Journal of Experimental Botany, Vol. 51, No. 352, pp. 1921-1929,
November 1, 2000
© 2000 Oxford University Press
Original Papers |
The strategy of the wheat plant in acclimating growth and grain production to nitrogen availability
Department of Crop Science, SLU, Box 44, S-230 53 Alnarp, Sweden
Received 12 May 2000; Accepted 22 June 2000
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Abstract |
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Two cultivars of spring wheat (Triticum aestivum L.) were grown to maturity in hydroponic cultures. Nitrogen accumulation was controlled by daily growth-limiting additions of nitrate together with all other nutrients in excess. Six different curves of N accumulation were used, with the same relative changes from day to day, but with different amplitudes. These curves were obtained by using the same mathematic formula of the N accumulation curves but varying the value of initial N content. The total amount of nitrogen added varied from 20 mg plant-1 to 65 mg plant-1. Plant bioproductivity showed a linear response to accumulated N. The number of grains per plant increased linearly with increased N availability whereas grain weights were essentially unaffected. Grain N concentrations and N content varied slightly, with highest values generally at the lower N availability levels. The quantitatively most important response to increased N availability was an increased number of earbearing tillers per plant. This varied from 0.1 tiller plant-1 at maturity when given 20 mg N plant-1, up to about 2 tillers plant-1 when given 65 mg N plant-1. Not all tillers that were initiated developed ears. The reduction of tillers seems to be one important mechanism in adapting plant productivity to N availability. Other individual characters influenced by N availability were straw height and the number of spikelets per spike. The two cultivars behaved in a qualitatively similar manner over the range of N availability even though they quantitatively differed in grain size, N concentrations and yield.
Key words: Nitrogen accumulation, nitrogen availability, tiller number, spring wheat, straw height.
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Introduction |
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Wheat is one of the most economically important cultivated plants. Modern culturing of wheat involves large land areas with intensive fertilization to achieve large yields and high protein concentrations. Most cultivars are selected to fit these culturing conditions. A growing environmental concern has focused on the intensive use of fertilizers and the concomitant leaching of nutrients from agricultural areas to water courses and coastal waters causing eutrophication. New trends in agriculture set new demands on the cultivars used, for example, cultivars fit for low input systems or ecological agriculture. Other desirable traits for improvement include baking quality and nutritional value.
As a result of centuries of both deliberate and inadvertent plant breeding, the varieties used today have little resemblance with their wild ancestors. Intensive breeding programmes have developed wheats with many desirable traits ranging from disease resistance and optimized morphology to grain protein composition. Until recently, most of the breeding has been done with traditional methods, i.e. crossings. Great effort has been put into selection of offspring which carry desired traits. Thanks to this work there exists a broad genetic material suited for a multitude of modern growth conditions. However, the selection of offspring has often been made under optimized environments and it is not unlikely that, at the same time as the cultivars have been improved in certain aspects, valuable traits such as efficient nutrient utilization under low nutrient availability conditions has been lost. Sometimes the development of new varieties with desired properties may have been hindered by the lack of knowledge of the physiology behind different traits. One reason for this has been the lack of techniques for growing cereals to full maturity and relevant development under fully controlled conditions. To be able to distinguish between broad environmentally imposed responses and fine-tuned genetically derived responses it is necessary to grow plants under conditions that are fully defined, can be varied and yet are reproducible. Nutrient conditions have proved difficult to keep under full control. Culturing in soil, whether in the field or under other conditions, gives only marginal control of the flow of nutrients to the root surface and the amounts of nutrients available to the plant. Culturing in hydroponics with external concentration of nutrients as a driving variable is also inadequate. Unless the concentrations of nutrients are extremely low and under precise control, there are only two options in concentration controlled cultures: excess supply or uncontrolled deficiency (MacDuff et al., 1993
). This is never the case in field cultures where there is a more or less continuous but usually growth-limiting flow of nutrients to the root surface. Growth of the plant is then acclimated to the flow of nutrients to the root. Changes in nutrient availability are seldom instantaneous but occur gradually over extended times allowing the plant a certain acclimation period to the prevailing conditions.
