JXB Advance Access originally published online on July 28, 2003
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Journal of Experimental Botany, Vol. 54, No. 390, pp. 2081-2090,
September 1, 2003
© 2003 Oxford University Press
The nitrogen and nitrate economy of butterhead lettuce (Lactuca sativa var. capitata L.)
Received 5 December 2002; Accepted 20 May 2003
1 Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK
2 Agricultural Engineering Department, Technion, Haifa 32000, Israel
3 INRA, Poitou-Charentes, 86600 Lusignan, France
* Present address and to whom correspondence should be sent: Division of Plant Sciences, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK. Fax: +44 (0) 115 9516334. E-mail: martin.broadley{at}nottingham.ac.uk
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Abstract |
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Quantifying and simulating the relationships between crop growth, total-nitrogen (total-N) and nitrate-N (NO3–-N) concentration can improve crop nutritional husbandry. In this study, the relationship between shoot relative growth rate (RGR) and shoot total-N, organic-N and NO3–-N concentration of hydroponically-grown lettuce (Lactuca sativa var. capitata L. cv. Kennedy) was described and simulated. Plants were grown hydroponically for up to 74 d. Nitrogen was supplied throughout (control; T1), or removed at 35 d (T2) and 54 d (T3), respectively, after sowing. The organic-N and NO3–-N concentration declined in the shoots of control plants with growth, until commercial maturity approached when organic-N and NO3–-N concentration increased. There were sub-linear relationships between both total-N and organic-N concen tration, and shoot RGR, in the N-limited treatments, i.e. shoot RGR approached an asymptote at high shoot N concentration. The proportional effects of total-N and organic-N concentration on shoot RGR were independent of plant age. A dynamic simulation model (‘Nicolet’), derived previously under different conditions, was used to simulate the growth, dry matter content, organic-N, and NO3–-N concentration of lettuce grown under the extreme N-stress conditions experienced by the plants. In view of the largely successful fitting of the model to experimental data, the model was used to interpret the results. Suggestions for model improvement are made.
Key words: Effective day-degree (EDD), excess carbon, Nicolet, nitrate, osmotica balance.
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Introduction |
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Large inputs of mineral fertilizer nitrogen (N) are routinely used to maintain the yield and quality of crops. Nitrogen not recovered by crops can pollute adjacent terrestrial and aquatic habitats. This can cause a reduction in biodiversity since species that are characteristic of infertile habitats do not tend to thrive following nutrient-enrichment (Grime, 2001). Further, certain crops can accumulate high levels of N in the form of nitrate-N (NO3–-N). The perception that high NO3–-N containing crops, in particular crops such as lettuce and spinach, may be detrimental to human health has led to maximum levels of NO3–-N to be defined for leafy salad crops in Europe (Commission of the European Communities, 2001). Thus, the efficient use of N is an important environmental and legal issue, in addition to the potential cost savings of reduced fertilizer use. Maxi mizing the nitrogen-use efficiency of crop production can be achieved (i) by optimizing the supply of N to meet the requirements of a crop during growth and development or (ii) by growing N-efficient crop genotypes. Although genetic variation in NO3–-N concentration of lettuce shoots has been demonstrated (Reinink, 1991; Escobar-Gutiérrez et al., 2002), the commercial release of low-NO3–-N or N-efficient lettuce cultivars has not yet been reported.
The N requirement of plants correlates with plant relative growth rate (RGR). Relative growth rate is the amount of dry matter produced per unit of existing dry matter over time. As plants grow in size, the volume of non-photosynthetic materials will increase faster than the area of photosynthetically-active surfaces, due to scaling constraints (Hardwick, 1987; Greenwood et al., 1990). Since non-photosynthetic materials contain less N than photosynthetically-active materials, both relative plant growth and plant N concentration decline during growth (Greenwood et al., 1990). Thus, positive relationships between N and RGR are observed in diverse plant types and in different environments (Field and Mooney, 1986; Ågren, 1988; Burns, 1994a, b).
One method to quantify the relationship between RGR and N concentration under extreme N-stress conditions is to grow plants in hydroponics and to remove N completely from the external nutrient solution in one set of plants (Walker et al., 2001). In plants whose N supply is removed, internal N reserves are recycled to maintain growth. Relationships between RGR and N concentration can subsequently be determined relative to a control supplied continuously with N. In hydroponically-grown young lettuce, RGR and plant N concentration are highly correlated and this relationship is sub-linear, i.e. shoot RGR approaches an asymptote at high shoot N concentration (Burns, 1994a, b; Broadley et al., 2000, 2001; Walker et al., 2001).
