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Organ-specific approaches describing crop growth of winter oilseed rape under optimal and N-limited conditions
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Research paper
Organ-specific approaches describing crop growth of winter oilseed rape under optimal and N-limited conditions Wiebke Weymann ∗ , Klaus Sieling, Henning Kage Institute of Crop Science and Plant Breeding, Christian-Albrechts-University, Hermann-Rodewald-Str. 9, 24118 Kiel, Germany
a r t i c l e
i n f o
Article history: Received 18 July 2016 Received in revised form 27 September 2016 Accepted 10 October 2016 Available online xxx Keywords: Winter oilseed rape Crop N response Dry matter partitioning Allometric relations N dilution curves
a b s t r a c t Carbon and nitrogen partitioning of winter oilseed rape differs under optimal and nitrogen (N) limited conditions. The quantitative description of these processes and their response to N deficiency is a prerequisite to develop process-oriented crop growth models capable to predict responses to a limited N supply. Dry matter (DM) partitioning, N dynamics and expansion of leaf, stem and pod area, as well as specific leaf area of oilseed rape were recorded during six seasons 2003/04–2005/06, and 2009/10, 2010/11 and 2012/13 within two series of field trials with varying N treatments at the experimental site Hohenschulen, northern Germany. DM partitioning is analysed using allometric relationships between leaf and stem DM as well as between stem and generative DM. The allometric relations between leaf and stem DM varied before and after beginning of stem elongation due to increasing DM allocation to stems during stem elongation. Allometric relations between DM fractions, however, were not affected by N treatment. N dilution curves, describing relations between N concentration and DM, differed between plant fractions, growth stages and N fertilization levels and indicated different response patterns under N limited conditions. This result is supported by relations between N amount and DM of leaves and stems, suggesting a sink priority for leaves under N deficiency. The approaches, describing green area expansion, dry matter partitioning and N distribution, can be used to improve dynamic crop growth models for oilseed rape. © 2016 Published by Elsevier B.V.
1. Introduction Winter oilseed rape is a major crop in central and northern Europe, especially in Germany, France and UK. Despite management optimization and breeding progress during the last decades, oilseed rape cultivation is characterized by highly variable seed yield (Rondanini et al., 2012), low nitrogen use efficiency (NUE) and low nitrogen harvest index compared to cereals (Schjoerring et al., 1995; Hocking et al., 1997; Dreccer et al., 2000). The increase of NUE is a major goal in agronomic research and plant breeding. NUE is divided into two components: N-uptake efficiency and N-utilization efficiency (Moll et al., 1982). For oilseed rape, it is assumed that N-uptake efficiency is comparably high because of an early developed deep and wide root system (Kamh et al., 2005). In contrast, N-utilization efficiency of oilseed rape crops tends to
∗ Corresponding author. E-mail addresses: weymann@pflanzenbau.uni-kiel.de, [email protected] (W. Weymann).
be low because of not simultaneous maximal mineralization rate and growth rate, as well as incomplete translocation of N from vegetative to generative plant parts (Lickfett, 1993; Wiesler et al., 2001a,b). In general, NUE is determined by the capacity to capture soil N, the capacity to use N for crop growth and the capacity to allocate N from vegetative to generative plant parts (Gastal et al., 2015). Detailed investigations on physiological processes of green area expansion, dry matter (DM) partitioning and N distribution under varying fertilization strategies are required in order to analyse options and limitations of improving NUE and N management for maximal crop production. N fertilization in autumn sown oilseed rape crops is mostly split into two applications in spring. First, N is applied at regrowth in spring and secondly at the beginning of stem elongation. Insufficient N supply by fertilization and mineralization can lead to temporal N deficiency. In general, N deficiency influences crop production by reduction of growth rates and by affecting light use efficiency (Bélanger et al., 1992) but specific crop responses differ according to growth stage and degree of N deficit.
http://dx.doi.org/10.1016/j.eja.2016.10.005 1161-0301/© 2016 Published by Elsevier B.V.
Please cite this article in press as: Weymann, W., et al., Organ-specific approaches describing crop growth of winter oilseed rape under optimal and N-limited conditions. Eur. J. Agron. (2016), http://dx.doi.org/10.1016/j.eja.2016.10.005
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Previous studies showed that N deficiency during autumn growth results in reduced dry matter accumulation before winter but these growth deficiencies are mostly compensated under sufficient water and N availability after start of regrowth in spring. Therefore, final yield is not affected by N deficiency during autumn growth in this case (Colnenne et al., 2002), but Rathke et al. (2005) showed that seed yield of oilseed rape is significantly influenced by N fertilization in spring. Crop N demand varies with growth stage and DM accumulation of crops (Gabrielle et al., 1998; Wiesler et al., 2001a). DM accumulation depends on the quantity of absorbed radiation, determined by photosynthetic active green area, and on light use efficiency as well as stress factors, considering temperature, N and water availability and management (Monteith and Moss, 1977). DM partitioning between plant parts can be described by allometric relations. Allometric approaches rely on a constant ratio of relative growth rates, resulting in a linear relationship between the natural logarithm of DM fractions (Thornley and Johnson, 1990). The relation between DM accumulation and N concentration in single plants and crops can be described by N dilution curves (Salette and Lemaire, 1981). N dilution curves show declining N concentration with increasing DM accumulation. N dilution curves were already estimated for several species (e.g. grass, wheat, maize and canola; Greenwood et al., 1991; Justes et al., 1994; Colnenne et al., 1998; Lemaire et al., 2008). Colnenne et al. (1998) calculated critical N dilution curves for canola. The critical N concentration for a given DM value was defined as N concentration necessary to achieve maximal growth rate (Lemaire and Salette, 1984). If actual N concentration is below the critical N concentration for a given DM value, crop growth is limited by N deficiency. Studies, concerning N dilution, only estimated curves for vegetative growth phases and total aboveground biomass. There is a lack of knowledge considering N dilution during generative growth phase and N dynamics within single plant organs. Studies of organ-specific N dynamics may offer the possibility to investigate crop responses of oilseed rape to N deficiency in more detail. The aims of the current study are (i) to investigate relationships between growth rates of plant parts, (ii) to investigate N dynamics within single plant parts and (iii) to estimate the effects of N management on these processes. Therefore, organ-specific responses to N deficiency are studied. Finally, the investigations may contribute to approaches for improving N-management and NUE by means of simulation studies with dynamic crop growth models.
