Our nitrogen ‘footprint’: the need for increased crop nitrogen use efficiency

Nitrogen (N) is an essential element for the growth and development of all living organisms, as it is a constituent of DNA, RNA, ATP and protein. In plants, N is also an essential component of other key compounds including chlorophyll, auxin, cytokinins, alkaloids and glucosinolates. Plants are the ultimate source of N and carbon for all animals including humans (Shewry, 2009; Halford et al., 2011). Despite the importance of N in metabolism, it is present in short supply in forms that can be assimilated by a plant, and as a result, low soil N availability is often the major nutrient factor limiting the growth and yield of crops. Synthetic N fertilisers have been used extensively to increase crop yield since the end of the Second World War. The bulk of this N is derived from ammonia synthesised by the Haber–Bosch process. This process was one of the most important ‘inventions’ of the 20th century, as it allowed the production of sufficient food for the growing world population and almost 50% of humanity is dependent upon it (Erisman et al., 2008). Currently, 100–125 Tg of synthetic N produced via the Haber–Bosch process is applied to agricultural systems each year (Galloway et al., 2008; Erisman et al., 2011; Fowler et al., 2013). A high proportion of this synthetic N fertiliser is used for cereal crops (Galloway et al., 2008; Mulvaney et al., 2009). In intensive agricultural production systems, as much as 50% of the N applied to the field is not used by the crop plant (Cameron et al., 2013). The surplus N may be lost to the aqueous and atmospheric environments where it can become a serious pollutant and a conservation concern. Nitrate (NO3−) and urea are very soluble and unlike ammonium (NH4+) which binds to negative charges in the soil, can run off into the surface water or flow into the groundwater (Goulding, 2000; Howden et al., 2013). Water contaminated by NO3− is often not potable and at high concentrations can be a serious risk for human health (Powlson et al., 2008; Bryan & van Grinsven, 2013). Ammonia volatilisation, nitrification to nitrous oxide and denitrification to N2 gas can be causes of N losses from the soil to the atmosphere (Cameron et al., 2013). There is no doubt that the production and use of synthetic N fertiliser has contributed to a range of environmental problems. In particular, considerable CO2 is released during the Haber–Bosch process in the production of hydrogen from methane and because of its high fossil fuel energy costs. Also, application of synthetic N fertiliser has contributed to increased levels of greenhouse gases, a decreased biodiversity within and outside agricultural systems and eutrophication of fresh waters, estuaries, coastal waters and nutrient-poor land habitats (Cameron et al., 2013; Erisman et al., 2013; Fowler et al., 2013). Recently, a tool called N-Calculator has been developed using a N ‘footprint’ model, to provide information on how individual and collective action results in the loss of N to the environment (Leach et al., 2012). The N-Calculator focuses on food and energy consumption, using average per capita data for a country. Leach et al. (2012) emphasised that ‘our lifestyle choices, and especially our food consumption, have major impacts on the N losses to the environment’. Websites are now available where a person's N footprint can be calculated: http://www.n-print.org/node/40; http://www.lancs.ac.uk/news/articles/2013/first-carbon-footprints-now-you-can-calculate-your-nitrogen-footprint/ [14 July 2013]. There is a need to reduce the use of N fertiliser in agricultural systems, and crops are being sought with greater N use efficiency (NUE) (Kant et al., 2011; Chardon et al., 2012; McAllister et al., 2012; Xu et al., 2012), taken here as dry matter or protein yield per unit N available to the crop. Over the past 10 years, the Annals of Applied Biology has published a number of papers on research which is relevant to increasing crop NUE: 12 of these papers are described here and are presented in full in the Annals of Applied Biology virtual issue ‘Crop Nitrogen Use Efficiency’. Andrews et al. (2004) assessed if genetic manipulation of the activities of N assimilation enzymes can result in increased potential yield and/or increased yield per unit N taken up by the plant. It was argued that the selection of plants, from either a genetically manipulated population or genetic resources, with expression of NO3− reductase/nitrite reductase primarily in either the root or shoot should increase plant/crop growth and hence the yield under specific environmental conditions. In addition, for cereals, the selection of plants with high cytosolic glutamine synthetase in senescing leaves, and in some cases high NADH-glutamate synthase in developing grains, could help maximise the allocation of plant N to seeds. Raven et al. (2005) firstly considered the role that resource limitation has had in the evolution of photosynthetic organisms on Earth, highlighting the restrictions on the biochemistry of organisms resulting from the intrinsic chemistry of the elements, and their availability during evolution. Many major evolutionary innovations can plausibly be considered as responses to a shortage of one or more resources. Secondly, the implications of the evolutionary response