Abstract
Crop nitrogen use efficiency (NUE) is crucial for sustainable food security as well as for a sustainable environment. It can be improved in the short term through improved fertilizer formulations and cropping practices under integrated nutrient management, but the inherent capacity of the plant to take up, retain and use the available nitrogen (N) has to be tackled biologically. The last decade has witnessed several major advances in our understanding on the biological determinants of N-response and N-use efficiency, which are opening up biotechnological opportunities for improvement in the medium to long term. This chapter highlights the various biological determinants including the uptake and assimilation of external N, remobilization of internal N, efflux or loss of N from plants. The emerging opportunities for NUE enhancement span a vast array of approaches including germplasm diversity, root architecture, molecular markers, phenomics, genomics and functional genomics, metabolomics and micro-Ribonucleic Acids (miRNAs). They are amenable to both transgenic, as well as non-transgenic selection/breeding options.
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References
Albinsky, D., Kusano, M., Higuchi, M., Hayashi, N., Kobayashi, M., Fukushima, A., et al. (2010). Metabolomic screening applied to rice FOX Arabidopsis lines leads to the identification of a gene-changing nitrogen metabolism. Molecular Plant, 3(1), 125–142.
Amiour, N., Imbaud, S., Clément, G., Agier, N., Zivy, M., Valot, B., et al. (2012). The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. Journal of Experimental Botany, 63(14), 5017–5033.
Andrews, M., & Lea, P. J. (2013). Our nitrogen ‘footprint’: The need for increased crop nitrogen use efficiency. Annals of Applied Biology, 163(2), 165–169.
Bi, Y. M., Kant, S., Clark, J., Gidda, S., Ming, F., Xu, J., et al. (2009). Increased nitrogen-use efficiency in transgenic rice plants over-expressing a nitrogen-responsive early nodulin gene identified from rice expression profiling. Plant, Cell & Environment, 32(12), 1749–1760.
Bordes, J., Ravel, C., Jaubertie, J., Duperrier, B., Gardet, O., Heumez, E., et al. (2013). Genomic regions associated with the nitrogen limitation response revealed in a global wheat core collection. Theoretical and Applied Genetics, 126(3), 805–822.
Bucksch, A., Burridge, J., York, L. M., Das, A., Nord, E., Weitz, J. S., & Lynch, J. P. (2014). Image-based high-throughput field phenotyping of crop roots. Plant Physiology, 166(2), 470–486.
Cameron, K., Di, H., & Moir, J. (2013). Nitrogen losses from the soil/plant system: A review. Annals of Applied Biology, 162(2), 145–173.
Chakraborty, N., & Raghuram, N. (2011). Nitrate sensing and signaling in genomewide plant N response. In V. Jain & P. Anandakumar (Eds.), Nitrogen use efficiency in plants (pp. 45–62). New Delhi: New India Publishing Agency.
Chardon, F., Barthélémy, J., Daniel-Vedele, F., & Masclaux-Daubresse, C. (2010). Natural variation of nitrate uptake and nitrogen use efficiency in Arabidopsis thaliana cultivated with limiting and ample nitrogen supply. Journal of Experimental Botany, 61(9), 2293–2302.
Coque, M., & Gallais, A. (2006). Genomic regions involved in response to grain yield selection at high and low nitrogen fertilization in maize. Theoretical and Applied Genetics, 112(7), 1205–1220.
De Dorlodot, S., Forster, B., Pagès, L., Price, A., Tuberosa, R., & Draye, X. (2007). Root system architecture: Opportunities and constraints for genetic improvement of crops. Trends in Plant Science, 12(10), 474–481.
Fischer, J. J., Beatty, P. H., Good, A. G., & Muench, D. G. (2013). Manipulation of microRNA expression to improve nitrogen use efficiency. Plant Science, 210, 70–81.
Forde, B. G. (2014). Nitrogen signalling pathways shaping root system architecture: An update. Current Opinion in Plant Biology, 21, 30–36.
Fukushima, A., & Kusano, M. (2014). A network perspective on nitrogen metabolism from model to crop plants using integrated ‘omics’ approaches. Journal of Experimental Botany, 65(19), 5619–5630.
Furbank, R. T., & Tester, M. (2011). Phenomics–technologies to relieve the phenotyping bottleneck. Trends in Plant Science, 16(12), 635–644.
Galloway, J. N., Townsend, A. R., Erisman, J. W., Bekunda, M., Cai, Z., Freney, J. R., et al. (2008). Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Science, 320(5878), 889–892.
