Divergent selection for grain protein affects nitrogen use in maize hybrids
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Field Crops Research 100 (2007) 82–90
www.elsevier.com/locate/fcr
Divergent selection for grain protein affects nitrogen
use in maize hybrids
Martı́n Uribelarrea, Stephen P. Moose, Frederick E. Below *
Department of Crop Sciences, 1201 W. Gregory, University of Illinois, Urbana, IL 61801, USA
Received 7 July 2005; received in revised form 24 May 2006; accepted 24 May 2006
Abstract
The Illinois high (IHP), low (ILP), and corresponding reverse (IRHP, and IRLP) protein–strains of maize represent genetic extremes for
differences in grain protein concentration. The objective of this study was to determine how divergent selection for grain protein affects N use in
hybrid plants. Inbreds derived from the protein–strains were crossed as males to a common tester and the resultant hybrids evaluated at eight N rates
in the field over 3 years. A more than two-fold difference in grain protein concentration was observed among the strain-hybrids with ILP averaging
65 g kg1, IRHP 89 g kg1, IRLP 111 g kg1, and IHP 148 g kg1 of grain protein. Except for IHP at the lowest N levels, the strain-hybrids were
similar in their whole shoot biomass production both pre- and post-flowering. Conversely, the strain-hybrids differed markedly in their uptake and
accumulation of plant N, and these differences were already evident at flowering before a grain sink was present. Although all hybrids had the same
overall N use efficiency at maturity (approximately 24 kg kg1 N), they differed in their N use components with IHP and IRLP exhibiting a higher
uptake efficiency, and ILP and IRHP exhibiting high utilization efficiency. The remobilization of leaf N was also more extensive for IHP and IRLP.
Changes in grain protein concentration from divergent selection were directly related to changes in uptake and use of N by the plant.
# 2006 Published by Elsevier B.V.
Keywords: Zea mays; N use efficiency; Biomass accumulation; Illinois protein strains; Maize
1. Introduction We use NUE here to encompass yield efficiency (the
increase in grain yield per unit of applied N fertilizer) and its
Modern agriculture is concerned with yield, the nutritional two components; uptake efficiency (the fraction of fertilizer
quality of the crop and the environmental impact of crop applied N found in the plant at maturity), and utilization
production. Efficient use of fertilizer N is therefore critical. efficiency (the ratio of grain yield to plant N). The N supply can
Because an adequate N supply is one of the main factors alter the relative importance of these two components, as under
powering yield of cereal crops (Below, 2002), annual high N inputs, NUE is mainly determined by the plant’s ability
applications of fertilizer N are the norm. About half of the to acquire N; whereas at low N, the ability to utilize absorbed N
110 kg ha1 annual increase in maize yields over the last half is generally more important (Moll et al., 1982; Ma et al., 1998).
century can be attributed to improved cultural practices, Many studies show that genotype can also impact NUE
especially N fertilizer use (Duvick, 1992; Sinclair, 1995). (Cerrato and Blackmer, 1990; Smiciklas and Below, 1990;
Variation in the N supply affects all phases of maize growth, Eghball and Maranville, 1993; Rice et al., 1995; Normand et al.,
including the development, activity, and senescence of leaves, 1997; Muchow, 1998; Ma et al., 1998, 1999; Cassman et al.,
and the initiation, growth, and composition of ovules (Muchow, 2002; Gastal and Lemaire, 2002). Because most modern
1988; Uhart and Andrade, 1995a, 1995b). Thus, understanding hybrids are selected according to their yield and N use under
the processes associated with the efficiency of N use (NUE), high rates of applied N (Castleberry et al., 1984; Bertin and
particularly N uptake and utilization, is of major importance in Gallais, 2000), limited genetic variability may exist among
designing crop management strategies and in developing commercial hybrids for N utilization, or for the remobilization
breeding programs for improved N use. of N from the stover to the grain (Purcino et al., 1998; Bertin
and Gallais, 2000).
