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Published online 31 May 2007
Published in Crop Sci 47:1186-1192 (2007)
© 2007 Crop Science Society of America
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CROP ECOLOGY, MANAGEMENT & QUALITY

Dry Matter and Nitrogen Partitioning Patterns in Bt and Non-Bt Near-Isoline Maize Hybrids

K. D. Subedi* and B. L. Ma

Eastern Cereal and Oilseed Research Center (ECORC), Central Experimental Farm, Research Branch, Agriculture and Agri-Food Canada, 960 Carling Ave., Ottawa, ON, Canada K1A 0C6

* Corresponding author (subedik{at}agr.gc.ca).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
While maize (Zea mays L.) hybrids with the Bt transgene from Bacillus thuringiensis have been gaining popularity, their dry matter (DM) production, N uptake, and whole-plant N dynamics have not been assessed to justify their added cost. A field experiment conducted for 2 yr in Ottawa, Canada, studied DM and N partitioning patterns, and N-use efficiency (NUE) of a conventional (Pioneer 3893) and its near-isoline transgenic hybrid (Pioneer 38W36 Bt). The hybrids were grown with two N treatments (0 kg N [N0] or 150 kg N ha–1 with 15N-labeled source [N150]). Plant samples were analyzed for DM, N concentration, and the fate of 15N at the V7, silking, and physiological maturity (PM) stages. Both hybrids were similar in harvest index, leaf chlorophyll content, and N concentrations and contents at the V7, silking, and PM stages. The Bt hybrid produced greater DM in leaves (42.1 vs. 37.5 g plant–1) and kernels (134 vs. 121 g plant–1) than its non-Bt counterpart, it also accumulated about 11% more N in kernels and on a whole-plant basis. Both hybrids had a similar partitioning of N and NUE in different plant parts. About 47% of the applied N was recovered at harvest, 70% of which was accumulated in the kernels of both hybrids. There was no indication that the Bt hybrid accumulated more N than its non-Bt near-isoline until the silking stage; the greater N content of the Bt hybrid at the PM stage was associated with greater DM in the kernels and leaves.

Abbreviations: a.e., atom enrichment • Bt, Bacillus thuringiensis • DM, dry matter • ECB, European corn borer • NUE, nitrogen use efficiency • PM, physiological maturity.


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
SINCE THEIR introduction in 1996, maize (Zea mays L.) hybrids genetically modified with a gene from a soil bacterium Bacillus thuringiensis (Bt) have been gaining popularity. These transgenic hybrids express an insecticidal crystalline {sigma}-endotoxin protein (Cry1Ab) that is solubilized and activated in the highly alkaline midgut of lepidopteran insects (Koziel et al., 1993). This technology has been proven to give an effective control of the European corn borer (ECB, Ostrinia nubilalis Hübner), one of the most destructive insect pests of maize (Heinrichs, 1988; Koziel et al., 1993).

The performance of Bt maize has been extensively studied against its target insect pest. The benefits of Bt maize are proven to give season-long protection from the ECB and reduced use of insecticides. Response of Bt maize against non-Bt counterparts have also been studied for drought and temperature stress (Seydou et al., 2000), plant population densities (Stanger and Lauer, 2006), endotoxin and N concentration (Bruns and Abel, 2003), lignin concentration (Jung and Sheaffer, 2004; Poerschmann et al., 2005), and silage quality (Fearing et al., 1997; Jung and Sheaffer, 2004). Whether or not any benefits of Bt maize are worth the extra cost for the seed premium is still questionable.

Recently, Ma and Subedi (2005), using pairs of Bt and non-Bt near-isolines, reported that under low or moderate ECB infestation, there was no benefit of the Bt hybrid on yield. Lauer and Wedberg (1999) found that the yield of Bt hybrids was 4 to 8% greater than standard hybrids when infested with ECB, but was 8% less than conventional hybrids with the use of an insecticide. Graeber et al. (1999) showed that under low ECB infestation, the Bt hybrids had no better agronomic performance than their near-isoline hybrids. Seydou et al. (2000) observed that there was a difference in total plant weight and grain yield between Bt and non-Bt hybrids because of the significant ECB damage in the non-Bt hybrids.