The conspicuous lack of information on the physiology behind many important nutrient-related traits in cereals is addressed in this paper. A suitable hydroponic technique for culturing cereals to maturity is presented and acclimation strategy of the wheat plant to variable nitrogen (N) availability is investigated. The study was initiated in order to investigate whether observed differences in yield could be explained in terms of differences in resource (N) utilization.
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Materials and methods |
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Two cultivars of spring wheat (Triticum aestivum L.) were grown to full maturity in hydroponic culture. The two cultivars were chosen because of their observed yield stability under varying field conditions. Cultivar Dragon is considered relatively stable with respect to yield and grain protein concentration whereas cultivar Sport gives a lower yield but higher grain protein concentration under favourable conditions. However, under some conditions, the performance of Sport is poorer than that of Dragon. Both cultivars were developed at Svalöf-Weibull AB, Svalöv, Sweden.
Seeds were germinated on wet filter paper in darkness at 20 °C for 5 d. The seedlings were then mounted in groups of four in black plastic blocks floating in black 2.0 l beakers with nutrient solution. The nutrient solution contained all necessary ions except nitrogen and was continuously stirred by air bubbling. The 2.0 l of N-free solution contained (mol m-3) K2SO4, 0.48; K2HPO4, 0.24: KH2PO4, 0.22; CaCl2, 0.18; MgCl2, 0.36; HCl, 50x10-3; FeCl3, 12.5x10-3; H3BO3, 18.5x10-3; MnCl2, 7.28x10-3; ZnCl2, 0.46x10-3; CuCl2, 0.48x10-3; Na2MoO4, 0.08x10-3; Fe-EDTA, 48.2x10-3.
After 7 d of nitrogen starvation the nutrient solution was replaced and subsequently changed weekly until final harvest. From the eighth day, the plants were given an additional dose of nutrients containing nitrogen together with all other nutrients. The N addition solution contained in mol m-3: K2SO4, 2.8; K2HPO4, 1.93; KH2PO4, 2.27; KNO3, 4.87; Ca(NO3)2, 15.49, Mg(NO3)2, 17.24; HNO3, 0.49, Fe(NO3)3, 0.13; H3BO3, 0.185; Mn(NO3)2, 72.8x10-3; Zn(NO3)2, 4.6x10-3, CuCl2, 4.72x10-3; Na2MoO4, 0.72x10-3. The size of the daily doses of nitrogen was calculated as Nt-N0 from the equation:
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Six different levels of total nitrogen accumulation were obtained by using six different N0-values (0.35, 0.5, 0.65, 0.8, 0.95, and 1.1 mg N grain-1). These values were not representative for the actual grain N content at the start of the experiment, but values used for the creation of the different N-accumulation curves. All plants were thus exposed to the same relative rates of nitrogen increment but the total amounts of nitrogen added varied between 20 to 65 mg N plant-1.
The plants were grown in climate chambers with a 16/8 h light/dark regime at 18/12 °C. A photon flux density of 250–300 µmol m-2 s-1 in the spectral range 400–700 nm was given by fluorescent tubes and tungstate bulbs. The relatively low light intensity, compared to sunlight, was not limiting for growth under the prevailing conditions of nitrogen-restricted growth (under similar light conditions stable growth rates of >0.20 d-1 were obtained for the first 5 weeks with the cultivar Dragon; O Hellgren and P Oscarson, unpublished results). The relative humidity was 70% throughout. A total of 186 containers with four plants per container were fairly evenly spread out in the climate chamber with a plant density of 16 containers m2. Plants were harvested at the ages of 62, 77, 86, 100, 112, and 126 d. Each harvest consisted of three containers of four plants (n=3) of each N level (a total of 18 containers=72 plants). The four plants in each container were not separated but each container was treated as one sample, the derived values being the mean of four plants. The final harvest at 126 d consisted of six containers of four plants (n=6) per N-level. The plants were divided into root, main stem vegetative parts, main stem grains, tiller vegetative parts, and tiller grains. After drying at 75 °C, the plant material was weighed and ground to fine powder for N analysis.
