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Does energy cost constitute the primary cause of ammonium toxicity in plants?

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Abstract

Nitrate (NO3) and ammonium (NH4+) are the main nitrogen (N) sources and key determinants for plant growth and development. In recent decades, NH4+, which is a double-sided N compound, has attracted considerable amounts of attention from researchers. Elucidating the mechanisms of NH4+ toxicity and exploring the means to overcome this toxicity are necessary to improve agricultural sustainability. In this review, we discuss the current knowledge concerning the energy consumption and production underlying NH4+ metabolism and toxicity in plants, such as N uptake; assimilation; cellular pH homeostasis; and functions of the plasma membrane (PM), vacuolar H+-ATPase and H+-pyrophosphatase (H+-PPase). We also discuss whether the overconsumption of energy is the primary cause of NH4+ toxicity or constitutes a fundamental strategy for plants to adapt to high-NH4+ stress. In addition, the effects of regulators on energy production and consumption and other physiological processes are listed for evaluating the possibility of high energy costs associated with NH4+ toxicity. This review is helpful for exploring the tolerance mechanisms and for developing NH4+-tolerant varieties as well as agronomic techniques to alleviate the effects of NH4+ stress in the field.

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References

  • Apudo AA, Cao Y, Wakibia J, Li W, Liu F (2016) Physiological plastic responses to acute NH4+-N toxicity in Myriophyllum spicatum L. cultured in high and low nutrient conditions. Environ Exp Bot 130:79–85

    Article  CAS  Google Scholar 

  • Ariz I, Artola E, Asensio AC, Cruchaga S, Aparicio-Tejo PM, Moran JF (2011) High irradiance increases NH4+ tolerance in Pisum sativum: higher carbon and energy availability improve ion balance but not N assimilation. J Plant Physiol 168:1009–1015

    Article  CAS  PubMed  Google Scholar 

  • Ariz I, Asensio AC, Zamarreño AM, García-Mina JM, Aparicio-Tejo PM, Moran JF (2013) Changes in the C/N balance caused by increasing external ammonium concentrations are driven by carbon and energy availabilities during ammonium nutrition in pea plants: the key roles of asparagine synthetase and anaplerotic enzymes. Physiol Plantarum 148(4):522–537. https://doi.org/10.1111/j.1399-3054.2012.01712.x

    Article  CAS  Google Scholar 

  • Babourina O, Voltchanskii K, McGann B, Newman I, Rengel Z (2007) Nitrate supply affects ammonium transport in canola roots. J Exp Bot 58(3):651–658. https://doi.org/10.1093/jxb/erl238

    Article  CAS  PubMed  Google Scholar 

  • Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942

    Article  PubMed  CAS  Google Scholar 

  • Bai L, Ma X, Zhang G, Song S, Zhou Y, Gao L, Miao Y, Song CP (2014) A receptor-like kinase mediates ammonium homeostasis and is important for the polar growth of root hairs in Arabidopsis. Plant Cell 26(4):1497–1511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balkos KD, Britto DT, Kronzucker HJ (2010) Optimization of ammonium acquisition and metabolism by potassium in rice (Oryza sativa L. cv. IR-72). Plant Cell Environ 33(1):23–34

    CAS  PubMed  Google Scholar 

  • Barreto RF, de Mello PR, Lúcio JCB, López-Díaz I, Carrera E, Carvalho RF (2021) Ammonium toxicity alleviation by silicon is dependent on cytokinins in tomato cv. Micro-Tom J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10314-5

    Article  Google Scholar 

  • Bejarano I, Marino D, Coleto I (2021) Arabidopsis MYB28 and MYB29 transcription factors are involved in ammonium-mediated alterations of root-system architecture. Plant Signal Behav 16(4):1879532. https://doi.org/10.1080/15592324.2021.1879532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bittsánszky A, Pilinszky K, Gyulai G, Komives T (2015) Overcoming ammonium toxicity. Plant Sci 231:184–190. https://doi.org/10.1016/j.plantsci.2014.12.005

    Article  CAS  PubMed  Google Scholar 

  • Blacquiere T, Hofstra R, Stulen I (1987) Ammonium and nitrate nutrition in Plantago lanceolata and Plantago major L. spp. major. I. Aspects of growth, chemical composition and root respiration. Plant Soil 104:129–141