Giehl, R. F., Gruber, B. D., & von Wirén, N. (2014). It’s time to make changes: Modulation of root system architecture by nutrient signals. Journal of Experimental Botany, 65(3), 769–778.
Good, A. G., & Beatty, P. H. (2011). Fertilizing nature: A tragedy of excess in the commons. PLoS Biology, 9(8), e1001124. https://doi.org/10.1371/journal.pbio.1001124
Good, G., Johnson, S. J., De Pauw, M., Carroll, R. T., Savidov, N., Vidmar, J., Lu, Z., Taylor, G., & Stroeher, V. (2007). Engineering nitrogen use efficiency with alanine aminotransferase. Canadian Journal of Botany, 85(3), 252–262.
Goodall, A. J., Kumar, P., & Tobin, A. K. (2013). Identification and expression analyses of cytosolic glutamine synthetase genes in barley (Hordeum vulgare L.). Plant and Cell Physiology, 54(4), 492–505.
Hakeem, K., Chandna, R., Ahmad, A., Qureshi, M. I., & Iqbal, M. (2012). Proteomic analysis for low and high nitrogen-responsive proteins in the leaves of rice genotypes grown at three nitrogen levels. Applied Biochemistry and Biotechnology, 168(4), 834–850.
Hakeem, K., Mir, B., Qureshi, M. I., Ahmad, A., & Iqbal, M. (2013). Physiological studies and proteomic analysis for differentially expressed proteins and their possible role in the root of N-efficient rice (Oryza sativa L.). Molecular Breeding, 32(4), 785–798.
Hawkesford, M. J. (2012). Improving nutrient use efficiency in crops. In eLS. Chichester: Wiley. https://doi.org/10.1002/9780470015902.a0023734.
Hu, H. C., Wang, Y. Y., & Tsay, Y. F. (2009). AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. The Plant Journal, 57(2), 264–278.
Humbert, S., Subedi, S., Cohn, J., Zeng, B., Bi, Y.-M., Chen, X., et al. (2013). Genome-wide expression profiling of maize in response to individual and combined water and nitrogen stresses. BMC Genomics, 14, 3. https://doi.org/10.1186/1471-2164-14-3
Igarashi, D., Ishizaki, T., Totsuka, K., & Ohsumi, C. (2009). ASN2 is a key enzyme in asparagine biosynthesis under ammonium sufficient conditions. Plant Biotechnology, 26(1), 153–159.
Jeuffroy, M.-H., Casadebaig, P., Debaeke, P., Loyce, C., & Meynard, J.-M. (2014). Agronomic model uses to predict cultivar performance in various environments and cropping systems. A Review. Agronomy for Sustainable Development, 34(1), 121–137.
Kamiji, Y., Pang, J., Milroy, S. P., & Palta, J. A. (2014). Shoot biomass in wheat is the driver for nitrogen uptake under low nitrogen supply, but not under high nitrogen supply. Field Crops Research, 165, 92–98.
Kindu, G., Tang, J., Yin, X., & Struik, P. (2014). Quantitative trait locus analysis of nitrogen use efficiency in barley (Hordeum vulgare L.). Euphytica, 199(1–2), 207–221.
Kumagai, E., Araki, T., Hamaoka, N., & Ueno, O. (2011). Ammonia emission from rice leaves in relation to photorespiration and genotypic differences in glutamine synthetase activity. Annals of Botany, 108(7), 1381–1386.
Kusano, M., Fukushima, A., Redestig, H., & Saito, K. (2011). Metabolomic approaches toward understanding nitrogen metabolism in plants. Journal of Experimental Botany, 62(4), 1439–1453.
Li, Q., Li, B.-H., Kronzucker, H. J., & Shi, W.-M. (2010). Root growth inhibition by NH4+ in Arabidopsis is mediated by the root tip and is linked to NH4+ efflux and GMPase activity. Plant, Cell & Environment, 33(9), 1529–1542.
Li, X.-M., Chen, X.-M., Xiao, Y.-G., Xia, X.-C., Wang, D.-S., He, Z.-H., & Wang, H.-J. (2014). Identification of QTLs for seedling vigor in winter wheat. Euphytica, 198(2), 199–209.
Liang, C., Tian, J., & Liao, H. (2013). Proteomics dissection of plant responses to mineral nutrient deficiency. Proteomics, 13(3–4), 624–636.