Nitrogen was analysed using a Carlo Erba NA1500 (Carlo Erba Strumentazione, Italy) elemental analyser.
Standard deviation is given for primary data (e.g. dry weights of parts etc.) when >10% of shown value.
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Results |
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By using six different values of initial N content, six different curves of N accumulation were obtained, with the same relative changes from day to day but with different absolute rates (Fig. 1
). The plants took up all the N added which was indicated by the good agreement between N added and measured N content (Fig. 2). This resulted in plants of different sizes (Fig. 3). A linear dependence of plant dry matter on plant N content was found over the whole range of N contents. Sport produced 0.141 g DW mg-1 N and Dragon produced 0.152 g DW mg-1 N. In field experiments, it is more or less impossible to get an estimate of root size and therefore the dry weight of only above-ground parts is most commonly used. Production of above-ground parts was 0.133 g DW mg-1 N in Sport and 0.136 g DW mg-1 N in Dragon.
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Growth of vegetative organs
All vegetative parts increased in weight with increased N availability (Fig. 3
). Most of the increase was found in the almost linear increase in tiller dry weight, which represented >40% of vegetative dry matter at the highest N level (Fig. 3; Table 1). The root and the main shoot also increased substantially in weight with N supply. The contribution of the root to total vegetative dry matter (Table 1) was relatively constant, except for at the lowest N level where compensatory root growth was observed (Oscarson et al., 1989a; Freijsen and Otten, 1987). The vegetative parts of the main shoot increased in weight with increased N level indicating that, at the lower N levels, not only tiller growth but also the development of the main shoot was limited (Fig. 3; Table 1). The main shoot also increased in height by 20–30% with increased N (Table 2). The increased weight of tillers was coupled to an increased number of tillers per plant at higher N levels (Fig. 4). The availability of N strongly affected the development of tillers, but also tiller reduction, as more than half of the tillers that started to grow never developed ears but died. The number of ear-bearing tillers showed an almost linear response with about 0.1 tiller spike per plant at the lowest N level up to 2 spike-bearing tillers per plant at the highest N level.
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The number of spikelets per spike increased by >25% in both the main shoot and in tiller spikes with increased N levels up to 56 mg N plant-1 (Table 2
). At the highest N level, the numbers of spikelets decreased compared to the 56 mg N plants as did main shoot straw height (Table 2).
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Grain production
The number of grains per spike in the main shoot increased by about 30% from the lowest to the highest N level (Fig. 5). As observed in Fig. 3, most of the increase in vegetative dry matter was attributed to tiller growth and this was reflected also in the number of tiller grains which increased with increased N availability. The total number of grains, like total dry weight, showed a linear relationship between plant production and N availability. It is obvious that the number of grains produced per plant was under strict control. In this investigation, nitrogen use efficiency can be expressed in terms of a grain production cost of about 0.56 mg N per grain.
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The dry matter yield of the main stem and tiller spikes increased with N availability (Fig. 6
). The increased yield in main stem spike was seen as an increased number of grains per spike (Fig. 5) distributed in an increased number of spikelets per spike (Table 2). The grain mean weight in the main stem spike was more or less constant over the whole range of N regimes (Fig. 6), and the same was observed for the mean number of grains per spikelet (Fig. 7). The results do not say where in the spike the extra grains were actually growing or if the extra spikelets were fertile.
