five open-pollinated varieties released before 1903 with four standard hybrid varieties released in the mid-1900s and four varieties released after 1990. Leaf gas exchange of each variety was measured under ambient midday field conditions on eight sunny days over two seasons in Beltsville, MD. Although there were significant differences among varieties in gs, A, Ci, and TE, no effect of era was significant for any variable except A. Of the four modern varieties tested, two had the highest gs and two had the lowest gs of any of the varieties compared, with high gs associated with low TE. These four varieties were further compared in a third year and were found to differ consistently in leaf TE but not in A. It is concluded that breeding over the last century has not increased gs or decreased leaf TE in sweet corn but that there is significant variation in TE among modern sweet corn varieties.
J.A. Bunce, USDA-ARS, Crop Systems and Global Change Lab., Beltsville Agricultural Research Center, 10300 Baltimore Ave., Beltsville MD 20705-2350. Received 7 Sept. 2010. *Corresponding author (
[email protected]). Abbreviations: A, photosynthetic carbon dioxide assimilation rate, ASD, air saturation deficit for water vapor, Ci, substomatal carbon dioxide concentration, g s, stomatal conductance, LAVPD, leaf to air difference in water vapor pressure; (se), sugary enhancer; (su) normal sugary; TE, transpiration efficiency.
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ncreasing competition for fresh water resources and forecasts of increased frequency of drought provide motivation for attempting to increase the efficiency of water use in crop production. While carbon isotope discrimation during photosynthesis can be used to estimate leaf transpiration efficiency (TE), the ratio of photosynthesis to transpiration, in C3 species (Brugnoli and Farquhar, 2000), isotope ratios have not been reliable indicators of TE in C4 species (Cabrera-Bosquet et al., 2009). In C3 species, lines with high leaf TE, which can lead to high crop water use efficiency, often have slower growth rates because of lower photosynthetic carbon dioxide assimilation rate (A) (Condon et al., 2004; Blum, 2009). In C4 species, which have operational substomatal carbon dioxide concentrations (Ci) in excess of those required to saturate A, trade-offs between TE and A may not occur (Bunce, 2010). In such cases it should be possible to genetically decrease crop water use without decreasing growth. In wheat (Triticum aestivum L.), crop breeding has indirectly greatly increased leaf stomatal conductance (gs) (Fisher et al., 1998; Jiang et al., 2003). This may also be the case in rice (Oryza sativa L.) (Wang et al., 2005; Horrie et al., 2006), and in sugar Published in Crop Sci. 51:793–799 (2011). doi: 10.2135/cropsci2010.09.0509 Published online 27 Jan. 2011. © Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher.
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beet (Beta vulgaris L.) high-yielding lines under favorable conditions had higher g s than lower yielding lines (Ober et al., 2005). Increasing g s, by itself, would decrease leaf TE for both C3 and C4 species, although it may increase growth. In this experiment, I tested whether an increase in g s and decrease in TE with breeding has occurred in sweet corn (Zea mays L.). Sweet corn production in the United States has largely changed over the last century from open-pollinated varieties to normal sugary (su) hybrid varieties beginning in the 1930s and since the late 1980s to predominantly sugary enhancer (se) hybrid varieties (Marshall, 1987). I compared four or five varieties from each of these eras of breeding for gs, TE, Ci, and A in field tests over two seasons.
