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The Nitrogen–Potassium Intersection: Membranes, Metabolism, and Mechanism

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The Nitrogen–Potassium Intersection: Membranes, Metabolism, and Mechanism Plant, Cell and Environment (2017) 40,2029–2041 doi: 10.1111/pce.12671 Review The nitrogen–potassium intersection: membranes, metabolism, and mechanism Devrim Coskun, Dev T. Britto & Herbert J. Kronzucker Department of Biological Sciences and the Canadian Centre for World Hunger Research (CCWHR), University of Toronto, 1265 Military Trail, Toronto, Ontario, Canada, M1C 1A4 ABSTRACT likely to rapidly enter plant root cells from the soil, particularly under conditions of high N supply and/or high pH (Coskun Nitrogen (N) and potassium (K) are the two most abundantly et al. 2013b). Because the dominant forms of N available to acquired mineral elements by plants, and their acquisition plants in most soils are the inorganic ions NH + and NO -, pathways interact in complex ways. Here, we review pivotal in- 4 3 however, they, with the K+ ion, will make up the central focus teractions with respect to root acquisition, storage, transloca- of our review. tion and metabolism, between the K+ ion and the two major Another distinction is that K+ ions, once taken up by plants, N sources, ammonium (NH +)andnitrate(NO-). The inter- 4 3 remain in this simple ionic state, while N-containing com- sections between N and K physiology are explored at a number pounds undergo numerous chemical reactions and become of organizational levels, from molecular-genetic processes, to covalently bonded within organic molecules throughout the compartmentation, to whole plant physiology, and discussed plant. This fundamental difference is reflected in the major in the context of both N-K cooperation and antagonism. Nutri- physiological roles the two elements play in plants. Nitrogen tional regulation and optimization of plant growth, yield, is an essential constituent of a vast array of metabolites and metabolism and water-use efficiency are also discussed. structural compounds, including proteins, nucleic acids, chloro- phyll, co-enzymes, phytohormones and secondary metabolites, fl fl Key-words: ammonium; assimilation; ef ux; in ux;nitrate;ni- while the main functions of K+ are as a major osmolyte and trogen-potassium interactions; plant productivity; translocation. source of positive charge for electrical homeostasis and enzyme activation (Evans & Wildes 1971; Leigh & Wyn Jones 1984; Britto & Kronzucker 2008; Marschner 2011). Thus, our discus- sion of the metabolic processes at the intersection of N and K INTRODUCTION physiology will focus on biochemical pathways involving the transformation of nitrogen. Nitrogen (N) and potassium (K) are required for plants to Thirdly, it is interesting that N enters the terrestrial bio- complete their life cycles and are the two nutrients acquired sphere chiefly from the atmosphere as a result of enzymatic in greatest quantities by roots (Oosterhuis et al. 2014). The processes in N -fixing soil bacteria (and today, via the industrial pathways by which these elements are transported and utilized 2 Haber–Bosch process), although weathering of bedrock N by plants intersect in significant ways, including the influences (itself primarily atmospherically derived), which ties up about exerted by potassium ions on nitrogen nutrition and physiol- 20% of the global N pool, can sometimes produce ecologically ogy, and vice versa, in terms of primary uptake of N and K at significant rates of nitrogen release (Holloway & Dahlgren the root plasma membrane, their transport, accumulation and 2002; Xu et al. 2012). By contrast, K+ must be replenished by assimilation within the plant, and the regulation of these meta- weathering of parent rock and release from exchangeable bolic and transport pathways. In this paper, we shall review and non-exchangeable sources, if not supplied as fertilizer what is known about these interactions, with special emphasis (Zhang et al. 2010). on mechanistic processes and plant productivity. + Soil NH4 concentrations tend to range between 0.1 and A few fundamental distinctions between these essential ele- - 1mM, while those of NO tend to be higher, often exceeding ments should be made at the outset. Firstly, while potassium is 3 1mM and reaching 10 mM or even higher following fertilization generally available to plants only as a simple monoatomic, or a burst of nitrification (Wolt 1994; Crawford & Glass 1998; monovalent cation, K+, nitrogen is available in the form of Owen & Jones 2001; Miller et al. 2007). Thus, the molar ratios diverse compounds, for example, as cationic ammonium of soil NO - to NH + typically range between 10 and 100 (Wolt (NH +), anionic nitrate (NO -) or as amino acids, which may 3 4 4 3 1994; Miller et al. 2007). In some soils, however, such as rice be cationic, anionic or zwitterionic, depending on the chemical paddies, bog lands and boreal and montane forests, anaerobic, species and soil pH. In addition, uncharged ammonia, NH ,is 3 acidic and reductive conditions reverse this scenario, with + - Correspondence: H. J. Kronzucker; e-mail: herbert.kronzucker@ NH4 concentrations exceeding those of NO3 (Gillman & Bell utoronto.ca 1978; Kronzucker et al. 1997, 2000). In the case of K+,soil ©2015JohnWiley&SonsLtd 2029 2030 D. Coskun et al. + concentrations tend to be similar to those of NH4 , or about 0.1–1mM (Wolt 1994; White, 2013). In some agricultural areas of the world, including China, India and the Philippines, the relatively small K+ pools are replenished at rates far lower than those of N replenishment, leading to nutritional imbal- ances, reduced productivity and eutrophication by N runoff (Dobermann et al. 1998; Hoa et al. 2006; Andrist-Rangel À et al. 2007; Zhang et al. 2010). The concentrations of NO3 , + + NH4 and K in soils can vary greatly, not only over regional scales but even within relatively small patches (Jungk & Claassen 1986; Wolt 1994; Miller et al. 2007; Cramer et al. 2009). Nitrate levels also tend to show greater heterogeneity in soils and can range over two orders of magnitude across relatively short distances (e.g. 4 m or less; Lark et al. 2004), + + whereas NH4 and K levels tend to vary more narrowly, about one order of magnitude over a similar scale. This is À partially due to the negative charge on NO3 , which results in a high degree of mobility within soils (Miller & Cramer 2004). Plant roots themselves directly increase soil heteroge- neity within the rhizosphere via N-uptake and K-uptake processes, producing zones of depletion (Scherer & Ahrens 1996; Hinsinger et al. 2005; Kayser & Isselstein 2005; Moody & Bell 2006; Andrist-Rangel et al. 2007). Soil concentrations of N and K are important not only Figure 1. The effect of varying levels of soil K+ and N on grain yield. because plant productivity can be limited by their scarcity but (a) The effect of increasing concentrations of N at three K+ levels on also because their excess can bring about toxicity and repress grain yield of barley grown hydroponically (redrawn from MacLeod + growth. Thus, optimum growth and yield curves, which can 1969). (b) The effect of increasing concentrations of K at three N levels fi vary greatly with plant species and environmental factors, are on grain yield of maize grown in the eld (redrawn from Loué 1980). typically seen with respect to these nutrients (Asher & Ozanne 1967; MacLeod 1969; Loué 1980; Britto & Kronzucker 2013). down its transmembrane electrochemical potential gradient, The shapes of such curves can be greatly influenced by the and the substrate’s thermodynamically ‘uphill’ influx into presence of other potentially limiting nutrients. In Fig. 1, this the cell, while passive uptake proceeds ‘downhill’ via ion type of influence is shown for K supply upon N optima (1a), channels (Hedrich & Schroeder 1989; Szczerba et al. 2009; and vice versa (1b). It is notable that the lowest provision Coskun et al. 2013a). It is worth noting that the distinction of K (1a) or N (1b) results in a relatively moderate N or K between HATS and LATS transporters is somewhat blurred, concentration (respectively) required to reach maximum yield and ion channels can at times function at low substrate con- À1 (i.e. about 6 mM Nor70kgha K), but this yield is still much centrations, while active-transporting carriers can operate at lower than can be reached with higher provision of the high concentrations (see succeeding text). In the case of À companion nutrient. NO3 , it is likely that, under most conditions, uptake is ther- modynamically active, because of the inside-negative electri- cal potential difference across the plasma membrane (Wang TRANSPORT et al. 2012). The plethora of transport proteins catalysing À + + It is rather remarkable that the transport functions involved the fluxes of NO3 ,NH4 and K under both HATS and À + + intheuptakeofNO3 ,NH4 and K from soil solution, LATS scenarios, many of which have been identified at the moving these ions across the plasma membrane and into genetic level, is consistent with the spatially and temporally the cytosol of the root cell, share a common feature: all have heterogeneous distributions of these substrates in the soil been characterized using two-mechanism models, which con- (see Introduction Section). However, it has been pointed À sist of saturable, high-affinity and linear, low-affinity trans- out that the transport of NO3 under many field conditions port systems (‘HATS’ and ‘LATS’) generally operating at might be catalysed primarily by low-affinity transporters, À low and high external substrate concentrations, respectively given the relatively high NO3 concentrations in soils, and À (Miller et al. 2007; Szczerba et al. 2009; Zhang et al. 2010). because the expression and activities of high-affinity NO3 + + À For the cations K and NH4 , these two types of transport transporters become down-regulated as soil [NO3 ]rises systems mechanistically contend with the two main thermo- (Miller et al. 2007). dynamic scenarios encountered by roots engaged in cation One of the best known interactions between N and K phys- + uptake: those that require active uptake (HATS conditions) iology in plants is the marked inhibitory effect that NH4 exerts and those that allow passive uptake (LATS conditions).
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