2. Materials and methods 2.1. Experimental sites and designs Data for analysis were taken from two field trials at the experimental farm Hohenschulen (54.3◦ N, 10.0◦ E), located in northern Germany. Hohenschulen is characterized by its humid climate, influenced by marine conditions. Long-term total rainfall average is 757 mm annually and temperature long-term average is 8.7 ◦ C (1981–2010). Main soil type at Hohenschulen is sandy loam with a pH value of 6.4 and an effective rooting depth of 100 cm. Water holding capacity in the effective rooting depth is about 184 mm. Experiment 1 (Exp. 1) was performed between 2003/04 and 2005/06 with four N treatments (0 kg N ha−1 , 80 kg N ha−1 , 160 kg N ha−1 , 240 kg N ha−1 ), which were applied as ammonium/urea solution in two applications at the beginning of regrowth in spring and the beginning of stem elongation. The experiment was performed with four replicates. The variety Talent was used and winter wheat was the preceding crop. Sowing dates
and seeding densities were chosen according to the best possible management practice. Experiment 2 (Exp. 2), performed during seasons 2009/10, 2010/11 and 2012/13, had 80 management treatments, including four sowing dates (early, normal, late, very late), four autumn N application levels (0 kg N ha−1 , 30 kg N ha−1 , 60 kg N ha−1 , 90 kg N ha−1 ) and five N treatments in spring (0 kg N ha−1 , 80 kg N ha−1 , 160 kg N ha−1 , 240 kg N ha−1 , 280 kg N ha−1 ). The experiment was performed with four replicates. The variety Visby was used with winter barley as preceding crop. 2.2. Measurements In Exp. 1, shoots from an area of 0.88 m2 were harvested several times during total vegetation period for analysis of green area index (GAI), total DM and total N amount. GAI was measured by LAI 2000 (LI-COR inc., USA). Shoots were fractionated into leaves, stems and generative organs. After drying and weighting, fractionated samples were ground for near infrared spectroscopy analysis of the N concentration (NIRSystems 5000 scanning monochromator, FOSS GmbH, Rellingen, Germany). Detailed information is given by Müller (2009). In Exp. 2, measurements were made about every second week from sowing until start of regrowth in spring. DM and N concentration of total shoot, leaves, stems and roots were observed. Root biomass was dug out and mainly represented tap root biomass. In addition, green leaf and stem area were determined by destructive (LI-3100C, LI-COR inc., USA) and non-destructive measurements (LAI 2000, LI-COR inc., USA). 2.3. Statistical analysis Influence of N treatment on relationships between DM fractions and between accumulated N and DM of single plant organs was tested by statistical analysis. The statistical tests were performed using R (version 2.15.2, R Core Team, 2013) with a level of significance of 5%. For linear regressions, representing the allometric relations between DM fraction and relations between GAI and N uptake and GAI and specific leaf area (SLA), the procedure lm was used. Differences in intercept and slope parameters between N treatment levels were analysed with an analysis of variance. Differences of N dilution curves between crops with different N treatment levels were tested by the procedure of Zar (2010). This method is able to test if parameter values estimated for each N treatment level by nls differ significantly. We estimated common intercept values for all N treatment levels but different slope parameters for each N treatment level, separately. These slope parameters were compared following the procedure of Zar (2010). In one case, no N dilution effect was observed. We assumed a constant mean N concentration, which may vary with N treatment. The differences between these mean N concentrations were tested by pairwise t-test. Due to multiple tests, level of significance for each test was adjusted according to the method of Holm (1979). 3. Results 3.1. Expansion of photosynthetic active green area GAI of winter oilseed rape crops varied during crop growth and between N treatment levels. GAI increased after the beginning of generative growth (Fig. 1). Unfertilized plots had a maximum GAI of about 3.5 at the end of flowering. In contrast, unstressed crops achieved a mean maximum GAI of up to 7.
Please cite this article in press as: Weymann, W., et al., Organ-specific approaches describing crop growth of winter oilseed rape under optimal and N-limited conditions. Eur. J. Agron. (2016), http://dx.doi.org/10.1016/j.eja.2016.10.005
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Fig. 1. Mean value of Green Area Index during different growth stages under consideration of N application during spring growth (Exp. 1, data from experimental year 2005/06).
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Fig. 3. Specific leaf area during different growth stages under consideration of N application during spring growth (Exp. 1, data from experimental year 2005/06).
Table 1 Functional parameters and statistical analysis of the linear relation a) between GAI and N uptake [kg N ha−1 ] (N uptake = a + GAI*b) and b) between GAI and SLA [cm2 g−1 ] (SLA = a + GAI*b). Characters designate siginifance of N application in spring on parameter values (Exp. 1). a) N application [kg ha−1 ] 0 80 160 240
Parameter a ns
Parameter b ns
0 0ns 0ns 0ns
R2
3.6 3.8ns 3.8ns 3.7ns
0.75 0.81 0.85 0.78
Parameter b
R2
b) N application [kg ha−1 ] 0 80 160 240
Parameter a ns
110.5 121.7ns 105.6ns 104.5ns
ns
19.5 20.3ns 24.1ns 27.1ns
0.69 0.51 0.74 0.82
Fig. 4. Relation between Green Area Index and specific leaf area from end of stem elongation until end of flowering under consideration of different levels of N application in spring (Exp. 1).
pattern to N treatment was observed for the linear relationships between N uptake and leaf area index (LAI) and between leaf N amount and LAI (data not shown). Besides GAI, also SLA varied during crop growth and between N treatments. After beginning of inflorescence emergence, unfertilized plots had a substantially lower SLA indicating thicker leaves than fertilized plots. Maximal SLA at the end of flowering was about 200 cm2 g−1 in unfertilized plots, while unstressed crops reached maximal SLA values of 300–400 cm2 g−1 (Fig. 3). From the end of stem elongation until end of flowering, SLA and GAI were linearly correlated (Fig. 4). Relations tend to vary between N treatment levels in spring. Unstressed crops had higher SLA values at a given GAI compared to unfertilized crops but differences were not significant (Table 1b). 3.2. Dry matter partitioning Fig. 2. Relation between total N uptake and Green Area Index under consideration of N application during spring growth (Exp. 1).
GAI was closely correlated with total N uptake (Table 1a, Fig. 2). Per 36 kg N ha−1 absorbed, one unit of GAI was produced. N treatment had no significant effect on this relation. The same response
DM partitioning of winter oilseed rape crops was described by allometric relationships. First, leaf and stem growth were closely related. This relation varied according to the growth stage of the crop (Table 2). From emergence until stem elongation, relative growth rates of stems and leaves correlated significantly (R2 = 0.91). In Fig. 5a, the allo-
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Fig. 5. Allometric relation between leaf and stem dry matter a) before stem elongation under consideration of N application in autumn (Exp. 1 + 2) and b) between stem elongation and onset of flowering under consideration of N application during spring growth (Exp. 1).
Table 2 Functional parameters and statistical analysis of the linear relation between leaf and stem dry matter (ln(stem dry matter) = a + ln(leaf dry matter)*b) before stem elongation (Exp. 1 + 2) and between stem elongation and onset of flowering (Exp. 1). Growth stage
Parameter a
Parameter b
R2
10–30 30–60
−1.04 −0.56
1.13 1.06
0.91 0.81
Table 3 Statistical analysis of the effect of N application on N dilution curves, describing the relationship between N concentration (Nc) and dry matter (DM) for different plant organs and growth stages (leaves: Nc = a + DM*b; stems, pods, tap roots: Nc = a + log(DM)b, R2 : coefficient of determination). Characters designate siginificance of N effects on parameter values. Plant organ
Growth stage
N application [kg ha−1 ]
Parameter a
Parameter b
R2
Leaves
10–30
0/-/30/-/60/-/90/-/0/0/0 0/40/40 0/80/80 0/120/120 0/-/30/-/60/-/90/-/0/0/0 0/40/40 0/80/80 0/120/120 0/0/0 0/40/40 0/80/80 0/120/120 0/-/30/-/60/-/90/-/-
5.93
−0.02a −0.02a −0.01b −0.01b –
0.30 0.60 0.62 0.58 –
−0.57a −0.47a,b −0.40a,b −0.34b −1.22a −1.07b −1.04b −1.03b −0.91a −0.76b −0.72b −0.70b −0.13ns −0.11ns −0.09ns −0.04ns
0.52 0.54 0.55 0.50 0.80 0.90 0.90 0.88 0.88 0.90 0.89 0.89 0.05 0.23 0.24 0.02
30–60
Stems
10–30
30–70
Fig. 6. Allometric relation between stem and generative dry matter until end of flowering under consideration of N application during spring growth (Exp. 1).
