Benchmarking nitrogen utilisation efficiency in wheat for Mediterranean and non-Mediterranean European regions

Field Crops Research 241 (2019) 107573

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Benchmarking nitrogen utilisation efficiency in wheat for Mediterranean and non-Mediterranean European regions

T

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Roxana Savina, , Victor O. Sadrasb,c, Gustavo A. Slafera,d a

Department of Crop and Forest Sciences, University of Lleida - AGROTECNIO Center, Av. R. Roure 191, 25198, Lleida, Spain South Australian Research and Development Institute, Australia c School of Agriculture, Food and Wine, The University of Adelaide, Australia d ICREA (Catalonian Institution for Research and Advanced Studies), Spain b

A R T I C LE I N FO

A B S T R A C T

Keywords: Triticum Nitrogen use efficiency Grain yield Grain nitrogen concentration Protein

Water and temperature stress during critical periods of grain yield formation are distinctive of wheat crops in Mediterranean environments. However, nitrogen (N) availability may also constrain grain yields in these environments. Benchmarks of yield response to N uptake in Mediterranean conditions are lacking, and extrapolation from non-Mediterranean environments is not warranted. We hypothesised that under Mediterranean environments (1) maximum N uptake would be lower, thus the range of N uptake would be narrower, and (2) N utilisation efficiency (NUtE, yield per unit N uptake) would be reduced along the whole range of N uptake than under non-Mediterranean conditions. To test these hypotheses, we compiled published data of yield and N uptake from Mediterranean (n = 340) and non-Mediterranean environments (n = 563) of Europe. Wheat in Mediterranean environments had lower average grain yield (4.1 vs 7.1 Mg ha−1), lower average N uptake (131 vs 166 kg N ha−1), lower average NUtE (33 vs 47 kg grain kg N−1), and higher average grain N concentration (2.4 vs 1.8%) than crops in non-Mediterranean environments. Boundary functions relating yield and nitrogen uptake captured the lower yield of wheat along the whole range of N uptake as hypothesised; these functions could be used for benchmarking wheat crops in Mediterranean regions of Europe, and possibly other Mediterranean environments.

1. Introduction Water is a major limiting factor for cereal production in Mediterranean regions (López-Bellido, 1992; Loss and Siddique, 1994; Ryan et al., 2006, 2008) and worldwide (Fereres and Soriano, 2007). This explains the widespread interest in water use and water use efficiency of cereals (e.g. Passioura, 1977; Sadras and Rodriguez, 2007; Katerji et al., 2008; Cossani et al., 2012) with benchmarks relating yield and water use for many crops across regions (e.g. French and Schultz, 1984; Sadras and Angus, 2006; Grassini et al., 2009a, b; Rattalino Edreira et al., 2018). However, differences across regions primarily associated with evaporative demand are relevant for water use efficiency, i.e. yield per unit evapotranspiration (e.g. Sadras and Angus, 2006; Rattalino Edreira et al., 2018). Despite the dominant role of water stress, shortage of nitrogen (N) often limits crop yield globally (Sinclair and Rufty, 2012), as well as in Mediterranean regions like Australia (Passioura, 2002) and the Mediterranean Basin (Abeledo et al., 2008; Cossani et al., 2011; Sadras et al.,

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2016). The dual effect of water and nitrogen supply is captured in the concept of co-limitation (reviewed by Cossani and Sadras, 2018). Thus, insufficient N may constrain both water use and water use efficiency even in drought-prone regions (Cooper et al., 1987; Asseng et al., 2001; Sadras, 2002; Passioura, 2002; Sadras et al., 2004; Sadras and Roget, 2004; Cossani et al., 2012). Benchmarks for N are lagging (Hochman et al., 2013; Ravier et al., 2017; Hoogmoed et al., 2018), and therefore it is unclear whether regional effects on the relationship between yield and N are limited to N uptake or they extend to include effects on N utilisation efficiency (NUtE) defined as the ratio between yield and N uptake (Moll et al., 1982; Slafer et al., 1990). Analyses of NUtE are more common in wetter, cooler regions where N fertilisation is used more widely and at higher doses, and where excess reactive N is an environmental concern (Foulkes et al., 1998; Muurinen et al., 2006; Foulkes et al., 2009). Analyses of the relationship between yield and N uptake in Mediterranean conditions are less frequent. Therefore, benchmarking agronomic practices in Mediterranean conditions might need thresholds for