Bruns and Abel (2003) found no difference between Bt and non-Bt hybrids in whole-plant N concentration. Ma and Subedi (2005) evaluated seven pairs of Bt and non-Bt hybrids and observed that under low to moderate ECB infestation, most Bt hybrids had similar to or lower total N content in the grain and higher N in stover than their respective non-Bt near-isolines. They concluded that within the same maturity group, it was the superior hybrids (non-Bt trait) that led to the greatest N accumulation and the highest grain yield.

Genotypic variation in N uptake and partitioning has been widely reported in conventional maize hybrids (Beauchamp et al., 1976; Chevalier and Scharder, 1977; Weiland and Ta, 1992; Ma and Dwyer, 1998; Bertin and Gallais, 2000). Ta and Weiland (1992) reported a significant role of the stalk in providing N for kernel development, and both N fertility and hybrids influenced the rate of N remobilization from vegetative tissues. Nevertheless, Subedi and Ma (2005b, 2005c), in greenhouse studies, found no difference in grain yield, total N acquisition, partitioning of 15N, and nitrogen use efficiency (NUE) among three contrasting maize hybrids. Bruns and Abel (2003) reported increased N concentration and {sigma}-endotoxin with increased supply of N in the whole plant of Bt maize hybrids at growth stage (GS) V5 (Ritchie et al., 1993). This indicates that Bt hybrids may differ in protein synthesis from their non-Bt counterparts. They also suggested that adequate supply of N fertilizer during the early growth stage appeared to be essential for Bt-endotoxin production by the plant. Fearing et al. (1997) reported that the highest amount of Cry1Ab protein was found to occur at anthesis, consistent with the time at which maximum plant vegetative biomass is reached, and was markedly lower later in senescing plants. Whether the response to N observed at an early growth stage (V5) remains consistent until late reproductive stage or physiological maturity (PM), however, is not known.

It is an established fact that for higher protein synthesis, greater N has to be taken up by the plant or N has to be remobilized from another part of the plant. Bruns and Abel (2003) found that {sigma}-endotoxin concentration was positively associated with whole-plant N concentration. Whether the Bt hybrids take more N from the soil than their non-Bt counterparts or they have greater remobilization has not been systematically studied. We hypothesized that Bt hybrids require more N to synthesize {sigma}-endotoxin protein, therefore they take more N from the soil than that taken up by their non-Bt counterparts. This is the continuation of a previous study in which a representative pair of Bt and non-Bt hybrids among the seven pairs used by Ma and Subedi (2005) has been used. The objective of this study was to determine the dry matter (DM) and N partitioning patterns and whole-plant N dynamics of Bt and non-Bt near-isoline maize hybrids using a 15N-labeling technique.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Experimental Design and Treatments
A field experiment was conducted in a sandy loam soil (coarse-loamy, mixed, mesic Endoaquolls) under a nonirrigated cropping system in Ottawa, ON, Canada (45°22' N, 75°43' W) in 2003 and 2004. The previous crops in the experimental plots were wheat (Triticum aestivum L.) for 2003 and oat (Avena sativa L.) for the 2004 experiment. Before land preparation, soil samples from the 0- to 30-cm depth were analyzed and found to contain 6.6 mg kg–1 NO3–N, 133 mg kg–1 P (Bray), and 128 mg kg–1 soil test K with a pH of 6.9 in 2003, and 5.3 mg kg–1 NO3–N, 42.8 mg kg–1 P, and 101 mg kg–1 K with a pH of 6.8 in 2004. Responses of two commercial near-isoline hybrids (Pioneer 3893 and Pioneer 38W36 Bt) were evaluated with two N treatments (0 kg N ha–1 [N0] and 150 kg N ha–1 with 5% 15N2–NH4NO3 enrichment [N150]). Treatments were laid out in a split-plot design with four replications in each year. The main plot was 82.3 m2 (12 rows of 9-m length, 76 cm apart) in which two hybrids were planted at a density of 75000 plants ha–1on 3 June in 2003 and 13 May in 2004. Before planting, fertilizer P and K were applied as per the soil test recommendations. An herbicide containing S-metolachlor {2-chloro-N-(2-ethyl-6-methylphenyl)-N-[(1S)-2-methoxy-1-methylethyl]acetamide}, atrazine [6-chloro-N-ethyl-N'-(1-methylethyl)-1,3,5-triazine-2,4-diamine] + benoxacor [4-(dichloroacetyl)-3,4-dihydro-3-methyl-2H-1,4-benzoxazine] at a rate of 3.3 L ha–1 was applied before planting. Nitrogen treatments were imposed at the V6 stage. Two subplots (three rows by 1 m by 0.76 m = 2.28 m2) were demarcated within the middle three rows of each main plot, in which the two N treatments were randomly allocated. No N fertilizer was added in the N0 treatment while in the N150 treatment, 5% 15N2–NH4NO3 fertilizer was diluted in water (i.e., 100 g fertilizer in 1 L water), and applied uniformly within the microplot, followed by flushing with 2 L of water to allow the fertilizer to enter the soil. In the N0 treatment, 3 L of tap water was applied at the same time.