metric relationship is shown for different N treatments during autumn growth. From stem elongation until onset of flowering, the relationship between leaf and stem growth slightly changed (R2 = 0.81, Fig. 5b). Proportion of stem growth of total shoot growth was enhanced, compared to the relation before start of stem elongation. Autumn and spring N treatments had no effect on the relationship between leaf and stem growth, neither before stem elongation nor afterwards. Besides leaf and stem growth, also stem and generative growth were correlated. Both DM fractions proportionally increased from
Pods
51–90
Tap roots
10–30
3.67a 4.97b 5.39c 5.49d 4.64
8.10
7.45
3.21
inflorescence emergence until end of flowering (R2 = 0.83, Fig. 6). Spring N did not affect this allometric relationship. 3.3. Organ-specific nitrogen dynamics N concentration of stems, pods, roots and leaves decreased with increasing DM accumulation. In order to quantify this decrease, “N dilution curves” (Salette and Lemaire, 1981) could be estimated. N dilution curves differed between plant organs, growth stages and N treatment levels (Table 3). The relation between stem N concentration and stem DM was described by logarithmic functions, which differed between growth stages and levels of N application (Fig. 7a, b). From emergence until
Please cite this article in press as: Weymann, W., et al., Organ-specific approaches describing crop growth of winter oilseed rape under optimal and N-limited conditions. Eur. J. Agron. (2016), http://dx.doi.org/10.1016/j.eja.2016.10.005
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Fig. 7. N dilution curves of stems a) before stem elongation under consideration of N application during autumn growth (Exp. 1 + 2) and b) after stem elongation under consideration of spring N application (Exp. 1).
stem elongation, N concentration varied between 1.5% and 6%. N application during autumn growth had an effect on the slopes of the functions, while a common intercept was estimated for all N treatment rates. The slope of the function representing crops with no N application was significantly steeper than the one representing crops with autumn N application of 90 kg N ha−1 . After beginning of stem elongation, slope of the N dilution curve representing crops with no N application significantly differed to slopes of functions belonging to crops with any N application in spring (Table 3). Similar to N dilution curves of stems, the relationship between N concentration and DM of the generative fraction can be described by logarithmic functions (Fig. 8). N concentration varied between 4% and 7% at inflorescence emergence and decreased to 1–4% after flowering. Thereby, unfertilized plots tended to have lower N concentrations, compared to fertilized plots. N fertilization in spring significantly affected the slopes of logarithmic functions, estimated for each N treatment level (Table 3). The function representing crops with no N application had a significantly steeper slope compared to functions representing crops with any N application in spring. In addition to the previously described above-ground plant parts, root N concentration decreased with increasing root DM until stem elongation. This relation can be described by logarithmic N dilution curves with slopes, estimated for each N treatment level separately and a common intercept (Fig. 9). N application during autumn did not significantly affect the slopes of these functions (Table 3), although crops with no or low N application tended to have lower root N concentration from emergence until stem elongation than unstressed crops. Relations between N concentration and DM of leaves differed compared to the ones of stems, pods and roots. Before beginning of stem elongation, the relation between leaf N concentration and leaf DM followed a linear regression (Fig. 10a, Table 3). Leaf N concentration varied between 3% and 7% and crops with low N application tended to have lower N concentrations than unstressed crops. Estimated with a common intercept for all treatment levels, N application during autumn growth affected the slopes of the dilution curves. Crops with autumn N application of 0 kg N ha−1 or 30 kg N ha−1 were represented by functions with significant steeper slopes than crops with higher autumn N application. From stem elongation until onset of flowering, leaf N concentration did not change with leaf DM. No N dilution effect was observed
but N application rate significantly affected mean leaf N concentration calculated for each N treatment level (Fig. 10b, Table 3). 3.4. Organ-specific responses of vegetative biomass to severe N deficiency The previously described N dilution curves have different function types and parameter values. This indicates organ-specific response patterns to N deficiency. To analyse crop response to N deficiency in more detail, we studied the relation between N amount and DM of vegetative biomass under N-unlimited conditions and under severe N deficiency. To define severe N deficiency, we looked for a lower bound of N concentrations by analysing the data for unfertilized treatment. The linear regression between N amount and DM of leaves varied before and after stem elongation but the response to Nlimitation was similar. N amount of leaves was reduced by 30–35% at a given DM value under severe N deficiency (Fig. 11a). In contrast to leaves, N amount of stems under severe N deficiency during autumn growth was reduced by about 50% at a given DM value compared to unstressed crops (Fig. 11b). After beginning of stem elongation during spring growth, relative reduction of N amount under severe N deficiency varied with DM growth. Relative reduction of stem N amount at a given DM value increased from 30% up to 66% with increasing stem DM. Before and after stem elongation, functional parameters describing the relation between N amount and DM of leaves and stems differed significantly between N levels (Table 4). 4. Discussion The effect of N supply on crop growth is based on several physiological processes, as green area expansion, DM partitioning and N distribution. This paper aims to analyse some of these effects for winter oilseed rape using data from field experiments with different N supply rates and sequential destructive samplings. Single measurements suggested GAI values up to 10. These high values might have been caused by boundary effects. Data showed that GAI and SLA differed according to N availability, as influenced by N application in spring. Unstressed crops had substantially higher SLA than those with low or no N supply. Higher SLA during spring growth for plots with high N application
Please cite this article in press as: Weymann, W., et al., Organ-specific approaches describing crop growth of winter oilseed rape under optimal and N-limited conditions. Eur. J. Agron. (2016), http://dx.doi.org/10.1016/j.eja.2016.10.005
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Fig. 8. N dilution curve of pods from the beginning of generative growth until end of pod growth under consideration of N application in spring (Exp. 1).
Fig. 9. N dilution curve of tap root under consideration of N application during autumn growth (Exp. 2).
Table 4 Functional parameters and statistical analysis of the relation between N amount (N) and dry matter (DM) of leaves and stems during different growth stages under optimal (N-unlimited) and critical (severe N deficiency) N supply. Significant differences between parameter were tested for each “plant organ × growth stage − combination” separately (leaves: N = DM*b; stems: N = (a + b*log(DM))*DM). Characters designate siginificance of N effects on parameter values. Plant organ
Growth stage
N supply
Parameter a
Parameter b
Leaves
10–30
critical optimal critical optimal critical optimal critical optimal
– – – – 0.06ns 0.06ns 0.06ns 0.06ns
0.034a 0.049b 0.033a 0.052b −0.026a −0.014b −0.023a −0.013b
30–60 Stems
10–30 30–60
could be caused by self-shading. Due to higher GAI, self-shading is more pronounced under optimal conditions, compared to N limited conditions. Self-shading induces translocation of assimilates and N compounds from vegetative to generative plant parts (Malagoli et al., 2005) and thereby reduces DM. For a constant leaf area this
leads to an increase of SLA. This response pattern was also observed for wheat (Ratjen and Kage, 2013) and barley (Sieling et al., 2015). In addition, differences in GAI and SLA may be caused by the limited leaf area expansion under N stress (Gastal and Lemaire, 1988). This leads to lower LAI at a given leaf DM and therefore to lower SLA values observed for unfertilized crops. Although GAI varied between N treatments, N uptake per unit GAI or LAI was not affected by N application. These results are in accordance with Lemaire et al. (2008), who observed no change of N uptake per unit LAI for canola crops. In contrast, N uptake per unit LAI was substantially lower under N limitation for maize crops. According to Lemaire et al. (2008), constant N uptake per unit GAI or LAI indicates that resource capture is reduced under N limitation. They suggested that canola reduces leaf mass per unit crop mass and therefore, higher proportion of assimilates is allocated to the stems under critical N conditions. Our data did not verify these observations, since allometric relationships between leaf and stem growth were not affected by the N status of the plant, neither before stem elongation nor afterwards. In addition, also the allometric relationship between stem and generative growth did not
Please cite this article in press as: Weymann, W., et al., Organ-specific approaches describing crop growth of winter oilseed rape under optimal and N-limited conditions. Eur. J. Agron. (2016), http://dx.doi.org/10.1016/j.eja.2016.10.005
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Fig. 10. N dilution curves of leaves a) before stem elongation under consideration of N application during autumn growth (Exp. 1 + 2) and b) after stem elongation under consideration of spring N application (Exp. 1).
