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Plant Nitrogen Uptake and Assimilation: Regulation of Cellular Ph Homeostasis applyparastyle "fig//caption/p[1]" parastyle "FigCapt" Journal of Experimental Botany, Vol. 71, No. 15 pp. 4380–4392, 2020 doi:10.1093/jxb/eraa150 Advance Access Publication 24 March 2020 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) REVIEW PAPER Plant nitrogen uptake and assimilation: regulation of cellular pH homeostasis Huimin Feng1,2, Xiaorong Fan1,2, Anthony J. Miller3, and Guohua Xu1,2,*, 1 State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing, China 2 MOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Nanjing Agricultural University, Nanjing 210095, China 3 Metabolic Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK * Correspondance: [email protected] Received 22 November 2019; Editorial decision 17 March 2020; Accepted 19 March 2020 Editor: Hideki Takahashi, Michigan State University, USA Abstract The enzymatic controlled metabolic processes in cells occur at their optimized pH ranges, therefore cellular pH homeostasis is fundamental for life. In plants, the nitrogen (N) source for uptake and assimilation, mainly in the forms – + of nitrate (NO3 ) and ammonium (NH4 ) quantitatively dominates the anion and cation equilibrium and the pH balance in cells. Here we review ionic and pH homeostasis in plant cells and regulation by N source from the rhizosphere to extra- and intracellular pH regulation for short- and long-distance N distribution and during N assimilation. In the pro- cess of N transport across membranes for uptake and compartmentation, both proton pumps and proton-coupled N transporters are essential, and their proton-binding sites may sense changes of apoplastic or intracellular pH. In addition, during N assimilation, carbon skeletons are required to synthesize amino acids, thus the combination of – + NO3 or NH4 transport and assimilation results in different net charge and numbers of protons in plant cells. Efficient maintenance of N-controlled cellular pH homeostasis may improve N uptake and use efficiency, as well as enhance the resistance to abiotic stresses. Keywords: Ammonium, assimilation, ATPase, charge balance, cellular pH, homeostasis, nitrate, pump, transport, uptake. Introduction Nitrogen (N) is required for plants to complete their life varies within different intracellular compartments and the cycles and is the most important nutrient acquired in greatest proton gradient is important for the viability of cells (Shen quantities by roots (Xu et al., 2012; Oosterhuis et al., 2014). et al., 2013). – + NO3 and NH4 are the most prominent forms of inorganic Within plant cells, several compartments with different pH N taken up by land plant species, and their root uptake rap- exist in parallel. The cytosol has pH values at 7.2–7.4 to en- idly causes primary effects on ionic and pH balance in plant sure proper biochemical reactions (Schumacher, 2014), while cells. Cellular homeostasis of ions and pH is fundamental to the vacuole and apoplast maintain more acidic pH levels at basic cellular processes and is needed to maintain normal plant 5.0–5.5 (Felle, 2001; Martinière et al., 2013a; Shen et al., 2013; growth and development as well as responses to stresses (Bassil Schumacher, 2014). Cytoplasmic pH (pHc) homeostasis is the and Blumwald, 2014; Reguera et al., 2015). In addition, pH result of a variety of processes. First, cytoplasmic chemical buf- fering components, such as bicarbonate, phosphate, and protein © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Nitrogen regulation of cellular pH homeostasis | 4381 + + buffers, play important roles in stabilizing pHc (Kurkdjian and influence on the membrane potential, namely K –NH4 com- + – Guern, 1989). Secondly, the physical pH-stat, which is proton petition and K –NO3 cooperation (Li et al., 2016; reviewed + + transport across membranes, contributes to pHc homeostasis by Coskun et al., 2017). NH4 competes with low-affinity K (Felle 2001; Britto and Kronzucker, 2005). The maintenance uptake and accumulation (Wang et al., 1996; Szczerba et al., of optimal pH in plant cells has to be tightly regulated and 2008; Hoopen et al., 2010; Chen et al., 2015). The acquisition + + – is established by different primary active H pumping com- rates of cationic K and anionic NO3 are often found to be plexes, such as the plasma membrane (PM) or P-type H+- positively correlated, probably due to improved charge balance + – ATPase (PM-ATPase), vacuolar H -ATPase (V-ATPase), and or activation of the enzymes involved in NO3 assimilation the vacuolar H+-pyrophosphatase (V-PPase) (Schumacher, (Hagin et al., 1990; Roosta and Schjoerring, 2008; Balkos et al., – 2006; Gaxiola et al., 2007; Marshansky and Futai, 2008). The 2010; Yang et al., 2014; Xia et al., 2015). NO3 is transported P-type ATPases can be present in both the PM and vacuole (Li from root to shoot with K+ as a counter ion in the xylem; thus, + – et al., 2016). The physical pH-stat is also determined by trans- limited K supply can result in high accumulations of NO3 in port of other ions to maintain the electrochemical balance, roots (Rufty et al., 1981; Förster and Jeschke, 1993). Knockout and H+-coupled ion transporters contribute to intracellular of the nitrate transporter AtNPF7.3/NRT1.5 in Arabidopsis – pH homeostasis (Gerendás and Schurr, 1999; Reguera et al., and OsNPF2.4 in rice not only decreased NO3 loading to 2015). Thirdly, a biochemical pH-stat participates in pHc regu- xylem sap, but also limited K+ content in the xylem (Lin et al., lation, including the metabolic processes of proton production 2008; Xia et al., 2015; Li et al., 2017), indicating the interaction – + or consumption, and organic acid production or degradation of NO3 and K in plant cells. – (Raven and Smith, 1976; Felle, 2001; Britto and Kronzucker, In the vacuole, the monovalent anions NO3 , malate, and 2005). For example, the malate anion shuttle between the Cl– show an interaction; for example, the Cl– concentra- – cytosol and vacuole is an important element of pHc regulation tion in leaves can be reduced by the NO3 supply (Glass and (Raven and Smith, 1976; Felle, 2001; Britto and Kronzucker, Siddiqi, 1985; Guo et al., 2017). Two maize nitrate transporters, – + – 2005). The primary root acquisition of NO3 and/or NH4 ZmNPF6.4 and ZmNPF6.6, are permeable to both NO3 and dominates anion and cation balance in plant cells, with up- Cl– (Wen et al., 2017), indicating that the two anions could take and vacuolar storage driven by PM-ATPases, V-ATPases, be facilitated by the similar transport systems in plants. There and V-PPases, while they consume energy and are essential are also chloride-specific MATE transporters in the vacuolar components of cellular pH homeostasis providing a ‘physical membrane (Zhang et al., 2017). Diurnal changes in vacuolar – + pH-stat’ (Serrano, 1990; Barkla and Pantoja, 1996; Sze et al., malate have been observed to compensate for NO3 and K 1999; Martinoia et al., 2000; Palmgren, 2001). In addition, the fluctuations (Niedziela et al., 1993). – + processes of NO3 and NH4 assimilation inside the cell are considered to consume or produce protons, contributing to Instant response of cellular membrane potential ‘biochemical pH-stat’ (Britto and Kronzucker, 2005; Fan et al., – and pH 2016, 2017). In addition, NO3 reduction leads to biochemical pH-stat by increasing malate and other organic acid anions The cell membrane potential (∆Ψ, negative inside the cell (van Beusichem et al., 1988; Lüttge et al., 2000; Pasqualini et al., compared with outside the cell) can be affected by fluxes of 2001). charged ions across the PM. An immediate physiological re- + – In this review, we summarize the general behaviours of N sponse of root cells to NH4 and NO3 exposure is a transient + – uptake, distribution, and assimilation inducing changes in plant change of ∆Ψ, which is caused by NH4 and NO3 influx cellular and rhizosphere pH. We discuss the regulatory mech- carrying H+ into the cell and compensated by activation of the anisms of the maintenance of cellular pH under altered N sup- PM H+-ATPase to repolarize and maintain ∆Ψ (Ullrich and plies in both physiology and molecular aspects. Novacky, 1990; Wang et al., 1994; Liu et al., 2017). However, the initial membrane depolarization was not commensurate + with the increased influx of NH3/NH4 (pKa 9.25) at pH Regulation of pH by N acquisition: from cell 6.25 in the medium in roots of barley, suggesting that the in- creased transport of electroneutral NH3 dominates uptake to rhizosphere – + (Coskun et al., 2013). NO3 is co-transported with H through – + In response to the uptake of varied N forms, plants change a symporter into cells, and the stoichiometry of NO3 and H – their ionic balance, cellular transmembrane electric potentials, is ~2 (Glass et al., 1992; Miller and Smith, 1996). Root NO3 and proton pumping activity, resulting in altered cellular and acquisition commonly leads to ∆Ψ depolarization of the cells rhizosphere pH. suggesting an H+ stoichiometry >1 (Meharg and Blatt, 1995; Mistrik and Ullrich, 1996; Britto and Kronzucker, 2005). It is controversial whether such transport
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