    Article  CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2002) NH4+ toxicity in higher plants: a critical review. J Plant Physiol 159:567–584

    Article  CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2005) Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms. Plant Cell Environ 28:1396–1409

    Article  CAS  Google Scholar 

  • Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2001) Futile transmembrane NH4+ cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258. https://doi.org/10.1073/pnas.061034698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brix H, Dyhr-Jensen K, Lorenzen B (2002) Root-zone acidity and nitrogen source affects Typha latifolia L. growth and uptake kinetics of ammonium and nitrate. J Exp Bot 53(379):2441–2450

    Article  CAS  PubMed  Google Scholar 

  • Cao T, Ni LY, Xie P (2004) Acute biochemical responses of a submersed macrophyte, Potamogeton crispus L., to high ammonium in an aquarium experiment. J Freshw Ecol 19:279–284. https://doi.org/10.1080/02705060.2004.9664542

    Article  CAS  Google Scholar 

  • Carr NF, Boaretto RM, Mattos D Jr (2020) Coffee seedlings growth under varied NO3-:NH4+ ratio: consequences for nitrogen metabolism, amino acids profile, and regulation of plasma membrane H+-ATPase. Plant Physiol Biochem 154:11–20. https://doi.org/10.1016/j.plaphy.2020.04.042

    Article  CAS  PubMed  Google Scholar 

  • Chaillou S, Vessey JK, Morot-Gaudry JF, Raper CD Jr, Henry LT, Boutin JP (1991) Expression of characteristics of ammonium nutrition as affected by pH of the root medium. J Exp Bot 42:189–196

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Guo S, Kronzucker HJ, Shi W (2013) Nitrogen use efficiency (NUE) in rice links to NH4+ toxicity and futile NH4+ cycling in roots. Plant Soil 369(1):351–363. https://doi.org/10.1007/s11104-012-1575-y

    Article  CAS  Google Scholar 

  • Chen HY, Chen YN, Wang HY, Liu ZT, Frommer WB, Ho CH (2020) Feedback inhibition of AMT1 NH4+-transporters mediated by CIPK15 kinase. BMC Biol 18:196. https://doi.org/10.1186/s12915-020-00934-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coleto I, Bejarano I, Marín-Peña AJ, Medina J, Rioja C, Burow M, Marino D (2021) Arabidopsis thaliana transcription factors MYB28 and MYB29 shape ammonium stress responses by regulating Fe homeostasis. New Phytol 229(2):1021–1035. https://doi.org/10.1111/nph.16918

    Article  CAS  PubMed  Google Scholar 

  • Coskun D, Britto DT, Li MY, Becker A, Kronzucker HJ (2013) Rapid ammonia gas transport accounts for futile transmembrane cycling under NH3/NH4+ toxicity in plant roots. Plant Physiol 163:1859–1867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cruz C, Bio AFM, Domínguez-Valdivia MD, Aparicio-Tejo PM, Lamsfus C, Martins-Louҫão MA (2006) How does glutamine synthetase activity determine plant tolerance to ammonium? Planta 223:1068–1080

    Article  CAS  PubMed  Google Scholar 

  • de la Peña M, González-Moro MB, Marino D (2019) Providing carbon skeletons to sustain amide synthesis in roots underlines the suitability of Brachypodium distachyon for the study of ammonium stress in cereals. AoB Plants 11(3):plz029

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De la Peña M, Javier Marín-Peña A, Urmeneta L, Coleto I, Castillo-González J, van Liempd SM, Falcón-Pérez JM, Álvarez-Fernández A, González-Moro MB, Marino D (2022) Ammonium nutrition interacts with iron homeostasis in Brachypodium distachyon. J Exp Bot 73:263–274. https://doi.org/10.1093/jxb/erab427

    Article  CAS  PubMed  Google Scholar 

  • de Souza Junior JP, Prado RDM, de Morais TCB, Frazão JJ, dos Santos Sarah MM, de Oliveira KR, de Paula RC (2021) Silicon fertigation and salicylic acid foliar spraying mitigate ammonium deficiency and toxicity in Eucalyptus spp. clonal seedlings. PLoS ONE 16(4):e0250436. https://doi.org/10.1371/journal.pone.0250436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di DW, Sun L, Zhang XN, Li GJ, Kronzucker HJ, Shi W (2018) Involvement of auxin in the regulation of ammonium tolerance in rice (Oryza sativa L.). Plant Soil 432:373–387