Fig. 11. Relationship between N amount and dry matter of a) leaves and b) stems before and after stem elongation (GS 30) under optimal (N-unlimited) and critical (severe N deficiency) N conditions (Exp. 1 + 2).
differ between N treatment levels. Summarizing, in contrast to previous suggestions based on results of Weiner (2004), who described changing allometric relationships of DM fractions in response to the environment, DM partitioning of oilseed rape did not significantly change in response to N application level. N dynamics during crop growth can be described by N dilution curves, showing the relation between N uptake and DM accumulation. This relationship was already described for several species (e.g. Greenwood et al., 1991; Justes et al., 1994; Plénet and Lemaire, 2000; Gastal and Lemaire, 2002). For oilseed rape, Colnenne et al. (1998) developed a critical N dilution curve, which represents the minimum shoot N concentration required for maximal shoot DM production from emergence until onset of flowering. Thereby a power function was used to describe decreasing N concentration in shoots with increasing shoot DM. Furthermore, N dilution curves are used to estimate N status of crops (Lemaire et al., 1989; Lemaire and Meynard, 1997). Mostly, the estimation of N status of crops indicates that crop growth stops if N concentration is zero (Gastal
et al., 2015) but this assumption neglects the part of structural N in plant tissue. We considered structural N, which is not used in growth processes, as the minimum N concentration remaining in plant tissue. Crop growth stops when N concentration is beneath minimum N concentration. Our data shows that each single plant organ of autumn sown oilseed rape has a specific N dilution curve responding specifically to N deficiency. Thereby leaf N concentration and leaf DM before stem elongation are linearly related, while leaf N concentration remains constant from stem elongation until onset of flowering. In contrast to leaves, relationships between N concentration and DM of stems, pods and roots follow declining logarithmic functions, indicating an increasing portion of structural components. Statistically significant differences between parameters of N dilution curves due to N treatment level indicate adaptation processes of the plant to N deficiency. These adaptation processes differ between plant organs. Therefore, an organ-specific analysis may be
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advantageous to describe physiological processes of N distribution and its effects on crop productivity. Decreasing leaf N concentration with increasing leaf DM before stem elongation may partly be explained by the decreasing level of irradiation in autumn during which the majority of the samplings have been taken. During this time, also SLA decreases substantially. During spring growth, however, radiation level increases. Despite self-shading induced senescence of leaves and loss of N, N concentration of leaves per unit DM does not decrease substantially, probably because N is redistributed together with carbon from older leaves to younger ones to provide maximal photosynthetic activity. In addition, the flower layer causes shading of leaves. Triboï-Blondel et al. (1988) and Merlo et al. (1995) observed a reduced nitrate reductase activity under low light conditions. Stems are negligible for photosynthesis and mainly serve as structural tissue. Therefore, N concentration of stems decreases substantially with increasing DM. These suggestions are in accordance with Colnenne et al. (1998), who explained change of allometric relation between shoot DM and accumulated N in shoots with an increase of lignified tissue, predominantly in stems. N concentration of generative organs decreases substantially with increasing DM, although N is translocated from senescing leaves to pods (Malagoli et al., 2005) and pods are predominantly responsible for photosynthesis after flowering (Gammelvind et al., 1996). This pattern can be explained by the DM distribution between pod walls and seeds. At the beginning of generative growth, pod growth is dominated by the development of photosynthetic active pod walls. Afterwards, growth of photosynthetic unproductive seeds dominates and pods start to mature (Habekotté, 1993). The redistribution of N during ripening is not represented by this dilution curve because latest measurements were taken at the end of pod growth. Besides N dynamics caused by crop growth, N dilution curves also indicate response pattern of single plant organs to N deficiency. The relation between N amount and DM of leaves and stems for N-unlimited conditions and severe N deficiency showed organspecific responses to N deficiency. Reduction of N amount at a given DM value due to N limitation reveals a more pronounced response of stems to N deficiency, compared to leaves. Therefore, oilseed rape seems to maintain high N contents in leaves to support photosynthetic activity, while N content of stems decreases under N limitation. This may reflect a buffer function of stem N under fluctuating N supply. We assume that the relationships, described in this study, are valid for several environments and under varying soil and weather conditions. The relations might differ between genotypes but detailed data is not available to include this question into the current study. Summarizing, allometric relationships and N dilution curves can be used in dynamic crop growth models to simulate DM partitioning and N distribution and to estimate organ-specific responses to N deficiency.
4.1. Implications for modelling The results of the current study suggest new approaches to describe physiological processes and responses of oilseed rape growth to temporal N deficiency during different growth phases. The allometric relations between leaf, stem and pod growth can be used to implement algorithms within dynamic crop growth models, either under optimal or under N-limited conditions. N dilution curves, estimated from unstressed crops and data gained from crops with severe N deficiency offer the opportunity to calculate the degree of N deficiency under consideration of structural N in plant tissues. In addition, organ-specific parameters of N dilution curves in dynamic crop growth models illustrate organ-
specific N dynamics during crop growth and detailed responses to N deficiency. Finally, these new approaches to describe physiological processes in dynamic crop growth models may improve simulated crop development under varying management strategies and environments. Funding This work was supported by the Union zur Förderung von Ölund Proteinpflanzen (UFOP). Acknowledgement We thank Karla Müller, Kirsten Schulz and Cordula Weise, who have provided the large amount of detailed data. References Bélanger, G., Gastal, F., Lemaire, G., 1992. Growth analysis of a tall fescue sward fertilized with different rates of nitrogen. Crop Sci. 32, 1371–1376. Colnenne, C., Meynard, J.M., Reau, R., Justes, E., Merrien, A., 1998. Determination of a critical nitrogen dilution curve for winter oilseed rape. Ann. Bot. 81, 311–317. Colnenne, C., Meynard, J.M., Roche, R., Reau, R., 2002. Effects of nitrogen deficiencies on autumnal growth of oilseed rape. Eur. J. Agron. 17, 11–28. Dreccer, M.F., Schapendonk, A.H.C.M., Slafer, G.A., Rabbinge, R., 2000. Comparative response of wheat and oilseed rape to nitrogen supply: absorption and utilisation efficiency of radiation and nitrogen during the reproductive stages determining yield. Plant Soil 220, 189–205. Gabrielle, B., Denoroy, P., Gosse, G., Justes, E., Andersen, M.N., 1998. Development and evaluation of a CERES-type model for winter oilseed rape. Field Crops Res. 57, 95–111. Gammelvind, L.H., Schjoerring, J.K., Mogensen, V.O., Jensen, C.R., Bock, J.G.H., 1996. Photosynthesis in leaves and siliques of winter oilseed rape (Brassica napus L.). Plant Soil 186, 227–236. Gastal, F., Lemaire, G., 1988. Study of a tall fescue sward grown under nitrogen deficiency conditions. In: Proceedings of the XIIth General Meeting of European Grassland Federation, Ireland, pp. 323–327. Gastal, F., Lemaire, G., 2002. N uptake and distribution in crops: an agronomical and ecophysiological perspective. J. Exp. Bot. 53, 789–799. Gastal, F., Lemaire, G., Durand, J.