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Tiller grain yield show a more complex picture. Firstly, as was shown in Fig. 4
, the number of tiller spikes increased with increased N availability as did the size of the tiller spikes (Table 2). The increased number of spikes contained more grains (Fig. 5). Both genotypes behaved similarly in these respects. In Sport, mean grain weight in tillers did not change with N availability and was about the same as in the main shoot. In Dragon, however, mean grain weights in the tillers were considerably lower compared to the main shoot in all but the two middle N levels, 38 and 47 mg N, respectively. No clear explanation for this was found. The yield in the tillers was thus the result mainly of three varying components: number of tiller spikes per plant, number of spikelets per spike and number of grains per spikelet and, in the case of Dragon, varying mean grain weight.
Harvest index (HI), grain yield per unit biomass, was unaffected by N availability if expressed per unit above-ground biomass or whole plant biomass (Table 1). The HI for both the whole plant (including root) was about 5% higher in Dragon. The same was true if HI was calculated on only above-ground parts. 5% in this respect was about 0.5 g higher grain yield per plant (Table 1).
Nitrogen distribution
All nitrogen added to the plants was taken up as there was full agreement between N added and N recovered in the plants (Fig. 2). This indicates that even at the highest N regime plant growth was limited by N availability as there would otherwise be a disagreement between N added and recovered.
The amount of N in the grains relative to whole plant N, i.e. nitrogen harvest index (NHI), did not change as a result of changed N availability, indicating that the N translocation efficiency was the same at different N levels (Table 1). The observed differences in HI between the two cultivars were less evident in NHI, the difference being 2–3%. The production of grains per unit nitrogen differed with about 8 g DW g-1 N, Dragon being the most productive, yielding 51 g DW g-1 N, whereas Sport produced about 43 g DW g-1 N.
Grain N concentrations were different at different N levels but the correlation was weak (Table 3). In the main stem grains, the N concentration varied between 1.52% and 1.80% of DW in Sport, whereas in Dragon the variation was smaller, 1.33–1.55%. The pattern was similar with tiller grain N concentration; 1.46–1.62% in Sport and 1.25–1.38% in Dragon. Measured grain N concentrations were higher in Sport than in Dragon, in full agreement with observed field results. A general tendency was that the grain N concentration decreased with increased N availability. The actual amount of N in each grain (Table 3) revealed that both main shoot and tiller grains in Sport contained about the same amount of N whereas, in Dragon, the grains vary in N-content without clear patterns or similarities between main shoot and tillers. The values of tiller grain N at the lowest N level should be taken with caution as tiller yield at this level was low.
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Of the 0.56 mg N required for production of one grain mentioned previously, between 0.36 and 0.40 mg actually ends up in the grains in Sport (Table 3
). The corresponding values for Dragon varied between 0.37 and 0.49 mg grain-1. The rest remained in the vegetative parts. The residual N in vegetative matter was about 30% of whole plant N, the distribution shown in Table 1.
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Discussion |
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Culturing
The influence of nutrient limitations on plant metabolism and development has previously been difficult to study as it has been difficult to mimic nutrient conditions in the field. In this study, the plants are at all times exposed to growth-limiting nutrient conditions, i.e. growth-limiting nitrogen availability. It has been shown earlier how growth of cereals acclimate to different levels of N limitation (Mattsson et al., 1991
, 1992a, b; Oscarson et al., 1995a, b; Oscarson, 1996). These papers show the irrelevance of using the concentration of nutrients in the medium as a driving variable and the importance of instead considering the flux density of nutrients to the root surface, as decisive for nutrient uptake. With the technique used here, N availability will oscillate on a daily basis as the medium is N depleted between additions. Plants will seem to be N sufficient until the daily addition is consumed and then uptake will cease and the plant is N deficient. However, looking at pools of N in the root or the export of N-containing compounds to the shoot these oscillations are smoothed out because of the relatively short period of the oscillation (Oscarson and Larsson, 1986). The implications of using daily additions of nutrient instead of more frequent additions has also been discussed previously by (Sands and Smethurst, 1995). Ideally, the flux approach can provide nutrients continuously to the plants at growth-limiting rates (Freijsen and Otten, 1987). In order to keep full control of N uptake and growth, the plants must at all times be growth-limited by N. As soon as other parameters become limiting, N accumulates in the plant and in the medium and control is lost. Under non-limiting growth conditions, tillering continues for an indefinite time with uneven maturation as a result (not shown here). To keep the plants N limited throughout development, the relative rates of N addition had to be stepwise decreased as vegetative growth and N demand decline after anthesis, favouring generative growth, i.e. grain filling. The technique used here, with daily additions of growth-limiting amounts of nitrate and different N0 values, made it possible to grow plants at different levels of N limitation under controlled conditions.