to resource limitation on the breeding of crop plants for sustainable low input agricultural systems were discussed. Production of N waste by livestock agriculture is a significant environmental concern in terms of pollution of land and water. In the rumens of cattle and sheep, the excessive proteolysis which contributes to inefficiency of nutrient use involves both the rumen microbial population and the intrinsic plant proteases that can mediate protein degradation in ingested fresh forage on exposure to the environmental stresses of the rumen. Kingston-Smith et al. (2006) used white clover plants dependent on NO3− supplied to the roots, to determine how the N status of the plant affects the rate of plant-mediated proteolysis in forage under conditions that simulate ingestion by grazing ruminants. Foliar protein content increased with increased NO3− supply. Regardless of NO3− supply, 50% of the protein was degraded in 6 h and 80% after 24 h. It was proposed that continued and extensive proteolysis occurs following leaf excision and exposure to rumen conditions because amino acid accumulation is insufficient to initiate those feedback systems that sense the cytoplasmic amino acid concentration and prevent excessive proteolysis during normal source–sink relations. For grain crops, yield per unit of N available from the soil can be divided into two processes: N uptake efficiency, the ability of the plant to remove N from the soil, normally present as NO3− or NH4+ ions, and the N utilisation efficiency, the ability of the plant to transfer N to the grain, predominantly present as protein. In a two part article, Lea and Azevedo (2006, 2007) highlighted the genes that may play a role in the processes that determine NO3− and NH4+ uptake efficiency from the soil and those controlling the enzymes of amino acid metabolism involved in transferring N to the protein in the grain. The ultimate aim was that this information could lead to improvements in N uptake and utilisation efficiency, employing breeding and genetic manipulation techniques. Serret et al. (2008) assessed the effect of N fertilisation level and genotypic variation on yield, N accumulation, NUE and its components (N uptake efficiency and N utilisation efficiency) and the stable carbon (δ13C) and N (δ15N) composition of mature grains and straw of 24 wheat genotypes grown under well-irrigated conditions. It was concluded that under their experimental conditions, natural abundances of 15N and 13C may provide complementary information on how N fertiliser is used by wheat. However, while grain yield, biomass, total N accumulated and NUE were greater in the most recently developed genotypes, there was only a tendency for higher δ15N in these genotypes and there was no clear trend for δ13C. Changes in NUE were paralleled by changes in N uptake rather than utilisation efficiency. Biological dinitrogen (N2) fixation utilising the bacterial enzyme nitrogenase is also an important source of N in agriculture and it has been estimated that 60 Tg of N is fixed per year in natural terrestrial ecosystems (Vitousek et al., 2013) and that an equivalent amount is fixed in anthropogenic agricultural terrestrial systems (Herridge et al., 2008), making a total of approximately 120 Tg per year. It has also been estimated that 140 Tg N is fixed per year globally in the oceans. Interestingly, both these total values are similar to that produced by the Haber–Bosch process (Fowler et al., 2013). The most important N2-fixing agents in agriculture are the symbiotic associations between legumes and rhizobia (Fustec et al., 2010; Liu et al., 2011). Nitrogen-fixing legumes can be utilised as a seed crop, a green manure or as the main N input into a pasture by growing it in association with grass. At the crop level, N loss to the environment relative to N accumulated by N2-fixing legumes is variable. For example, in the case of non-fertilised grain legumes for which the harvested part is taken off-site and relatively little residual N is left in the soil, loss of N per unit N accumulated is likely to be very low. However, N losses relative to N accumulated are likely to be similar for a grass/legume pasture and a N-fertilised grass pasture of comparable productivity, although greenhouse gas emissions resulting from N fertiliser production would be avoided with the grass/legume pasture (Andrews et al., 2009). Andrews et al. (2009) carried out a cost–benefit analysis based on biochemical principles of the photon and water costs of the various biochemical and transport processes involved in plant growth, N assimilation, pH regulation and osmolarity generation, per unit N assimilated with NH4+, NO3− or N2 as N sources. It was estimated that the photon and water costs are, respectively, likely to be around 5% and 7% greater for N2 fixation than for a combination of NH4+ and root and shoot NO3− assimilation as occurs with most crops. The potential of symbiotic N2 fixation and other major positive plant microbial interactions in agricultural systems such as mycorrhizas and grass fungal endophytes was considered further in a separate Special Issue of Annals of Applied Biology ‘Positive plant microbial interactions’ (Andrews et al., 2012). Also, in his Editorial, Valkonen (2013) emphasised the importance of understanding the interactions between plants, microorganisms and invertebrate