-L., Louarn, G., 2015. Quantifying crop responses to nitrogen and avenues to improve nitrogen-use efficiency. In: Sadras, V.O., Calderini, D. (Eds.), Crop Physiology. , 2nd edn. Elsevier, London, pp. 161–206. Greenwood, D.J., Gastal, F., Lemaire, G., Draycott, A., Millard, P., Neeteson, J.J., 1991. Growth rate and%N of field grown crops: theory and experiments. Ann. Bot. 67, 181–190. Habekotté, B., 1993. Quantitative analysis of pod formation: seed set and seed filling in winter oilseed rape (Brassica napus L.) under field conditions. Field Crops Res. 35, 21–33. Hocking, P.J., Randall, P.J., DeMarco, D., 1997. The response of dryland canola to nitrogen fertilizer: partitioning and mobilization of dry matter and nitrogen, and nitrogen effects on yield components. Field Crops Res. 54, 201–220. Holm, S., 1979. A simple sequentially rejective multiple test procedure. Scandin. J. Stat. 6, 65–70. Justes, E., Mary, B., Meynard, J.-M., Machet, J.-M., Thelier-Huches, L., 1994. Determination of a critical nitrogen dilution curve for winter wheat crops. Ann. Bot. 74, 397–407. Kamh, M., Wiesler, F., Ulas, A., Horst, W.J., 2005. Root growth and N-uptake activity of oilseed rape (Brassica napus L.) cultivars differing in nitrogen efficiency. J. Plant Nutr. Soil Sci. 168, 130–137. Lemaire, G., Meynard, J.M., 1997. Use of nitrogen nutrition index for the analysis of agronomical data. In: Lemaire, G. (Ed.), Diagnosis of the Nitrogen Status in Crops. Springer-Verlag, Berlin, pp. 45–55. Lemaire, G., Salette, J., 1984. Relation entre dynamique de croissance et dynamique de prélèvement d’azote pour un peuplement de graminées fourragères. I. Etude de l’effet du milieu. Agronomie 4, 423–430. Lemaire, G., Gastal, F., Salette, J., 1989. Analysis of the effect of N nutrition on dry matter yield of a sward by reference to potential yield and optimum N content. In: XVI International Grassland Congress, Nice, pp. 179–180. Lemaire, G., van Oosterom, E., Jeuffroy, M.-H., Gastal, F., Massignam, A., 2008. Crop species present different qualitative types of response to N deficiency during their vegetative growth. Field Crops Res. 105, 253–265. Lickfett, T., 1993. Auswirkungen verminderter Produktionsintensität in zwei Rapsfruchtfolgen auf Elemente des N-Haushaltes im System Boden— Pflanze, 1st edn. Cuvillier, Göttingen. Müller, K., 2009. Remote Sensing and Simulation Modelling as Tools for Improving Nitrogen Efficiency for Winter Oilseed Rape (Brassica Napus L.). Christian-Albrechts-University, Kiel, Germany (PhD Thesis). Malagoli, P., Lainé, P., Rossato, L., Ourry, A., 2005. Dynamics of nitrogen uptake and mobilization in field-grown winter oilseed rape (Brassica napus) from stem
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Schjoerring, J.K., Bock, J.G.H., Gammelvind, L.H., Jensen, C.R., Mogensen, V.O., 1995. Nitrogen incorporation and remobilization in different shoot components of field-grown winter oilseed rape (Brassica napus L.) as affected by rate of nitrogen application and irrigation. Plant Soil 177, 255–264. Sieling, K., Böttcher, U., Kage, H., 2015. Dry matter partitioning and canopy traits in wheat and barley under varying N supply. Eur. J. Agron. 74, 1–8. Thornley, J.H.M., Johnson, I.R., 1990. Plant and crop modelling. In: A Mathematical Approach to Plant and Crop Physiology. Clarendon Press, Oxford. Triboï-Blondel, A.-M., Messaoud, J., Rousseau, P., 1988. Mise en place et fonctionnement des feuilles de colza d’hiver: relations azote-carbone et sénescence. Agronomie 8, 779–786. Weiner, J., 2004. Allocation, plasticity and allometry in plants. Perspectives in plant ecology. Evol. Syst. 6, 207–215. Wiesler, F., Behrens, T., Horst, W.J., 2001a. The role of nitrogen-efficient cultivars in sustainable agriculture. Sci. World J. 1, 61–69. Wiesler, F., Behrens, T., Horst, W.J., 2001b. Nitrogen efficiency of contrasting rape ideotypes. In: Horst, W.J., Schenk, M.K., Bürkert, A., Claassen, N., Flessa, H., Frommer, W.B., Goldbach, H., Olfs, H.-W., Römheld, V., Sattelmacher, B., Schmidhalter, U., Schubert, S., v. Wirén, N., Wittenmayer, L. (Eds.), Plant Nutrition. Springer, Dordrecht: Netherlands, pp. 60–61. Zar, J.H., 2010. Biostatistical Analysis, 5th edition. Prentice-Hall/Pearson, USA.
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Organ-specific approaches describing crop growth of winter oilseed rape under optimal and N-limited conditions Wiebke Weymann ∗ , Klaus Sieling, Henning Kage Institute of Crop Science and Plant Breeding, Christian-Albrechts-University, Hermann-Rodewald-Str. 9, 24118 Kiel, Germany
a r t i c l e
i n f o
Article history: Received 18 July 2016 Received in revised form 27 September 2016 Accepted 10 October 2016 Available online xxx Keywords: Winter oilseed rape Crop N response Dry matter partitioning Allometric relations N dilution curves
a b s t r a c t Carbon and nitrogen partitioning of winter oilseed rape differs under optimal and nitrogen (N) limited conditions. The quantitative description of these processes and their response to N deficiency is a prerequisite to develop process-oriented crop growth models capable to predict responses to a limited N supply. Dry matter (DM) partitioning, N dynamics and expansion of leaf, stem and pod area, as well as specific leaf area of oilseed rape were recorded during six seasons 2003/04–2005/06, and 2009/10, 2010/11 and 2012/13 within two series of field trials with varying N treatments at the experimental site Hohenschulen, northern Germany. DM partitioning is analysed using allometric relationships between leaf and stem DM as well as between stem and generative DM. The allometric relations between leaf and stem DM varied before and after beginning of stem elongation due to increasing DM allocation to stems during stem elongation. Allometric relations between DM fractions, however, were not affected by N treatment. N dilution curves, describing relations between N concentration and DM, differed between plant fractions, growth stages and N fertilization levels and indicated different response patterns under N limited conditions. This result is supported by relations between N amount and DM of leaves and stems, suggesting a sink priority for leaves under N deficiency. The approaches, describing green area expansion, dry matter partitioning and N distribution, can be used to improve dynamic crop growth models for oilseed rape. © 2016 Published by Elsevier B.V.
1. Introduction Winter oilseed rape is a major crop in central and northern Europe, especially in Germany, France and UK. Despite management optimization and breeding progress during the last decades, oilseed rape cultivation is characterized by highly variable seed yield (Rondanini et al., 2012), low nitrogen use efficiency (NUE) and low nitrogen harvest index compared to cereals (Schjoerring et al., 1995; Hocking et al., 1997; Dreccer et al., 2000). The increase of NUE is a major goal in agronomic research and plant breeding. NUE is divided into two components: N-uptake efficiency and N-utilization efficiency (Moll et al., 1982). For oilseed rape, it is assumed that N-uptake efficiency is comparably high because of an early developed deep and wide root system (Kamh et al., 2005). In contrast, N-utilization efficiency of oilseed rape crops tends to
∗ Corresponding author. E-mail addresses: weymann@pflanzenbau.uni-kiel.de, [email protected] (W. Weymann).
be low because of not simultaneous maximal mineralization rate and growth rate, as well as incomplete translocation of N from vegetative to generative plant parts (Lickfett, 1993; Wiesler et al., 2001a,b). In general, NUE is determined by the capacity to capture soil N, the capacity to use N for crop growth and the capacity to allocate N from vegetative to generative plant parts (Gastal et al., 2015). Detailed investigations on physiological processes of green area expansion, dry matter (DM) partitioning and N distribution under varying fertilization strategies are required in order to analyse options and limitations of improving NUE and N management for maximal crop production. N fertilization in autumn sown oilseed rape crops is mostly split into two applications in spring. First, N is applied at regrowth in spring and secondly at the beginning of stem elongation. Insufficient N supply by fertilization and mineralization can lead to temporal N deficiency. In general, N deficiency influences crop production by reduction of growth rates and by affecting light use efficiency (Bélanger et al., 1992) but specific crop responses differ according to growth stage and degree of N deficit.