The plants took up all N added and increased N availability led to increased growth. There is only limited capacity to accumulate and store N for later use in the plant. When cell storage capacity is filled, nitrate uptake is down-regulated (Clarkson, 1986; Oscarson et al., 1989b). This results in accumulation of nitrate in the medium as the plant cannot take it all up and nitrate is subsequently lost when the medium is changed. This would result in a discrepancy between added and recovered N. Another sign of lost growth control and accumulation and storage of N would be a decline in biomass production per unit N as stored N does not take part in dry matter production. That all nitrate added was detected in the plants (Fig. 2), and that the dry matter production per unit N was constant (Fig. 3; Table 1), shows that the plants were growth-limited by N throughout the whole growth period.
Growth and N utilization
Increased availability of N resulted in increased vegetative and generative production of the plant. No single trait seemed responsible for the full response but rather a number of processes were integrated. Considering the linear relationship between N availability and the total number of grains in the plant it is tempting to single out grain number as the most important character responsible for the plasticity in production with respect to N availability. However, there are many individual processes that, integrated, are responsible for increased yield. The more N, the longer the main stem, with a spike that contained slightly more spikelets and grains. As the main shoot cannot harbour all of the increase in grain production, main shoot growth is co-ordinated with additional tiller grain production. Grain nitrogen relations show considerable variation in grain N concentration in relation to changes in N availability.
Partially degraining the main spike has resulted in compensatory grain growth in the remaining grains (Ma et al., 1990; Perez et al., 1989; Barneix and Guitman, 1993). Grain weight increased as did the N content. This was interpreted as source limitation of grain growth while in other experiments the plants showed no changes in grain weight and, in these cases, the plants were considered sink limited. Similar results were presented in experiments where the sterilization of florets led to more grain setting and greater grain growth in the untreated spikelets (Walpole and Morgan, 1973). That grain weight was essentially the same at all N levels presented here indicates that plant growth and grain production were well acclimated to N availability as more N did not result in larger grains but rather in more grains. Under these circumstances the increase in source resources led to production of more sinks, i.e. tillers and grains. Grain N concentration, however, showed variation with higher grain N concentrations at lower N availability, indicating that there was still N storage capacity in the grains not used at higher N levels. The results were similar for both cultivars, with the highest N concentrations in plants receiving 29 mg N plant-1. These plants gave the lowest yield per N (Table 1), leaving slightly more N for the grains produced. Some measured parameters differed quantitatively between the two genotypes, but the pattern of the response to increased N level was essentially similar in both genotypes.
Tiller production showed great plasticity with respect to N availability, similar to other observations (Longnecker et al., 1993). At all N levels, the plant produced more tillers than actually ended up setting grain. Tiller mortality has also been observed in other investigations, but the mechanism is still unclear (Thorne and Wood, 1988; Simmons et al., 1982). It is possible that overproduction of tillers is a strategic mechanism for flexibility towards resource availability by producing slightly more tillers than can be supported. If more nutrients become available, these extra tillers can be included in the overall resource allocation scheme. If no extra nutrients are available, support to these extra tillers is withdrawn and the nutrients remobilized for use in the rest of the plant. This reasoning much resembles that suggested for priority of grain filling (Bremner and Rawson, 1978) that, when assimilate is in short supply, the basal grain in each spikelet has priority over other grains. When in better supply, assimilates are also allocated to apical grains. This ensures that the quality of each and every grain produced is as high as possible under the prevailing conditions.