    Article  CAS  Google Scholar 

  • Di DW, Sun L, Wang M, Wu J, Kronzucker HJ, Fang S, Chu J, Shi W, Li G (2021) WRKY46 promotes ammonium tolerance in Arabidopsis by repressing NUDX9 and IAA-conjugating genes and by inhibiting NH4+ efflux in the root elongation zone. New Phytol 232:190–207. https://doi.org/10.1111/nph.17554

    Article  CAS  PubMed  Google Scholar 

  • Dou YY, Wang BZ, Chen LY, Yin DQ (2013) Alleviating versus stimulating effects of bicarbonate on the growth of Vallisneria natans under ammonia stress. Environ Sci Pollut Res 20:5281–5288. https://doi.org/10.1007/s11356-013-1514-3

    Article  CAS  Google Scholar 

  • Du WY, Zhang YX, Si JS, Zhang Y, Fan SJ, Xia HY, Kong LA (2021) Nitrate alleviates ammonium toxicity in wheat (Triticum aestivum L.) by regulating tricarboxylic acid cycle and reducing rhizospheric acidification and oxidative damage. Plant Signal Behav. https://doi.org/10.1080/15592324.2021.1991687

    Article  PubMed  PubMed Central  Google Scholar 

  • Escobar MA, Geisler DA, Rasmusson AG (2006) Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate. Plant J 45:775–788

    Article  CAS  PubMed  Google Scholar 

  • Esteban R, Ariz I, Cruz C, Moran JF (2016) Mechanisms of ammonium toxicity and the quest for tolerance. Plant Sci 248:92–101

    Article  CAS  PubMed  Google Scholar 

  • Falhof J, Pedersen JT, Fuglsang AT, Palmgren M (2016) Plasma membrane H+-ATPase regulation in the center of plant physiology. Mol Plant 9:323–337. https://doi.org/10.1016/j.molp.2015.11.002

    Article  CAS  PubMed  Google Scholar 

  • Gao J, Liu L, Ma N, Yang J, Dong Z, Zhang J, Zhang JL, Cai M (2020) Effect of ammonia stress on carbon metabolism in tolerant aquatic plant-Myriophyllum aquaticum. Environ Pollut 263:114412

    Article  CAS  PubMed  Google Scholar 

  • Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214. https://doi.org/10.1016/j.febslet.2007.03.050

    Article  CAS  PubMed  Google Scholar 

  • Geisseler D, Doane TA, Horwath WR (2009) Determining potential glutamine synthetase and glutamate dehydrogenase activity in soil. Soil Biol Biochem 41(8):1741–1749

    Article  CAS  Google Scholar 

  • González-Moro MB, González-Moro I, de la Peña M, Estavillo JM, Aparicio-Tejo PM, Marino D, González-Murua C, Vega-Mas I (2021) A multi-species analysis defines anaplerotic enzymes and amides as metabolic markers for ammonium nutrition. Front Plant Sci 11:632285. https://doi.org/10.3389/fpls.2020.632285

    Article  PubMed  PubMed Central  Google Scholar 

  • Guan M, de Bang TC, Pedersen C, Schjoerring JK (2016) Cytosolic glutamine synthetase Gln1;2 is the main isozyme contributing to GS1 activity and can be up-regulated to relieve ammonium toxicity. Plant Physiol 171(3):1921–1933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo S, Schinner K, Sattelmacher B, Hansen UP (2005) Different apparent CO2 compensation points in nitrate- and ammonium-grown Phaseolus vulgaris and the relationship to non-photorespiratory CO2 evolution. Physiol Plantarum 123:288–301

    Article  CAS  Google Scholar 

  • Hachiya T, Sakakibara H (2017) Interactions between nitrate and ammonium in their uptake, allocation, assimilation, and in plants. J Exp Bot 68:2501–2512

    CAS  PubMed  Google Scholar 

  • Hachiya T, Watanabe CK, Boom C, Tholen D, Takahara K, Kawai-Yamada M, Uchimiya H, Uesono Y, Terashima I, Noguchi K (2010) Ammonium-dependent respiratory increase is dependent on the cytochrome pathway in Arabidopsis thaliana shoots. Plant Cell Environ 33:1888–1897