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Previous studies showed that N deficiency during autumn growth results in reduced dry matter accumulation before winter but these growth deficiencies are mostly compensated under sufficient water and N availability after start of regrowth in spring. Therefore, final yield is not affected by N deficiency during autumn growth in this case (Colnenne et al., 2002), but Rathke et al. (2005) showed that seed yield of oilseed rape is significantly influenced by N fertilization in spring. Crop N demand varies with growth stage and DM accumulation of crops (Gabrielle et al., 1998; Wiesler et al., 2001a). DM accumulation depends on the quantity of absorbed radiation, determined by photosynthetic active green area, and on light use efficiency as well as stress factors, considering temperature, N and water availability and management (Monteith and Moss, 1977). DM partitioning between plant parts can be described by allometric relations. Allometric approaches rely on a constant ratio of relative growth rates, resulting in a linear relationship between the natural logarithm of DM fractions (Thornley and Johnson, 1990). The relation between DM accumulation and N concentration in single plants and crops can be described by N dilution curves (Salette and Lemaire, 1981). N dilution curves show declining N concentration with increasing DM accumulation. N dilution curves were already estimated for several species (e.g. grass, wheat, maize and canola; Greenwood et al., 1991; Justes et al., 1994; Colnenne et al., 1998; Lemaire et al., 2008). Colnenne et al. (1998) calculated critical N dilution curves for canola. The critical N concentration for a given DM value was defined as N concentration necessary to achieve maximal growth rate (Lemaire and Salette, 1984). If actual N concentration is below the critical N concentration for a given DM value, crop growth is limited by N deficiency. Studies, concerning N dilution, only estimated curves for vegetative growth phases and total aboveground biomass. There is a lack of knowledge considering N dilution during generative growth phase and N dynamics within single plant organs. Studies of organ-specific N dynamics may offer the possibility to investigate crop responses of oilseed rape to N deficiency in more detail. The aims of the current study are (i) to investigate relationships between growth rates of plant parts, (ii) to investigate N dynamics within single plant parts and (iii) to estimate the effects of N management on these processes. Therefore, organ-specific responses to N deficiency are studied. Finally, the investigations may contribute to approaches for improving N-management and NUE by means of simulation studies with dynamic crop growth models.
2. Materials and methods 2.1. Experimental sites and designs Data for analysis were taken from two field trials at the experimental farm Hohenschulen (54.3◦ N, 10.0◦ E), located in northern Germany. Hohenschulen is characterized by its humid climate, influenced by marine conditions. Long-term total rainfall average is 757 mm annually and temperature long-term average is 8.7 ◦ C (1981–2010). Main soil type at Hohenschulen is sandy loam with a pH value of 6.4 and an effective rooting depth of 100 cm. Water holding capacity in the effective rooting depth is about 184 mm. Experiment 1 (Exp. 1) was performed between 2003/04 and 2005/06 with four N treatments (0 kg N ha−1 , 80 kg N ha−1 , 160 kg N ha−1 , 240 kg N ha−1 ), which were applied as ammonium/urea solution in two applications at the beginning of regrowth in spring and the beginning of stem elongation. The experiment was performed with four replicates. The variety Talent was used and winter wheat was the preceding crop. Sowing dates
and seeding densities were chosen according to the best possible management practice. Experiment 2 (Exp. 2), performed during seasons 2009/10, 2010/11 and 2012/13, had 80 management treatments, including four sowing dates (early, normal, late, very late), four autumn N application levels (0 kg N ha−1 , 30 kg N ha−1 , 60 kg N ha−1 , 90 kg N ha−1 ) and five N treatments in spring (0 kg N ha−1 , 80 kg N ha−1 , 160 kg N ha−1 , 240 kg N ha−1 , 280 kg N ha−1 ). The experiment was performed with four replicates. The variety Visby was used with winter barley as preceding crop. 2.2. Measurements In Exp. 1, shoots from an area of 0.88 m2 were harvested several times during total vegetation period for analysis of green area index (GAI), total DM and total N amount. GAI was measured by LAI 2000 (LI-COR inc., USA). Shoots were fractionated into leaves, stems and generative organs. After drying and weighting, fractionated samples were ground for near infrared spectroscopy analysis of the N concentration (NIRSystems 5000 scanning monochromator, FOSS GmbH, Rellingen, Germany). Detailed information is given by Müller (2009). In Exp. 2, measurements were made about every second week from sowing until start of regrowth in spring. DM and N concentration of total shoot, leaves, stems and roots were observed. Root biomass was dug out and mainly represented tap root biomass. In addition, green leaf and stem area were determined by destructive (LI-3100C, LI-COR inc., USA) and non-destructive measurements (LAI 2000, LI-COR inc., USA). 2.3. Statistical analysis Influence of N treatment on relationships between DM fractions and between accumulated N and DM of single plant organs was tested by statistical analysis. The statistical tests were performed using R (version 2.15.2, R Core Team, 2013) with a level of significance of 5%. For linear regressions, representing the allometric relations between DM fraction and relations between GAI and N uptake and GAI and specific leaf area (SLA), the procedure lm was used. Differences in intercept and slope parameters between N treatment levels were analysed with an analysis of variance. Differences of N dilution curves between crops with different N treatment levels were tested by the procedure of Zar (2010). This method is able to test if parameter values estimated for each N treatment level by nls differ significantly. We estimated common intercept values for all N treatment levels but different slope parameters for each N treatment level, separately. These slope parameters were compared following the procedure of Zar (2010). In one case, no N dilution effect was observed. We assumed a constant mean N concentration, which may vary with N treatment. The differences between these mean N concentrations were tested by pairwise t-test. Due to multiple tests, level of significance for each test was adjusted according to the method of Holm (1979). 3. Results 3.1. Expansion of photosynthetic active green area GAI of winter oilseed rape crops varied during crop growth and between N treatment levels. GAI increased after the beginning of generative growth (Fig. 1). Unfertilized plots had a maximum GAI of about 3.5 at the end of flowering. In contrast, unstressed crops achieved a mean maximum GAI of up to 7.
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Fig. 1. Mean value of Green Area Index during different growth stages under consideration of N application during spring growth (Exp. 1, data from experimental year 2005/06).
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Fig. 3. Specific leaf area during different growth stages under consideration of N application during spring growth (Exp. 1, data from experimental year 2005/06).
Table 1 Functional parameters and statistical analysis of the linear relation a) between GAI and N uptake [kg N ha−1 ] (N uptake = a + GAI*b) and b) between GAI and SLA [cm2 g−1 ] (SLA = a + GAI*b). Characters designate siginifance of N application in spring on parameter values (Exp. 1). a) N application [kg ha−1 ] 0 80 160 240
Parameter a ns
Parameter b ns
0 0ns 0ns 0ns
R2
3.6 3.8ns 3.8ns 3.7ns
0.75 0.81 0.85 0.78
Parameter b
R2
b) N application [kg ha−1 ] 0 80 160 240
Parameter a ns
110.5 121.7ns 105.6ns 104.5ns
ns
19.5 20.3ns 24.1ns 27.1ns
0.69 0.51 0.74 0.82
Fig. 4. Relation between Green Area Index and specific leaf area from end of stem elongation until end of flowering under consideration of different levels of N application in spring (Exp. 1).
pattern to N treatment was observed for the linear relationships between N uptake and leaf area index (LAI) and between leaf N amount and LAI (data not shown). Besides GAI, also SLA varied during crop growth and between N treatments. After beginning of inflorescence emergence, unfertilized plots had a substantially lower SLA indicating thicker leaves than fertilized plots. Maximal SLA at the end of flowering was about 200 cm2 g−1 in unfertilized plots, while unstressed crops reached maximal SLA values of 300–400 cm2 g−1 (Fig. 3). From the end of stem elongation until end of flowering, SLA and GAI were linearly correlated (Fig. 4). Relations tend to vary between N treatment levels in spring. Unstressed crops had higher SLA values at a given GAI compared to unfertilized crops but differences were not significant (Table 1b). 3.2. Dry matter partitioning Fig. 2. Relation between total N uptake and Green Area Index under consideration of N application during spring growth (Exp. 1).
