3 Energetics of Nitrogen Acquisition
Annual Plant Reviews book series, Volume 42: Nitrogen Metabolism in Plants in the Post-genomic Era
Arnold J. Bloom,
Arnold J. Bloom
Department of Plant Sciences, University of California at Davis, Davis, CA, 95161 USA
Search for more papers by this authorArnold J. Bloom,
Arnold J. Bloom
Department of Plant Sciences, University of California at Davis, Davis, CA, 95161 USA
Search for more papers by this authorFirst published: 19 April 2018
This article was originally published in 2011 in Nitrogen Metabolism in Plants in the Post-genomic Era, Volume 42 (ISBN ) of the Annual Plant Reviews book series, this volume edited by . The article was republished in Annual Plant Reviews online in April 2018.
Abstract
Plants employ a variety of mechanisms to acquire nitrogen from their environment ranging from carnivory to symbiotic relationships with bacteria. Most plants, however, obtain the majority of their nitrogen as nitrate and ammonium that their roots absorb from soils. To compete successfully against soil micro-organisms for soil nitrate or ammonium, plants adjust their growth, development and physiology to exploit the distinct properties of each ion.
Nitrate is more mobile than ammonium through most soils. Plants can store high concentrations of nitrate, but not ammonium, within their tissues. Yet, assimilation of nitrate into amino acids is far more energy-intensive than that of ammonium. Plants offset some of the energy costs of nitrate assimilation by coupling it with photorespiration. Rising carbon dioxide levels in the atmosphere inhibits photorespiration and, thereby, nitrate assimilation. Therefore, ammonium and nitrate management will become even more critical in the future.
References
- Adamec, L. (1997) Mineral nutrition of carniorous plants: a review. Botanical Reviews 63, 273–295.
- Andrews, M. (1986) The partitioning of nitrate assimilation between root and shoot of higher plants. Plant, Cell and Environment 9, 511–519.
- Baluska, F., Volkmann, D. & Barlow, P.W. (1996) Specialized zones of development in roots: view from the cellular level. Plant Physiology 112, 3–4.
- Bingham, I.J., Blackwood, J.M. & Stevenson, E.A. (1997) Site, scale and time-course for adjustments in lateral root initiation in wheat following changes in C and N supply. Annals of Botany 80, 97–106.
- Bloom, A.J. (1994) Crop acquisition of ammonium and nitrate. In: K.J. Boote, J.M. Bennett, T.R. Sinclair & G.M. Paulsen (eds) Physiology and Determination of Crop Yield. ASA, CSSA, SSSA, Madison, WI, pp. 303–309.
- Bloom, A.J. (1996) Nitrogen dynamics in plant growth systems. Life Support and Biosphere Sciences 3, 35–41.
- Bloom, A.J. (1997a) Interactions between inorganic nitrogen nutrition and root development. Zeitshrift für Pflanzennährung und Bodenkunde 160, 253–259.
-
Bloom, A.J.
(1997b)
Nitrogen as a limiting factor: crop acquisition of ammonium and nitrate. In:
L.E. Jackson (ed.)
Ecology in Agriculture.
Academic Press,
San Diego, CA, pp.
145–172.
10.1016/B978-012378260-1/50006-3 Google Scholar
- Bloom, A.J. (2002) Mineral nutrition. In: L. Taiz & E. Zeiger (eds) Plant Physiology, 3rd edition. Sinauer Associates, Sunderland, MA, pp. 67–86.
- Bloom, A.J. (2010) Global Climate Change: A Convergence of Disciplines. Sinauer Assoc., Sunderland, MA.
- Bloom, A.J., Sukrapanna, S.S. & Warner, R.L. (1992) Root respiration associated with ammonium and nitrate absorption and assimilation by barley. Plant Physiology 99, 1294–1301.
- Bloom, A.J., Jackson, L.E. & Smart, D.R. (1993) Root growth as a function of ammonium and nitrate in the root zone. Plant, Cell and Environment 16, 199–206.
- Bloom, A.J., Meyerhoff, P.A., Taylor, A.R., et al. (2002a) Root development and absorption of ammonium and nitrate from the rhizosphere. Journal of Plant Growth Regulation 21, 416–431.
- Bloom, A.J., Smart, D.R., Nguyen, D.T., et al. (2002b) Nitrogen assimilation and growth of wheat under elevated carbon dioxide. Proceedings of the National Academy of Sciences of the United States of America 99, 1730–1735.
- Bloom, A.J., Zwieniecki, M.A., Passioura, J.B., et al. (2004) Water relations under root chilling in a sensitive and tolerant tomato species. Plant, Cell and Environment 27, 971–979.
- Bloom, A.J., Frensch, J. & Taylor, A.R. (2006) Influence of inorganic nitrogen and pH on the elongation of maize seminal roots. Annals of Botany 97, 867–873.
