Quantifying crop nitrogen status for comparisons of agronomic practices and genotypes

Field Crops Research 164 (2014) 54–64

Contents lists available at ScienceDirect

Field Crops Research journal homepage: www.elsevier.com/locate/fcr

Quantifying crop nitrogen status for comparisons of agronomic practices and genotypes Victor O. Sadras a, *, Gilles Lemaire b a b

South Australian Research and Development Institute, Waite Campus, Australia Honorary Researcher, INRA Lusignan, France

A R T I C L E I N F O

A B S T R A C T

Article history: Received 25 March 2014 Received in revised form 13 May 2014 Accepted 13 May 2014 Available online xxx

The nitrogen economy of the crop is a critical driver of biomass and grain production, and its importance is reflected in a large, worldwide research effort to link nitrogen, growth and yield. Particular research questions require measurement of specific traits, hence the need to quantify multiple, often complementary traits including crop nitrogen uptake, nitrogen use efficiency and its components, nitrogen concentration in the crop and its parts, down to relevant enzymes (e.g. nitrate reductase) and other products of gene expression. Nitrogen uptake, however, is co-regulated by both soil nitrogen availability and crop biomass accumulation; hence, crop nitrogen uptake or shoot nitrogen concentration reflect univocally crop nitrogen status only if comparisons are made at similar biomass. Although the allometric relationships between biomass and nitrogen uptake have been established for over two decades, many studies still report results in terms of nominal treatments, e.g. high vs low nitrogen, which are uninformative; curves relating yield and fertiliser rate, which are of local interest but provide little insight on the underlying processes and have low generic value; and nitrogen-related traits that are incomplete or inadequate to quantify crop nutrition status. Often, the allometric relationships between nitrogen and biomass are overlooked. In this opinion paper, we summarise the already well established concepts of dilution curves and nitrogen nutrition index, outline the standard partitioning of nitrogen use efficiency, and highlight the confounded effects in nitrogen use efficiency when the allometric relationship between nitrogen uptake and biomass is ignored. A sample of recent papers is used to survey the most common approaches to characterise nitrogen related traits. We illustrate the application of dilution curves and nitrogen nutrition index in the assessment and interpretation of crop responses to agronomic practices and comparisons of wheat cultivars and maize hybrids. ã 2014 Elsevier B.V. All rights reserved.

Keywords: Yield Water Fertiliser Allometry Nitrogen nutrition index

1. Introduction The importance of nitrogen for crop production cannot be understated. On a historic time scale, agronomic practices improving the availability of nitrogen and water, combined with germplasm able to capture the benefits of enhanced resources, have been the main drivers of improvement in crop yield (Sinclair and Rufty, 2012). Indeed, selective pressure for yield and agronomic adaptation has dramatically improved the nitrogen economy of cereals in cropping systems with high (Foulkes et al., 1998; Haegele et al., 2013) and low nitrogen inputs (Sadras and Lawson, 2013).

* Corresponding author. Tel.: +61 8 83039661. E-mail address: [email protected] (V.O. Sadras). http://dx.doi.org/10.1016/j.fcr.2014.05.006 0378-4290/ ã 2014 Elsevier B.V. All rights reserved.

Data aggregated at large scales in space (national to global), and time (decades), thus reveal close associations between crop production and fertiliser use (Tilman et al., 2002). Large scale observations, however, could lead to inappropriate generalisations, such as the proposition to improve crop yield whilst reducing nitrogen input irrespective of current practices and soil fertility in particular cropping systems. Nutrient balance, i.e. the difference between the inputs and outputs to the system, is commonly used to detect environmentally undesirable excess nutrient (Sassenrath et al., 2013). However, a system can achieve close-to-zero nitrogen balance at low yield, hence the incompleteness of these balances for tactical decisions aiming at both high yield and low environmental impact. Current nitrogen input meets both high production and low environmental footprint in irrigated maizebased systems of USA (Grassini and Cassman, 2012), maybe excessive and offers opportunities for reduction in some cropping systems of China (Chuan et al., 2013), and is often insufficient and

V.O. Sadras, G. Lemaire / Field Crops Research 164 (2014) 54–64

needs to be increased in many semi-arid environments with low soil fertility in both large-scale mechanised (Angus, 2001; Sadras and Roget, 2004) and subsistence cropping systems (Rockström and deRouw, 1997; Rockström et al., 1999). Clearly, nitrogen management to achieve high yield and low environmental footprint needs to be assessed and solved locally; this requires adequate metrics to characterise crop nutritional status. Adequate metrics must be used to rigorously test the proposition that replacement of mineral fertilisers with organic fertilisers, and crop legumes (biological N2 fixation) could satisfy increasing food demand and reduce both nitrogen leaching and greenhouse emissions (Kirchmann and Bergström, 2008; Connor and Mínguez, 2012). Physiological and genetic studies aiming at understanding and improving the nitrogen economy of crop varieties also require proper measures of crop nitrogen status. Statistical analysis of nominal treatments, e.g. high vs low nitrogen, is uninformative and curves relating yield and fertiliser rate may have local interest but provide little insight on the underlying processes and have low generic value. Nitrogen use efficiency is defined as the increment of yield for each added unit of N fertiliser and can be expressed as the product of three factors: the N uptake efficiency (i.e. the increment in N uptake by the crop per unit of increment in N supply to the soil); the N conversion efficiency, also termed utilisation efficiency (i.e. the increment in biomass per unit of N uptake) and harvest index (Lemaire and Gastal, 2009). Nitrogen uptake, however, is co-regulated by both soil nitrogen availability and crop biomass accumulation (Devienne-Barret et al., 2000); hence, crop nitrogen uptake or shoot nitrogen concentration reflect univocally crop nitrogen status only if comparisons are made at similar biomass (Lemaire and Gastal, 2009). The nitrogen nutrition index is a theoretically sound and agronomically relevant method to quantify the nitrogen status of the crop based on robust nitrogen dilution curves which effectively separate biomass as a component of nitrogen uptake (Greenwood et al.,1990; Justes et al.,1994; Lemaire and Gastal,1997; Lemaire et al., 2008). Although these concepts have been established for over two decades, many papers report results in terms of nominal treatments, or nitrogen-related indices that provide incomplete or inadequate quantification of crop nutrition status. In this opinion paper, we summarise the well established concepts of dilution curves and nitrogen nutrition index, outline the standard partitioning of nitrogen use efficiency, and highlight the confounded effects in nitrogen use efficiency when the allometric relationship between nitrogen uptake and biomass is ignored. A sample of recent papers is used to survey the most common approaches to characterise nitrogen-related traits. Finally, we illustrate the application of dilution curves and nitrogen nutrition index in the assessment and interpretation of crop responses to agronomic practices and comparisons of wheat cultivars and maize hybrids. 2. Dilution curves and nitrogen nutrition index 2.1. Overview Lemaire and Salette (1984a,b) and Greenwood et al. 1990 showed that the critical shoot nitrogen concentration,1 i.e. the minimum crop nitrogen concentration for maximum biomass growth rate, declines with increasing crop biomass. This relationship between critical crop nitrogen concentration %Nc and the maximum crop biomass Wc has been empirically represented by a negative allometric function, called critical N dilution curve:

1

In this paper, crop nitrogen concentration (%N and related variables) refers to shoot only. Likewise, crop nitrogen uptake refers to the total amount of nitrogen in shoots unless specified otherwise.

%Nc ¼

10aW b c

55

(1)

where b is a dimensionless coefficient, and a is the crop nitrogen concentration when Wc = 1 t ha1. Box 1 outlines the theory of nitrogen dilution in crop canopies. By multiplying the two members of Eq. (1) by Wc an allometric relationship between critical nitrogen uptake (Ncupt), i.e., the minimum N uptake for achieving the maximum crop biomass, and crop biomass is obtained: Ncupt ¼ aW ð1bÞ c

(2)

The coefficient 10a represents the crop nitrogen uptake, in kg N ha1, for a crop biomass of 1 t ha1. Coefficients a and b have been determined for many species (Table 1). It is then possible by using the critical N dilution curve for a given crop species to derive a nitrogen nutrition index NNI, as shown in Fig. 1, for quantifying the nitrogen status of any crop in any situation: NNI ¼

%Nactual %Nc

(3)

where %Nactual is the actual crop nitrogen concentration corresponding to the actual biomass Wactual. For NNI > 1 the crop nitrogen status can be considered as non-limiting, so any increase in N supply would not increase crop biomass, and for NNI < 1 the crop nitrogen status can be considered as limited by N supply. The NNI, therefore, provides a measure of nitrogen status accounting for the dilution of nitrogen in growing crops. Nevertheless, several limitations of this method have to be emphasised: (i) The theory underlying the dilution curve is restricted to the

vegetative period when only two compartments, metabolic and structural, are relevant (Box 1). During the period of yield formation, e.g. grain filling in seed crops or storage of carbohydrates and proteins in root and tuber crops, a third compartment and translocation processes have to be considered, which restricts the validity of Eq. (1). So, the limit for using NNI as a diagnostic tool is the flowering stage for annual grain crops. (ii) The theory describes the nitrogen dilution process within a population of plants competing for light. In absence of competition, i.e. isolated plants, the dilution process is slower (Lemaire and Gastal, 2009). So, Eq. (1) cannot be used for early growth (leaf area index < 1) when plants can be considered as more or less isolated (Lemaire et al., 2008) or for crops having too low plant densities. Specific nitrogen dilution curves have to be established for these situations. (iii) The critical nitrogen concentration declines with water deficit, and parameters of dilution curves are, therefore, affected by crop water status (Belanger et al., 2001; Errecart et al., 2014). This constrains the application of the NNI in water-deficient crops. However, the critical nitrogen concentration scales with crop water status (Fig. 2) thus providing an interesting quantitative link between nitrogen and water economies of crops that deserves further research, as outlined in Section 2.2.