In this study, the growth and N concentration (and form) of lettuce shoots was quantified in plants grown until commercial maturity under different N regimes. A lettuce variety with an inherently high NO3–-N concentration was chosen for this purpose (Escobar-Gutiérrez et al., 2002). The effect of plant age on the responses of plants to limiting N was determined by imposing treatments that caused the shoot N concentration to differ at different stages of plant development. The growth, dry matter content, and N concentration and form of lettuce shoots was simulated using a model (‘Nicolet’) derived previously under different conditions (Seginer et al., 1998, 1999; Seginer, 2003).
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Materials and methods |
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Environmental conditions
The experiment was carried out from 25 August until 7 November 2000 in a glasshouse compartment at Wellesbourne, UK (latitude 52° 12' 18" N, longitude 1° 36' 00" W; 48.8 m above sea level). The glasshouse was set to maintain temperatures of 25 °C by day and 15 °C at night using automatic vents and supplementary heating. Natural light was supplemented using 400 W Na-vapour lamps. Automatic shades prevented plant wilting during early growth. Ventilation ensured that ambient CO2 concentrations approximated 370 µmol mol–1. Light levels (PAR in W m–2), calculated from solar radiation measured with 1 m solarimeters (Lancashire, 1981), and temperature (°C), were recorded at the four corners of the glasshouse compartment every 5 min during the experiment. Cumulative daily light and temperature levels were estimated from 18 d after sowing (DAS), the day before the first harvest.
Plant material
Lettuce plants (Lactuca sativa var. capitata L. cv. Kennedy), supplied as pelleted seed (Elsoms Seeds Ltd, Spalding, Lincs., UK), were sown in rockwool blocks (3.5x3.5x4 cm; Grodan, Hedehusene, Denmark) and watered with tap water in plastic trays. After germination, the seedlings were watered with a full-strength nutrient solution (Table 1). At 14 DAS the plants were transplanted in their individual rockwool blocks to the NFT system.
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Hydroponic system (a nutrient-film technique; NFT)
The NFT system comprised 12 individual gullies (5.15 m length x 0.11 m width x 0.05 m depth) constructed from flat-bottomed PVC guttering. The gullies were spaced 0.26 m apart (centre-to-centre) in two groups of six within the same glasshouse compartment. Seventy-two holes (diameter 4.5 cm), each of a sufficient size to contain a single rockwool block, were cut at equal distances (every 6 cm) along 4.32 m strips of PVC. One of these strips was secured to the top of each gully and the remaining 0.83 m of guttering was covered with a separate strip of PVC containing no holes. A single rockwool block was placed in each hole so that the base rested directly on the bottom of the gully. Each gully was connected to two storage tanks that each contained 200 l of nutrient solution. Taps were used to control which tank supplied which gully. This allowed for different N treatments to be imposed during the experiment. In all, three different N treatments were imposed: (i) nutrient solution supplied continually (control, T1), (ii) N withdrawn 35 DAS (T2) and (iii) N withdrawn 54 DAS (T3). In the solution lacking N, NH4NO3 and Ca(NO3)2 were replaced by CaSO4 (Table 1). Solutions were changed at least weekly. The solutions were monitored for nutrient depletion every three days, using a continuous flow colorimetric method on a flow-injection analyser (FIASTAR 5012, FOSS Tecator, Sweden) to analyse for NO3–-N, and inductively-coupled plasma emission spectrophotometry (JY24, Jobin-Yvon ISA, France) to analyse for P, K, Ca, Mg, and Na. The nutrient solutions were pumped from the storage tanks to the top-end of the gullies. Subsequently, the nutrient solutions flowed along the bottom of the gullies under the influence of gravity (the gradient was <2°) and drained back into the tanks. The flow rates were controlled using taps, to ensure that the nutrient solutions flowed in a thin film (c. 2 mm in depth) along the bottom of each gully. During the experiment, individual plants were sampled, and the resulting gaps in the PVC strips were immediately covered to maintain humidity and to minimize algal growth within the gullies.
Experimental design
The experiment was designed so that the 12 gullies (each running along a north–south axis) were arranged into four units (along the east–west axis). Thus, each unit contained three gullies, one for each of the three treatments, randomly allocated within each unit. Four sections were imposed along each gully; each section contained 18 plants. At each sampling date, one plant was taken from each section of each gully and the four plants from each gully were bulked for analyses. Overall, therefore, the experiment was designed so that positional effects within the glasshouse were minimized. Analyses of variance were performed to assess the effects of treatment and of sampling date within treatment assuming a split-plot design: treatments applied to main plots whilst sampling date applied to subplots. All statistical analyses were performed using GenStat (Fifth Edition, Release 4.2, VSN International, Oxford, UK).