Liao, C., Peng, Y., Ma, W., Liu, R., Li, C., & Li, X. (2012). Proteomic analysis revealed nitrogen-mediated metabolic, developmental, and hormonal regulation of maize (Zea mays L.) ear growth. Journal of Experimental Botany, 63(14), 5275–5288.
Marchive, C., Roudier, F., Castaings, L., Bréhaut, V., Blondet, E., Colot, V., et al. (2013). Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nature Communications, 4, 1713. https://doi.org/10.1038/ncomms2650
Masclaux-Daubresse, C., Reisdorf-Cren, M., Pageau, K., Lelandais, M., Grandjean, O., Kronenberger, J., et al. (2006). Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. Plant Physiology, 140(2), 444–456.
McAllister, C. H., Beatty, P. H., & Good, A. G. (2012). Engineering nitrogen use efficient crop plants: The current status. Plant Biotechnology Journal, 10(9), 1011–1025.
McDougall, P. (2011). The cost and time involved in the discovery, development and authorisation of a new plant biotechnology derived trait. A consultancy study for Crop Life International. Midlothian, UK: Phillips McDougall.
Møller, A. L. B., Pedas, P. A. I., Andersen, B., Svensson, B., Schjoerring, J. K., & Finnie, C. (2011). Responses of barley root and shoot proteomes to long-term nitrogen deficiency, short-term nitrogen starvation and ammonium. Plant, Cell & Environment, 34(12), 2024–2037.
Okumoto, S., & Pilot, G. (2011). Amino acid export in plants: A missing link in nitrogen cycling. Molecular Plant, 4(3), 453–463.
Orman-Ligeza, B., Civava, R., de Dorlodot, S., & Draye, X. (2014). Root system architecture. In A. Morte & A. Varma (Eds.), Root engineering (pp. 39–56). Berlin Heidelberg: Springer.
Parry, M. A., & Hawkesford, M. J. (2012). An integrated approach to crop genetic improvement. Journal of Integrative Plant Biology, 54(4), 250–259.
Pathak, R., Ahmad, A., Lochab, S., & Raghuram, N. (2008). Molecular physiology of plant nitrogen use efficiency and biotechnological options for its enhancement. Current Science, 94(11), 1394–1403.
Pathak, R., Lochab, S., & Raghuram, N. (2011). Improving nitrogen use efficiency. In M. Moo-Young (Ed.) Comprehensive biotechnology. Volume 4: Agricultural and related biotechnologies (pp. 209–218). Oxford: Elsevier.
Patterson, K., Cakmak, T., Cooper, A., Lager, I., Rasmusson, A. G., & Escobar, M. A. (2010). Distinct signalling pathways and transcriptome response signatures differentiate ammonium-and nitrate-supplied plants. Plant, Cell & Environment, 33(9), 1486–1501.
Pavlík, M., Pavlíková, D., & Vašíčková, S. (2010). Infrared spectroscopy-based metabolomic analysis of maize growing under different nitrogen nutrition. Plant, Soil and Environment, 56(11), 533–540.
Poiré, R., Chochois, V., Sirault, X. R., Vogel, J. P., Watt, M., & Furbank, R. T. (2014). Digital imaging approaches for phenotyping whole plant nitrogen and phosphorus response in Brachypodium distachyon. Journal of Integrative Plant Biology, 56(8), 781–796.
Privalle, L. S., Chen, J., Clapper, G., Hunst, P., Spiegelhalter, F., & Zhong, C. X. (2012). Development of an agricultural biotechnology crop product: Testing from discovery to commercialization. Journal of Agricultural and Food Chemistry, 60(41), 10179–10187.
Quraishi, U. M., Abrouk, M., Murat, F., Pont, C., Foucrier, S., Desmaizieres, G., et al. (2011). Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. The Plant Journal, 65(5), 745–756.
Rachmilevitch, S., Cousins, A. B., & Bloom, A. J. (2004). Nitrate assimilation in plant shoots depends on photorespiration. Proceedings of the National Academy of Sciences of the United States of America, 101(31), 11506–11510.
Rothstein, S. J., Bi, Y.-M., Coneva, V., Han, M., & Good, A. (2014). The challenges of commercializing second-generation transgenic crop traits necessitate the development of international public sector research infrastructure. Journal of Experimental Botany, 65(19), 5673–5682.
Ruzicka, D. R., Barrios-Masias, F. H., Hausmann, N. T., Jackson, L. E., & Schachtman, D. P. (2010). Tomato root transcriptome response to a nitrogen-enriched soil patch. BMC Plant Biology, 10(1), 75.