2.2. Effect of water deficit Soil water limitation affects several aspects of crop nitrogen nutrition, as reviewed in Gonzalez-Dugo et al. (2010). Water deficit reduces crop nitrogen uptake in many species including temperate grasses (Lemaire et al., 1996; Gonzalez-Dugo et al., 2005), wheat (Sadras et al., 2004), maize (Pandey et al., 2000) and sunflower (Gonzalez-Dugo et al., 2010). The use of NNI for evaluating the crop

56

V.O. Sadras, G. Lemaire / Field Crops Research 164 (2014) 54–64

Box 1. Theoretical framework of N dilution in crop canopies A theoretical framework has been developed for explaining the close relationship between crop N demand and crop biomass accumulation rate (Greenwood et al., 1990; Lemaire and Gastal, 1997; Lemaire et al., 2008). The hypothesis is that crop mass W is composed of two compartments: Wm the metabolic tissues involved directly in growth processes (photosynthesis and meristem activity) with a high nitrogen concentration %Nm, and Ws the structural tissues involved in plant architecture and transport with a low nitrogen concentration %Ns. Then: W ¼ Wm þ Ws

(B1)

and: 1 ð%N m W m þ %N s W s Þ (B2) W If we assume that Wm increases allometrically with W (Niklas, 1994; Lemaire and Gastal, 1997; Lemaire et al., 2007; Lemaire et al., 2008) then %N ¼

W m ¼ kW a

(B3)

and then: %N ¼ kð%N m  %N s ÞW a1 þ %N s

(B4)

This equation, with parameters k and a discussed below, reflects the nitrogen dilution process as the crop grows. Wheat (Justes et al., 1994) and maize (Plénet and Lemaire, 1999) returned similar %Ns, i.e. >0.77 and 0.82, respectively, while %Nm was 6.47 for wheat and 4.81 for maize thus reflecting differences in metabolic pathway between C3 and C4 species. Fitting Eq. (B4) to data representing the critical crop N concentration (%Nc), i.e. the minimum nitrogen concentration required at a given crop biomass for maximum biomass growth, allows the distinction between data points (%N, W) corresponding either to supra-optimal or sub-optimal nitrogen supply. The nitrogen status of any crop, as defined by its actual biomass Wactual and its actual nitrogen concentration %Nactual, could then be evaluated with the index: NNI 0 ¼

%N actual  %N s %N c  %N s

(B5)

An empirical simplification of Eq. (B4) can be used: %N c ¼ aW b c

(B6)

and by multiplying both members of Eq. (B6) by Wc we can express the critical crop nitrogen uptake Ncupt: N cupt ¼ 10aW ð1bÞ c

(B7) 1

1

where the coefficient 10 is introduced when Ncupt is expressed in kg N ha while Wc is expressed in t ha . Eq. (B7) corresponds to the critical N uptake – biomass trajectory during crop growth (Fig. 3). The implicit assumption that %Ns = 0 is acceptable because Eqs. (B4) and (B6) are very close to each other for W < 20 t ha1 and this is sufficient for most crops in a broad range of agronomic conditions. The parameters of Eq. (B6) have been determined for many species (Table 1). The value of allometric coefficient a has been approached by Lemaire et al. (2007) on the assumption that the metabolic compartment Wm scales with the leaf area index (LAI) of the canopy: W m ¼ pLAI

(B8)

leading to an allometric relationship between LAI and crop biomass W: k LAI ¼ W a p

(B9)

where the coefficient k/p is the LAI for W = 1 t ha1. Lemaire et al., 2007 showed that coefficients a (Eqs. (B3), (B4), (B9)) and 1  b (Eq. (B7)) are similar for many crop species. The identity a  1  b would thus explain the proportionality between nitrogen accumulation in shoot and LAI expansion observed empirically for many species (Grindlay et al., 1993; Grindlay, 1997; Plénet and Lemaire, 1999 Lemaire et al., 2005); by combining Eqs. (B7), (B8) and (B9): 10ap LAI (B10) k This theoretical framework explaining the allometry between crop nitrogen uptake and biomass (Eq. (B7)) implies that crop growth itself controls of crop nitrogen uptake. Physiological and molecular studies demonstrate that the shoot regulates root nitrogen absorption capacity through two signals, a positive one associated to carbon supply and a negative one associated to reduced nitrogen down flow signalling plant N satiety (Lejay et al., 1999; Forde, 2002). Thus, crop nitrogen uptake is co-regulated by both soil nitrogen availability and crop growth capacity; as crop biomass increases the competition for light increases leading to two coupled processes: (i) a decrease in carbon supply to roots and (ii) an increase of nitrogen redistribution within canopy with associated negative feedback control of plant nitrogne uptake. Devienne-Barret et al. (2000) formalised this co-regulation of N uptake using a Michaelis–Menten equation relating the regulation of root absorption by soil N supply and the derivative of Eq. (B7) to account for the feed-back control by plant growth:
   dN upt dW C ¼ að1  bÞW b V (B11) dt max K þ C dt N upt ¼

where the first part of the equation is the derivative of Eq. (B7) representing of the rate of N uptake by the maximum biomass growth rate of the crop, and the second part is the regulation of N absorption by soil N supply; V and K are the coefficients of the Michaelis–Menten formula and C is the actual NO3 concentration in soil solution. So, as presented in Fig. 3, it is possible to draw crop nitrogen uptake vs biomass trajectories during crop growth for different values of C, representing steady-state soil N supply. This conceptual framework is used to untangle the components of nitrogen conversion efficiency in Section 3.3.

V.O. Sadras, G. Lemaire / Field Crops Research 164 (2014) 54–64

57

Table 1 Coefficients a and b of Eq. (1) %Nc = a Wcb for different crop species. Crop species

a (g N 100 gDM1)

b (unitless)

References

Temperate grasses (C3) Alfalfa (C3) Pea (C3) Wheat (C3) Canola (C3) Sunflower (C3) Rice (C3) Tomato (C3) Cabbage (C3) Maize (C4) Sorghum (C4) Tropical grasses (C4)

4.8 4.8 5.1 5.3 4.5 4.5 5.2 4.5 5.1 3.4 3.9 3.6

0.32 0.33 0.32 0.44 0.25 0.42 0.52 0.33 0.33 0.37 0.39 0.34

Lemaire and Salette (1984a,b) Lemaire et al. (1985) Ney et al. (1997) Justes et al. (1994) Colnenne et al. (1998) Debaeke et al. (2012) Sheehy et al. (1998) Tei et al. (2002) Ekbladh and Witter (2010) Plénet and Lemaire (1999) Plénet and Cruz (1997) Duru et al. (1997)

nitrogen status under different conditions of soil water availability allows a clear distinction between the two confounded effects of water stress: (i) a reduction of crop growth and the attenuation of nitrogen dilution leading to an increased crop nitrogen concentration in stressed stands as compared with non-stressed ones; and (ii) a reduction of nitrogen availability in dry soil leading to a reduction in crop nitrogen concentration. The relative importance of these two opposite effects depends on the repartition of mineral nitrogen and water along the soil profile according to root architecture (Durand et al., 2010). Thus, comparison of crop species and varieties under different combinations of water and nitrogen supply must be accompanied by the analysis of nitrogenwater interactions using allometric indices of crop nitrogen status to separate direct effect of water stress from its indirect effect mediated by nitrogen nutrition, as shown by Lemaire et al. (1996) in comparisons of maize and sorghum. Recent field studies on tall fescue show that the critical crop nitrogen concentration under water deficit is lower than the critical plant N concentration in well-watered stands (Fig. 2). This reduction in critical nitrogen concentration with water stress corresponds to an intrinsic reduction of crop nitrogen demand under water stress as shown by Gonzalez-Dugo et al. (2012) in controlled conditions due to (i) a fundamental change in the allometry between structural (Ws) and metabolic (Wm) components of plant biomass, and (ii) an increasing importance of nonstructural carbohydrate storage that would require a third plant compartment (Wnsc) within the theoretical framework in Box 1.