The Illinois protein strains, which are the result of long term
* Corresponding author. Tel.: +1 217 333 9745; fax: +1 217 333 8377. divergent selection for grain protein concentration are unique
E-mail address: fbelow@uiuc.edu (F.E. Below). within the maize germplasm. Illinois high protein (IHP) and
0378-4290/$ – see front matter # 2006 Published by Elsevier B.V.
doi:10.1016/j.fcr.2006.05.008M. Uribelarrea et al. / Field Crops Research 100 (2007) 82–90 83
Illinois low protein (ILP) have been continuously selected for growth stages. Treatments consisted of the factorial combina-
over 100 cycles; whereas the Illinois reverse low protein (IRLP) tion of the four protein-strain hybrids and eight fertilizer rates
and Illinois reverse high protein (IRHP) strains are the result of arranged in a randomized complete block design with four
reversing selection in ILP and IHP beginning with cycle 48. replications. Each experimental unit consisted of four-row plots
Evaluations of the strains during the past 100 cycles have that were 5.3 m long 3 m wide, with one of the central rows
continually demonstrated the effectiveness of this program in reserved for final yield determination and the other used for
altering grain protein level (Woodworth et al., 1974; Dudley destructive plant samplings.
et al., 1974; Dudley and Lambert, 1992; Rizzi et al., 1996), as
well as a number of other plant traits. The wide variation in 2.2. Crop measurements
protein and dry matter production of these strains must have
been accompanied by corresponding changes in N and C N acquisition and partitioning were assessed using whole
metabolism in the plant, and the Illinois protein strains have shoots sampled at two growth stages; R1 (i.e. beginning of
previously been shown to differ in N metabolism (Wyss et al., anthesis and visible silks), and R6 (physiological maturity) when
1991; Lohaus et al., 1998; Below et al., 2004). This variation, 50% of the plants exhibiting a visible black layer at the base of the
and the fact that the strains share a common parental kernels. By R6, maize plants are considered to have attained their
background, makes them unique experimental material for maximum biomass (Ritchie et al., 1997), and we used shoot dry
studying physiological and biochemical mechanisms asso- weight as a relative indicator of net canopy photosynthesis.
ciated with differences in maize productivity. Because of the large differences in grain composition among
Our approach was to make hybrids of each of the strains these hybrids, we also calculated the energy equivalent
(including the reverse strains) using inbreds derived from (MJ ha1) of the grain biomass using standard caloric values
generation 90 crossed to a common tester, then to evaluate these (Hedin et al., 1998) and the respective starch, oil and protein
materials in the field for NUE and its main components. concentrations of the grain (Uribelarrea et al., 2004).
Uribelarrea et al. (2004) showed that these hybrids had grain At each harvest, four representative plants were separated into
protein concentrations which reflected the strain parents, and leaf, stalk (including leaf sheaths), reproductive support tissues
that they differed in their use of N (Below et al., 2004). Our (tassel, husks and cob at R6, or ear-shoot at R1), and grain (only at
objective in this study was to understand how differences in the R6 sampling). Reproductive and grain fractions were placed into
acquisition, utilization, and remobilization of N are associated a forced-draft oven (75 8C), while the fresh weight of the entire
with divergent selection for grain protein. leaf and stalk sample was determined prior to shredding. An
aliquot of the shredded material was weighed fresh and then
2. Materials and methods oven-dried (75 8C). The dry weight of each plant fraction was
calculated using the fresh weight and the moisture level.
2.1. Field site, cultural practices and treatment Individual plant samples were ground in a Wiley mill to pass a 20
arrangements mesh screen, and analyzed for total N concentration (g kg1)
using a combustion technique (NA2000 N-Protein, Fisons
Field experiments were conducted at the Department of Instruments). The total N content (g N plant1) was calculated
Crop Sciences Research and Education Center in Champaign, by multiplying the dry weight by the N concentration.