GAI was closely correlated with total N uptake (Table 1a, Fig. 2). Per 36 kg N ha−1 absorbed, one unit of GAI was produced. N treatment had no significant effect on this relation. The same response
DM partitioning of winter oilseed rape crops was described by allometric relationships. First, leaf and stem growth were closely related. This relation varied according to the growth stage of the crop (Table 2). From emergence until stem elongation, relative growth rates of stems and leaves correlated significantly (R2 = 0.91). In Fig. 5a, the allo-
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Fig. 5. Allometric relation between leaf and stem dry matter a) before stem elongation under consideration of N application in autumn (Exp. 1 + 2) and b) between stem elongation and onset of flowering under consideration of N application during spring growth (Exp. 1).
Table 2 Functional parameters and statistical analysis of the linear relation between leaf and stem dry matter (ln(stem dry matter) = a + ln(leaf dry matter)*b) before stem elongation (Exp. 1 + 2) and between stem elongation and onset of flowering (Exp. 1). Growth stage
Parameter a
Parameter b
R2
10–30 30–60
−1.04 −0.56
1.13 1.06
0.91 0.81
Table 3 Statistical analysis of the effect of N application on N dilution curves, describing the relationship between N concentration (Nc) and dry matter (DM) for different plant organs and growth stages (leaves: Nc = a + DM*b; stems, pods, tap roots: Nc = a + log(DM)b, R2 : coefficient of determination). Characters designate siginificance of N effects on parameter values. Plant organ
Growth stage
N application [kg ha−1 ]
Parameter a
Parameter b
R2
Leaves
10–30
0/-/30/-/60/-/90/-/0/0/0 0/40/40 0/80/80 0/120/120 0/-/30/-/60/-/90/-/0/0/0 0/40/40 0/80/80 0/120/120 0/0/0 0/40/40 0/80/80 0/120/120 0/-/30/-/60/-/90/-/-
5.93
−0.02a −0.02a −0.01b −0.01b –
0.30 0.60 0.62 0.58 –
−0.57a −0.47a,b −0.40a,b −0.34b −1.22a −1.07b −1.04b −1.03b −0.91a −0.76b −0.72b −0.70b −0.13ns −0.11ns −0.09ns −0.04ns
0.52 0.54 0.55 0.50 0.80 0.90 0.90 0.88 0.88 0.90 0.89 0.89 0.05 0.23 0.24 0.02
30–60
Stems
10–30
30–70
Fig. 6. Allometric relation between stem and generative dry matter until end of flowering under consideration of N application during spring growth (Exp. 1).
metric relationship is shown for different N treatments during autumn growth. From stem elongation until onset of flowering, the relationship between leaf and stem growth slightly changed (R2 = 0.81, Fig. 5b). Proportion of stem growth of total shoot growth was enhanced, compared to the relation before start of stem elongation. Autumn and spring N treatments had no effect on the relationship between leaf and stem growth, neither before stem elongation nor afterwards. Besides leaf and stem growth, also stem and generative growth were correlated. Both DM fractions proportionally increased from
Pods
51–90
Tap roots
10–30
3.67a 4.97b 5.39c 5.49d 4.64
8.10
7.45
3.21
inflorescence emergence until end of flowering (R2 = 0.83, Fig. 6). Spring N did not affect this allometric relationship. 3.3. Organ-specific nitrogen dynamics N concentration of stems, pods, roots and leaves decreased with increasing DM accumulation. In order to quantify this decrease, “N dilution curves” (Salette and Lemaire, 1981) could be estimated. N dilution curves differed between plant organs, growth stages and N treatment levels (Table 3). The relation between stem N concentration and stem DM was described by logarithmic functions, which differed between growth stages and levels of N application (Fig. 7a, b). From emergence until
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Fig. 7. N dilution curves of stems a) before stem elongation under consideration of N application during autumn growth (Exp. 1 + 2) and b) after stem elongation under consideration of spring N application (Exp. 1).
stem elongation, N concentration varied between 1.5% and 6%. N application during autumn growth had an effect on the slopes of the functions, while a common intercept was estimated for all N treatment rates. The slope of the function representing crops with no N application was significantly steeper than the one representing crops with autumn N application of 90 kg N ha−1 . After beginning of stem elongation, slope of the N dilution curve representing crops with no N application significantly differed to slopes of functions belonging to crops with any N application in spring (Table 3). Similar to N dilution curves of stems, the relationship between N concentration and DM of the generative fraction can be described by logarithmic functions (Fig. 8). N concentration varied between 4% and 7% at inflorescence emergence and decreased to 1–4% after flowering. Thereby, unfertilized plots tended to have lower N concentrations, compared to fertilized plots. N fertilization in spring significantly affected the slopes of logarithmic functions, estimated for each N treatment level (Table 3). The function representing crops with no N application had a significantly steeper slope compared to functions representing crops with any N application in spring. In addition to the previously described above-ground plant parts, root N concentration decreased with increasing root DM until stem elongation. This relation can be described by logarithmic N dilution curves with slopes, estimated for each N treatment level separately and a common intercept (Fig. 9). N application during autumn did not significantly affect the slopes of these functions (Table 3), although crops with no or low N application tended to have lower root N concentration from emergence until stem elongation than unstressed crops. Relations between N concentration and DM of leaves differed compared to the ones of stems, pods and roots. Before beginning of stem elongation, the relation between leaf N concentration and leaf DM followed a linear regression (Fig. 10a, Table 3). Leaf N concentration varied between 3% and 7% and crops with low N application tended to have lower N concentrations than unstressed crops. Estimated with a common intercept for all treatment levels, N application during autumn growth affected the slopes of the dilution curves. Crops with autumn N application of 0 kg N ha−1 or 30 kg N ha−1 were represented by functions with significant steeper slopes than crops with higher autumn N application. From stem elongation until onset of flowering, leaf N concentration did not change with leaf DM. No N dilution effect was observed
but N application rate significantly affected mean leaf N concentration calculated for each N treatment level (Fig. 10b, Table 3). 3.4. Organ-specific responses of vegetative biomass to severe N deficiency The previously described N dilution curves have different function types and parameter values. This indicates organ-specific response patterns to N deficiency. To analyse crop response to N deficiency in more detail, we studied the relation between N amount and DM of vegetative biomass under N-unlimited conditions and under severe N deficiency. To define severe N deficiency, we looked for a lower bound of N concentrations by analysing the data for unfertilized treatment. The linear regression between N amount and DM of leaves varied before and after stem elongation but the response to Nlimitation was similar. N amount of leaves was reduced by 30–35% at a given DM value under severe N deficiency (Fig. 11a). In contrast to leaves, N amount of stems under severe N deficiency during autumn growth was reduced by about 50% at a given DM value compared to unstressed crops (Fig. 11b). After beginning of stem elongation during spring growth, relative reduction of N amount under severe N deficiency varied with DM growth. Relative reduction of stem N amount at a given DM value increased from 30% up to 66% with increasing stem DM. Before and after stem elongation, functional parameters describing the relation between N amount and DM of leaves and stems differed significantly between N levels (Table 4). 4. Discussion The effect of N supply on crop growth is based on several physiological processes, as green area expansion, DM partitioning and N distribution. This paper aims to analyse some of these effects for winter oilseed rape using data from field experiments with different N supply rates and sequential destructive samplings. Single measurements suggested GAI values up to 10. These high values might have been caused by boundary effects. Data showed that GAI and SLA differed according to N availability, as influenced by N application in spring. Unstressed crops had substantially higher SLA than those with low or no N supply. Higher SLA during spring growth for plots with high N application
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Fig. 8. N dilution curve of pods from the beginning of generative growth until end of pod growth under consideration of N application in spring (Exp. 1).