- Bret-Harte, M.S. & Silk, W.K. (1994a) Fluxes and deposition rates of solutes in growing roots of Zea mays . Journal of Experimental Botany 45, 1733–1742.
- Bret-Harte, M.S. & Silk, W.K. (1994b) Nonvascular, symplasmic diffusion of sucrose cannot satisfy the carbon demands of growth in the primary root tip of Zea mays L. Plant Physiology 105, 19–33.
- Brouwer, R. (1967) Beziehungen zwischen Spross- und Wurzelwachstum. Angewandte Botanik 41, 244–250.
- Brown, L.R., Chandler, W.U., Flavin, J., et al. (1987) State of the World: A Worldwatch Institute Report on Progress toward a Sustainable Society. W.W. Norton & Co, New York.
- Cousins, A.B. & Bloom, A.J. (2003) Influence of elevated CO2 and nitrogen nutrition on photosynthesis and nitrate photoassimilation in maize (Zea mays L.). Plant, Cell and Environment 26, 1525–1530.
- Cousins, A.B. & Bloom, A.J. (2004) Oxygen consumption during leaf nitrate assimilation in a C3 and C4 plant: the role of mitochondrial respiration. Plant, Cell and Environment 27, 1537–1545.
-
Darwin, C.
(1875)
Insectivorous Plants.
John Murray,
London.
10.5962/bhl.title.99933 Google Scholar
-
DeClerck, F. &
Singer, M.J.
(2003)
Looking back 60 years, California soils maintain overall chemical quality.
California Agriculture
57,
38–41.
10.3733/ca.v057n02p38 Google Scholar
- Dixon, K.W., Pate, J.S. & Bailey, W.J. (1980) Nitrogen nutrition of the tuberous sundew Drosera erythrorhiza Lindl. with special reference to catch of arthropod fauna by its glandular leaves. Australian Journal of Botany 28, 283–297.
- Drew, M.C. (1975) Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist 75, 479–490.
- Dukes, J.S., Chiariello, N.R., Cleland, E.E., et al. (2005) Responses of grassland production to single and multiple global environmental changes. PLoS Biology 3, 1829–1837.
- Ellison, A.M. (2006) Nutrient limitation and stoichiometry of carnivorous plants. Plant Biology 8, 740–747.
- Ellison, A.M. & Gotelli, N.J. (2001) Evolutionary ecology of carnivorous plants. Trends in Ecology and Evolution 16, 623–629.
- Ellison, A.M., Gotelli, N.J., Brewer, J.S., et al. (2003) The evolutionary ecology of carnivorous plants. Advances in Ecological Research 33, 1–74.
- Epstein, E. & Bloom, A.J. (2005) Mineral Nutrition of Plants: Principles and Perspectives, 2nd edition. Sinauer Associates, Sunderland, MA.
- Erickson, J.E., Megonigal, J.P., Peresta, G., et al. (2007) Salinity and sea level mediate elevated CO2 effects on C3-C4 plant interactions and tissue nitrogen in a Chesapeake Bay tidal wetland. Global Change Biology 13, 202–215.
- FAOSTAT (2008) Fertilizer Usage. Available at http://faostat.fao.org/site/575/default.aspx#ancor (accessed 2 September 2008).
- Forde, B.G. (2002) The role of long-distance signalling in plant responses to nitrate and other nutrients. Journal of Experimental Botany 53, 39–43.
- Galloway, J.N., Dentener, F.J., Capone, D.G., et al. (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70, 153–226.
- Glass, A.D.M. (1988) Nitrogen uptake by plant roots. ISI Atlas of Science: Animal and Plant Sciences 1, 151–156.
- Govindarajulu, M., Pfeffer, P.E., Jin, H.R., et al. (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819–823.
- Grime, J.P., Crick, J.C. & Rincon, J.E. (1986) The ecological significance of plasticity. In: D.H. Jennings & A.J. Trewavas (eds) Plasticity in Plants. Company of Biologists Limited, Cambridge, pp. 5–29.
- Hackett, C. (1972) A method of applying nutrients locally to roots under controlled conditions, and some morphological effects of locally applied nitrate on the branching of wheat roots. Australian Journal of Biological Sciences 25, 1169–1180.
- Hawkins, H.J., Johansen, A. & George, E. (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant and Soil 226, 275–285.
-
Haynes, R.J.
(1986)
Uptake and assimilation of mineral nitrogen by plants. In:
R.J. Haynes (ed.)
Mineral Nitrogen in the Plant Soil System.
Academic Press,
Orlando, pp.
303–378.
10.1016/B978-0-12-334910-1.50010-8 Google Scholar
- He, X.H., Critchley, C. & Bledsoe, C. (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). Critical Reviews in Plant Sciences 22, 531–567.