Illinois during the 2001–2003 growing seasons, on plots that
had previously been shown to be responsive to N fertilizer Table 1
(Gentry et al., 2001). The soil type and cultural practices were Significance level of the fixed effects for each of the measured variables, for the
as previously reported (Uribelarrea et al., 2004). Briefly, the soil protein-strain hybrids grown at Champaign, IL, between 2001 and 2003
was a Drummer silty clay loam with an average organic matter Measured variable Source of variation
of 3.7% and a pH of 6.2. The field was under a maize–soybean Hybrid N rate Hybrid N rate
rotation, with the location of the experimental plots alternated
R1 biomass NS NS 0.0001
each year. Plots were kept weed-free with chemical control and
R1 N content 0.0088 0.0001 0.0472
hand cultivation, and crops were irrigated, when necessary. R1 N uptake 0.0001 0.0001 0.0745
Hybrids of the Illinois protein strains were produced by
R6 biomass 0.0270 0.0001 0.0514
crossing inbreds made from generation 90 of IHP and ILP and R6 N content 0.0725 0.0001 0.0001
generation 42 of IRHP and IRLP as males to FR1064 as the Post-flowering N uptake 0.0518 0.0030 0.0001
tester. Hybrids were over seeded on 26 April 2001, on 25 May
Stover N remobilization 0.0001 NS NS
2002, and 22 April 2003 and thinned to a stand density of Leaf N remobilization 0.0002 0.0458 NS
65,000 plants ha1. The delay in planting date in 2002 was due Stalk N remobilization 0.0001 NS NS
to above average precipitation during April and May (270 mm NUE NS 0.0001 NS
in 2002 compared to a 30-year average of 200 mm). Each of the N uptake 0.0103 0.0003 NS
hybrids was grown under eight rates of fertilizer N (0– N utilization 0.0783 0.0198 NS
238 kg ha1) in 34 kg increments. The fertilizer was hand A threshold of 0.10 was used to determine a significant effect of the different
applied in a diffuse band down the center of the row as sources of variation over the measured variables. NS means that term was not
ammonium sulfate and incorporated between the V2 and V3 significant.84 M. Uribelarrea et al. / Field Crops Research 100 (2007) 82–90
Table 2
Equation parameters for the effect of N rate on the different measured variables for the Illinois protein-strain hybrids grown at Champaign, IL, between 2001 and 2003
Measured variable Protein-strain hybrid Regression equation parameters§
Intercept Linear term Quadratic
(x) term (x2)
R1 biomass FR1064 IHP 82 11.6 102 NS
(g plant1) FR1064 ILP 93z NS NS
FR1064 IRLP 96 NS NS
FR1064 IRHP 93 NS NS
R1 N content FR1064 IHP 0.70 4.1 103 NS
(g plant1) FR1064 ILP 0.90 1.6 103 NS
FR1064 IRLP 0.83 2.2 101 NS
FR1064 IRHP 0.76 2.4 103 NS
R1 N uptake FR1064 IHP 0.65 3.5 103 8.7 106
(kg kg1) FR1064 ILP 0.17 8.2 104 2.2 106
FR1064 IRLP 0.64 4.8 103 1.2 106
FR1064 IRHP 0.45 3.0 103 8.0 106
R6 biomass FR1064 IHP 154 6.0 101 1.2 103