Plant measurements
Plants were sampled at 16 different times between 19 and 74 DAS, when the crop was visually judged to be at commercial maturity. Shoot fresh and dry weights, shoot NO3–-N concentration, shoot total-N concentration and shoot total-C concentration on a percentage dry tissue basis were measured. Shoot dry weights were used to estimate the absolute growth rates (AGR) and the relative growth rates (RGR) of plants, using the FITSCHNUTE procedure in GenStat (Burns et al., 1997). Shoot growth was expressed as a function of accumulated light and temperature (cumulative effective day-degree units; EDD), assuming a dimensionless light efficiency factor of 0.1 and a base temperature of 0 °C (Scaife et al., 1987). Nitrate-N concentration was quantified using a continuous flow colormetric method on a flow-injection analyser (FIASTAR 5012, FOSS Tecator, Sweden) as described previously (Broadley et al., 2001). Total-N and total-C concentrations were quantified directly on 0.5–1 g of dried and milled plant material using a C:N analyser (CN2000, LECO, Stockport, UK). Organic-N concentration was assumed to represent the difference between total-N and NO3–-N concentration. For the first three harvests, plant material was bulked across three gullies to obtain sufficient plant material for mineral analyses.
The ‘Nicolet’ model
A model, derived previously under different conditions (Seginer et al., 1998, 1999; Seginer, 2003), was developed to simulate the growth, dry matter content and N concentration and form during shoot growth. The model is described schematically in Fig. 1.
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Briefly, the model is composed of three compartments, ‘structure’, ‘vacuole’ and ‘excess-carbon’ (excess-C). Within the ‘vacuole’, the soluble organic and mineral compounds complement each other to contribute to a constant total osmotic pressure. Within the ‘structure’ and ‘excess-C’ compartments, the C and organic-N compounds are considered to be osmotically neutral. The structural-N-to-C ratio and the water-to-structural-C ratio are assumed to be constant. The fluxes are controlled (1) by the environmental conditions (photosynthesis is controlled by light and CO2, structural growth by temperature, and N uptake by nutrient concentration), (2) by the ground cover (size) of the crop, and (3) by attenuation functions, which reflect the inhibition of certain processes. The photosynthesis and N uptake are modelled as Michaelis–Menten functions, and respiration and growth are formulated as exponential functions of temperature (Q10=2). The effective ground cover approaches 1 asymptotically and all fluxes are directly proportional to it. The attenuation functions control flows in times of stress, protecting the vacuole from C over-filling and over-draining and regulating the storage and recovery flows of the excess-C compartment. More details and justification of the formulation and assumptions of the model are published elsewhere (Seginer, 2003).
The model has been designed to simulate two distinct N-stress levels. (1) ‘Mild’ stress, where the excess-C compartment is essentially empty. The composition of the vacuole fluctuates between carbohydrate ‘saturation’ and mineral ‘saturation’, depending on the C source–sink balance. The accompanying changes in water content and organic-N concentration are minimal. (2) ‘Severe’ stress, where growth (leaf expansion) is severely limited, either, as here, by N availability, or for other reasons. The limited growth creates an excess of carbohydrates, which saturate the vacuole, displacing the mineral compounds, including NO3–-N. When the vacuole is C-saturated while the photosynthetic machinery continues to produce, albeit at a reduced rate, the excess carbohydrates accumulate in the excess-C compartment. This increases the (non-structural) dry matter content without the ‘normal’ accompanying increase in water and organic-N, and results in a high dry matter, and a low organic-N, content.
The ‘Nicolet’ model has 19 parameters, but five parameter adjustments dominated the fitting process. These parameters were (1) the photosynthetic efficiency, which controls the dry matter accumulation rate, (2) the growth-to-respiration ratio, which controls the carbon source-to-sink balance, (3) the fraction of excess C partitioned to the excess-C compartment, which controls the ‘excess’-to-‘normal’ C ratio, (4) the water-to-structure ratio, which controls the dry matter content, and (5) the structural N-to-C ratio, which controls the organic-N content. The initial values of the parameters were taken from previous experiments (Seginer et al., 1998, 1999; Seginer, 2003; R Linker and I Seginer, unpublished observations) and were improved by inspecting simulations of the new data. Since destructive sampling thinned the crop stand, the resulting delay in canopy closure, compared to normal agricultural situations, was accounted for.