From an agronomic point of view, nitrogen use efficiency (NUE) is the increment of yield (DY) for each added unit of N fertiliser (DNf), i.e. the slope of the curve relating yield and rate of fertiliser. As this curve is asymptotic, NUE declines with increasing nitrogen rate (Belder et al., 2005; Kim et al., 2008; Sadras and Rodriguez, 2010). Such a global definition of NUE does not allow the identification of traits controlling NUE because crops respond to total N supply (Ntot) including fertiliser (Nf) and soil N supply (Nsoil). Thus, according to variation in Nsoil due to both soil and climate, different amounts of total nitrogen can be obtained with the same amount of fertiliser, then leading to large differences in NUE not directly attributable to species or genotypes. Moll et al. (1982) defined NUE as the yield produced per unit of available nitrogen in the soil. Hence, NUE can be divided into two components: (i) the N uptake efficiency (NuptE), defined as the increment in

crop N uptake per unit of increment in soil N supply; (ii) the N conversion efficiency (NCE), defined as the capacity of

the crop to produce a supplement of biomass per unit of increment of N uptake. This is also termed utilisation efficiency. According to crop species, yield represents either the above ground biomass, as for forage crops, or the grain biomass as for cereals, grain legumes or oil seed crops. In grain crops, it is then necessary to take into account the harvest index (HI). Thus, NUE can be split as follows:

3. Nitrogen use efficiency NUE ¼

3.1. Overview

Shoot N concentration

Improving nitrogen use efficiency is a major goal in plant breeding for sustainable agriculture (Hirel and Lemaire, 2005).

Supra-optimal N nutrition

%Nc %Nactual

Critical shoot N concentration Actual shoot N concentration

Sub-optimal N nutrition

DNupt DW DY   DNtot DNupt DW

NUE ¼ Nupt E  NCE  HI

(4) (5)

Therefore, NUE can be considered as resulting from three types of processes: (i) the capacity of the crop to capture soil nitrogen, NuptE; (ii) the capacity of the crop to use nitrogen for biomass elaboration, N conversion efficiency, NCE; and (iii) the capacity of the crop to allocate carbon to grain. 3.2. Nitrogen uptake efficiency

critical N dilution curve %Nc = a Wc-b

Wactual Crop biomass Fig. 1. The critical N-dilution curve of annual crops. %N is shoot nitrogen concentration, with subscripts indicating actual (a) and critical (c).

As suggested by the close dynamic relationship between crop nitrogen uptake and crop biomass accumulation leading to N dilution curves (Section 2, Box 1), the rate of crop N uptake is coregulated by soil N availability and crop growth rate (DevienneBarret et al., 2000). Two important consequences can be deduced: (i) Any genotypic or environmental factor (other than nitrogen

supply) enhancing the crop growth rate increases de facto the nitrogen uptake capacity of the crop. So NuptE increases with

58

Relative critical N concentration

V.O. Sadras, G. Lemaire / Field Crops Research 164 (2014) 54–64

1.0 0.8 0.6 0.4 0.2 0.0 0.0

0.2

0.4

0.6

0.8

1.0

Relative evapotranspiration Fig. 2. The critical nitrogen concentration of tall fescue scales to crop water availability. Relative critical nitrogen concentration and relative evapotranspiration are ratios between the respective variables in water-deficient and well-watered crops. Source: Errecart et al. (2014).

crop biomass, and then crops producing more shoot biomass should have a higher NuptE than their counterparts with lower shoot biomass. (ii) Because the response curve of crop N uptake to soil N supply tends to be asymptotic NuptE of crops declines as soil N supply increases. In conclusion, variations in NuptE driven by genotype and environment should involve a co-variable analysis allowing interpretations at equivalent crop biomass and similar nitrogen supply; otherwise, the results would be confounded with these trivial effects. In order to overcome this difficulty, we propose to determine systematically the NNI for each genotype and to rank genotypes on their NNI under similar nitrogen supply. 3.3. Nitrogen conversion efficiency Fig. 3 represents the trajectory of nitrogen uptake against crop biomass for crops with limiting and non-limiting nitrogen supply corresponding to critical nitrogen status. This approach to analyse

Fig. 3. Components of the nitrogen conversion efficiency (NCE) analysed in terms of N uptake vs crop biomass trajectories for steady-state N supply corresponding to sub-optimum (red curve) and optimum (black curve) nitrogen supply. Optimum nitrogen supply corresponds to the critical crop N concentration. The first component D(Nupt)1 corresponds to the quantity of N necessary for the crop to reach its critical N concentration, and its NCE is zero. The second component D(Nupt)2 corresponds to the quantity of N necessary to support the increment in biomass DW, with NCE = DW/DN = 1/10 abW (1  b) that increases with crop biomass. Adapted from Lemaire and Gastal (2009). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

NCE, and its assumptions, has been described in Lemaire and Gastal (2009), who also consider nitrogen supply above the critical level. Briefly, each trajectory represents a virtual crop nitrogen status maintained by steady-state N supply, whereas a real crop in a changing environment could shift between trajectories in response to changes in N supply, as illustrated with the dotted line in Fig. 3. The slope of each curve is DNupt/DW which is the reciprocal of NCE. The supplement of nitrogen taken up by the crop, DNupt, due to the increase in N supply, can be defined as the sum of two components: (i) D(Nupt)1, the additional N uptake required for the N-limited crop to reach the corresponding critical level, and (ii) D(Nupt)2, the supplemental increase in N uptake associated to the additional growth (DW) with higher N supply. The NCE corresponding to D(Nupt)1 is zero as the increment in N uptake is made at a constant crop biomass. The NCE of D(Nupt)2 can be approached by the derivative of Eq. (2): dNupt ¼ 10að1  bÞW b dW

(6)

This equation indicates that the efficiency of conversion of absorbed nitrogen (DW/DNupt) increases with increasing crop biomass. Such an analysis allows the identification of two sources of variation in NCE. Firstly, when factors other than nitrogen supply (e.g. improved variety, increased water supply) increase crop biomass, then NCE increases with crop biomass. Secondly, when nitrogen supply increases crop biomass, then the allocation of nitrogen to restoring crop nitrogen status reduces NCE. This approach allows the study of nitrogen conversion efficiency as a dynamic process where time has to be considered explicitly through crop growth rate: the higher the crop growth rate, the higher the NCE of the crop. Then, it allows for the trivial effect of biomass per se: a small crop, either because of genetic or other environmental constraints other than nitrogen supply will have a lower NCE as compared to a bigger crop. In consequence, comparison of NCE across species, cultivars or agronomic practices must be done at similar biomass and under similar crop nitrogen status otherwise the results would be polluted by the trivial effect of crop size. 4. Overview of approaches used in crop nitrogen studies Here, we aim at illustrating the diversity of approaches in crop nitrogen studies using a sample of recent publications (Appendix A), rather than providing an exhaustive analysis of methods. Soil indices and crop traits vary depending on the focus of the study. Where the focus is soil processes, crop nitrogen status is normally less relevant. For example, Cao et al. (2013b) evaluated the effect of agronomic practices on ammonia volatilization from