Corresponding author. E-mail address: [email protected] (R. Savin).

https://doi.org/10.1016/j.fcr.2019.107573 Received 8 January 2019; Received in revised form 8 July 2019; Accepted 12 July 2019 0378-4290/ © 2019 Elsevier B.V. All rights reserved.

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2018 in two leading journals in Agronomy and Crop Physiology (Field Crops Research and European Journal of Agronomy). Where yield and N uptake were reported, data were retrieved from tables or figures, digitalised using Getdata Graph Digitizer (www.getdata-graph-digitizer. com). We also retrieved data on grain nitrogen concentration when available. The database (Table 1) include Mediterranean (n = 340) and nonMediterranean regions (n = 563). Mediterranean regions in our data set included locations in Spain (no papers reported data from non-Mediterranean regions of N Spain), Italy, Greece and the southern parts of France. Non-Mediterranean regions included Northern Europe, and the northern regions of France (Table 1). 2.2. Data analysis Box plots were used to summarise frequency distributions of key traits. Scatter plots of yield (y) against nitrogen uptake at maturity (x) were used to compare both regions, and logarithmic models [y = a + b ln(x)] were fitted for each region to both the whole data set and the 99th yield percentile (Cade and Noon, 2003). The slope of the curve for the whole data represents NUtE, and the slope of the curve for 99th yield percentile represents the boundary NUtEMAX (Fig. 1). In addition, we calculated NUtE for each individual treatment in each particular experiment as the ratio between yield and N uptake (Moll et al., 1982). Yield gaps were calculated as the difference between yield estimated with the fitted boundary function and actual yields. SigmaPlot v. 14 was use to carried out the statistical analysis.

Fig. 1. Working hypothesis. In comparison to wetter and cooler environments, the Mediterranean growing conditions would reduce (1) the upper limit of nitrogen uptake (arrow 1), and (2) nitrogen utilisation efficiency, i.e. the slope of the curve relating yield and nitrogen uptake for both the highest yields at each level of N uptake (NUtEMAX) captured with the 99th yield percentile (solid curve, arrow 2), and average yield at each level of N uptake (NUtE) captured with all data (dashed curve, arrow 3).

NUtE from other regions. But extrapolations from wetter, cooler environments to Mediterranean regions are not warranted for several reasons. For example, harvest index of wheat in northern Europe is approaching its theoretical limit (Austin et al., 1980; Peltonen-Sainio et al., 2008), but this seems an unrealistic limit for Mediterranean environments (Acreche et al., 2009; Sener et al., 2009) where the severity of water and heat stress increases with reproductive development. Therefore, it may be expected that yield response to N uptake be constrained in Mediterranean regions not only through reduced N uptake but also through limiting NUtE. We hypothesised that the functions relating yield and N uptake will have (1) a lower maximum N uptake (then, a narrower range of N uptake), and (2) a lower NUtE in Mediterranean than in nonMediterranean environments (Fig. 1). Consequently, the yield achieved at each N uptake would be diminished proportionally in Mediterranean environments. As we expect similar variation in actual NUtE between Mediterranean and non-Mediterranean regions, the penalty in NUtE would be similar for the average conditions (considering the whole range of variation in yield) and for the maximum yield at each N uptake, NUtEMAX (defined for the 99th yield percentile at a given N uptake). Therefore, the minimum N uptake for reproductive output (the abscissa-intercept) would be unaffected (Fig. 1). To test these hypotheses, we used published data of wheat yield response to N uptake in Mediterranean and non-Mediterranean conditions. Whereas Mediterranean environments are well defined, particularly in terms of rainfall seasonality (diCastri and Mooney, 1973), “non-Mediterranean” is a broad category which includes regions that could be subjected to severe stresses such as the continental environments of the North American Great Plains or the Loess Plateau in China (Sadras and Angus, 2006). To account for this, we restricted the comparison to European environments, where “non-Mediterranean” is mostly favourable conditions conducive to high yield potential (e.g. Porter and Semenov, 2005).