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Results |
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Shoot relative growth rates and responses to nitrogen limitation
The cumulative temperature increase was approximately linear whilst the rate of cumulative light interception declined during the experiment (Fig. 2). Shoot fresh and dry weights increased as a function of EDD in all treatments, although increases were considerably slower in plants whose N supply was removed at 439 EDD (35 DAS) and 869 EDD (54 DAS) (Fig. 3a). Richards’ and Gompertz growth functions were selected automatically for the three treatments (Table 2). These fits accounted for almost all of the variation in shoot growth in all treatments (r2 >0.985, df=1, 15), and fitted shoot dry weights are presented in Fig. 3b. Shoot AGR and RGR as a function of EDD differed between treatments (Fig. 4). The responses induced by the withdrawal of N included an increase in the dry weight:fresh weight ratio and a decrease in the C concentration of the shoots (Fig. 5). In T2 shoots these changes were more marked than in T3.
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Shoot nitrogen forms and concentration
In control shoots, there was a gradual decline in organic-N and NO3–-N until the plants had grown for 800 EDD (Fig. 6a). After this period, the NO3–-N concentration of control shoots increased rapidly and the organic-N increased slightly. In T2 shoots, a rapid and almost complete loss of shoot NO3–-N followed the removal of N supply (Fig. 6b). This was parallelled by a decline in organic-N to an asymptotic minimum concentration of c. 1% dry wt, although the organic-N decline was less rapid than the NO3–-N. In T3 shoots, the NO3–-N levels had increased slightly (in parallel with T1 shoots) when the N-limited treatment was imposed (Fig. 6c). However, there was minimal NO3–-N in the shoots at this time, and the NO3–-N continued to decline after this point. The organic-N declined in T3 shoots following the removal of N, but not to the asymptotic level of 1% observed in T2 shoots.
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Quantifying relationships between shoot nitrogen concentration and relative growth rate
Relative growth rate declined in all treatments over the course of the experiment (Fig. 7). As a function of total-N concentration, RGR increased in a sub-linear manner in T2 and T3 shoots. To compare treatments imposed at different ages, RGR was calculated as a proportion of the control RGR at each harvest (RGR/RGRcontrol). The relationship between total-N concentration and proportional RGR were similar in T2 and T3 shoots, although in T3 shoots, the N concentration and proportional RGR did not decline to the same level as T2 plants (Fig. 8a). This effect was dominated by organic-N concentration (Fig. 8b) and proportional RGR was largely independent of NO3–-N concentration (Fig. 8c). Control data are presented in the same figure for comparison (Fig. 8a–c). A further age-related effect was the increase in organic-N in control shoots during the latter stages of growth (Fig. 6). The effects of N concentration (dominated by organic-N components) on RGR, expressed as proportions of the N concentration and RGR of the control data, are similar for T2 and T3 shoots (Fig. 9). Thus, proportionally, the effects of total-N and organic-N concentration on plant RGR were independent of plant age.
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Model simulations
Despite the extreme differences in the growth responses between the treatments, particularly between T1 and T2, the ‘Nicolet’ model fitted the experimental data well on visual inspection (Fig. 10). The following observations could be made. (1) In control (T1) shoots, exponential growth was limited to the first 2 weeks following the first harvest, followed by a reduction in RGR. This is seen most clearly in the shoot fresh weight trajectories, which are presented on a logarithmic scale. There is, however, no clear transition to a linear stage, as can best be seen in the dry weight data, which are presented on a linear scale. (2) The initial decrease and later increase of NO3–-N concentration in the control (T1) plant shoots was simulated well. (3) In T2, shoot fresh weight did not increase further after N was withdrawn, whilst dry shoot weight increased, albeit more slowly than control (T1) shoots. The large subsequent increases in dry matter content were simulated well. (4) The model simulated the almost-complete loss of NO3–-N shortly after N-withdrawal (T2, T3). The scatter of measured points in the first few days following transplanting in T2 and T3 may correspond to the large daily fluctuations in NO3–-N concentration which are predicted by the model. (5) The model could only predict the general trends in the organic-N concentration of the shoots.
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Discussion |
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Quantifying shoot growth and shoot nitrogen concentration and form
The effectiveness of an objective curve-fitting procedure, used to estimate RGR of shoots, was consistent with previous studies to estimate RGR of whole-plants (Burns et al., 1997; Broadley et al., 2000; Walker et al., 2001). Removing N supply to lettuce considerably reduced shoot growth. Reductions in the shoot growth of N-limited plants correlate with decreases in leaf area, a reallocation of C from shoots to roots and a reduction in net C assimilation (Broadley et al., 2000; Le Bot et al., 2001). In this study, there was an increase in the dry weight:fresh weight ratio and a decrease in the C concentration of the shoots under N-limitation and it is thus consistent with other studies.