    Article  CAS  PubMed  Google Scholar 

  • Hachiya T, Watanabe CK, Fujimoto M, Ishikawa T, Takahara K, Kawai-Yamada M, Uchimiya H, Uesono Y, Terashima I, Noguchi K (2012) Nitrate addition alleviates ammonium toxicity without lessening ammonium accumulation, organic acid depletion and inorganic cation depletion in Arabidopsis thaliana shoots. Plant Cell Physiol 53(3):577–591. https://doi.org/10.1093/pcp/pcs012

    Article  CAS  PubMed  Google Scholar 

  • Hachiya T, Inaba J, Wakazaki M, Sato M, Toyooka K, Miyagi A, Kawai-Yamada M, Sugiura D, Nakagawa T, Kiba T, Gojon A, Sakakibara H (2021) Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana. Nat Commun 12:4944. https://doi.org/10.1038/s41467-021-25238-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howitt SM, Udvardi MK (2000) Structure, function and regulation of ammonium transporters in plants. BBA-Biomembranes 1465:152–170. https://doi.org/10.1016/S0005-2736(00)00136-X

    Article  CAS  PubMed  Google Scholar 

  • Husted S, Schjoerring JK (1995) Apoplastic pH and ammonium concentration in leaves of Brassica napus L. Plant Physiol 109:1453–1460. https://doi.org/10.1104/pp.109.4.1453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ijato T, Porras-Murillo R, Ganz P, Ludewig U, Neuhäuser B (2021) Concentration-dependent physiological and transcriptional adaptations of wheat seedlings to ammonium. Physiol Plantarum 171(3):28–342

    Article  CAS  Google Scholar 

  • Jia L, Xie Y, Wang Z, Luo L, Zhang C, Pélissier PM, Parizot B, Qi W, Zhang J, Hu Z, Motte H, Luo L, Xu G, Beeckman T, Xuan W (2020) Rice plants respond to ammonium stress by adopting a helical root growth pattern. Plant J 104(4):1023–1037

    Article  CAS  PubMed  Google Scholar 

  • Jian S, Liao Q, Song H, Liu Q, Lepo JE, Guan C, Zhang J, Ismail AM, Zhang Z (2018) NRT1.1-related NH4+ toxicity is associated with a disturbed balance between NH4+ uptake and assimilation. Plant Physiol 178:1473–1488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jossier M, Bouly JP, Meimoun P, Arjmand A, Lessard P, Hawley S, Grahame Hardie D (2009) SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J 59:316–328

    Article  CAS  PubMed  Google Scholar 

  • Kempinski CF, Haffar R, Barth C (2011) Toward the mechanism of NH4+ sensitivity mediated by Arabidopsis GDP-mannose pyrophosphorylase. Plant Cell Environ 34:847–858

    Article  CAS  PubMed  Google Scholar 

  • Körner S, Das SK, Veenstra S, Vermaat JE (2001) The effect of pH variation at the ammonium/ammonia equilibrium in wastewater and its toxicity to Lemna gibba. Aquat Bot 71:71–78

    Article  Google Scholar 

  • Lacoul P, Freedman B (2006) Environmental influences on aquatic plants in freshwater ecosystems. Freshw Rev 14:89–136

    Google Scholar 

  • Lasa B, Frechilla S, Apricio-Tejo PM, Lamsfus C (2002) Alternative pathway respiration is associated with ammonium ion sensitivity in spinach and pea plants. Plant Growth Regul 37:49–55

    Article  CAS  Google Scholar 

  • Li Q, Li BH, Kronzucker HJ, Shi WM (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 Environ 33:1529–1542

    CAS  PubMed  Google Scholar 

  • Li G, Zhang L, Wang M, Di D, Kronzucker HJ, Shi W (2019) The Arabidopsis AMOT1/EIN3 gene plays an important role in the amelioration of ammonium toxicity. J Exp Bot 70:375–1388

    Article  CAS  Google Scholar 

  • Li S, Liu C, Tan X, Tan B, He Y, Li N (2020) Interactive effects of light and nitrogen on Pakchoi (Brassica chinensis L.) growth and soil enzyme activity in an underground environment. Agronomy 10:1772. https://doi.org/10.3390/agronomy10111772