Sato, S., & Yanagisawa, S. (2014). Characterization of metabolic states of Arabidopsis thaliana under diverse carbon and nitrogen nutrient conditions via targeted metabolomic analysis. Plant and Cell Physiology, 55(2), 306–319.
Simons, M., Saha, R., Guillard, L., Clément, G., Armengaud, P., Cañas, R., Maranas, C. D., Lea, P. J., & Hirel, B. (2014). Nitrogen-use efficiency in maize (Zea mays L.): from ‘omics’ studies to metabolic modelling. Journal of Experimental Botany, 65(19), 5657–5671.
Smith, S., & De Smet, I. (2012). Root system architecture: Insights from Arabidopsis and cereal crops. Philosophical Transactions of the Royal Society B: Biological Sciences, 367(1595), 1441–1452.
Sorgona, A., Lupini, A., Mercati, F., Di Dio, L., Sunseri, F., & Abenavoli, M. R. (2011). Nitrate uptake along the maize primary root: An integrated physiological and molecular approach. Plant, Cell & Environment, 34(7), 1127–1140.
Sun, J.-J., Guo, Y., Zhang, G.-Z., Gao, M.-G., Zhang, G.-H., Kong, F.-M., et al. (2013). QTL mapping for seedling traits under different nitrogen forms in wheat. Euphytica, 191(3), 317–331.
Sutton, M. A., Bleeker, A., Howard, C., Bekunda, M., Grizzetti, B., de Vries, W., van Grinsven, H. J. M., Abrol, Y. P., Adhya, T. K., Billen, G., Davidson, E. A., Datta, A., Diaz, R., Erisman, J. W., Liu, X. J., Oenema, O., Palm, C., Raghuram, N., Reis, S., Scholz, R. W., Sims, T., Westhoek, H., & Zhang, F. S. (2013). Our Nutrient World: The challenge to produce more food and energy with less pollution. Global overview of Nutrient Management. Edinburgh: Centre for Ecology and Hydrology (CEH) on behalf of the Global Partnership on Nutrient Management and the International Nitrogen Initiative.
Varshney, R. K., Bansal, K. C., Aggarwal, P. K., Datta, S. K., & Craufurd, P. Q. (2011). Agricultural biotechnology for crop improvement in a variable climate: Hope or hype? Trends in Plant Science, 16(7), 363–371.
Villordon, A. Q., Ginzberg, I., & Firon, N. (2014). Root architecture and root and tuber crop productivity. Trends in Plant Science, 19(7), 419–425.
Vitousek, P., Cassman, K., Cleveland, C., Crews, T., Field, C., Grimm, N., et al. (2002). Towards an ecological understanding of biological nitrogen fixation. In E. Boyer & R. Howarth (Eds.), The nitrogen cycle at regional to global scales (pp. 1–45). Netherlands: Springer.
Wang, R., Guegler, K., LaBrie, S. T., & Crawford, N. M. (2000). Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. The Plant Cell Online, 12(8), 1491–1509.
Wei, H., Yordanov, Y. S., Georgieva, T., Li, X., & Busov, V. (2013). Nitrogen deprivation promotes Populus root growth through global transcriptome reprogramming and activation of hierarchical genetic networks. New Phytologist, 200(2), 483–497.
Wu, W., & Cheng, S. (2014). Root genetic research, an opportunity and challenge to rice improvement. Field Crops Research, 165, 111–124.
Xu, G., Fan, X., & Miller, A. J. (2012). Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology, 63, 153–182.
Zeng, H., Wang, G., Hu, X., Wang, H., Du, L., & Zhu, Y. (2014). Role of microRNAs in plant responses to nutrient stress. Plant and Soil, 374(1–2), 1005–1021.
Acknowledgements
VBS and JAP are thankful to ICAR and CSIR (India) for their fellowships. This work was supported in part by grants to NR from ICAR under NICRA, through CRIDA, Hyderabad, India and the Indian Department of Biotechnology under the NEWS India-UK Virtual Joint Network.
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Sinha, V.B., Jangam, A.P., Raghuram, N. (2020). Biological Determinants of Crop Nitrogen Use Efficiency and Biotechnological Avenues for Improvement. In: Sutton, M.A., et al. Just Enough Nitrogen. Springer, Cham. https://doi.org/10.1007/978-3-030-58065-0_11
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