V.O. Sadras, G. Lemaire / Field Crops Research 164 (2014) 54–64

paddy fields (study #3 in Appendix), Liang et al. (2013) aimed at establishing the fate of 15N-labeled fertiliser in soil with different management history (study #15) and Muñoz-Romero et al. (2013) measured the effects of tillage system on N rhizodeposition (Study #17); proper quantification of the nitrogen status of the crop in these type of studies is therefore less important. Methods to establish crop nitrogen status for agronomic (e.g. fertiliser management) and breeding (e.g. screening of lines/hybrids) applications seek reliability and convenience. Spectral methods are, therefore, of interest as they are non-destructive and amenable to rapid and relatively inexpensive screening. Wang et al. (2013a) for example related spectral indices against measured biomass and nitrogen concentration (study #22); however, these traits are related (Section 2), and therefore, confounded in the spectral indices. Other papers also related spectral indices and nitrogen concentration of plants or plant parts (e.g. studies #8, #9). In comparison, Cao et al. (2013a) compared spectral indices against the nitrogen nutrition index, thereby effectively separating crop biomass and nitrogen status (study #4). If the aim is to use rapid measurement tools to assess crop nitrogen status, tests and calibrations should be better performed using the nitrogen nutrition index as the reference. Nitrogen use efficiency, and its physiological and agronomic components (Section 3), is a target trait for both agronomic and genetic improvement (Appendix A). Janssen et al., 1990 emphasised that the relationship between yield and nitrogen uptake is bounded between two lines representing maximum dilution and maximum accumulation. Maximum dilution results from poor nitrogen availability in relation to other growth factors and corresponds to maximum yield per unit nitrogen uptake, whereas maximum accumulation results from nitrogen abundance in relation to other growth factors and corresponds to the lowest yield per unit nitrogen uptake. This is reflected in a strong, inverse relationship between yield per unit nitrogen uptake and grain protein concentration (Cassman et al., 2002; Sadras, 2006; Lemaire and Gastal, 2009). The relationship between yield and nutrient uptake is a key element in the framework of Janssen et al., 1990 to quantify soil fertility using crop yield as a yardstick, and the recent work of Xu et al. (2013) illustrates its application in maize cropping systems of China (study #25, Appendix A). The simultaneous consideration of N, P, and K is an important attribute of this model as soils with low fertility – particularly in the tropics – generally lack all three macronutrients. Physiological questions on the assimilation and allocation of reduced and inorganic nitrogen among plant parts cannot be solved with a single perspective. Depending on the level of organisation of interest (Sadras and Richards, 2014), target traits range from gene expression to crop partitioning coefficients. Ben Slimane et al. (2013) investigated the physiological regulation of nitrogen mobilisation from wheat vegetative organs to grain and measured a set of traits including nitrogen related metabolites (proteins, amino acids, nitrate), activity of key enzymes (glutamine synthetase, glutamate dehydrogenase, nitrate reductase, endoprotease) and nitrogen content in shoot components. This work compared wheat with low and high nitrogen supply. However, instead of a nominal characterisation, the authors referred their treatments to the nitrogen nutrition index measured at Zadocks GS57, i.e. NNI = 0.5 vs 0.8 (study #2). This accurate and unequivocal characterisation of timing and intensity of nitrogen deficit allows for both the repetition of the experiments under similar conditions and comparisons with other studies where the nitrogen status is different but properly characterised with comparable metrics. 5. Accounting for the allometry of crop biomass and nitrogen uptake Section 2 outlined the allometric relationship between nitrogen concentration and biomass leading to the concepts of dilution

59

curves and nitrogen nutrition index and Section 3 the standard partitioning of nitrogen use efficiency components, highlighting the confounded effects in nitrogen uptake efficiency when the allometric relationship between nitrogen uptake and biomass is ignored. The previous section presented examples of common approaches to investigate aspects of crop nitrogen economy. In most cases, the allometric relationships between nitrogen and biomass are overlooked. Indeed, studies where results are analysed in terms of nominal treatment effects are not uncommon (Appendix A). This often means that no links are established between outcomes (e.g. crop yield, grain protein concentration) and crop nitrogen status. Whilst there is value in nominally identifying superior practices or varieties, scientific progress requires explanations, which in turn require adequate assessment of crop nitrogen status. Furthermore, agricultural practices can have direct effects on crop nitrogen status (e.g. N fertilizer application) and indirect effects mediated by changes in biomass (e.g. irrigation, sowing date) which can be separated using allometric tools such as the nitrogen nutrition index (Section 2, Box 1). Here, we illustrate the application of allometric concepts in the assessment and interpretation of crop responses to agronomic practices and comparisons of cultivars. 5.1. Assessment of agronomic practices The response of crop yield to nitrogen supply is critical for the management of fertiliser, and for other practices (e.g. stubble retention) which could modify the relative supply and demand of nitrogen. A common approach for studying the effect of nitrogen supply on crop yield is based on yield response curves. This approach has two main limitations. First, total nitrogen available for the crop depends on initial soil supply, mineralisation during the growing season, and additional inputs including fertiliser and rainfall (Angus, 2001). Quantification of all these components is difficult. Mineralisation rates are modulated by soil temperature and moisture, and are highly variable in space and time (Sadras and Baldock, 2003). Moreover, the actual amount of mineral nitrogen in the root zone is not necessarily fully available to crops, as uptake is influenced by many factors including biological, chemical and physical soil attributes (Gill et al., 2008; Dunbabin et al., 2009; Richardson et al., 2009) and supply of water and other nutrients (Janssen et al., 1990; Sadras et al., 2012a). Second, other environmental and genetic factors influence crop yield in addition to nitrogen. Multiple sources of variation lead to a diversity of response curves; hence, impairing both understanding and predictive capacity. The perspective of yield response curves is, therefore, constrained to empirical statistical models with poor capacity for extrapolation. Some of these problems can be overcome by relating actual yield (Yactual) relative to attainable yield in N-sufficient crops (Ymax) and NNI. Direct quantification of the crop nitrogen status removes the need to explicitly account for soil nitrogen availability; the NNI integrates nitrogen supply and demand accounting for biomass-dependent changes in nitrogen concentration. Third, the Yactual/Ymax ratio can be calculated using experimentally or modelled Ymax; this type of yield normalisation is common in the assessment and management of crop responses to water (Doorenbos and Pruit, 1977; Steduto et al., 2012). Thus, the relationship between Yactual/Ymax and NNI is a more generic representation of crop response to nitrogen deficiency. Fig. 4 shows the relationship between the relative accumulation of biomass (Wactual/Wmax) and the NNI for swards of tall fescue grown at different seasons and with a large range of nitrogen fertilisation rates. For each season and nitrogen supply, sward regrowth was analysed through weekly sampling for determination of both crop biomass and plant nitrogen concentration and

60

V.O. Sadras, G. Lemaire / Field Crops Research 164 (2014) 54–64

Fig. 4. Relationship between the relative biomass accumulation (Wactual/Wmax) and the nitrogen status of tall fescue swards growing with large range of N fertiliser rates at different seasons. Sward nitrogen status is quantified as: (a) instantaneous NNI determined weekly during each regrowth period according to Eq. (3); (b) integrated NNI as the P weighted mean of instantaneous NNI from the start of growth until the date of sampling: Integrated NNI = 1/D NNIi.di with D, the number of days from the start of regrowth, NNIi the NNI determined at each sampling i and di the interval between two successive samplings. For this integration the values of NNIi are limited to one; (c) integrated NNI’ according to Eq. (B8) with Ns = 0.7. Inset illustrates the integration method. Adapted from Lemaire and Gastal (1997).

then NNI calculation [Eq. (3)]. The relationship between NNI at each sampling and the relative herbage biomass is clearly nonlinear, with biomass response reaching a plateau as NNI approaches 1 (Fig. 4a). When NNI is calculated as the weighted mean of sequential samplings from the start of regrowth, the relationship becomes linear (Fig. 4b). The reason for this difference is that soil nitrogen availability tends to decrease as sward nitrogen uptake progress, and NNI declines with time of regrowth. So, the NNI at each sampling date is an exaggeration of the severity of the overall N deficiency experienced by swards since the start of the regrowth period. This exaggeration is more important for intermediate nitrogen rates where fertiliser is applied at the start of regrowth whilst the distortion is smaller for unfertilised treatments. So, the time course of NNI during the growing season could be as important as knowledge of its final value at harvest. The integrated NNI’ accounting’ for nitrogen concentration linked to structural biomass [Eq. (B5)], returns a relationship with Wactual/ Wmax which is close to the y = x line; thus, indicating a strict proportionality (Fig. 4c). For wheat and maize, the integrated NNI was also used to analyse the effect of both severity and timing of nitrogen deficiency on grain yield and its components, biomass and harvest index, grain number and size (Plénet and Cruz, 1997; Jeuffroy and Bouchard, 1999). Ciampitti et al., 2012 developed a phenotyping framework to predict nitrogen uptake, nitrogen use efficiency and yield of maize. Using a four-step physiological perspective, they link (i) ear-leaf greenness (measured with SPAD) with leaf nitrogen concentration, (ii) leaf nitrogen concentration with nitrogen nutrition index, and nitrogen nutrition index with both (iii) crop nitrogen uptake and (iv) grain yield. Their framework relies on a robust nitrogen dilution curve and rests on the nitrogen nutrition index to capture the main agronomic levers for the maize crop, namely, sowing density and rate of nitrogen fertiliser rate.