3. Results 3.1. Overview: yield, nitrogen uptake, nitrogen utilisation efficiency, and grain protein concentration Wheat in Mediterranean environments had lower average grain yield than in non-Mediterranean environments (4.1 vs 7.1 Mg ha−1). Differences in average yield between environments related more to yield under favourable conditions than with yield under stress; i.e. the difference in 90th percentile yield (6.2 vs 9.9 Mg ha−1) was almost twice that in the 10th percentile (1.9 vs 3.8 Mg ha−1) (Fig. 2). Mediterranean environments also had lower average N uptake (131 vs 166 kg N ha−1). Although N uptake was affected in the same direction, the magnitude of the difference in average yield was much larger (c. 42 and 21%, respectively). Consequently, Mediterranean environments had lower average NUtE (33 vs 47 kg grain DM kg N−1), and higher average grain N concentration (2.4 vs 1.8%) than their counterparts in non-Mediterranean environments (Fig. 2). 3.2. Relationships between yield and nitrogen uptake Scatter plots of yield vs N uptake showed regional clustering, with crops in non-Mediterranean environments out-yielding their Mediterranean counterparts at a given N uptake (Fig. 3a). Owing to the lower maximum N uptake in Mediterranean environments, the range of N uptake was lower in Mediterranean than in non-Mediterranean environments. The log-models fitted to all data and to the 99th yield percentile captured the regional difference in N utilisation efficiency; evidencing that the constrain imposed by Mediterranean environments was not only to the actual yields, but also to the maximum achievable yield, for each particular level of N uptake (Fig. 3b, Table 2). The difference between Mediterranean and non-Mediterranean regions in yield calculated from the curves fitted to the 99th yield percentile increased as N uptake increased from 50 to 300 kg N ha−1 (Fig. 3c). However, the relative differences averaged 30% through the range of N uptake (Fig. 3c). There was a trade-off between N utilisation efficiency and grain N concentration, both within and across regions captured with a single

2. Method 2.1. Data sources We compiled a data set of wheat (Triticum spp.) grain yield and uptake of nitrogen at maturity in experiments carried out in Europe. To warrant the objectivity of the data used to test these hypotheses we screened each single paper published from 1 January 2000 to 30 August 2

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Table 1 Ranges of grain yield and nitrogen (N) uptake, experimental sources of variation, country, environment (Mediterranean, M; non-Mediterranean, NM) of the data set of wheat (Triticum spp.) compiled from studies published in Field Crops Research and European Journal of Agronomy from 1 January 2000 to 30 August 2018. Country (environment)

Sources of variation

Grain yield (Mg ha−1)

N uptake (kg ha−1)

Source

France (NM) Germany (NM) France (NM, M) Sweden (NM) France (NM) Belgium (NM) Denmark (NM) France (NM) Denmark (NM) England (NM) Ireland (NM) France (NM) Ireland (NM) Denmark (NM) England (NM) France, England (NM) England (NM) Germany (NM) England (NM) Denmark (NM) England (NM) Sweden (NM) Denmark (NM) Switzerland (NM) Italy (M) Italy (M) Italy (M) Italy (M) Greece (M) Italy (M) Italy (M) Spain (M) SE France (M) SW France (M) Italy (M) Spain (M) Spain (M) Italy (M) France (M) Greece (M) Spain (M) Spain (M) Spain (M) Italy (M) Italy (M) Spain (M)