- Hobbie, E.A., Colpaert, J.V., White, M.W., et al. (2008) Nitrogen form, availability, and mycorrhizal colonization affect biomass and nitrogen isotope patterns in Pinus sylvestris . Plant and Soil 310, 121–136.
- Idso, S.B., Kimball, B.A. & Hendrix, D.L. (1996) Effects of atmospheric CO2 enrichment on chlorophyll and nitrogen concentrations of sour orange tree leaves. Environmental and Experimental Botany 36, 323–331.
- Igamberdiev, A.U., Bykova, N.V., Lea, P.J., et al. (2001) The role of photorespiration in redox and energy balance of photosynthetic plant cells: a study with a barley mutant deficient in glycine decarboxylase. Physiologia Plantarum 111, 427–438.
- IPCC (2007) Summary for policymakers. In: S. Solomon, D. Qin, M. Manning, et al. (eds) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp. 1–18.
- Jackson, L.E. & Bloom, A.J. (1990) Root distribution in relation to soil nitrogen availability in field-grown tomatoes. Plant and Soil 128, 115–126.
- Keeney, D.R., Chen, R.L. & Graetz, D.A. (1971) Importance of denitrification and nitrate reduction in sediments to nitrogen budgets of lakes. Nature 233, 66–67.
- Kimball, B.A., Idso, S.B., Johnson, S., et al. (2007) Seventeen years of carbon dioxide enrichment of sour orange trees: final results. Global Change Biology 13, 2171–2183.
- Korner, C. (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytologist 172, 393–411.
- Lea, P.J. & Azevedo, R.A. (2006) Nitrogen use efficiency. 1. Uptake of nitrogen from the soil. Annals of Applied Biology 149, 243–247.
- Lea, P.J., Blackwell, R.D. & Joy, K.W. (1992) Ammonia assimilation in higher plants. In: K. Mengel & D.J. Pilbeam (eds) Nitrogen Metabolism of Plants, Vol. 33, Proceedings of the Phytochemical Society of Europe. Clarendon Press, Oxford, pp. 153–186.
- Linkohr, B.I., Williamson, L.C., Fitter, A.H., et al. (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant Journal 29, 751–760.
- Lipson, D. & Nasholm, T. (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128, 305–316.
- Loque, D. & von Wiren, N. (2004) Regulatory levels for the transport of ammonium in plant roots. Journal of Experimental Botany 55, 1293–1305.
- Lundberg, J.O., Weitzberg, E., Cole, J.A., et al. (2004) Opinion: nitrate, bacteria and human health. Nature Reviews Microbiology 2, 593–602.
- Lundquist, P.O. (2005) Carbon cost of nitrogenase activity in Frankia Alnus incana root nodules. Plant and Soil 273, 235–244.
- Marschner, H. (1995) Mineral Nutrition of Higher Plants, 2nd edition. Academic Press, London.
- McIntyre, G.I. (2001) Control of plant development by limiting factors: a nutritional perspective. Physiologia Plantarum 113, 165–175.
- Miller, A.J. & Smith, S.J. (2008) Cytosolic nitrate ion homeostasis: could it have a role in sensing nitrogen status? Annals of Botany 101, 485–489.
- Moreno-Vivian, C., Cabello, P., Martinez-Luque, M., et al. (1999) Prokaryotic nitrate reduction: Molecular properties and functional distinction among bacterial nitrate reductases. Journal of Bacteriology 181, 6573–6584.
- National Research Council (1989) Alternative Agriculture. National Academy Press, Washington, D.C.
- Neff, J.C., Chapin, F.S. & Vitousek, P.M. (2003) Breaks in the cycle: dissolved organic nitrogen in terrestrial ecosystems. Frontiers in Ecology and the Environment 1, 205–211.
- Nolan, B.T. & Hitt, K.J. (2006) Vulnerability of shallow groundwater and drinking-water wells to nitrate in the United States. Environmental Science and Technology 40, 7834–7840.
- Nye, P.H. & Tinker, P.B. (1977) Solute Movement in the Soil-Root System. University of California Press, Berkeley, CA.
- Pate, J.S. (1973) Uptake, assimilation and transport of nitrogen compounds by plants. Soil Biology and Biochemistry 5, 109–119.
-
Pate, J.S. &
Layzell, D.B.
(1990)
Energetics and biological costs of nitrogen assimilation. In:
B.J. Miflin,
P. Lea (eds)
The Biochemistry of Plants, Intermediary Nitrogen Metabolism, Vol.
16.
Academic Press,
San Diego, CA, pp.
1–42.