5.2. Comparison of wheat cultivars and maize hybrids Table 2 illustrates the dramatic changes in nitrogen-related traits of cereals resulting from selection for yield and agronomic adaptation. In study 1, Haegele et al. (2013) compared maize hybrids released in the USA between 1967 and 2006. Selection for yield consistently improved nitrogen use efficiency, nitrogen uptake efficiency, yield per unit nitrogen uptake in unfertilised checks and reduced protein concentration at the highest rate of fertilisation only (Table 2). They reported no clear trends in stover biomass yield between hybrids representing different eras, and increasing higher harvest index with year of hybrid release, indicative of increased total biomass at harvest. The links between nitrogen related traits and total biomass were not explored. In study 2, Foulkes et al. (1998) compared British winter wheat varieties capturing the period 1969–1988. Most traits increased with year of cultivar release except grain nitrogen offtake in unfertilised crops which declined with year of cultivar release (Table 2). Further experiments showed that shoot biomass of British winter wheat increased with year of cultivar release between 1972 and 1995 (Shearman et al., 2005); hence, the confounded effect of breeding on biomass and nitrogen traits. In study 3, Sadras and Lawson (2013) compared Australian wheats released between 1958 and 2007. Selective pressure for yield in the water and nitrogen scarce environments of Australia, increased N uptake and N uptake per unit soil N increased with year of release. Shoot biomass also increased (Sadras et al., 2012b), and a positive correlation between NNI and year of release, unequivocally demonstrated an improvement in the nitrogen status of crops irrespective of biomass.

V.O. Sadras, G. Lemaire / Field Crops Research 164 (2014) 54–64

61

Table 2 Examples of changes in nitrogen related traits of cereals in response to selection for yield and agronomic adaptation. Studya

Trait

Response

1

Nitrogen use efficiency Nitrogen uptake efficiency Yield per unit N uptake in unfertilised crops Plant N content at silking Plant N content at physiological maturity Grain N concentration Grain N offtake in unfertilised crops Optimum amount of N fertiliser Grain N offtake with optimum amount of N fertiliser Apparent N fertiliser recovery Crop yield per unit N offtake in unfertilised crops N uptake N uptake per unit soil N Nitrogen nutrition index Grain N concentration

Increased with year of release Increased with year of release Increased with year of release Unchanged Increased with year of release at 67 and 252 kg ha1 but not in unfertilised crop Decreased with year of cultivar release at 252 kg N ha1 but not with lower N supply Decreased with year of release Increased with year of release Increased with year of release

2

3

Increased with year of release Increased with year of release Increased with year of release Increased with year of release Increased with year of release Decreased with year of release under conditions favouring high (>12%) but not low grain protein concentration

a Study 1: American, single-cross maize hybrids released between 1967 and 2006; three rates of N (0, 67 and 252 kg ha1) in two seasons (Haegele et al., 2013); study 2: British wheat varieties released between 1969 and 1988; 22 sites/seasons (Foulkes et al., 1998); study 3: Australian wheat varieties released between 1958 and 2007; 5–7 environments from combination of season/location and nitrogen supply (Sadras and Lawson, 2013).

6. Conclusion Nitrogen nutrition of crops is important and attracts considerable research resources. However, many studies still report results in terms of nominal treatments, e.g. high vs low nitrogen, which are uninformative; curves relating yield and fertiliser rate, which are of local interest but provide little insight on the underlying processes and have low generic value; and nitrogen-related traits that are incomplete or inadequate to quantify crop nutrition status. Often, the allometric relationships between nitrogen and biomass are overlooked. In some cases, the relevant component traits, i.e. biomass and nitrogen uptake or concentration, are measured but

not analysed in the proper allometric framework. In some cases, e.g. typical studies of nitrogen use efficiency in field crops, traits are measured only at maturity. Little additional effort including additional sampling during critical stages before grain fill and analysis of data in terms of dilution curves and nitrogen nutrition index would greatly increase the return from research investment. Acknowledgement VOS research is supported by the Grains Research and Development Corporation of Australia.

Appendix A Crop or plant nitrogen traits used in a sample of publications. Papers published in Field Crops Research and Crop and Pasture Science in 2013 were screened for nitrogen in the title; reviews, modelling papers and studies in legumes were excluded. #

Focus

1.

N dilution curves in rice

2.

3. 4. 5.

6.

7.

8.

9.

10.

Crop or plant nitrogen traits

Comment

Shoot N concentration, NNI, accumulated N Differences in parameters of dilution curves deficit capture phenotypic differences between Indica and Japonica rice Compares crops with accurately defined N deficit Regulation of N mobilization from vegetative N related metabolites (proteins, amino organs to fill the wheat grain acids, nitrate) and enzymatic activities; N in in terms of timing (GS57) and intensity (NNI = 0.5 shoot components, NNI vs 0.8) Effect of management practice on the fate of N N uptake, N concentration in grain and Nominal treatment effects; no links between and NUE of rice; soil emphasis straw, apparent N recovery outcomes Estimate plant nitrogen status with 43 vegetation indices, plant N concentration, NNI correlates with spectral indices multispectral sensor N uptake, NNI Relationship between grain yield and N uptake, N uptake; NUE; internal efficiency (kg grain Yield vs nutrient uptake relationships used to and to estimate N (and also P and K) optimal per kg N uptake); reciprocal internal identify balanced, deficient and excessive supply requirements for a target yield efficiency (kg N in shoot per ton of grain); nitrogen harvest index Effect of seeding rate on yield and NUE Absorbed N from fertiliser and soil, shoot N Detailed dissection of components of NUE at uptake, N uptake efficiency; N utilisation harvest efficiency; NUE; nitrogen harvest index; grain N concentration Nominal treatment effects Effects of tillage, crop residue and N rate on yield and water productivity of irrigated cotton, winter wheat and maize; soil emphasis Estimate wheat leaf N content and leaf mass per Leaf N content, leaf N per unit area Combination of leaf N content and leaf mass per unit area with near-infrared spectroscopy unit area permitted predict leaf nitrogen per unit area N uptake of shoot parts (stem, leaf, ear) and Spectral index correlates with ear N uptake and N Spectral high-throughput assessment of sources and sinks during grain filling of wheat N partitioning coefficient; grain N partitioning (but one season, six cultivars) cultivars concentration Functional response to N deficit of C3 and C4 Specific leaf nitrogen; shoot N concentration Published dilution curves are used to benchmark crops effects of N rates during crop season; NNI is not reported and some traits (e.g. radiation use efficiency) are presented against nominal N rates

Source Ata-Ul-Karim et al. (2013) Ben Slimane et al. (2013) Cao et al. (2013b) Cao et al. (2013a) Chuan et al. (2013)

Dai et al. (2013)

Devkota et al. (2013) Ecarnot et al. (2013) Erdle et al. (2013) Fletcher et al. (2013)

62

V.O. Sadras, G. Lemaire / Field Crops Research 164 (2014) 54–64

Appendix A (Continued) (Continued) #

Focus

Crop or plant nitrogen traits

11.

Effect of controlled-release urea and subsoiling on maize yield, nitrogen and water use efficiency; soil emphasis Rice tillering response to plant density and nitrogen rate Estimate tobacco leaf nitrogen concentration with hyperspectral reflectance Field performance of Bt rice in response to nitrogen rate Soil emphasis including microbial biomass and profiles of soil N Effect of site-specific nitrogen management and alternate wetting and drying irrigation on rice yield, nitrogen and water use efficiencies Effects of the tillage system on N rhizodeposition in wheat; soil emphasis

N uptake (total, and partitioned between Nominal treatment effects grain and straw), N uptake efficiency, nitrate reductase activity Nominal treatment effects N uptake, shoot N concentration

12. 13. 14. 15. 16.

17.

18.

21.

Maize accumulation and partitioning of dry matter, N, P and K after silking Management effects on N use efficiency and yield of rice Sorghum cultivar, row spacing and nitrogen rate interactions Effect of N management on rice yield and NUE

22.

Spectral quantification of rice N status

23.

Effects of nitrogen and water supply on wheat water use efficiency and carbon isotope discrimination Effect of N rate and site on camelina yield and NUE Relationship between grain yield and nutrient accumulation

19. 20.

24. 25.

26. 27.

28. 29. 30.

31.

Effects of N and water management on rice yield, water and N use efficiency End-of-season maize stalk nitrate as indicator of N status Effect of mid-season N application on t rice yield and NUE Effect of N, water and agronomic management on rice yield and NUE Effect of S supply on amino acid composition and concentrations of total S, total N, sulphateS, nitrate-N, and soluble protein in the leaves of tropical pastures Dry matter and N accumulation, partitioning, translocation in oilseed rape

32.

Yield responses to N, P, K, or S fertiliser

33.