MATERIALS AND METHODS Era Comparison Thirteen varieties of sweet corn (Zea mays L.) were used in this test. The five open-pollinated varieties, Golden Bantam, Luther Hill, Stowell’s Evergreen, Black Mexican, and Country Gentleman, were all released before 1903. Seeds were obtained from Southern Exposure Seed Exchange, Mineral, VA. The four (su) hybrid varieties used, Early Sunglow, Golden Cross Bantam, Silver Queen, and Honey and Cream, were released in the mid-1900s. The four (se) hybrid varieties used, Breeders Choice, Early Choice, Peaches and Cream, and Silver Choice, were released after 1990. Seeds of the normal sugary and sugary enhancer varieties were obtained from W. Atlee Burpee and Company, Warminster, PA. All varieties were grown in a field plot at the South Farm of the Beltsville Agricultural Research Center, Beltsville, MD, in 2007 and 2008. The plot had a fi ne, loamy, mixed Fluvaquentic Dystrochrept soil. There was a water table at about 1.5 m depth. There were two blocks containing all varieties each year. Within each block, there were three rows of each line with 75 cm between rows and 30 cm between plants within rows. The positions of varieties within blocks were random. Plots were fertilized with 150 kg ha−1 of N, as ammonium nitrate, split between a preplant application at plowing and a side-dress application at approximately 35 cm crop height, and 40 kg ha−1 of P and 100 kg ha−1 of K as preplant applications. Fertilizer rates were based on soil tests and recommendations of the State of Maryland Nutrient Management System (University of Maryland, 2001). Plots were planted in mid May of each year. Plots were not irrigated, but no significant soil moisture deficits occurred during the measurement periods, based on the fact that the water potential at 20 cm depth was never less than −0.05 MPa, as measured with soil matric water potential sensors (Decagon Devices, Pullman, WA). Leaf gas exchange measurements were made on a total of 8 d during the months of June and July of 2007 and 2008, during the vegetative, flowering, and early grain filling periods. Leaf gas exchange was measured in full midday sunlight, using a CIRAS-1 portable photosynthesis system (PP Systems, Amesbury, MA). A sunlit 2.5 cm2 section of a mature leaf was enclosed in a broad leaf cuvette and exposed to air at the ambient air temperature and 375 794
to 385 μmol mol−1 external [CO2]. Leaves measured were either the youngest or second youngest fully expanded leaves. Measurements were taken on sections of leaves that were in full sunlight and nearly perpendicular to the sun in situ. Leaf orientation was not changed during the measurement of leaf gas exchange. The boundary layer conductance to water vapor for leaf material in the cuvette was 4.3 mol m−2 s−1. The water vapor content of air entering the cuvette was set to 50 to 70% of that of outside air, depending on the day, so that on average the water vapor pressure of air around the measured section of leaves was equal to that of ambient outside air on a given day. The same flow rate through the cuvette (6.7 cm3 s−1) and water vapor content of incoming air was used for all leaves. Steady state values of A, gs, Ci, and environmental conditions were recorded within 1 min of enclosing a section of a leaf in the cuvette. Tests showed that no change in gs in response to conditions inside the cuvette occurred in that time. Because the flow rate through the cuvette and the incoming humidity were the same for each leaf on a given date, the leaf to air difference in water vapor pressure (LAVPD) during the measurement varied inversely with gs. To eliminate effects of this source of variation in LAVPD on estimates of TE, the transpiration rates used in determining TE were calculated for each leaf as the product of gs and the air saturation deficit for water vapor (ASD) on that date rather than using the LAVPD inside the cuvette (Bunce, 2010). On each measurement date one leaf of an interior plant of each line was measured in each of the two blocks. Tests of differences among the three eras of breeding in leaf gas exchange parameters were conducted using two-way ANOVA, with measurements classified by measurement date, regardless of the year, and by era of breeding. Means were compared using Tukey’s HSD test. Tests of differences among individual varieties were similarly conducted using two-way ANOVA.
Comparison of Varieties with Contrasting Transpiration Efficiency The two varieties with the highest mean leaf TE in the 2007 and 2008 data, Peaches and Cream and Silver Choice, and the two varieties with the lowest mean TE, Breeders Choice and Early Choice, were also grown in 2009. The field plot, the fertilizer treatments, and the plant spacing were the same as in the prior years. There were four replicate blocks in 2009, each containing all four varieties. Leaf gas exchange measurements as described earlier were taken on three measurement dates in July 2009, sampling an interior plant of each variety in each of the four blocks. Differences among the four varieties in gas exchange parameters in 2009 were tested using two-way ANOVA, with measurements classified by line and by measurement date. Means were compared using Tukey’s HSD test. Differences among the four varieties in gas exchange parameters in all 3 yr combined were tested using two-way ANOVA, with measurements classified by line and by measurement date, regardless of year. Means were compared using Tukey’s HSD test. Relationships among leaf gas exchange parameters and environmental variables were examined in these four varieties using regression analysis on data for all 3 yr combined. Differences among varieties in linear regressions were tested using analysis of covariance. All statistical tests were implemented using JMP v.5 (SAS Institute, Cary, NC), and a probability level of 0.05 was used for all tests.