Measurements
Phenological events were recorded from emergence to PM. The number of plants in each microplot was counted at the V6 growth stage and at PM. In 2004, one plant from each microplot was harvested at V7 (i.e., 1 wk after N application) and at silking to analyze DM and tissue N concentrations. Harvesting was done from the middle row of each microplot. At silking, leaf greenness was measured in the ear leaf of five random plants within the microplots using a chlorophyll meter (SPAD 502, Minolta Camera Co., Tokyo), and the average values of the five readings were recorded. At PM, the total number of plants in each microplot was counted and three plants from the middle row of the microplots were harvested at crown level. Stalk-lodged plants, if any, were avoided while sampling. Leaves and ears were separated from the shoot. The total number of kernels per ear was counted. Husks were mixed with the leaf portions while cobs were added to the stalk portion. Roots were dug at about 15-cm depth using a shovel. All visible and intact roots were collected and washed thoroughly with tap water. Plant samples including roots were oven dried at 80°C for >72 h, and DM was recorded.

Samples Preparation and Nitrogen Analysis
All plant parts were ground to pass through a 1-mm screen using a cyclone grinder. Total N concentration in different plant parts was analyzed using a micro-Kjeldahl method (Jones, 1991). The samples of the N150 treatment were also analyzed for 15N atom enrichment (a.e.). Plant samples and reference material (pea grain flour) were redried at 60°C for 24 h before weighing. Samples weighing 1 ± 0.2 mg were separately loaded in tin capsules. Nitrogen concentration was determined by automated dry combustion–gas chromatography using a Carlo-Erba T1500 Elemental Analyzer (Carlo Erba, Milan, Italy). The N isotope ratio was measured using a DELTA-plus isotope ratio mass spectrometer (Finnegan MAT, Germany).

The NUE was calculated following Liang and MacKenzie (1994), modified by Ma and Dwyer (1998) as follows:

where Wi and Ni are the ith component dry weight (g plant–1) and total N concentration (fraction), respectively, 15Ni1 and 15Ni0 are the 15N a.e. percentage in the ith component of the 15N-labeled and unlabeled plants, f is the total amount of N applied (g pot–1) through NH4NO3, and a and b are the 15N a.e. percentage in the fertilizer (5%) and background (0.37%), respectively.

Data Analysis
The experimental data for each year were subjected to analysis of variance separately as well as combined across 2 yr, using the general linear model (SAS Institute, 1996). Treatment mean differences were separated by the least significant difference (LSD0.05) test when the F tests were significant (P ≤ 0.05). The 15N concentrations, content, and NUE in different plant parts of the N150 treatment between the two hybrids were compared using a t-test.