Yield responses to N fertiliser

34.

Fallow management effects on N, water and wheat yield

35.

Comment

Leaf nitrogen concentration NUE and its components

Nominal treatment effects

NUE

Nominal treatment effects

N partial factor productivity (yield/N rate); internal N use efficiency (yield/N uptake)

Nominal treatment effects

Source Hu et al. (2013)

Huang et al. (2013) Jia et al. (2013) Jiang et al. (2013) Liang et al. (2013) Liu et al. (2013)

amount of N derived from rhizodeposition; Plant leaves were labelled with 15N to estimate the Muñozamount of N transferred to root and soil N, N uptake in plant parts Romero et al. (2013) Ning et al. N concentration and changes in N content in Comparison of old and new varieties plant organs pre- and post-silking (2013) N content in crop parts; nitrogen use Nominal treatment effects Qin et al. efficiency and its components (2013) Nominal treatment effects Sawargaonkar NUE et al. (2013) NUE and its components Nominal treatment effects Sui et al. (2013) N content Spectral indices correlate with both crop size Wang et al. (biomass, leaf area index) and N content (2013a) Straw and grain N content Nominal treatment effects; correlations between Wang et al. N content and both water use efficiency and (2013b) carbon isotope discrimination NUE Nominal treatment effects Wysocki et al. (2013) N in straw, grain, and N-harvest index; NUE QUEFTS (quantitative evaluation of the fertility of Xu et al. (2013) and components tropical soils) approach to investigate N–P–K in farmers fields Nominal treatment effects; correlations between Ye et al. (2013) NUE and components traits Zhang et al. N uptake and translocation, nitrate Linear + plateau relationships of N uptake and concentration in stalk grain yield vs N availability but linear relationship (2013a) with stalk nitrate Nominal treatment effects Zhang et al. NUE and components (2013b) Nominal treatment effects Zhao et al. NUE and components (2013) Schmidt et al. Total N, nitrate-N, N:S ratio Relationships between S supply and total N, nitrate-N, N:S ratio, soluble amino acids, soluble (2013) protein; relationship between biomass and N:S ratio Papantoniou Post-anthesis N translocation, contribution Seasonal dynamics of N accumulation and of pre-anthesis N to pod N; seed weight per partitioning et al. (2013) unit N uptake; nitrogen harvest index Soil focus; no crop N traits Soil nutrient–yield relationships Watmuff et al. (2013) Soil focus; no crop N traits Soil nutrient–yield relationships Bell et al. (2013) Effects of weed control on storage of N and water Hunt et al. Grain protein; soil focus for nitrogen in soil (2013) N uptake and related traits, e.g uptake per Changed root phenotype and improved nutrient Ma et al. unit root lenght uptake with banded placement of fertiliser (2013) 15

References Angus, J.F., 2001. Nitrogen supply and demand in Australian agriculture. Aus. J. Exp. Agric. 41, 277–288. Ata-Ul-Karim, S.T., Yao, X., Liu, X., Cao, W., Zhu, Y., 2013. Development of critical nitrogen dilution curve of Japonica rice in Yangtze River Reaches. Field Crops Res. 149, 149–158. Belanger, G., Walsh, J.R., Richards, J.E., Milburn, P.H., Ziadi, N., 2001. Critical nitrogen curve and nitrogen nutrition index for potato in eastern Canada. Am. J. Potato Res. 78, 355–364. Belder, P., Bouman, B.A.M., Spiertz, J.H.J., Peng, S., Castañeda, A.R., Visperas, R.M., 2005. Crop performance, nitrogen and water use in flooded and aerobic rice. Plant Soil 273, 167–182.

Bell, M.J., Strong, W., Elliott, D., Walker, C., 2013. Soil nitrogen — crop response calibration relationships and criteria for winter cereal crops grown in Australia. Crop Past Sci. 64, 442–460. Ben Slimane, R., Bancal, P., Bancal, M.-O., 2013. Down-regulation by stems and sheaths of grain filling with mobilized nitrogen in wheat. Field Crops Res. 140, 59–68. Cao, Q., Miao, Y., Wang, H., Huang, S., Cheng, S., Khosla, R., Jiang, R., 2013a. Nondestructive estimation of rice plant nitrogen status with crop circle multispectral active canopy sensor. Field Crops Res. 154, 133–144. Cao, Y., Tian, Y., Yin, B., Zhu, Z., 2013b. Assessment of ammonia volatilization from paddy fields under crop management practices aimed to increase grain yield and N efficiency. Field Crops Res. 147, 23–31. Cassman, K.G., Dobermann, A., Walters, D.T., 2002. Agroecosystems, nitrogen-use efficiency, and nitrogen management. Ambio 31, 132–140. Chuan, L., He, P., Jin, J., Li, S., Grant, C., Xu, X., Qiu, S., Zhao, S., Zhou, W., 2013. Estimating nutrient uptake requirements for wheat in China. Field Crops Res. 146, 96–104.

V.O. Sadras, G. Lemaire / Field Crops Research 164 (2014) 54–64 Ciampitti, I.A., Zhang, H., Friedemann, P., Vyn, T.J., 2012. Potential physiological frameworks for mid-season field phenotyping of final plant nitrogen uptake, nitrogen use efficiency, and grain yield in maize. Crop Sci. 52, 2728–2742. 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. Connor, D.J., Mínguez, M.I., 2012. Evolution not revolution of farming systems will best feed and green the world. Global Food Secur. 1, 106–113. Dai, X., Zhou, X., Jia, D., Xiao, L., Kong, H., He, M., 2013. Managing the seeding rate to improve nitrogen-use efficiency of winter wheat. Field Crops Res. 154, 100–109. Debaeke, P., van Oosterom, E.J., Justes, E., Champolivier, L., Merrien, A., Aguirrezabal, L.A.N., Gonzalez-Dugo, V., Massignam, A.M., Montemurro, F., 2012. A speciesspecific critical nitrogen dilution curve for sunflower (Helianthus annuus L.). Field Crops Res. 136, 76–84. Devienne-Barret, F., Justes, E., Machet, J.M., Mary, B., 2000. Integrated control of nitrate uptake by crop growth rate and soil nitrate availability under field conditions. Ann. Bot. 86, 995–1005. Devkota, M., Martius, C., Lamers, J.P.A., Sayre, K.D., Devkota, K.P., Gupta, R.K., Egamberdiev, O., Vlek, P.L.G., 2013. Combining permanent beds and residue retention with nitrogen fertilization improves crop yields and water productivity in irrigated arid lands under cotton, wheat and maize. Field Crops Res. 149, 105–114. Doorenbos, J., Pruit, W.O., 1977. Crop water requeriments. FAO Irrigation and Drainage. FAO, Rome p. 24. Dunbabin, V.M., Armstrong, R.D., Officer, S.J., Norton, R.M., 2009. Identifying fertiliser management strategies to maximise nitrogen and phosphorus acquisition by wheat in two contrasting soils from Victoria, Australia. Aust. J. Soil Res. 47, 74–90. Durand, J.-L., Gonzalez-Dugo, V., Gastal, F., 2010. How much do water deficits alter the nitrogen nutrition status of forage crops? Nutr. Cycl. Agroecosyst. 88, 231–243. Duru, M., Lemaire, G., Cruz, P., 1997. The nitrogen requirement of major agricultural crops: grasslands. In: Lemaire, G. (Ed.), Diagnosis of the Nitrogen Status in Crops. Springer-Verlag, Helideberg. Ecarnot, M., Compan, F., Roumet, P., 2013. Assessing leaf nitrogen content and leaf mass per unit area of wheat in the field throughout plant cycle with a portable spectrometer. Field Crops Res. 140, 44–50. Ekbladh, G., Witter, E., 2010. Determination of the critical nitrogen concentration of white cabbage. Eur. J. Agron. 33, 276–284. Erdle, K., Mistele, B., Schmidhalter, U., 2013. Spectral high-throughput assessments of phenotypic differences in biomass and nitrogen partitioning during grain filling of wheat under high yielding Western European conditions. Field Crops Res. 141, 16–26. Errecart, P.M., Agnusdei, M.G., Lattanzi, F.A., Marino, M.A., Berone, G.D., 2014. Critical nitrogen concentration declines with soil water availability in tall fescue. Crop Sci. 54, 318–330. Fletcher, A.L., Johnstone, P.R., Chakwizira, E., Brown, H.E., 2013. Radiation capture and radiation use efficiency in response to N supply for crop species with contrasting canopies. Field Crops Res. 150, 126–134. Forde, B.G., 2002. The role of long distance signalling in plant responses to nitrate and other nutrients. J. Exp. Bot. 53, 39–43. Foulkes, M.J., Sylvester-Bradley, R., Scott, R.K., 1998. Evidence for differences between winter wheat cultivars in acquisition of soil mineral nitrogen and uptake and utilization of applied fertilizer nitrogen. J. Agric. Sci. 130, 29–44. Gill, J.S., Sale, P.W.G., Tang, C., 2008. Amelioration of dense sodic subsoil using organic amendments increases wheat yield more than using gypsum in a high rainfall zone of southern Australia. Field Crops Res. 107, 265–275. Gonzalez-Dugo, V., Durand, J.-L., Gastal, F., 2010. Water deficit and nitrogen nutrition of crops. A review. Agron. Sustainable Dev. 30, 529–544. Gonzalez-Dugo, V., Durand, J.L., Gastal, F., Bariac, T., Poincheval, J., Bardou, G., Biron, P., Cousson, L., Eprinchard, A., Millet, G., Richard, P., Terrasson, J.P., 2012. Restricted root-to-shoot translocation and decreased sink size are responsible for limited nitrogen uptake in three grass species under water deficit. Environ. Exp. Bot. 75, 258–267. Gonzalez-Dugo, V., Durand, J.L., Gastal, F., Picon-Cochard, C., 2005. Short-term response of the nitrogen nutrition status of tall fescue and Italian ryegrass swards under water deficit. Aust. J. Agric. Res 56, 1269–1276. Grassini, P., Cassman, K.G., 2012. High-yield maize with large net energy yield and small global warming intensity. Proc. Natl. Acad. Sci. U. S. A. 109, 1074–1079. Greenwood, D.J., Lemaire, G., Gosse, G., Cruz, P., Draycott, A., Neeteson, J.J., 1990. Decline in percentage N of C3 and C4 crops with increasing plant mass. Ann. Bot. 66, 425–436. Grindlay, D.J.C., 1997. Towards an explanation of crop nitrogen demand based on the optimization of leaf nitrogen per unit leaf area. J. Agric. Sci. 128, 377–396. Grindlay, D.J.C., Sylvester-Bradley, R., Scott, R.K., 1993. Nitrogen uptake of young vegetative plants in relation to green area. J. Sci. Food Agric. 63, 116. Haegele, J.W., Cook, K.A., Nichols, D.M., Below, F.E., 2013. Changes in nitrogen use traits associated with genetic improvement for grain yield of maize hybrids released in different decades. Crop Sci. 53, 1256–1268. Hirel, B., Lemaire, G., 2005. From agronomy and ecophysiology to molecular genetics for improving nitrogen use efficiency in crops. J. Crop Improv. 15, 213–257. Hu, H., Ning, T., Li, Z., Han, H., Zhang, Z., Qin, S., Zheng, Y., 2013. Coupling effects of urea types and subsoiling on nitrogen–water use and yield of different varieties of maize in northern China. Field Crops Res. 142, 85–94. Huang, M., Yang, C., Ji, Q., Jiang, L., Tan, J., Li, Y., 2013. Tillering responses of rice to plant density and nitrogen rate in a subtropical environment of southern China. Field Crops Res. 149, 187–192.