The tiller spikes produced more grains per spikelet with increased N levels, whereas in the main shoot spike, this value did not change. At low N availability, there were few grains per spikelet in the tillers but, as more N was available, more grains were filled. The main stem spikes were initiated early and, at this time, the nutritional differences may have been small compared to when tiller spike meristems were initiated. The main stem spikes were thus more uniform in size. When grain filling started in the main shoot spikes, about the same relative amounts of N were available for the growing grains. When tiller spikes were initiated, it is possible that low N availability resulted in smaller spikes with fewer florets. It is also possible that, when tiller grain filling started, more florets were aborted at lower N availability. It was not possible to distinguish between these two possibilities in this investigation. With respect to the overall results presented, the most important mechanism responsible for the plasticity in response to nutrient availability lies in the formation and reduction of tillers. As was observed with main stem development, the patterns of tiller response to increased N level were essentially similar in both genotypes. Several authors have reported differences in grain number, size and content depending on differences in N availability with time (Maidel et al., 1998). Part of this is likely to be the result of the inability of the plant to acclimate grain production to rapid environmental changes (Herrström, Eklund and P Oscarson, unpublished results), whereas, if the plants are given a chance to acclimate to slow changes in N availability, the grains produced are fairly similar in content and size and only grain number changes.
The response to long-term differences in N availability was mainly through characters associated with meristem development: tillers per plant, spikelets per spike and grains per spikelet. Similar responses have been observed in root development (Drew, 1975; Agrell et al., 1994). Short-term changes in N availability may have a similar effect if they coincide with the time of spike meristem initiation. The development of tiller meristems seems to have a broader time frame as tiller growth may start late during ontogeny if appropriate growth conditions occur. If changes in N availability take place during times other than meristem initiation, other mechanisms such as tiller reduction or floret abortion (Siddique et al., 1989; Marshall and Ellis, 1998) still allow for the plant to acclimate grain production to nutrient conditions. The mechanism sensing the level of N availability and inducing development of additional sinks is as yet uncertain. It has been observed that nitrogen limitation in suspension cultures of Acer cells caused cell division to stop in the G1 phase (Gould et al., 1981). Sugar beet cells in suspension culture entered the G0 phase as a consequence of nutrient depletion (Fowler et al., 1998). Regulation of the cell cycle has been studied intensively (Chasan, 1995), and it does not seem unlikely that some nitrogenous compound, either nitrate or another N-containing compound like an amino acid, could act as a regulator of cell proliferation and differentiation at the gene level. Deficiency of this compound would inevitably lead to cessation of meristem growth, or, excess could lead to stimulation of meristem development. This idea is further substantiated by earlier results (Bussink and Osmani, 1998) which showed that cyclin-dependent kinases functioned as integrators of environmental signals and developmental decisions in Aspergillus. This, however, calls for further investigation.
Baking quality
Baking quality of wheat meal is influenced not only by the protein concentration but also by the protein composition (Payne et al., 1987; Johansson and Svensson, 1995). It is observed here that the N concentration in the grains varied to some extent depending on N availability. How this influences baking quality is not known. Factors influencing baking quality are poorly understood and hard to analyse in terms of chemical properties. The plant material produced here is to be investigated regarding protein composition and protein aggregation properties.
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Conclusion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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This investigation was initiated in order to study the patterns of plant production at different levels of N availability and the mechanisms with which the wheat plant responds to increased N levels. The aim was to investigate whether differences in the use of N could explain differences in performance between the two spring wheat cultivars Dragon and Sport. It can be concluded, however, that none of the characters measured here concerning nitrogen use efficiency explained the sometimes poor performance and baking quality of Sport. Under controlled laboratory conditions, both genotypes behaved in a similar manner even though they sometimes differed quantitatively. The productivity of the plants, measured as the performance of different traits, increased in a more or less linear manner with increased N availability. Even at low N levels, the plants still produced grains, at a lesser number, but with seemingly similar quality. There was a linear relationship between grain number and N availability. Most of the increased productivity at higher N availability could be attributed to an increased number of tillers per plant and, to some extent, by more spikelets per spike.