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Table 1. Mean values of transpiration efficiency (TE), substomatal carbon dioxide concentration (Ci), photosynthetic carbon dioxide assimilation rate (A), and stomatal conductance (gs) of 13 sweet corn varieties from three eras of breeding, averaged across eight measurement dates in 2007 and 2008. Varieties are classified by era as “open pollinated” (op), “normal sugary” hybrids (su), and “sugary enhanced” hybrids (se). All variety, date, and variety × date interaction terms were significant at the 0.01 probability level for all variables. Variety Country Gentleman Golden Bantam Luther Hill Stowell’s Evergreen Black Mexican Golden Cross Bantam Early Sunglow Honey and Cream Silver Queen Breeders Choice Early Choice Peaches and Cream Silver Choice
Era
TE
Ci
A
gs
op op op op op su su su su se se se se
mmol mol−1 6.0 5.6 6.0 5.5 5.8 5.7 5.9 5.5 5.7 5.0 5.0 6.4 6.4
μmol mol−1 201 215 205 212 205 211 202 209 205 225 221 196 200
μmol m−2 s−1 50.9 50.6 47.9 53.8 51.9 51.2 54.2 55.2 52.1 50.6 54.8 50.0 47.6
mmol m−2 s−1 732 757 669 784 749 745 808 808 755 863 925 603 578
RESULTS Era Comparison Mean leaf temperatures and ASD ranged from 26 to 31°C and from 0.9 to 1.9 kPa on the different measurement dates, respectively. Averaged across measurement dates, leaf TE varied by a factor of 1.27 among the 13 varieties, g s varied by a factor of 1.60, A varied by a factor of 1.16, and Ci by a factor of 1.15, with significant differences among varieties in all of these leaf gas exchange parameters (Table 1). The variety × measurement date term was also significant for all of these parameters, so direct means comparisons have limited meaning and are not presented. Despite differences among individual varieties in leaf gas exchange, there was no significant effect of era of breeding on TE, g s, or Ci (Fig. 1). In comparing eras, there was no significant interaction between era and measurement date for TE, g s, Ci, or A. The measurement date term included different years, stages of growth, and immediate environmental conditions, so we cannot reject the hypothesis that these factors had no effect on these comparisons. Mean A and g s were both 4 to 5% higher for the (su) era group than the newer or older groups of varieties, and this difference was significant for A (Fig. 1).
lower g s and Ci and higher TE than Breeders Choice and Early Choice (Fig. 2), with no significant variety × date interactions. The measurement date term included different years, stages of growth, and immediate environmental conditions. The highest and lowest TE varieties differed by a factor of 1.30 in TE and 1.40 in gs. The natural log of g s decreased with ASD in all four varieties (Fig. 3). Analysis of covariance indicated no significant differences in slopes of the linear regressions among the varieties (p = 0.64). Including temperature along with ASD in multiple linear regressions indicated a significant positive effect of temperature on ln(g s) in all varieties and increased the slope of the response to ASD by about 25% in all varieties compared with those shown in Fig. 3. Substomatal carbon dioxide concentration decreased with ASD in all four varieties, but the slopes of the linear regressions were not significantly different among the varieties (Fig. 4). The lowest individual Ci value observed was 100 μmol mol−1. Values of A decreased on average about 10% over the observed range of ASD, but linear regressions were significant for only one of the four varieties, and there were no significant differences in response among the varieties (not shown). Leaf TE was poorly correlated with ASD in all of the varieties, with the largest r 2 value being 0.04 (not shown).
Comparison of Varieties with Contrasting Transpiration Efficiency
DISCUSSION
In 2009 TE was significantly higher in the Peaches and Cream and Silver Choice varieties than in Breeders Choice and Early Choice varieties (Table 2), which agrees with the data for these varieties in the 2007 and 2008 data. There were no significant variety × date interactions in this test for any of the measured parameters. Averaged over the 3 yr, there were no differences in A among those varieties, while Peaches and Cream and Silver Choice had
Based on this sample of four or five varieties from each of three eras of breeding, I found no support for an increase in g s or a decrease in TE over the past approximately 100 yr of breeding of sweet corn. Thus the occurrence of midday Ci values above those required to saturate A in modern sweet corn varieties probably was not an indirect result of increased g s during recent selection for other crop properties.