63

Hunt, J.R., Browne, C., McBeath, T.M., Verburg, K., Craig, S., Whitbread, A.M., 2013. Summer fallow weed control and residue management impacts on winter crop yield though soil water and N accumulation in a winter-dominant, low rainfall region of southern Australia. Crop Past Sci. 64, 922–934. Janssen, B.H., Guiking, F.C.T., Vandereijk, D., Smaling, E.M.A., Wolf, J., Vanreuler, H., 1990. A system for quantitative-evaluation of the fertility of tropical soils (QUEFTS). Geoderma 46, 299–318. Jeuffroy, M.H., Bouchard, C., 1999. Intensity and duration of nitrogen deficiency on wheat grain number. Crop Sci. 39, 1385–1393. Jia, F., Liu, G., Liu, D., Zhang, Y., Fan, W., Xing, X., 2013. Comparison of different methods for estimating nitrogen concentration in flue-cured tobacco leaves based on hyperspectral reflectance. Field Crops Res. 150, 108–114. Jiang, Y., Huang, S., Cai, M., Li, C., Kong, X., Zhang, F., Mohamed, I., Cao, C., 2013. Yield changes of Bt-MH63 with cry1C* or cry2A* genes compared with MH63 (Oryza sativa) under different nitrogen levels. Field Crops Res. 151, 101–106. Justes, E., Mary, B., Meynard, J.M., Machet, J.M., Thelierhuche, L., 1994. Determination of a critical nitrogen dilution curve for winter wheat crops. Ann. Bot. 74, 397–407. Kim, K.I., Clay, D.E., Carlson, C.G., Clay, S.A., Trooien, T., 2008. Do synergistic relationships between nitrogen and water influence the ability of corn to use nitrogen derived from fertilizer and soil? Agron. J. 100, 551–556. Kirchmann, H., Bergström, L., 2008. Organic Crop Production – Ambitions and Limitations. Springer. Lejay, L., Tillard, P., Lepetit, M., Olive, F.D., Filleur, S., Daniel-Vedele, F., Gojon, A., 1999. Molecular and functional regulation of two NO3- uptake systems by Nand C-status of Arabidopsis plants. Plant J. 18, 509–519. Lemaire, G., Avice, J.C., Kim, T.H., Ourry, A., 2005. Developmental changes in shoot N dynamics of lucerne (Medicago sativa L.) in relation to leaf growth dynamics as a function of plant density and hierarchical position within the canopy. J. Exp. Bot. 56, 1437. Lemaire, G., Charrier, X., Hebert, Y., 1996. Nitrogen uptake capacities of maize and sorghum crops in different nitrogen and water supply conditions. Agronomie 16, 231–246. Lemaire, G., Cruz, P., Gosse, G., Chartier, M., 1985. Etude des relations entre la dynamique de prélèvement dazote et le dynamique de croissance en matière sèche dun peuplement de luzerne (Medicago sativa L.). Agronomie 5, 685–692. Lemaire, G., Gastal, F., 1997. N uptake and distribution in plant canopies. In: Lemaire, G. (Ed.), Diagnosis of the Nitrogen Status in Crops. Springer-Verlag, Heildeberg, pp. 3–41. Lemaire, G., Gastal, F., 2009. Quantifying crop responses to nitrogen deficiency and avenues to improve nitrogen-use efficiency. In: Sadras, V.O., Calderini, D.F. (Eds.), Crop Physiology: Applications for Genetic Improvement and Agronomy. Academic Press, San Diego, pp. 171–211. Lemaire, G., Jeuffroy, M.-H., Gastal, F., 2008. Diagnosis tool for plant and crop N status in vegetative stage theory and practices for crop N management. Eur. J. Agron. 28, 614–624. Lemaire, G., Salette, J., 1984a. Relation entre dynamique de croissance et dynamique de prélèvement dazote pour un peuplement de graminées fourragères. I Etude de leffet du milieu. Agronomie 4, 423–430. Lemaire, G., Salette, J., 1984b. Relation entre dynamique de croissance et dynamique de prélèvement dazote pour un peuplement de graminées fourragères. II Etude de la variabilité entre genotypes. Agronomie 4, 431–436. Lemaire, G., van Oosterom, E., Sheehy, J., Jeuffroy, M.H., Massignam, A., Rossato, L., 2007. Is crop N demand more closely related to dry matter accumulation or leaf area expansion during vegetative growth? Field Crops Res. 100, 91– 106. Liang, B., Zhao, W., Yang, X., Zhou, J., 2013. Fate of nitrogen-15 as influenced by soil and nutrient management history in a 19-year wheat–maize experiment. Field Crops Res. 144, 126–134. Liu, L., Chen, T., Wang, Z., Zhang, H., Yang, J., Zhang, J., 2013. Combination of sitespecific nitrogen management and alternate wetting and drying irrigation increases grain yield and nitrogen and water use efficiency in super rice. Field Crops Res. 154, 226–235. Ma, Q., Tang, H., Rengel, Z., Shen, J., 2013. Banding phosphorus and ammonium enhances nutrient uptake by maize via modifying root spatial distribution. Crop Past Sci. 64, 965–975. Moll, R.H., Kamprath, E.J., Jackson, W.A., 1982. Analysis and interpretation of factors which contribute to efficiency of nitrogen-utilization. Agron. J. 74, 562–564. Muñoz-Romero, V., López-Bellido, R.J., Redondo, R., López-Bellido, L., 2013. Nitrogen rhizodeposition by wheat under different tillage systems in a rainfed Vertisol. Field Crops Res. 144, 148–153. Ney, B., Doe, T., Sagan, M., 1997. The nitrogen requirement of major agricultural crops: grains legumes. In: Lemaire, G. (Ed.), Diagnosis of the Nitrogen Status in Crops. Springer-Verlag, Heildeberg, pp. 107–117. Niklas, K.J., 1994. Plant Allometry: The Scaling of Form and Process. University of Chicago Press, Chicago. Ning, P., Li, S., Yu, P., Zhang, Y., Li, C., 2013. Post-silking accumulation and partitioning of dry matter, nitrogen, phosphorus and potassium in maize varieties differing in leaf longevity. Field Crops Res. 144, 19–27. Pandey, R.K., Maranville, J.W., Admou, A., 2000. Deficit irrigation and nitrogen effects on maize in a Sahelian environment I. Grain yield and yield components. Agric. Water Manage. 46, 1–13. Papantoniou, A.N., Tsialtas, J.T., Papakosta, D.K., 2013. Dry matter and nitrogen partitioning and translocation in winter oilseed rape (Brassica napus L.) grown under rainfed mediterranean conditions. Crop Past Sci. 64, 115–122.