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Acknowledgments |
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This research was supported by the Swedish Council for Forestry and Agricultural Research.
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Notes |
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1 Fax: +46 418 667 081. E-mail: Petter.Oscarsson{at}vf.slu.se
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References |
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Agrell D, Oscarson P, Larsson C-M.1994. Translocation of N to and from barley roots: its dependence on local nitrate supply in split-root culture. Physiologia Plantarum 90, 467–474.
Barneix AJ, Guitman MR.1993. Leaf regulation of the nitrogen concentration in the grain of wheat plants. Journal of Experimental Botany 44, 1607–1612.
Bremner PM, Rawson HM.1978. The weights of individual grains of the wheat ear in relation to their growth potential, the supply of assimilate and interaction between grains. Australian Journal of Plant Physiology 5, 61–72.
Bussink H-J, Osmani SA.1998. A cyclin-dependent kinase family member (PHOA) is required to link developmental fate to environmental conditions in Aspergillus nidulans. The EMBO Journal 17, 3990–4003.[Web of Science][Medline]
Chasan R.1995. STARTing the cell cycle. The Plant Cell 7, 1–3.[Web of Science]
Clarkson DT.1986. Regulation of the absorption and release of nitrate by plants: A review of current ideas and methodology. In: Lambers H, Neeteson JJ, Stulen I, eds. Developments in plant sciences, Vol. 19. Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants. Dordrecht: Martinus Nijhoff Publishers, 3–27.
Drew MC.1975. Comparison of the effects of localised supply of phosphate, nitrate, ammonium, and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist 75, 479–490.[Web of Science]
Fowler MR, Kirby MJ, Slater A, Scott NW, Elliott MC.1998. The entry of sugar beet cells into the G0 state involves extensive re-programming of gene expression mechanisms via transcriptional and translational controls. Plant Science 136, 79–91.
Freijsen AHJ, Otten H.1987. A comparison of the response of two Plantago species to nitrate availability in culture experiments with exponential nutrient addition. Oecologia 74, 389–395.
Gould AR, Everett NP, Wang TL, Street HE.1981. Studies on the control of the cell cycle in cultured plant cells. I. Effects of nutrient limitation and nutrient starvation. Protoplasma 106, 1–13.
Johansson E, Svensson G.1995. Contribution of the high molecular weight glutenin subunit 21* to breadmaking quality of Swedish wheats. Cereal Chemistry 72, 287–290.
Longnecker N, Kirby EJM, Robson A.1993. Leaf emergence, tiller growth and apical development of nitrogen-deficient spring wheat. Crop Science 33, 154–160.
Ma Y-Z, MacKown CT, Van Sanford DA.1990. Sink manipulation in wheat: compensatory changes in kernel size. Crop Science 30, 1099–1105.
MacDuff JH, Jarvis SC, Larsson C-M, Oscarson P.1993. Plant growth in relation to the supply and uptake of 
: a comparison between relative addition rate and external concentration as driving variables. Journal of Experimental Botany 44, 1475–1484.
Maidel F-X, Stiksel E, Retzer F, Fischeck G.1998. Effect of varied N-fertilization on yield formation of winter wheat under particular consideration of mainstems and tillers. Journal of Agronomy and Crop Science 180, 15–22.
Marshall B, Ellis RP.1998. Growth, yield and grain quality of barley (Hordeum vulgare L.) in response to nitrogen uptake. 1. A low cost, controlled nutrient supply system. Journal of Experimental Botany 49, 1049–1057.
Mattson M, Lundborg T, Larsson M, Larsson C-M.1991. Nitrogen utilization in N-limited barley during vegetative and generative growth. I. Growth and nitrate uptake kinetics in vegetative cultures grown at different relative rates of nitrate-N. Journal of Experimental Botany 42, 197–205.