season, genotypes, N doses season, N doses sites N doses seasons, genotypes, N doses N doses, sowing densities seasons, intercropping with clover N doses sites, seasons, manure doses, catch crops seasons, genotypes, N doses sites, seasons, genotypes, manure and N genotypes, N doses season, N doses, tillage, straw incorporation sites, seasons, genotypes, N doses season, genotypes, fungicides doses, late N and water doses sites, season, genotypes, N doses season, N doses genotypes genotypes, N doses seasons, genotypes, N doses, sowing dates season, genotypes, N doses sites, genotypes, N doses seasons, crop rotation, N and manure doses season, genotypes, N and manure doses species season, genotypes, sowing density season, genotypes, sowing dates, N doses season, genotypes, N doses, irrigation season, N doses season, N doses season, genotypes, N and S doses season, tillage, rotation, N doses sites, season, N doses and intercropping with lover season, cropping system, N doses season, clipping (simulate grazing) season, tillage, rotation, N, doses season, N timing Seasons, wáter and N doses season, density, intercropping with pea, N doses season, genotypes, N, doses season, species, N season, tillage, rotation season, species, genotypes, N season, tillage, crop sequence, N doses site, season, tillage, N doses season, genotypes, N

4.5–9.0 8.8–9.3 4.8–9.2 5.2–8.0 9.6–11.3 6.8–8.5 3.6–5.8 3.8–8.4 2.2–5.2 9.0–11.0 3.9–12.2 4.6–8.9 2.8–8.7 4.2–10.7 6.4–9.5 4.0–8.9 5.4–12.7 8.2–9.4 2.4–9.7 8.6–9.9 4.6–9.4 2.3–13.7 4.1–9.3 2.6–6.4 3.9 3.8–6.5 3.0–5.7 3.0–5.9 2.0–2.9 1.1–3.6 3.7–4.8 1.6–4.9 2.8–4.1 3.6–6.1 3.1–4.9 0.7–4.8 4.7–6.7 3.6–7.3 1.0–6.9 4.3–6.0 1.4–8.7 2.6–5.2 0.6–8.7 2.7–5.1 1.5–5.6 4.6–10.2

91–276 211–276 98–256 154–187 251–335 97–194 97–139 74–195 58–131 200–250 69–242 129–278 47–261 53–258 196–248 93–290 94–369 216–281 41–261 134–199 163–367 59–339 187–225 57–190 125 148–190 93–152 72–166 77–191 32–89 108–149 67–144 67–106 155–240 111–190 27–129 114–234 59–156 44–209 170–257 48–241 92–160 42–301 86–178 54–207 101–269

Le Gouis et al., 2000 Sticksel et al., 2000 David et al., 2004 Delin and Stenberg, 2014 Le Bail et al., 2005 Reyniers et al., 2006 Thorsted et al., 2006 Martre et al., 2006 Olesen et at. 2009 Barraclough et al., 2010 Meade et al., 2011 Allard et al., 2013 Brennan et al., 2014 Oelofse et al., 2015 Gooding et al., 2007 Gaju et al., 2011 Pask et al., 2012 Erdle et al., 2013 Barraclough et al., 2014 Rasmussen and Thorup-Kristensen, 2016 Gaju et al., 2016 Hamnér et al., 2017 Suarez-Tapia et al., 2017 Büchi et al. 2016 Giunta et al., 2009 Arduini et al., 2006 Giunta et al., 2007 Ercoli et al., 2008 Dordas, 2009 Basso et al., 2010 Ercoli et al., 2011 López-Bellido et al., 2012 Vrignon-Brenas et al., 2016 Plaza-Bonilla et al., 2017 Giunta et al., 2017 López-Bellido and López-Bellido, 2001 López Bellido et al., 2005 Albrizio et al., 2010 Bedoussac and Justes, 2011 Koutroubas et al., 2012 Cossani et al., 2012 Muñoz-Romero et al., 2013 Marti et al., 2014 Ruisi et al., 2016 Giambalvo et al., 2018 Elia et al. 2018

4. Discussion

non-linear function (Fig. 4). Grain N concentration accounted for 27% of the variation in yield gap (i.e. difference between actual yield and the 99th yield curve) in Mediterranean environments, and for 58% of the variation in yield gap for their non-Mediterranean counterparts.