(g plant1) FR1064 ILP 184 5.5 101 1.4 103
FR1064 IRLP 195 3.7 101 6.9 104
FR1064 IRHP 182 6.8 101 2.0 103
R6 N content FR1064 IHP 1.10 1.2 102 1.0 105
(g plant1) FR1064 ILP 1.20 6.8 103 1.0 105
FR1064 IRLP 1.32 9.5 103 1.0 105
FR1064 IRHP 1.27 8.5 103 1.0 105
Post-flowering N uptake FR1064 IHP 0.61 7.2 103 1.0 105
(g plant1) FR1064 ILP 0.39 4.1 103 1.0 105
FR1064 IRLP 0.66 5.4 103 1.0 105
FR1064 IRHP 0.64 7.2 103 1.0 105
Stover N remobilization FR1064 IHP 0.28 3.4 103 8.8 106
(g N plant1) FR1064 ILP 0.34 NS NS
FR1064 IRLP 0.21 2.6 103 1.4 105
FR1064 IRHP 0.18 NS NS
Leaf N remobilization FR1064 IHP 0.17 2.2 103 6.1 106
(g N plant1) FR1064 ILP 0.22 NS NS
FR1064 IRLP 0.15 1.3 103 4.5 106
FR1064 IRHP 0.17 NS NS
Stalk N remobilization FR1064 IHP 0.09 NS NS
(g N plant1) FR1064 ILP 0.04 NS NS
FR1064 IRLP 0.02 NS NS
FR1064 IRHP 0.04 NS NS
NUE (kg kg1) FR1064 IHP 43 2.0 101 3.3 104
FR1064 ILP 40 2.0 101 3.3 104
FR1064 IRLP 44 2.0 101 3.3 104
FR1064 IRHP 41 2.0 101 3.3 104
N uptake efficiency FR1064 IHP 0.83 1.1 103 NS
(kg kg1) FR1064 ILP 0.55 1.1 103 NS
FR1064 IRLP 0.67 1.1 103 NS
FR1064 IRHP 0.64 1.1 103 NS
N utilization efficiency FR1064 IHP 47 9.3 102 NS
(kg kg1) FR1064 ILP 65 9.3 102 NS
FR1064 IRLP 61 9.3 102 NS
FR1064 IRHP 57 9.3 102 NS
§
x = fertilizer N rate (kg ha1); NS means term was non significant.
z
Value averaged across N rates since parameters from corresponding equation were non significant (P < 0.10).M. Uribelarrea et al. / Field Crops Research 100 (2007) 82–90 85
Table 3 yield, and plant N content, NUE (kg grain kg1 fertilizer N) and
Grain protein concentration, grain yield and grain energy equivalent for the
its components, N uptake (kg plant N kg1 fertilizer N) and N
protein-strain hybrids grown in Champaign, IL, between 2001 and 2003
utilization (kg grain kg1 plant N), were calculated as shown in
Strain-hybrid Year Protein Grain yield Grain energy Eqs. (1)–(3):
concentration (Mg ha1) equivalent
(g kg1) (MJ ha1) GYX GY0
NUE ¼ 1000 (1)
FR1064 IHP 2001 170 7.4 223 NRX
2002 144 7.0 215
2003 131 8.2 271 NTX NT0
Average 148 7.5 236 N uptake ¼ (2)
NRX
FR1064 ILP 2001 68 9.0 270
2002 62 7.6 234 GYX GY0
2003 64 9.1 302 N utilization ¼ 1000 (3)
NTX NT0
Average 65 8.6 269
FR1064 IRLP 2001 131 7.8 241 where GYX and GY0 correspond to the grain yield (Mg ha1) at
2002 102 7.2 222 the X and 0 fertilizer rates (kg ha1); NRX is the fertilizer N rate
2003 100 9.1 312 X (kg ha1), and NTX and NT0 represent the total plant N
Average 111 8.0 258 content at 0 and X N rates (kg ha1). The N remobilization from
FR1064 IRHP 2001 97 8.8 308 the leaves, stalk and stover was calculated as the difference in N
2002 87 8.8 240 content in each fraction between R1 and R6.
2003 84 9.6 279
Average 89 9.1 276
2.3. Statistical analysis
Values presented are the maximum levels obtained as a function of applied N.
