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First published online November 20, 2003; 10.1104/pp.103.030585 Plant Physiology 133:1959-1967 (2003) © 2003 American Society of Plant Biologists Modeling Grain Nitrogen Accumulation and Protein Composition to Understand the Sink/Source Regulations of Nitrogen Remobilization for WheatUnité d'Agronomie, Institut National de la Recherche Agronomique, F-63039 Clermont-Ferrand cedex 2, France (P.M., E.T.); Department of Agricultural Sciences, Royal Veterinary and Agricultural University, 2630 Taastrup, Denmark (J.R.P.); and New Zealand Institute for Crop and Food Research Ltd., Private Bag 4704, Christchurch, New Zealand (P.D.J.)
A functional explanation for the regulation of grain nitrogen (N) accumulation in cereal by environmental and genetic factors remains elusive. Here, new mechanistic hypotheses of grain N accumulation are proposed and tested for wheat (Triticum aestivum). First, we tested experimentally the hypothesis that grain N accumulation is mostly source regulated. Four contrasting cultivars, in terms of their grain N concentrations and yield potentials, were grown with non-limiting N supply. Grain number per ear was reduced by removing the top part of the ear at anthesis. Reduction in grain number gave a significant increase in N content per grain for all cultivars, showing that grain N accumulation was source regulated. However, on a per ear basis, cultivars with a high grain number fully compensated their N accumulation for reduced grain number at anthesis. Cultivars with a lower grain number did not compensate completely, and grain N per ear was decreased by 16%. Second, new mechanistic hypotheses of the origins of grain N source regulation and its response to environment were tested by simulation. The hypotheses were: (a) The regulation by N sources of grain N accumulation applies only for the storage proteins (i.e. gliadin and glutenin fractions); (b) accumulation of structural and metabolic proteins (i.e. albumin-globulin and amphiphilic fractions) is sink-regulated; and (c) N partitioning between gliadins and glutenins is constant during grain development and unmodified by growing conditions. Comparison of experimental and simulation results of the accumulation of grain protein fractions under wide ranges of N fertilization, temperatures, and irrigation supported these hypotheses.
One challenge for global nutrition in the next decade is to increase food yield per unit ground area in a sustainable manner while maintaining its end use value (Cassman, 1999  ; Tilman, 1999; Tilman et al., 2002). Grain protein concentration and composition are major determinants of grain nutritional value (Feil, 1997). The concentration of Lys in grain, the most limiting amino acid in cereals for human and monogastric animals, increases with increasing grain protein concentration (Feil, 1997) despite the decrease of its concentration in total protein (Mossé et al., 1985). Grain protein concentration and composition are also the major determinants of flour functional properties (Weegels et al., 1996; Shewry and Halford, 2002). However, the inverse relationship between grain yield and protein concentration, reported for several species, may prevent breeders from improving these two traits simultaneously (Stewart and Dwyer, 1990; Delzer et al., 1995; Feil, 1997; Brancourt-Hulmel et al., 2003). To break this inverse relationship, genetic increments in grain protein yield must keep pace with those in grain yield. Therefore, efforts to overcome the inverse relationship between grain yield and protein concentration must concentrate on improving grain protein accumulation per square meter and per grain (Feil, 1997; Triboï and Triboï-Blondel, 2002).
An increase in grain protein content may come from either improved capacity of the grain to accumulate nitrogen (N) or through greater N supply to the grains (Triboï and Triboï-Blondel, 2002
Grain proteins can be divided into structural/metabolic (Nstru) and storage (Nsto) proteins (Shewry and Halford, 2002
In this study, we manipulated the sink to source ratio of four contrasted wheat cultivars to show that, overall, grain N is regulated by the supply of N to the grain. This was further confirmed by a simulation study using the wheat simulation model Sirius (Jamieson and Semenov, 2000
Grain N Accumulation Is Source Regulated for Both High- and Low-Yielding Cultivars
First, we analyzed the level of supply limitation of grain N accumulation in four cultivars with different potential grain numbers per square meter, an increase in which has been one of the major factors contributing to grain yield increases over the last 40 years (Reynolds et al., 1999 Grain yield, yield components, and N content and concentration for the four cultivars and the different treatments show that, under normal conditions, grain number per ear was highest for the cultivars Arche and Récital, intermediate for Renan, and lowest for Tamaro (Table I). Grain yield was not significantly different for the cultivars Arche, Récital, and Renan but was 52% to 60% lower for Tamaro compared with the three other cultivars. The four cultivars analyzed could be separated as low (Arche and Récital) and high (Renan and Tamaro) protein cultivars (Table I).