animals if integrated pest management is to be successful in the improvement of crop productivity. Insect pests continue to have a major effect on agricultural production and the movement of insects from one crop to another can be particularly detrimental (Mazzi & Dorn, 2012). Two papers are presented within the virtual issue here that show N supply to plants can affect their associated insects. Aqueel & Leather (2012) examined the biological control potential (functional response and consumption) of each developmental stage of the coccinellid predator Harmonia axyridis to the cereal aphids, Rhopalosiphum padi and Sitobion avenae on wheat receiving different levels of N. Findings provide important information for determining the stage of the predator's release at specific N fertiliser levels because its unnecessary use may suppress other natural enemies in the field via intraguild interactions. The study also determined how the predator's rate of successful search, and the handling time for the cereal aphids, varies at different N levels. It was found, for example, that increased N application increased N content of the wheat and the body weight of the aphids feeding on them. In addition, H. axyridis consumed more aphids on low N fertilised plants, suggesting a compensatory consumption to overcome lower aphid size. It was concluded that low N fertilised crops will need less predators to control the smaller, less fecund aphids and careful management would avoid the unnecessary overuse of predators. Butler et al. (2012) used a categorical random effects meta-analysis and a vote count meta-analysis to examine the effects of N, phosphorus (P), potassium (K) and NPK fertiliser on insect population dynamics. It was confirmed that, in general, the application of N fertiliser has a significant positive effect on insect populations, although this depends on the environment in which the study is conducted. Insects that remove sap from the phloem showed a much stronger response to fertilisers than chewing insects. Phloem-feeding insects, in particular aphids, have the capacity to utilise efficiently the relatively low N content of the phloem, due to the presence of symbiotic microorganisms (e.g. Buchnera) that are able to synthesise essential amino acids (Macdonald et al., 2012). This study provided an invaluable flag post in the ongoing research investigating fertiliser effects on ecosystems. The major problem with the production of synthetic N fertilisers derived from the Haber–Bosch process is the large amount of energy required, which has been estimated as 2.5% of the total global supply (Erisman et al., 2008). For this reason, various forms of organic N fertilisers have been proposed as suitable alternatives (Huo et al., 2012). In a detailed analysis of wheat production, Tuomisto et al. (2012) compared ‘conventional’, organic and integrated farm management (IFM) systems with respect to their land use, energy use and 100 years global warming potential. Life cycle assessment was used to simulate the impacts of the three systems along the production chain from input production up to the farm gate. The IFM system models were designed to combine the best practices from organic and conventional systems to reduce negative environmental impacts without significant yield reductions. Generally, N-fixing legumes in rotations were used as an alternative to synthetic N fertiliser. It was demonstrated that reductions in energy requirement could be achieved by replacing synthetic N fertiliser with anaerobically treated food waste and N-fixing cover crops. It was concluded that IFM systems have the greatest potential to conserve the environment and maintain yields. Crop NUE decreases with increased N supply but it can also be dependent on the form of N taken up and utilised. Thus, to maximise crop NUE, a thorough understanding of the effects of the different forms of N on crop plants is required. Andrews et al. (2013) reviewed the literature on N form effects on plants at different stages of their development, critically assessing the possible mechanisms of these effects. In particular, NO3− was compared with the other forms of N utilised by plants. It was concluded that the form of N available to plants can affect their time and rate of seed germination, leaf expansion and function, dry matter partitioning between shoot and root and root architecture. The magnitude of these effects is dependent on environmental factors outside the supply of N. The mechanism of these effects is variable. Assessment of the importance of root or shoot NO3− assimilation under different environmental conditions was highlighted as an important area for further study. The ‘Crop Nitrogen Use Efficiency’ virtual issue closes with the Cameron et al. (2013) review of N losses from the soil/plant system. This review described the N cycle in temperate soil/plant systems, the processes involved in each of the individual N loss pathways, the factors affecting the amounts of losses and the methods that are available to reduce these losses. It was shown that careful management of temperate soil/plant systems using best management practices and newly developed technologies can increase the sustainability of agriculture and reduce its impact on the environment. We are grateful to Prof. John A. Raven for his critical reading of the manuscript.