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Growing Conditions
The year 2003 was generally wet with excess rain during May; as a result, the experiment was planted later than normal; however, mean air temperatures during the growing season (June–September) were warm enough (15–22°C) to accumulate crop heat units (Brown and Bootsma, 1993) that were sufficient (>2900) for the hybrids used in the study. Rain was well distributed during the growing season so that the crop did not experience any notable effects of drought. The total precipitation during the growing season was >300 mm. In 2004, there was sufficient precipitation (>350 mm) through evenly distributed rainfalls. The crop did not experience any adverse temperature or moisture stresses during either growing season. The accumulated crop heat units were slightly greater in 2004 than in 2003. Subjective observations in the field showed no evidence of significant stalk lodging and breakage due to ECB in the non-Bt hybrids in either year.

Morphology and Phenology
There were no hybrid x N interactions for any of the parameters measured. Therefore, the results are presented based on main effects of hybrid (Table 1). Both hybrids had 16 leaves in 2003 but there were 17 leaves per plant in 2004. Similarly, the size of yield components, grain yield, and total DM were slightly greater in 2004 than in 2003, possibly because of the longer growing season in 2004. The 2004 crop took 15 d more to reach PM than in 2003 (113 vs. 128 d). Crop heat units were similar in both years, however, and the Bt hybrid (Pioneer 38W36 Bt) took 2 to 3 d more than the non-Bt isoline hybrid (Pioneer 3893) to reach 50% silking and PM.


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  		Table 1. Differences between the Bt and non-Bt maize near-isoline hybrids for various parameters measured, averaged across two N treatments (0 N and 150 kg N ha–1) for 2 yr.

 
Response of Hybrids to Dry Matter Partitioning
There were no differences between the hybrids in the number of plants and ears per microplot (Table 1). The number of kernels per ear and DM in kernels and leaves were greater in the Bt hybrid than the non-Bt hybrid, but there were no differences between the hybrids in the root and stalk DM and DM on a whole-plant basis. Irrespective of N treatment, DM increased by 282% from V7 to silking, and by 160% from silking to PM stage in both hybrids. The greatest DM was accumulated in kernels (~50%), followed by stalks (27%), leaves (16%), and roots (8%), and hybrids did not differ in the proportion of total DM partitioned within different plant parts. This partitioning of DM followed a similar pattern as previously reported by Dwyer et al. (1994) and Subedi and Ma (2005c, 2005a). The hybrids were also not different in harvest index and leaf greenness (i.e., SPAD readings).

Nitrogen Uptake and Partitioning by Hybrids
Although there was no difference in the N concentration in different parts (Table 1), N content followed a similar pattern of DM partitioning such that the Bt hybrid had greater N content in kernels and in the whole plant than its non-Bt counterpart (Fig. 1). The greater N content of the Bt hybrid was associated with its greater DM in the kernels and on a whole-plant basis.


Figure 1
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  		Figure 1. Partitioning of N content in different plant parts individually and on a whole-plant basis of Pioneer 3893 and Pioneer 38W36 Bt maize hybrids at physiological maturity, averaged across two N treatments for 2 yr. The bars labeled with different letters within each component are significantly different (P ≤ 0.05).

 
In 2004, at 1 wk after fertilizer N application, plants of both hybrids took up only 5% of the total 15N content measured at PM, while by silking, the accumulation of 15N was about 66%. The enrichment of 15N a.e. percentage was not different between the two hybrids for all plant parts except roots and stalk (Table 2). The 15N enrichments in both roots and kernels were significantly greater in the non-Bt hybrid. The values of 15N a.e. percentage closely resembled the concentrations reported in a greenhouse study (Subedi and Ma, 2005b). Although there was a difference between the two hybrids in N content in kernels, no significant difference was observed between the hybrids in 15N content in all plant parts for both years (Fig. 2). The partitioning of 15N content into different components also followed a similar pattern of total N content (Fig. 2), and hybrids did not differ.