The ear halving treatment at anthesis reduced the number of grains per ear (i.e. per square meter) by 26% to 32%. This treatment leaded to an increase in N content per grain of 37%, 43%, 25%, and 14% for Arche, Récital, Renan, and Tamaro, respectively (Table I). However, not all cultivars fully compensated for the reduced grain number. Grain N per ear decreased by 16% for the two cultivars with the lower grain number per square meter (i.e. Renan and Tamaro; Fig. 1). In contrast, grain N per ear was not modified by the reduction in grain number per ear at anthesis for the two cultivars with the higher grain number per square meter (i.e. Arche and Récital).
Ear halving at 250 °Cd after anthesis reduced the sink size by 37% to 40%, leading to an increase of N content per grain of 29%, 24%, 12%, and 9% for Arche, Récital, Renan, and Tamaro, respectively (Table I), whereas grain N per ear decreased by 22% to 33% for all four cultivars (Fig. 1).
Regulation of grain N accumulation was further analyzed by simulating N uptake and redistribution for wheat crops grown in the field with a combination of rates and timings of N fertilization and in controlled environments, where different postanthesis temperatures and watering regimes were applied postanthesis. The wheat simulation model Sirius was used to simulate dry matter and N accumulation in the different organs of the crops for these experiments. Simulated and observed kinetics of grain N accumulation for the different experimental treatments agreed well (data not shown), and simulated and observed final grain N were well correlated (r2 = 0.83, 16 degrees of freedom [d.f.]; Fig. 2). The square root of the mean square error of prediction was 2.5 g N m-2 over a range of 5.4 to 23.8 g N m-2.
Consideration of the protein fractions in the grain gives a new perspective to the supply regulation of grain N accumulation. An example of the kinetics of accumulation of Nstru, Ngli, and Ngln obtained for crops grown in the field with a combination of two rates and timings of N fertilization is shown in Figure 3. Pre-anthesis N fertilization increased only slightly (7%) the final quantity of Nstru but increased the final quantities of Ngli and Ngln by 33% and 22%, respectively (Fig. 3, A and C). Under conditions of preanthesis N shortage, N fertilization at anthesis increased the final quantity of Nstru by 25% but that of Ngli and Ngln by 95% and 49%, respectively (Fig. 3, A and B). Under conditions of normal pre-anthesis N fertilization, postanthesis N fertilization increased the final quantity of Nstru, Ngli, and Ngln by 3%, 26%, and 9%, respectively (Fig. 3, C and D). Thus, the accumulation of Ngli and Ngln are significantly enhanced by N fertilization, whereas Nstru is little affected.
The model of accumulation of grain protein fractions described here gave accurate simulations of the accumulation of Nstru, Ngli, and Ngln, even for conditions of non-limiting soil N supply, such as the treatment H15 (Fig. 3). Similar agreement was observed for the 14 other treatments of Figure 2 (data not shown). Simulated and observed Ngli (r2 = 0.86, 16 d.f.) and Ngln (r2 = 0.96, 16 d.f.) at harvest ripeness were well correlated (Fig. 4). The square root of the mean square error of prediction was 26 µg N grain-1 over a range of 84 to 315 µg N grain-1 for Ngli and 31 µg N grain-1 over a range of 215 to 508 µg N grain-1 for Ngln.
The supply limitation of grain N uptake may apply predominantly at a particular stage of the development of the grain. Hence, we used our model of grain N partitioning to analyze the joint evolution of the demand for Nstru (Nstrudemand) and the supply of total N (Ntotsupply; Fig. 5). During the first 10 to 15 d after anthesis, Ntotsupply balanced Nstrudemand, indicating that grain N accumulation during that period was sink regulated. Nevertheless, during the period of accumulation of storage protein, i.e. from approximately 15 d after anthesis to grain maturity, Ntotsupply was 2 to 3 times higher than Nstrudemand, indicating that the accumulation of grain N was then limited by the supply of N.
The experiments and simulations reported here were designed to analyze the source/sink regulation of grain N accumulation and to assess its genetic variability. Several lines of evidence from studies on detached ears cultured in vitro (Barlow et al., 1983 ; Corke and Atsmon, 1988) and isolated plants cultivated in pots under controlled environments (Barneix and Guitman, 1993; Dreccer et al., 1997) have suggested that grain N accumulation for many cereal species is source regulated, but apparently this never has been investigated at the canopy level under field or controlled environment conditions, and most studies have been limited to one genotype. Moreover, no functional hypothesis has been proposed to account for the source regulation of grain N accumulation. We modified the sink to source ratio of four contrasted genotypes of wheat grown in the field. The results show that the level of source regulation of grain N accumulation depends on the genotypes, but none of the genotypes were sink limited. The hypotheses framed above have been formulated in a simulation model that predicted the dynamic changes of grain protein composition, an important nutritional and economic trait for cereals. The simulation results presented here support these hypotheses over a broad range of environmental conditions.