Fig. 9. N dilution curve of tap root under consideration of N application during autumn growth (Exp. 2).
Table 4 Functional parameters and statistical analysis of the relation between N amount (N) and dry matter (DM) of leaves and stems during different growth stages under optimal (N-unlimited) and critical (severe N deficiency) N supply. Significant differences between parameter were tested for each “plant organ × growth stage − combination” separately (leaves: N = DM*b; stems: N = (a + b*log(DM))*DM). Characters designate siginificance of N effects on parameter values. Plant organ
Growth stage
N supply
Parameter a
Parameter b
Leaves
10–30
critical optimal critical optimal critical optimal critical optimal
– – – – 0.06ns 0.06ns 0.06ns 0.06ns
0.034a 0.049b 0.033a 0.052b −0.026a −0.014b −0.023a −0.013b
30–60 Stems
10–30 30–60
could be caused by self-shading. Due to higher GAI, self-shading is more pronounced under optimal conditions, compared to N limited conditions. Self-shading induces translocation of assimilates and N compounds from vegetative to generative plant parts (Malagoli et al., 2005) and thereby reduces DM. For a constant leaf area this
leads to an increase of SLA. This response pattern was also observed for wheat (Ratjen and Kage, 2013) and barley (Sieling et al., 2015). In addition, differences in GAI and SLA may be caused by the limited leaf area expansion under N stress (Gastal and Lemaire, 1988). This leads to lower LAI at a given leaf DM and therefore to lower SLA values observed for unfertilized crops. Although GAI varied between N treatments, N uptake per unit GAI or LAI was not affected by N application. These results are in accordance with Lemaire et al. (2008), who observed no change of N uptake per unit LAI for canola crops. In contrast, N uptake per unit LAI was substantially lower under N limitation for maize crops. According to Lemaire et al. (2008), constant N uptake per unit GAI or LAI indicates that resource capture is reduced under N limitation. They suggested that canola reduces leaf mass per unit crop mass and therefore, higher proportion of assimilates is allocated to the stems under critical N conditions. Our data did not verify these observations, since allometric relationships between leaf and stem growth were not affected by the N status of the plant, neither before stem elongation nor afterwards. In addition, also the allometric relationship between stem and generative growth did not
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Fig. 10. N dilution curves of leaves a) before stem elongation under consideration of N application during autumn growth (Exp. 1 + 2) and b) after stem elongation under consideration of spring N application (Exp. 1).
Fig. 11. Relationship between N amount and dry matter of a) leaves and b) stems before and after stem elongation (GS 30) under optimal (N-unlimited) and critical (severe N deficiency) N conditions (Exp. 1 + 2).
differ between N treatment levels. Summarizing, in contrast to previous suggestions based on results of Weiner (2004), who described changing allometric relationships of DM fractions in response to the environment, DM partitioning of oilseed rape did not significantly change in response to N application level. N dynamics during crop growth can be described by N dilution curves, showing the relation between N uptake and DM accumulation. This relationship was already described for several species (e.g. Greenwood et al., 1991; Justes et al., 1994; Plénet and Lemaire, 2000; Gastal and Lemaire, 2002). For oilseed rape, Colnenne et al. (1998) developed a critical N dilution curve, which represents the minimum shoot N concentration required for maximal shoot DM production from emergence until onset of flowering. Thereby a power function was used to describe decreasing N concentration in shoots with increasing shoot DM. Furthermore, N dilution curves are used to estimate N status of crops (Lemaire et al., 1989; Lemaire and Meynard, 1997). Mostly, the estimation of N status of crops indicates that crop growth stops if N concentration is zero (Gastal
et al., 2015) but this assumption neglects the part of structural N in plant tissue. We considered structural N, which is not used in growth processes, as the minimum N concentration remaining in plant tissue. Crop growth stops when N concentration is beneath minimum N concentration. Our data shows that each single plant organ of autumn sown oilseed rape has a specific N dilution curve responding specifically to N deficiency. Thereby leaf N concentration and leaf DM before stem elongation are linearly related, while leaf N concentration remains constant from stem elongation until onset of flowering. In contrast to leaves, relationships between N concentration and DM of stems, pods and roots follow declining logarithmic functions, indicating an increasing portion of structural components. Statistically significant differences between parameters of N dilution curves due to N treatment level indicate adaptation processes of the plant to N deficiency. These adaptation processes differ between plant organs. Therefore, an organ-specific analysis may be
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advantageous to describe physiological processes of N distribution and its effects on crop productivity. Decreasing leaf N concentration with increasing leaf DM before stem elongation may partly be explained by the decreasing level of irradiation in autumn during which the majority of the samplings have been taken. During this time, also SLA decreases substantially. During spring growth, however, radiation level increases. Despite self-shading induced senescence of leaves and loss of N, N concentration of leaves per unit DM does not decrease substantially, probably because N is redistributed together with carbon from older leaves to younger ones to provide maximal photosynthetic activity. In addition, the flower layer causes shading of leaves. Triboï-Blondel et al. (1988) and Merlo et al. (1995) observed a reduced nitrate reductase activity under low light conditions. Stems are negligible for photosynthesis and mainly serve as structural tissue. Therefore, N concentration of stems decreases substantially with increasing DM. These suggestions are in accordance with Colnenne et al. (1998), who explained change of allometric relation between shoot DM and accumulated N in shoots with an increase of lignified tissue, predominantly in stems. N concentration of generative organs decreases substantially with increasing DM, although N is translocated from senescing leaves to pods (Malagoli et al., 2005) and pods are predominantly responsible for photosynthesis after flowering (Gammelvind et al., 1996). This pattern can be explained by the DM distribution between pod walls and seeds. At the beginning of generative growth, pod growth is dominated by the development of photosynthetic active pod walls. Afterwards, growth of photosynthetic unproductive seeds dominates and pods start to mature (Habekotté, 1993). The redistribution of N during ripening is not represented by this dilution curve because latest measurements were taken at the end of pod growth. Besides N dynamics caused by crop growth, N dilution curves also indicate response pattern of single plant organs to N deficiency. The relation between N amount and DM of leaves and stems for N-unlimited conditions and severe N deficiency showed organspecific responses to N deficiency. Reduction of N amount at a given DM value due to N limitation reveals a more pronounced response of stems to N deficiency, compared to leaves. Therefore, oilseed rape seems to maintain high N contents in leaves to support photosynthetic activity, while N content of stems decreases under N limitation. This may reflect a buffer function of stem N under fluctuating N supply. We assume that the relationships, described in this study, are valid for several environments and under varying soil and weather conditions. The relations might differ between genotypes but detailed data is not available to include this question into the current study. Summarizing, allometric relationships and N dilution curves can be used in dynamic crop growth models to simulate DM partitioning and N distribution and to estimate organ-specific responses to N deficiency.
4.1. Implications for modelling The results of the current study suggest new approaches to describe physiological processes and responses of oilseed rape growth to temporal N deficiency during different growth phases. The allometric relations between leaf, stem and pod growth can be used to implement algorithms within dynamic crop growth models, either under optimal or under N-limited conditions. N dilution curves, estimated from unstressed crops and data gained from crops with severe N deficiency offer the opportunity to calculate the degree of N deficiency under consideration of structural N in plant tissues. In addition, organ-specific parameters of N dilution curves in dynamic crop growth models illustrate organ-
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