As expected, average yield was lower in Mediterranean than in nonMediterranean conditions. Differences in average yield between regions Fig. 2. Frequency distribution of grain yield, nitrogen uptake, nitrogen utilisation efficiency and grain nitrogen concentration of wheat in Mediterranean and non-Mediterranean environments of Europe. Nitrogen utilisation efficiency was calculated as the ratio between yield and nitrogen uptake. For grain yield, nitrogen uptake and nitrogen utilisation efficiency, n = 340 in Mediterranean, and n = 563 in nonMediterranean environments; for grain nitrogen concentration, n = 208 and n = 539, respectively.

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Fig. 3. (a) Wheat yield as a function of nitrogen uptake at maturity in Mediterranean (closed symbols) and non-Mediterranean (open symbols) environments of Europe. (b) Curves fitted to all data (dashed) or 99th yield percentile (solid) for Mediterranean and nonMediterranean environments. Parameters of the curves are in Table 2. (c) Difference between Mediterranean and non-Mediterranean regions in yield calculated from the curves fitted to the 99th yield percentile, as a function of nitrogen uptake. Numbers indicate percent difference between regions at nitrogen uptake of 50, 150 and 300 kgN ha−1.

Table 2 Parameters ( ± s.e.) of the model y = a + b ln(x) for wheat crops in Mediterranean and non-Mediterranean regions of Europe, where y is yield (Mg ha−1) and x is nitrogen uptake (kg N ha−1). The model was fitted to all data, and to the 99th yield percentile; all fitted functions had P < 0.0001. Data and curves are shown in Fig. 3. Environment

Yield

a

Mediterranean Non-Mediterranean Mediterranean Non-Mediterranean

all data

−10.251 −12.083 −10.785 −15.192

99th percentile

R2

b ± ± ± ±

0.467 0.516 2.373 1.640

3.010 4.943 3.492 4.943

± ± ± ±

0.097 0.328 0.495 0.328

0.74 0.71 0.86 0.96

Fig. 4. Grain nitrogen concentration as a function of nitrogen utilisation efficiency of wheat crops in Mediterranean (closed symbols) and nonMediterranean (open symbols) environments of Europe.

were mostly driven by differences in yield under favourable conditions, with a smaller contribution from differences in yield under stress. Mediterranean conditions in Europe (Savin et al., 2015) and Australia (Chenu et al., 2013), constrain yield by recurrent and severe water and thermal stress during the critical periods of grain set and filling. This characteristic progression of stress impairs reproductive growth more than vegetative growth, and hence N uptake is less restricted than yield as most N is absorbed before anthesis (e.g. Barraclough et al., 2014). This accounts for the reduction in yield that largely exceeded that on N uptake (Figs. 2 and 3). However, maximum N uptake was also impaired by Mediterranean conditions. Thus, Mediterranean conditions reduced the potential capacity of the crop to capture of N, supporting our first hypothesis (Fig. 1). In both Mediterranean and non-Mediterranean conditions yield

Fig. 5. Comparison of wheat yield – nitrogen uptake relationships in the Mediterranean region of Europe (red) and the Mediterranean regions of Southeastern and Western Australia (green). Inset shows the Australian data and the curve for 99th yield percentile from Europe. Parameters of the model y = a + b ln(x) fitted to Australian data are: a = −7.304 ± 1.9225, b = 2.644 ± 0.4463 for the 99th yield percentile (R2 = 0.81, P = 0.0004), and a = −4.596 ± 0.278, b = 1.7398 ± 0.0645 for all the data (R2 = 0.65, P < 0.0001). Data for Australian crops are from Sadras et al. (2016), restricted to Victoria, South Australia and Western Australia (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).