Ear halving increases the availability of N to the remaining grains either at anthesis or 250 °Cd later, when cell division has ended and grain growth is solely due to cell expansion (Gleadow et al., 1982 We were able accurately to predict total grain N accumulation over a large range of grain N for Thésée, a high-yield potential and grain number cultivar, by assuming grain N accumulation to be determined by the size of the source of N, defined as the total nonstructural crop N at anthesis. This gives further support to the previous conclusion that, overall, the accumulation of grain N, at least for high-yielding cultivars with high grain number, is regulated by the source of N and not by the activity of the grain.
Using the model of accumulation of protein fractions described here, the comparison of the simulated demand and supply of grain N suggested that grain N accumulation was sink limited or colimited by both source and sink for the first 10 to 15 d after anthesis. This emphasizes the importance of the early stage of grain development, characterized by active cell division in the endosperm, in setting the potential grain size and Nstru. In contrast with the early phase of grain development, grain N accumulation was always source limited during the grain filling period, even when soil N was non-limiting. Moreover, simulations and observations of the accumulation of grain protein fractions for developing grains obtained from plants grown in the field with different rates and timings of N fertilization and in the controlled environment chambers with different postanthesis temperatures and watering regimes agreed well, verifying the hypothesis that the supply limitation of grain N accumulation results from the accumulation of storage proteins and not from that of structural proteins. Thus, the sink/source limitation of grain protein accumulation is related to differences in the timing of deposition between structural/metabolic proteins versus storage proteins, as postulated earlier for barley (Dreccer et al., 1997
The source regulation of the accumulation of storage proteins gives a mechanistic explanation of the effect of overexpressing glutenin genes on protein composition and concentration where the transformation of wheat with high-Mr glutenin subunit genes results in increased quantities and proportions of the high-Mr glutenin subunits (Altpeter et al., 1996
The hypothesis introduced in our simulation model of grain protein accumulation that the partitioning coefficient for Ngli and Ngln is constant during grain development and is not modified by the growth conditions was verified. This implies that any modification of the gliadins to glutenins ratio is only the result of modification of total N content per grain and that the processes leading to the synthesis of storage proteins in the grain are not affected by the concentration of N. We observed similar result for the albumin-globulin and the amphiphilic proteins, the constituent of Nstru (data not shown). Preliminary data indicate that this is true for the other cultivars studied here, i.e. Arche, Récital, Renan, and Tamaro (V. Samoil, P. Martre, and E. Triboï, unpublished data), and, importantly, the same partitioning parameters applied. These results imply that the protein fractions and amino acids composition of wheat grains from widely different cultivars can be deduced directly from the total quantity of N per grain. Furthermore, we suggest that the genotype-environment interactions for the composition of protein fractions reported earlier (Graybosch et al., 1996
Functional genomics and proteomics studies aiming at understanding the regulation of grain protein level and composition for cereals, especially wheat (Clarke et al., 2001
All experiments were at Clermont-Ferrand, France (45°47' N, 3°10' E, 329-m elevation) with winter wheat (Triticum aestivum) cv Thésée, Arche, Récital, Renan, and Tamaro.
Source/sink regulation of grain N accumulation was studied in the field for four cultivars (Arche, Récital, Renan, and Tamaro) with contrasting potential grain number, grain yield, and grain protein concentration. One main plot of 202 m2 was sown for each cultivar on November 7, 2001 at a density of 300 grains m-2. The crops were rain fed. Accumulated rainfall from sowing to anthesis and from anthesis to grain maturity was 124 to 174 and 115 to 135 mm depending on the cultivar, respectively. Average air temperature from sowing to anthesis and from anthesis to grain maturity was 6.8°C to 7.3°C and 17.8°C to 18.7°C depending on the cultivar, respectively. The crops received 10 g N m-2 on March 3, 2002 and 15 g N m-2 on April 30, 2002. Anthesis was recorded on May 24, 15, 21, and 28, 2002 for Arche, Récital, Renan, and Tamaro, respectively. The source to sink ratio was artificially manipulated by removing the top one-half or so of the ears from the main stems on three 0.5-m-2 subplots per cultivar. At the same time, three 0.5-m-2 control subplots were identified for each cultivar. Ear halving was performed either at anthesis or 249, 277, 254, and 244 °Cd later for Arche, Récital, Renan, and Tamaro, respectively. Samples of 0.5 m2 were taken in each subplot at the time when ears were halved and at grain maturity. Three replicates were used per N treatment.