Effects of fertilizer N rate for the four hybrids during the 3
For yield determination, all ears in the unsampled center row years were analyzed with the MIXED procedure in SAS (SAS
of each plot were harvested and mechanically shelled, and Institute, 2000), and the parameters of the respective
weight and moisture level determined. Dry grain yield was polynomial regressions were also fitted when the effect of N
expressed as Mg ha1 at 0% moisture. Using the data from grain rate was significant. The hybrid and N rate factors were
Fig. 1. Nitrogen rate effect on above-ground biomass (A), N content per plant (B), and N uptake efficiency (C) at flowering (R1) for the Illinois protein-strain hybrids
grown at Champaign, IL, between 2001 and 2003. The best polynomial regression model was fitted when the effect of N rate over the corresponding variable was
significant. The fitted equation parameters are presented in Table 2.86 M. Uribelarrea et al. / Field Crops Research 100 (2007) 82–90
Fig. 2. Nitrogen rate effect on above-ground biomass (A), N content per plant (B), and post-flowering N uptake (C) at physiological maturity (R6) for the Illinois
protein-strain hybrids grown at Champaign, IL, between 2001 and 2003. The best polynomial regression model was fitted when the effect of N rate over the
corresponding variable was significant. The fitted equation parameters are presented in Table 2.
considered fixed, and years (and its interaction with the fixed The protein-strain hybrids all produced similar shoot
effects) and replications as random factors. Since there was no biomass at flowering, and vegetative biomass was only
interaction between hybrid, N rate and year, we pooled years for influenced by the N rate in IHP (Fig. 1A). In contrast, plant
a better visualization of the effects of N. N accumulation increased linearly with N rate in each hybrid
Significance levels of fixed effects for each of the measured (Fig. 1B). The IHP-hybrid accumulated the most vegetative
variables are shown in Table 1, and the regression equation plant N (Table 3). The other three protein-strain hybrids all
parameters for the response to N rate of the variables are shown contained similar amounts of plant N at flowering, and all
in Table 2. responded to a lesser extent to incremental increases in the N
rate than did IHP (Table 3).
3. Results The N uptake efficiency at flowering (R1) differed among
the hybrids, and generally decreased with an increase in N
3.1. Biomass and N accumulation supply (Fig. 1C). The two hybrids with the highest concentra-
tions of grain protein (IHP and IRLP) exhibited higher
As previously reported (Uribelarrea et al., 2004), the
protein concentrations of the protein-strain hybrids reflected Table 4
the strain parents, with IHP and ILP having average grain Dry weight harvest index (HI), nitrogen harvest index (NHI), and percentage of
protein concentrations of 148 and 65 g kg1, respectively total plant N accumulation at flowering for the protein-strain hybrids grown at
Champaign, IL, between 2001 and 2003
(Table 3). The two reverse strains were intermediate with
IRLP having 111 g kg1 of grain protein and IRHP Strain-hybrid HI (%) NHI (%) N uptake at
flowering (%)
87 g kg1. The hybrids with the lowest grain protein
concentrations ILP and IRHP out-yielding the higher-protein FR1064 IHP 40 68 48
hybrids (IHP and IRLP) (Table 3). Similar differences were FR1064 ILP 46 51 64
FR1064 IRLP 41 62 48
observed among the strain-hybrids for grain energy
FR1064 IRHP 45 62 51
equivalent, with the two high protein hybrids exhibiting
lower average values than the two low protein hybrids LSD (P < 0.10) 3 4 6
(247 MJ ha1 versus 272 MJ ha1). Values are averaged across N rates.M. Uribelarrea et al. / Field Crops Research 100 (2007) 82–90 87
Fig. 3. Nitrogen rate effect on N remobilization between R1 and R6 for the stover (A), leaf (B), and stalk (C) fractions, for the Illinois protein-strain hybrids grown at
Champaign, IL, between 2001 and 2003. Positive values indicate accumulation of N in the plant fraction, while negative values represent N remobilization from the
plant fraction. Dashed lines indicate no remobilization or accumulation. The best polynomial regression model was fitted when the effect of N rate over the
corresponding variable was significant. The fitted equation parameters are presented in Table 2.