64

V.O. Sadras, G. Lemaire / Field Crops Research 164 (2014) 54–64

Plénet, D., Cruz, P., 1997. The nitrogen requirement of major agricultural crops: grasslands. In: Lemaire, G. (Ed.), Diagnosis of the Nitrogen Status in Crops. Springer-Verlag, Heildeberg, pp. 93–106. Plénet, D., Lemaire, G., 1999. Relationships between dynamics of nitrogen uptake and dry matter accumulation in maize crops. Determination of critical N concentration. Plant Soil 216, 65–82. Qin, J., Impa, S.M., Tang, Q., Yang, S., Yang, J., Tao, Y., Jagadish, K.S.V., 2013. Integrated nutrient, water and other agronomic options to enhance rice grain yield and N use efficiency in double-season rice crop. Field Crops Res. 148, 15–23. Richardson, A.E., Barea, J.M., McNeill, A.M., Prigent-Combaret, C., 2009. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321, 305–339. Rockström, J., Barron, J., Brouwer, J., Galle, S., DeRouw, A., 1999. On-farm spatial and temporal variability of soil and water in pearl millet cultivation. Soil Sci. Am. J. 63, 1308–1319. Rockström, J., deRouw, A., 1997. Water, nutrients and slope position in on-farm pearl millet cultivation in the Sahel. Plant Soil 195, 311–327. Sadras, V.O., 2006. The N:P stoichiometry of cereal, grain legume and oilseed crops. Field Crops Res. 95, 13–29. Sadras, V.O., Baldock, J., Cox, J., Bellotti, B., 2004. Crop rotation effect on wheat grain yield as mediated by changes in the degree of water and nitrogen co-limitation. Aust. J. Agric. Res 55, 599–607. Sadras, V.O., Baldock, J.A., 2003. Influence of size of rainfall events on water-driven processes. II. Soil nitrogen mineralisation in a semi-arid environment. Aust. J. Agric. Res 54, 353–361. Sadras, V.O., Lawson, C., 2013. Nitrogen and water-use efficiency of Australian wheat varieties released between 1958 and 2007. Eur. J. Argon. 46, 34–41. Sadras, V.O., Lawson, C., Hooper, P., McDonald, G.K., 2012a. Contribution of summer rainfall and nitrogen to the yield and water use efficiency of wheat in mediterranean-type environments of south Australia. Eur. J. Agron. 36, 41–54. Sadras, V.O., Lawson, C., Montoro, A., 2012b. Photosynthetic traits of Australian wheat varieties released between 1958 and 2007. Field Crops Research 134, 19– 29. Sadras, V.O., Richards, R.A., 2014. Improvement of crop yield in dry environments: benchmarks, levels of organisation and the role of nitrogen. J. Exp. Bot. 65, 1981– 1995. Sadras, V.O., Rodriguez, D., 2010. Modelling the nitrogen-driven trade-off between nitrogen utilisation efficiency and water use efficiency of wheat in eastern Australia. Field Crops Res. 118, 297–305. Sadras, V.O., Roget, D.K., 2004. Production and environmental aspects of cropping intensification in a semiarid environment of southeastern Australia. Agron. J. 96, 236–246. Sassenrath, G.F., Schneider, J.M., Gaj, R., Grzebisz, W., Halloran, J.M., 2013. Nitrogen balance as an indicator of environmental impact: toward sustainable agricultural production. Renew. Agric. Food Syst. 28, 276–289. Sawargaonkar, G.L., Patil, M.D., Wani, S.P., Pavani, E., Reddy, B.V.S.R., Marimuthu, S., 2013. Nitrogen response and water use efficiency of sweet sorghum cultivars. Field Crops Res. 149, 245–251.

Schmidt, F., De Bona, F.D., Monteiro, F.A., 2013. Sulfur limitation increases nitrate and amino acid pools in tropical forages. Crop Past Sci. 64, 51–60. Shearman, V.J., Sylvester-Bradley, R., Scott, R.K., Foulkes, M.J., 2005. Physiological processes associated with wheat yield progress in the UK. Crop Sci. 45, 175–185. Sheehy, J.E., Dionora, M.J.A., Mitchell, P.L., Peng, S., Cassman, K.G., Lemaire, G., Williams, R.L., 1998. Critical nitrogen concentrations: implications for highyielding rice (Oryza sativa L.) cultivars in the tropics. Field Crops Res. 59, 31–41. Sinclair, T.R., Rufty, T.W., 2012. Nitrogen and water resources commonly limit crop yield increases, not necessarily plant genetics. Global Food Secur. 1, 94–98. Steduto, P., Hsiao, T.C., Fereres, E., Raes, D., 2012. Crop Yield Response to Water. FAO, Rome. Sui, B., Feng, X., Tian, G., Hu, X., Shen, Q., Guo, S., 2013. Optimizing nitrogen supply increases rice yield and nitrogen use efficiency by regulating yield formation factors. Field Crops Res. 150, 99–107. Tei, F., Benincasa, P., Guiducci, M., 2002. Critical nitrogen concentration in processing tomato. Eur. J. Agron. 18, 45–55. Tilman, D., Cassman, K.G., Pamela, A., Matson, P.A., Naylor, R., Polasky, S., 2002. Agricultural sustainability and intensive production practices. Nature Biotech. 418, 671–677. Wang, Y., Wang, D., Zhang, G., Wang, J., 2013a. Estimating nitrogen status of rice using the image segmentation of G-R thresholding method. Field Crops Res. 149, 33–39. Wang, Y., Zhang, X., Liu, X., Zhang, X., Shao, L., Sun, H., Chen, S., 2013b. The effects of nitrogen supply and water regime on instantaneous WUE, time-integrated WUE and carbon isotope discrimination in winter wheat. Field Crops Res. 144, 236– 244. Watmuff, G., Reuter, D.J., Speirs, S.D., 2013. Methodologies for assembling and interrogating N, P, K, and S soil test calibrations for Australian cereal, oilseed and pulse crops. Crop Past. Sci. 64, 424–434. Wysocki, D.J., Chastain, T.G., Schillinger, W.F., Guy, S.O., Karow, R.S., 2013. Camelina: seed yield response to applied nitrogen and sulfur. Field Crops Res. 145, 60–66. Xu, X., He, P., Pampolino, M.F., Chuan, L., Johnston, A.M., Qiu, S., Zhao, S., Zhou, W., 2013. Nutrient requirements for maize in China based on QUEFTS analysis. Field Crops Res. 150, 115–125. Ye, Y., Liang, X., Chen, Y., Liu, J., Gu, J., Guo, R., Li, L., 2013. Alternate wetting and drying irrigation and controlled-release nitrogen fertilizer in late-season rice. Effects on dry matter accumulation, yield, water and nitrogen use. Field Crops Res. 144, 212–224. Zhang, S., Yue, S., Yan, P., Qiu, M., Chen, X., Cui, Z., 2013a. Testing the suitability of the end-of-season stalk nitrate test for summer corn (Zea mays L.) production in China. Field Crops Res. 154, 153–157. Zhang, Z., Chu, G., Liu, L., Wang, Z., Wang, X., Zhang, H., Yang, J., Zhang, J., 2013b. Midseason nitrogen application strategies for rice varieties differing in panicle size. Field Crops Res. 150, 9–18. Zhao, G., Miao, Y., Wang, H., Su, M., Fan, M., Zhang, F., Jiang, R., Zhang, Z., Liu, C., Liu, P., Ma, D., 2013. A preliminary precision rice management system for increasing both grain yield and nitrogen use efficiency. Field Crops Res. 154, 23–30.