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  		Table 2. Concentrations (atom enrichment [a.e.]%) and content of 15N in different plant parts of Pioneer 3893 and its near isoline transgenic hybrid (Pioneer 38W36Bt) grown with 150 kg N ha–1 enriched with 5% 15N2–NH4NO3, averaged across 2 yr.

 

Figure 2
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  		Figure 2. Distribution of dry matter (DM), N content, 15N content, and N use efficiency (NUE) among roots, stalks, leaves, and kernels of a maize plant labeled with 5% 15N2–NH4NO3, averaged across 2 yr.

 
The partitioning of DM, N content, 15N content, and NUE among different plant parts were the same in both hybrids, and the kernel was the dominant sink for all of these parameters (Fig. 3). Overall NUE was only 47%, of which >33% was contributed from kernels, and roots accounted for <2% NUE (Fig. 4). These results are also in agreement with the findings of the initial study by Ma and Subedi (2005) that there was no advantage in N uptake and NUE of Bt hybrids compared with their conventional counterparts.


Figure 3
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  		Figure 3. Effect of N treatment on the partitioning of dry matter in a maize plant at physiological maturity stage averaged across two hybrids for 2 yr. The bars labeled with different letters within each component are significantly different (P ≤ 0.05). The N treatments are N0 = 0 kg N ha–1 and N150 = 150 kg N ha–1 with 5% 15N2–NH4NO3.

 

Figure 4
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  		Figure 4. Effect of N treatment on N concentration in a maize plant at physiological maturity stage averaged across two hybrids for 2 yr. The bars labeled with different letters within each component are significantly different (P ≤ 0.05). Nitrogen treatments are N0 = 0 kg N ha–1 and N150 = 150 kg N ha–1 with 5% 15N2–NH4NO3.

 
Effect of Nitrogen on Dry Matter Production and Partitioning
Irrespective of N treatment and hybrid, DM per plant increased by almost fourfold from V7 to silking stage (29 vs. 109 g plant–1) and >1.5 times from silking to PM (109 vs. 283 g plant–1) (hybrid averages in Table 1). The increase in DM from V7 to silking stage was much greater in the N150 (300%) than in N0 (246%) (data not shown). A similar pattern of treatment difference was observed in the DM increment from silking to PM. The effect of N was not apparent on DM within a week of fertilizer application, but there were substantial differences between N treatments at silking and PM. Irrespective of hybrid, the N150 treatment had greater DM in all plant parts measured than the N0 treatment (Fig. 3).

Nitrogen Uptake and Partitioning
No significant interactions were observed between hybrid x N, year x N, or year x hybrid on N uptake and partitioning at all stages of measurement. There was no difference between the two N treatments in N concentration until the V7 stage (mean 20.5 g kg–1), but N concentrations were different at silking (11.0 g kg–1 in N0 vs. 15.0 g kg–1in N150), and in all plant parts at PM (Fig. 4). A similar pattern was observed for the N content at PM: the N150 treatment had significantly greater N contents than N0 in all plant parts individually or when expressed on a whole-plant basis (Fig. 5).


Figure 5
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  		Figure 5. Effect of N treatment on N content in a maize plant at physiological maturity stage averaged across two hybrids for 2 yr. The bars labeled with different letters within each component are significantly different (P < 0.05). Nitrogen treatments are N0 = 0 kg N ha–1 and N150 = 150 kg N ha–1 with 5% 15N2–NH4NO3.