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Competitiveness of Spain. SARDI-GRDC bilateral Project (DAS 00,166 BA) funded VOS work.

increased non-linearly with N uptake, in accordance to the diminishing returns of resource utilisation (Gastal et al., 2015). The parameters of the fitted curves differed between the two conditions, capturing the dual constraint of the Mediterranean environment on N uptake and the slope of the curve NUtE at any particular N uptake. These effects on NUtE mirrored those on the NUtEMAX (supplementary Fig. S1), and increased with N uptake. Mediterranean environments had lower NUtE and NUtEMAX across the whole range of N uptake, supporting the second hypothesis (Fig. 1). This penalty on the efficiency in converting N uptake into yield is again related to the dynamics of most common stresses in Mediterranean environments affecting more the reproductive than the vegetative growth; which also explains the relatively lower yield potential of wheat (Abeledo et al., 2008). We speculate that in other stressful environments, where the pattern of stress is not progressive as in Mediterranean regions, yield would be penalised chiefly through reduced N uptake rather than NUtE. That is the impairment of vegetative and reproductive outputs would be similar, should the stress be more uniform through the growing season. Then, the relative importance of N uptake and NUtE in other stressful environments will depend on the patterns of stress in relation to crop ontogeny. In this study we restricted the analysis to Mediterranean regions of Europe, but the conclusions may apply to other Mediterranean environments, primarily defined by a high concentration (at least 65%) of annual rainfall in the winter-half year (di Castri and Mooney, 1973). This proposition is supported by the overlap in the relationship between yield and N uptake in Mediterranean environments of Europe (this study) and that of wheat crops in the Mediterranean environments of South Eastern and Western Australia (Fig. 5). Indeed, the curve representing NUtEMAX for Mediterranean Europe is a reasonable boundary for wheat crops in winter-rainfall environments of Australia (Fig. 5 inset). The trade-off between grain N concentration and NUtE is widespread for both environmental and genetic sources of variation (Pedro et al., 2011; Ferrante et al., 2012; Wang et al., 2017), and has been verified in our analysis (Fig. 4). Interestingly, in this study a single relationship applied to both Mediterranean and non-Mediterranean conditions; i.e. the main reason why on average the N concentration of wheat in Mediterranean regions tends to be higher than that in cooler, wetter non-Mediterranean regions of Europe seems to be a consequence of the penalty imposed to NUtE by Mediterranean conditions. This would further support the idea that whilst grain filling is sink limited (Borrás et al., 2004; Serrago et al., 2013), N accumulation in the grain is source-limited (Dreccer et al., 1997; Martre et al., 2003; Acreche and Slafer, 2009), and the outcome of the two process is the dilution/concentration effect determining grain N concentration. Thus, the constraints imposed by Mediterranean conditions to yield at each N uptake diminished the dilution of grain N and consequently increased N percentage of the grains. In addition, it is interesting to note that at the highest values of NUtE all points were close to regression line, whereas at intermediate/low values of NutE there was more variation (Fig. 4). This implies that differences in NHI were also accounting for variation in NutE for a particular level of grain N concentration. Therefore, in breeding programs in which elite lines have already high values of NUtE, lowering grain N concentration may be unavoidable to further increasing NutE, which may be relevant in future breeding. We conclude that the prevalent patterns of water and thermal stress in Mediterranean conditions impose a dual constraint to N uptake and NUtE of wheat, with a generalised trade-off between NUtE and grain N concentration. The curves fitted to the large database in this study can be used for benchmarking yield against N uptake in Mediterranean regions of Europe, and possibly other Mediterranean environments.

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Acknowledgements RS and GAS participation in this study was in the context of their project AGL2015-69595-R of the Ministry of Economy and 5

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