Mattson M, Lundborg T, Larsson M, Larsson C-M.1992a. Nitrogen utilization in N-limited barley during vegetative and generative growth. II. Method for monitoring generative growth and development in solution culture. Journal of Experimental Botany 43, 15–23.
Mattson M, Lundborg T, Larsson M, Larsson C-M.1992b. Nitrogen utilization in N-limited barley during vegetative and generative growth. III. Post-anthesis kinetics of net nitrate uptake and the role of relative root size in determining the capacity for nitrate acquisition. Journal of Experimental Botany 43, 25–30.
Oscarson P.1996. Transport of recently absorbed 15N nitrate to individual spikelets in spring wheat grown in solution culture. Annals of Botany 78, 479–488.
Oscarson P, Ingemarsson B, Larsson C-M.1989a. Growth and nitrate uptake properties of plants grown at different relative rates of nitrogen supply. I. Growth of Pisum and Lemna in relation to nitrogen. Plant, Cell and Environment 12, 779–785.
Oscarson P, Ingemarsson B, Larsson C-M.1989b. Growth and nitrate uptake properties of plants grown at different relative rates of nitrogen supply.II. Activity and affinity of the nitrate uptake system. Plant, Cell and Environment 12, 787–794.
Oscarson P, Larsson C-M.1986. Relations between uptake and utilization of in Pisum growing under nitrogen limitation. Physiologia Plantarum 67, 109–117.
Oscarson P, Lundborg T, Larsson M, Larsson C-M.1995a. Genotypic differences in N uptake and N utilization for spring wheat (Triticum aestivum L.) grown hydroponically. Crop Science 35, 1056–1062.
Oscarson P. Lundborg T, Larsson M, Larsson C-M.1995b. Fate and effects on yield components of extra applications of nitrogen on spring wheat (Triticum aestivum L.) grown in solution culture. Plant and Soil 175, 17–188.
Payne PI, Nightingale MA, Krattiger AF, Holt LM.1987. The relationship between HMW glutenin subunit composition and the bread-making quality in British-grown wheat varieties. Journal of the Sciences of Food and Agriculture 40, 51–65.
Pérez P, Martínez-Carrasco R, Martin Del Molino IM, Rojo B, Ulloa M.1989. Nitrogen uptake and accumulation in grains of three winter wheat varieties with altered source-sink ratios. Journal of Experimental Botany 40, 707–710.
Sands PJ, Smethurst PJ.1995. Modelling nitrogen uptake in Ingestad units using Michaelis–Menten kinetics. Australian Journal of Plant Physiology 22, 823–831.
Siddique KHM, Kirby EJM, Perry MW.1989. Ear:stem ratio in old and modern wheat varieties, relationship with improvement in number of grains per ear and yield. Field Crops Research 21, 59–78.
Simmons SR, Rasmusson DC, Wiersma JV.1982. Tillering in barley:Genotype, row spacing and seeding rate effects. Crop Science 22, 801–805.
Thorne GN, Wood DW.1988. Contributions of shoot categories to growth and yield of winter wheat. Journal of Agricultural Science, Cambridge 111, 285–294.
Walpole PR, Morgan DG.1973. The effects of sterilisation on grain number and grain weight in wheat ears. Annals of Botany 37, 1041–1048.
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  P. Bancal Decorrelating source and sink determinism of nitrogen remobilization during grain filling in wheat Ann. Bot., June 1, 2009; 103(8): 1315 - 1324. [Abstract] [Full Text] [PDF]
|
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|
|
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|
 M. C. Falk, B. M. Chassy, S. K. Harlander, T. J. Hoban IV, M. N. McGloughlin, and A. R. Akhlaghi Food Biotechnology: Benefits and Concerns J. Nutr., June 1, 2002; 132(6): 1384 - 1390. [Abstract] [Full Text] [PDF]
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