10.1016/B978-0-08-092616-2.50007-3 Google Scholar
- Paungfoo-Lonhienne, C., Lonhienne, T.G.A., Rentsch, D., et al. (2008) Plants can use protein as a nitrogen source without assistance from other organisms. Proceedings of the National Academy of Sciences of the United States of America 105, 4524–4529.
- 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, 11506–11510.
- Rasse, D.P., Peresta, G. & Drake, B.G. (2005) Seventeen years of elevated CO2 exposure in a Chesapeake Bay Wetland: sustained but contrasting responses of plant growth and CO2 uptake. Global Change Biology 11, 369–377.
- Reis, V.M., Baldani, J.I., Baldani, V.L.D., et al. (2000) Biological dinitrogen fixation in gramineae and palm trees. Critical Reviews in Plant Sciences 19, 227–247.
-
Rhodes, D.,
Nadolska-Orczyk, A. &
Rich, P.J.
(2002)
Salinity, osmolytes and compatible solutes. In:
A. Läuchli &
U. Lüttge (eds)
Salinity: Environment-Plants-Molecules.
Kluwer Academic Publishers,
Dordrecht, pp.
181–204.
10.1007/0-306-48155-3_9 Google Scholar
- Ritchie, R.J. (2006) Estimation of cytoplasmic nitrate and its electrochemical potential in barley roots using (NO3 −)−13 N and compartmental analysis. New Phytologist 171, 643–655.
- Robinson, D., Hodge, A., Griffiths, B.S., et al. (1999) Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proceedings of the Royal Society of London Series B 266, 431–435.
- Robinson, J.M. & Baysdorfer, C. (1985) Interrelationships between photosynthetic carbon and nitrogen metabolism in mature soybean leaves and isolated leaf mesophyll cells. In: R.L. Heath & J. Preiss (eds) Regulation of Carbon Partitioning in Photosynthetic Tissue. American Association of Plant Physiologists, Rockville, MD, pp. 333–357.
- Salvagiotti, F., Cassman, K.G., Specht, J.E., et al. (2008) Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crops Research 108, 1–13.
- Sattelmacher, B. & Thoms, K. (1989) Root growth and 14C-translocation into the roots of maize (Zea mays L.) as influenced by local nitrate supply. Zeitshrift für Pflanzennährung und Bodenkunde 152, 7–10.
- Schulze, E.D., Gebauer, G., Schulze, W., et al. (1991) The utilization of nitrogen from insect capture by different growth forms of Drosera from Southwest Australia. Oecologia 87, 240–246.
- Schulze, W. & Schulze, E.D. (1990) Insect capture and growth of the insectivorous Drosera rotundifolia L. Oecologia 82, 427–429.
- Searles, P.S. & Bloom, A.J. (2003) Nitrate photoassimilation in tomato leaves under short-term exposure to elevated carbon dioxide and low oxygen. Plant, Cell and Environment 26, 1247–1255.
- Siebrecht, S., Mack, G. & Tischner, R. (1995) Function and contribution of the root tip in the induction of NO3- uptake along the barley root axis. Journal of Experimental Botany 46, 1669–1676.
- Smart, D.R. & Bloom, A.J. (1998) Investigations of ion absorption during NH4 +exposure I. Relationship between H+ efflux and NO3 −absorption. Journal of Experimental Botany 49, 95–100.
- Taylor, A.R. & Bloom, A.J. (1998) Ammonium, nitrate, and proton fluxes along the maize root. Plant, Cell and Environment 21, 1255–1263.
- Vessey, J.K. (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant and Soil 255, 571–586.
- Vessey, J.K., Pawlowski, K. & Bergman, B. (2005) Root-based N2-fixing symbioses: legumes, actinorhizal plants, Parasponia sp and cycads. Plant and Soil 274, 51–78.
- Voisin, A.S., Salon, C., Jeudy, C., et al. (2003) Symbiotic N2 fixation activity in relation to C economy of Pisum sativum L. as a function of plant phenology. Journal of Experimental Botany 54, 2733–2744.
- Walter, A., Feil, R. & Schurr, U. (2003) Expansion dynamics, metabolite composition and substance transfer of the primary root growth zone of Zea mays L. grown in different external nutrient availabilities. Plant, Cell and Environment 26, 1451–1466.
- Williams, L.E. & Miller, A.J. (2001) Transporters responsible for the uptake and partitioning of nitrogenous solutes. Annual Review of Plant Physiology and Plant Molecular Biology 52, 659–688.
- Wray, L.V., Ferson, A.E., Rohrer, K., et al. (1996) TnrA, a transcription factor required for global nitrogen regulation in Bacillus subtilis . Proceedings of the National Academy of Sciences of the United States of America 93, 8841–8845.
- Zhang, H. & Forde, B.G. (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407–409.
- Zhang, H.M., Jennings, A., Barlow, P.W., et al. (1999) Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences of the United States of America 96, 6529–6534.
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