 
Similar to N concentration, there was no difference in N content (mean of 0.59 g plant–1) within 1 wk of N fertilizer application (i.e., V7), but a substantial difference was observed between the fertilized and unfertilized treatments at silking (1.81 vs. 1.02 g plant–1) and PM (2.54 vs. 1.63 g plant–1). At PM, >70% of the total N uptake was accumulated in the kernels followed by the stalks, leaves, and roots (Fig. 2), and hybrids did not differ in N partitioning in different parts. In the N150 treatment, N accumulation at the V7 growth stage was only 23% of the total N at harvest, while by silking, about 61% of the total plant N was taken up. In the N0 treatment, N accumulations at the V7 and silking stages were 33 and 62%, respectively, of the total plant N at PM. This indicates that most of the plant total N content in the fertilized treatment was accumulated after the V7 growth stage. As Fearing et al. (1997) have reported, the maximum {sigma}-endotoxin protein was accumulated at anthesis. Our study showed no difference between the two hybrids in total plant DM and N concentration and content at this stage (i.e., silking), suggesting that the Bt hybrid was not superior in terms of N acquisition to its non-Bt counterpart. Greater N contents in kernel and leaves at the PM stage of the Bt hybrid was simply due to greater DM in these components.

Lack of an interaction between N and hybrid suggests that the increased availability of N may not increase the synthesis of endotoxin as proposed by Bruns and Abel (2003). Plant samplings at the V7 and silking stages showed no difference between the hybrids in DM production and N acquisition. The greater N content in the kernels of the Bt hybrid at PM was mainly associated with greater DM in this component; the N concentration in kernels was similar to that of the non-Bt hybrid (Table 1). The results of this study are consistent with the findings of a greenhouse study by Subedi and Ma (2005a, 2005b) that three contrasting maize hybrids did not differ in DM production, N uptake and partitioning, or NUE. Although Weiland and Ta (1992) observed that hybrids with greater leaf and stalk weights at grain filling accumulated more 15N in kernels, in the current study, despite the Bt hybrid having significantly greater leaf DM, there was no difference in kernel 15N content between them.

The total N uptake in the N0 treatment at PM was only about 52% of the total N content in the N150 treatment (1.45 vs. 2.79 g plant–1), while the total DM and kernel DM in the N0 treatment were 73% (211 vs. 291 g plant–1) and 68% (102 vs. 151 g plant–1), respectively, of the fertilized treatment (N150). This indicates that there was a considerable amount of N released through mineralization during the growing season. Moreover, there was a substantial amount of unaccounted N in the N150 treatment, resulting in a smaller NUE (47%). The in-season N supply from the soil seems to be one of the reasons why there is always a small yield gap between the N0 and full dose of N applications in the humid environment of eastern Canada, as reported by Ma et al. (2005) and Subedi and Ma (2005d). Whether or not the NUE would have been greater if fertilizer N was applied at preplant than at the V6 growth stage has not been evaluated in this study. Ma et al. (2005) demonstrated, however, in the same growing environment, that side-dressed N at the V6 to V8 growth stage had greater N recovery than preplant-applied N.


   CONCLUSIONS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
The purpose of this study was to assess whether the Bt and non-Bt near-isoline maize hybrids differ in their N and DM partitioning patterns. The Bt hybrid tended to produce greater DM in leaves and kernels than its counterpart. There was no difference between the hybrids in N concentration and content at V7 and silking. At PM, the Bt hybrid had accumulated greater N in kernels and leaves than its non-Bt counterpart, which was attributed to the greater DM in kernels. No difference was observed between the hybrids in concentration and content of 15N at V7, silking, and in different plant parts at PM. There was no evidence that the Bt hybrid remobilized N from the stalk to meet the requirement for the synthesis of endotoxin against the ECB, because both hybrids had a similar N partitioning pattern. Under the conditions tested, i.e., low to moderate ECB pressure, the Bt hybrid produced greater DM in kernels and leaves but there was no superiority of Bt maize over its non-Bt counterpart in terms of N concentration, N partitioning, or NUE. Further studies with more pairs of isolines and determination of {sigma}-endotoxins concentrations at different growth stages will be useful to understand how much labeled N ends up in the endotoxin fraction.


   ACKNOWLEDGMENTS
 
We gratefully acknowledge the excellent technical assistance of D. Balchin, L. Evenson, and V. Deslauriers of Agriculture and Agri-Food Canada. ECORC contribution no. 06-704.


   NOTES
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 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
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Received for publication September 18, 2006.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 




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