efficiencies of vegetative N uptake, and a sharper negative There were minor differences in the timing of N
response to increases in N supply. Conversely, ILP had the acquisition, with all hybrids except ILP acquiring around
lowest N uptake efficiency at R1, which was fairly constant for 50% of their plant N after flowering (Table 4). The hybrids
all N rates. differed, however, in their magnitude of post-flowering N
In contrast to R1, at physiological maturity both biomass and uptake, with IHP and IRLP exhibiting the highest maximum
N accumulation were affected by the hybrid and by the N rate levels of post-flowering N accumulation and a greater
(Fig. 2). The final biomass of IHP and IRLP responded to N rate response to increases in N rate (Fig. 2C). The strain-hybrids
with a higher slope, while the lower protein hybrids exhibited a also differed in remobilization of N from the stover, with IHP
more tempered increase in biomass with N rate (Fig. 2A; having the greatest remobilization, which increased with N
Table 3). When grown with the optimum N rate, the final supply (Fig. 3A). IHP also exhibited the greatest N
biomass production was relatively similar for all the protein- remobilization from the leaves (on average 0.33 g N plant1).
strain hybrids. Conversely, the dry weight harvest index (HI) 1). The remobilization of leaf N was enhanced by N rate in
(i.e. the proportion of the total above ground biomass both IHP and IRLP, but not in ILP and IRHP (Fig. 3A). IHP
represented by grain) differed among the strain-hybrids with was the only hybrid with measurable remobilization of N
the highest yielding hybrids (ILP and IRHP) having the highest from the stalk, which unlike leaves was not affected by the N
values (Table 4). supply (Fig. 3C).
The response in plant N accumulation was similar to
biomass with IHP and IRLP being more responsive to N than 3.2. Nitrogen use efficiency
the other two hybrids (Fig. 2B; Table 3). The 3.1 g plant1 of
N accumulated, on average by IHP and IRLP equates to a The overall N use efficiency (NUE) was similar among the
seasonal net acquisition of 201 kg N ha1, which was 40 kg hybrids (on average 24 kg kg1 N), and was negatively affected
more than IRHP and 69 kg more than ILP. The harvest index by N rate (Fig. 4A). The hybrids differed, however, in the main
for grain N (NHI) was not affected by N supply, although the components of NUE, N uptake and N utilization (Fig. 4).
IHP-hybrid had the highest and ILP the lowest NHI Differences in N uptake efficiency were related to the levels of
(Table 4). grain protein (r = 0.54; P 0.05), as well as to the differences88 M. Uribelarrea et al. / Field Crops Research 100 (2007) 82–90
Fig. 4. Nitrogen rate effect on N use efficiency (NUE) (A) and its two components: N uptake (B), and N utilization (C), for the Illinois protein-strain hybrids grown at
Champaign, IL, between 2001 and 2003. The best polynomial regression model was fitted when the effect of N rate over the corresponding variable was significant.
The fitted equation parameters are presented in Table 2.
in grain yield between years (Fig. 4B; Table 3). IHP had the absorption and translocation of N (Lohaus et al., 1998; Rizzi
highest overall values of N uptake efficiency and ILP the et al., 1996).
lowest, with the corresponding reverse-strain hybrids exhibit- An adequate N rate was needed for the IHP-hybrid to manifest
ing intermediate values of N uptake efficiency). In every case, its superior N accumulation, as at N levels of 100 kg ha1 or
N uptake exhibited a negative linear response to N supply lower it accumulated the same or lower amounts of vegetative N
(Table 3). as did the other hybrids. The IHP- and IRLP-hybrids also
N utilization efficiency was also affected by hybrid and by N exhibited more efficient pre-flowering N uptake than the two
rate (Fig. 4C). As opposed to N uptake, IHP exhibited the low-protein hybrids, and a greater magnitude of post-flowering N
lowest utilization efficiency, while ILP was the most efficient. accumulation. The difference in pre-flowering N uptake shows
The reverse-strains hybrids had similar values of utilization that the genetic differences in N metabolism are manifested
efficiency, falling in between those for IHP and ILP. before the grain is developed. A positive relationship between
pre-flowering leaf NO3 and grain yield and N concentration has
4. Discussion been reported by Hirel et al. (2001), who proposed that a high
capacity to store nitrate during vegetative growth was associated
A number of distinct differences in plant N use and growth with yield improvement. Similarly, our results show that N
were evident in the strain-hybrids. As reported previously for accumulation by the vegetative biomass can be enhanced by
the IHP and ILP strains (Wyss et al., 1991), the strain-hybrids selection for grain protein.