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Figure 1. Mean values of transpiration efficiency (TE), stomatal conductance (gs), photosynthetic carbon dioxide assimilation rate (A), and substomatal carbon dioxide concentration (Ci) in sweet corn varieties from three eras of breeding, described as “open pollinated” (op), “normal sugary” (su), and “sugary enhanced” (se), measured in 2007 and 2008. Columns with different letters were different at the 0.05 level of probability using Tukey’s HSD comparison. See text for the varieties included in each era group. Table 2. Mean values of transpiration efficiency (TE), substomatal carbon dioxide concentration (Ci), photosynthetic carbon dioxide assimilation rate (A), and stomatal conductance (gs) of four sweet corn varieties averaged across three measurement dates in 2009. Means within columns followed by the same letter were not significantly different using Tukey’s Honestly Significant Difference test. Variety
TE
mmol mol Breeders Choice 4.6 b† Early Choice 4.7 b Peaches and Cream 6.2 a Silver Choice 6.0 a Variety *** Date ** Variety × date NS‡
Ci −1
μmol mol 192 a 192 a 149 b 155 b *** *** NS
A −1
gs −2
μmol m s 58.6 a 54.5 a 60.5 a 59.3 a NS *** NS
−1
mmol m−2 s−1 851 a 788 a 669 b 667 b ** *** NS
**Significant at the 0.01 probability level. ***Significant at the 0.001 probability level. † Means followed by the same letter were not significantly different using Tukey’s Honestly Significant Difference test. ‡ NS, not significant.
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The only statistically significant difference among the mean values of leaf gas exchange parameters from the three eras of breeding was higher A in the (su) hybrids. This result suggests that A may have increased with the development of hybrid varieties, and may have decreased during the development of the (se) hybrids. However, the change in mean A was less than 5%, and it would require a larger sample of varieties to be confident of the generality of that pattern. Among the four (se) hybrid varieties examined, there were consistent, significant differences in midday leaf TE of about 30%. The differences in TE occurred because of differences in g s but not A. This work therefore identified two modern sweet corn varieties having high TE without lower A under midday field conditions. Similar variation in TE based on variation in gs rather than A has been found among modern lines of field corn (Bunce, 2010). Differences among sorghum [Sorghum bicolor (L.) Moench] lines in leaf TE under field conditions have also been
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Figure 2. Mean values of transpiration efficiency (TE), stomatal conductance (gs), photosynthetic carbon dioxide assimilation rate (A), and substomatal carbon dioxide concentration (Ci) in four sweet corn varieties measured in 2007, 2008, and 2009. Columns with different letters were different at the 0.05 level of probability using Tukey’s HSD comparison.
identified, but often the variation is primarily related to differences in A rather than g s or transpiration in sorghum (Peng and Krieg, 1992; Balota et al., 2008). The substantial scatter in the relationships between g s and ASD (Fig. 3) partly reflects the variation in temperature across these measurements, which strongly affects g s in corn (e.g., Bunce, 2010). Nevertheless, ASD affected g s and Ci with nonsignificantly different slopes in all of the four corn varieties compared and had only a minor effect on A, so there was little impact of ASD on the TE comparisons. The lack of a substantial effect of ASD on TE comparisons indicates that reliable genotype comparisons could be obtained using relatively few measurement dates. The differences in leaf g s of about 40% found among the four (se) hybrid sweet corn varieties would result in smaller differences in transpiration at the canopy scale because of differences in leaf temperature resulting from the differences in transpiration, the presence of leaf CROP SCIENCE, VOL. 51, MARCH– APRIL 2011
boundary layer and canopy aerodynamic resistances to water vapor movement, and other feedback processes ( Jarvis and McNaughton, 1986). Bunce (2010) used the mean midday values of g s, leaf boundary layer conductance, and air temperature for field corn grown in large plots in Beltsville to estimate that midday canopy transpiration of field corn would differ on average by about 32% as much as the difference in midday leaf g s. Thus a 40% difference in leaf g s would be expected to result in roughly a 13% difference in midday canopy transpiration, which could produce a substantial reduction in crop water use. It is concluded that breeding over the last century has not increased g s or decreased leaf TE in sweet corn. However, there is significant variation in TE among modern sweet corn varieties, which is related to differences in g s rather than A and could potentially be exploited to decrease crop water use without decreasing growth.
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Figure 3. Relationships between the natural log of stomatal conductance [ln(gs)] and the air saturation deficit for water vapor (ASD) at the time of measurement for four sweet corn varieties measured on eleven days over 3 yr. Two or four leaves were measured for each variety on each date. Linear regressions are shown. The slopes of the regressions did not differ significantly among the four varieties.
Figure 4. Relationships between the substomatal carbon dioxide concentration (Ci) and the air saturation deficit for water vapor (ASD) at the time of measurement for four sweet corn varieties measured on eleven days over 3 yr. Two or four leaves were measured for each variety on each date. Linear regressions are shown. The slopes of the regressions did not differ significantly among the four varieties.
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