There was a gradual decline in the shoot organic-N and NO3–-N concentration during the first two-thirds of the growth of control plants. This may reflect the volume of non-photosynthetic materials, containing little N, increasing faster than the area of photosynthetically-active surfaces (Greenwood et al., 1990). However, in late-growth of control plants, there were large increases in NO3–-N concentration and a small increase in organic-N concentration. Accumulation of NO3–-N in shoot tissues can occur when leaves are shaded, photosynthesis becomes light-limited and NO3–-N reduction declines. Thus, increases in NO3–-N levels in control shoots may have been due to self-shading as ‘hearting’ commenced (where the inner leaves behave essentially as a storage organ), and/or the overall decline in incident light during this phase.
The amount of N in the shoots remained constant following N-withdrawal in T2 and T3. Thus, no significant quantities of N were reallocated to roots. There were sub-linear relationships between RGR and total-N concentration in T2 and T3 shoots, but not in control shoots. Therefore, these results from lettuce shoots grown to commercial maturity are consistent with studies on young lettuce whole-plants (Burns, 1994a, b; Burns et al., 1997; Broadley et al., 2000; Walker et al., 2001). However, the absolute decline in RGR with declining shoot N concentration in T2 and T3 differed. In T2 plants, the RGR declined gradually with declining shoot N concentration until the total-N of the shoot was c. 2%. Subsequently, RGR declined rapidly until growth ceased at c. 1% N. In T3 plants, the decline in RGR with decreasing shoot N concentration commenced from a lower absolute RGR and shoot N concentration did not decline to a level which halted growth. However, expressing RGR and N concentration data as proportions of control values allows T2 and T3 shoots to be compared directly by removing age-related effects. On this proportional basis, the effects of total-N and organic-N on RGR were independent of plant age.
Modelling
The ‘Nicolet’ model predicted well most of the experimental data under both normal growth conditions and under extreme N stress. Thus, since the model was developed under independent experimental conditions it can be used to interpret the experimental results and it can also highlight areas that require further investigation. The model implies that the initial decrease and later increase of NO3–-N concentration in the control (T1), arises from changes in the C source–sink balance under ‘mild’ stress conditions, in particular due to a reduction in light intensity towards the end of the experiment. Whether a drop in incident light or self-shading or both factors, contributed to the increase in shoot NO3–-N concentration could be tested using widely-spaced plants grown under controlled environmental conditions.
The immediate cessation of fresh shoot growth upon N interruption, and the slow continued increase in dry shoot growth in T2, was predicted well by the model. The model implies that this response was due to a cessation in leaf expansion, whilst excess C continued to accumulate in leaves and/or other organs.
The model could only predict general trends in organic-N concentration. A lack of precision was observed because the water and organic-N content of the lettuce shoots were not proportional, as assumed by the model. If the environmental conditions are constant, the model predicts that the composition of the crop equilibrates with these conditions and does not change. Therefore, aside from predicting a decreasing RGR during canopy closure, the model cannot account for other developmental effects. In light of this evidence, it would be appropriate to test and adjust the model on data from different lettuce cultivars in different environmental conditions and over their full period of growth and development.
Perspective
This study has described a sub-linear relationship between RGR and N concentration in lettuce, and it has determined that the proportional effects of this relationship are independent of plant age. Thus, periods of N deprivation at any early stage of crop growth will affect yields, although this effect is likely to be smaller as crops approach maturity, or if N is resupplied. A common practice to reduce NO3–-N concentration of hydroponically-grown lettuce is to withhold N a few days before harvest. These results confirm that NO3–-N levels could be reduced with minimal effects on fresh weight, if the crops are sufficiently large.
Overall, the ‘Nicolet’ model simulations agree with observations under the experimental conditions reported here. The model can therefore yield physiological insights even though specific parameter adjustments are required because the model is not fully robust (Seginer, 2003). The sensitivity of the model to genetic differences between cultivars of plants, to plant developmental effects, and to differences in experimental and measurement techniques should be studied further so that model refinements can be made. However, the success of the simulations presented in this study illustrate how nutritional decision support for fertilizer advice could be provided if certain input values are known.
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Acknowledgements |
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The HRI authors acknowledge the support of the Department for the Environment, Food and Rural Affairs (Defra), UK, who funded this work. The development of the ‘Nicolet’ model by IS (segineri{at}techunix.technion.ac.il) was sponsored by an EU project FAIR6-CT98-4362. We thank Andrew Mead for advice on experimental design.
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