To study the effects of postanthesis temperature and drought at the canopy level, crops of wheat cv Thésée were grown in 2-m2 containers in controlled environment closed-top chambers under natural light (Triboï et al., 2003 Interactions between postanthesis temperature and drought were studied in a 2nd year of experiments where two air temperatures (-5°C and +5°C, average temperature of 12.6°C and 19.9°C, respectively) were applied from 5 d after anthesis to grain maturity. The crops were rain fed from sowing to anthesis and received 226 mm of rainfall during that period. One container for each temperature treatment received 25 to 50 mm of water every 4 to 7 d until harvest maturity to replace measured crop evapotranspiration (treatments -5W and +5W), whereas the other container received 5% to 15% of the measured crop evapotranspiration from anthesis to harvest maturity (treatments -5D and +5D). Crop evapotranspiration and, thus, crop water requirements under the controlled environment chambers were computed from measurements of the volume of water condensed on the cold exchanger of the chambers and the difference of air vapor pressure between the outlet and inlet of the chambers. One controlled environment chamber/container was used per treatment. To study the dynamic accumulation of total N and protein fractions, three replicates each of 20 plants (approximately 0.25 m2) were collected every 50 to 130 °Cd from anthesis to grain maturity. Plants were sampled from the northern side of the containers through their southern side. To minimize the border effects, for each sampling date, the northernmost raw was discarded, and after each sampling, a net of the high of the crop was placed in place of the last raw removed.
The effect of N availability at anthesis in relation to the level of N nutrition before anthesis was studied in a field experiment for crops of wheat cv Thésée sown at a density of 300 seeds m-2 (Triboï et al., 2003
Grains were separated, and their dry mass was determined on sub-samples after oven drying at 70°C to constant mass. The remaining grains were frozen in liquid N, freeze dried, and stored at 4°C before analysis.
The protein fractions albumin-globulin, amphiphilic, gliadin, and glutenin were sequentially extracted from whole meal flour (Triboï et al., 2003
We used the wheat simulation model Sirius V99 (Jamieson and Semenov, 2000 The initial quantity of soil organic N at sowing was adjusted in Sirius to match the observed crop N content at anthesis using the treatments 0 and L0 for the controlled environment closed-top chamber and field experiments, respectively. Phenological development was not part of this study. Thus, the phyllochron in Sirius was adjusted so that the simulated and observed anthesis dates matched. A phyllochron value of 93 °Cd was used for the controlled environment chamber experiments, and 112 °Cd was used for the field experiments. Where appropriate, others genetic parameters in Sirius were set as for wheat cv Claire.
Although grain yield and protein content are regulated at the square meter scale (Jamieson and Semenov, 2000
 gli is the partitioning coefficient for Ngli.
The daily flux of Nstru was expressed as the minimum of the daily demand for Nstru (Nstrudemand) and the daily supply of total N (Ntotsupply). Based on previous work (Stone and Nicolas, 1996
 is the average daily temperature, Tt is the thermal time after anthesis, base 0°C, and Dcd and Der are the durations in thermal time of the cell division and DNA endoreduplication phases, respectively.
Based on previous work for grain of maize (Zea mays; Tsai et al., 1980
Using treatment 0 of the experiment in the controlled environment chambers, kcd and
The authors thank Drs. Stefan M. Henton and Jean-Francois Soussana and Mr. Robert F. Zyskowski for helpful discussions, and Drs. Gérard Branlard, Maarten J. Chrispeels, Tony Fischer, Peter R. Shewry, and Thomas R. Sinclair for comments on an earlier version of this manuscript. Miss Sandrire Revaillot, Mrs. Joëlle Messaoud, Mr. Bernard Bonnemoy, Mr. Michel Martignac, and Mr. Robert Falcimagne are thanked for their skillful technical assistance. Received July 21, 2003; returned for revision August 20, 2003; accepted September 4, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.030585. * Corresponding author; e-mail pmartre{at}clermont.inra.fr; fax 33-473-624-457.
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TOP
ABSTRACT
RESULTS
, treatment -5; 
, 0; 
,+5; 
,+5/+10; and 
,+10/+5) or with different postanthesis temperatures and watering regimes ([hexagon], -5W; 
, M0; 
, M3; 
, M15; 
, H0; 
, H3; and [hexagonblack], H15). Treatments are denoted as outlined in "Materials and Methods." The solid line is y = x.