also produced similar amounts of plant biomass at flowering, The strain-hybrids also produced the same biomass at
indicative of similar levels of light interception and net canopy physiological maturity, even though IHP appeared to have
photosynthesis during the vegetative growth phase. Conversely, poorer growth when N was deficient. Post-flowering N uptake
plant N accumulation and N uptake efficiency were markedly was greatest in IHP and IRLP, intermediate in IRHP, and lowest
affected by both the hybrid and by the N rate. The much greater in the ILP-hybrid, which is in agreement with differences in
N accumulation by the IHP-hybrid than the other hybrids is in their sink demand for N (Uribelarrea et al., 2004). Similar to the
agreement with the idea that the IHP strain is enhanced in the strains themselves (Wyss et al., 1991; Rizzi et al., 1996; BelowM. Uribelarrea et al. / Field Crops Research 100 (2007) 82–90 89
et al., 2004), the IHP-hybrid exhibited substantial remobiliza- Cerrato, M.E., Blackmer, A.M., 1990. Comparison of models for descr-
ibing corn yield response to nitrogen fertilizer. Agron. J. 82, 138–
tion of N from the leaves and stalk, and had the lowest grain
143.
yield and HI. Dudley, J.W., Lambert, R.J., Alexander, D.E., 1974. Seventy generations of
The strain-hybrids had the same overall NUE, but differed selection for oil and protein in the maize kernel. In: Dudley, J.W. (Ed.),
markedly in the strategy they employed to achieve it with IHP Seventy Generations of Selection for Oil and Protein in Maize.Crop Science
and IRLP having higher efficiencies of N uptake, and ILP and Society of America, Madison, WI, pp. 181–211.
IRHP being more efficient in N utilization. We expect that high Dudley, J.W., Lambert, R.J., 1992. Ninety generations of selection for oil and
protein in maize. Maydica 37, 81–87.
N uptake efficiency would be associated with roots and nitrate Duvick, D.N., 1992. Genetic contributions to advances in yield in U.S. maize.
uptake, and high utilization efficiency with the degree of kernel Maydica 37, 69–79.
set and starch synthesis. Previous studies of the strains Eghball, B., Maranville, J.W., 1993. Root development and nitrogen influx of
themselves showed that roots of IHP are more efficient at corn genotypes grown under combined drought and nitrogen stresses.
Agron. J. 85, 147–152.
absorbing, reducing, and translocating N than ILP, while the
Gastal, F., Lemaire, G., 2002. N uptake and distribution in crops:
grain of ILP has higher levels of sugars and enhanced activities an agronomical and ecophysiological perspective. J. Exp. Bot. 53,
of enzymes associated with starch synthesis than does IHP (see 789–799.
review by Below et al., 2004). N uptake efficiency declined Gentry, L.E., Below, F.E., David, M.B., Bergerou, J.A., 2001. Source of the
with N rate to a greater extent than did N utilization efficiency, soybean N credit in maize production. Plant Soil. 236, 175–184.
which may be because high levels of available N saturate the Hedin, P.A., Williams, W.P., Buckley, P.M., 1998. Caloric analyses of the
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these hybrids makes them unique genetic materials for asparagine in the Illinois low protein and Illinois high protein strains of
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