    Article  CAS  Google Scholar 

  • Liang G, Song H, Xiao Y, Zhang Z (2021) Ammonium accumulation caused by reduced tonoplast V-ATPase activity in Arabidopsis thaliana. Int J Mol Sci 22:2. https://doi.org/10.3390/jims22010002

    Article  CAS  Google Scholar 

  • Liu Y, von Wirén N (2017) Ammonium as a signal for physiological and morphological responses in plants. J Exp Bot 63:3777–3788

    Google Scholar 

  • Liu Y, Sun J, Tian Z, Hakeem A, Wang F, Jiang D, Cao W, Adkins SW, Dai T (2017) Physiological responses of wheat (Triticum aestivum L.) germination to elevated ammonium concentrations: reserve mobilization, sugar utilization, and antioxidant metabolism. Plant Growth Regul 81:209–220

    Article  CAS  Google Scholar 

  • Liu L, Bi XY, Sheng S, Gong YY, Pu WX, Ke J, Huang PJ, Yang YL, Liu LH (2021a) Evidence that exogenous urea acts as a potent cue to alleviate ammonium-inhibition of root system growth of cotton plant (Gossypium hirsutum). Physiol Plantarum 171(1):137–150. https://doi.org/10.1111/ppl.13222

    Article  CAS  Google Scholar 

  • Liu Y, Li YX, Li YX, Tian ZW, Hu JL, Adkins S, Dai TB (2021b) Changes of oxidative metabolism in the roots of wheat (Triticum aestivum L.) seedlings in response to elevated ammonium concentrations. J Integr Agri 20(5):1216–1228

    Article  CAS  Google Scholar 

  • Luo J, Qin JL, Li H, Liu TX, Polle A, Peng CH, Luo ZB (2013) Net fluxes of ammonium and nitrate in connection with plasma membrane H+-ATPases in fine roots of Populus popularis. Planta 237:919–931. https://doi.org/10.1007/s00425-012-1807-7

    Article  CAS  PubMed  Google Scholar 

  • Ma XL, Zhu CH, Yang N, Gan LJ, Xia K (2016) γ-Aminobutyric acid addition alleviates ammonium toxicity by limiting ammonium accumulation in rice (Oryza sativa) seedlings. Physiol Plantarum 158:389–401

    Article  CAS  Google Scholar 

  • Magalháes J, Huber D, Tsai C (1992) Evidence of increased 15N-ammonium assimilation in tomato plants with exogenous α-ketoglutarate. Plant Sci 85:135–141

    Article  Google Scholar 

  • Moda LR, de Mello PR, de Souza Júnior JP, da Silva Júnior GB, dos Santos LCN, Soares MVG, Kadyampakeni DM (2021) Response of orange seedlings to the proportion of nitrate-ammonium in the nutrient solution and the benefits of phosphorus in ammonia toxicity. Sci Hortic 285:110166. https://doi.org/10.1016/j.scienta.2021.110166

    Article  CAS  Google Scholar 

  • Ochieng W, Xian L, Nasimiyu AT, Muthui SW, Ndirangu LN, Otieno DO, Wan T, Liu F (2021) Exploring the ammonium detoxification mechanism of young and mature leaves of the macrophyte Potamogeton lucens. Aqua Toxicol 237:105879. https://doi.org/10.1016/j.aquatox.2021.105879

    Article  CAS  Google Scholar 

  • Omari RE, Rueda-López M, Avila C, Crespillo R, Nhiri M, Cánovas FM (2010) Ammonium tolerance and the regulation of two cytosolic glutamine synthetases in the roots of sorghum. Funct Plant Biol 37:55–63

    Article  CAS  Google Scholar 

  • Podgórska A, Gieczewska K, Łukawska-Kuźma K, Rasmusson AG, Gardeström P, Szal B (2013) Long-term ammonium nutrition of Arabidopsis increases the extrachloroplastic NAD(P)H/NAD(P)+ ratio and mitochondrial reactive oxygen species level in leaves but does not impair photosynthetic capacity. Plant Cell Environ 36:2034–2045. https://doi.org/10.1111/pce.12113

    Article  CAS  PubMed  Google Scholar 

  • Podgórska A, Ostaszewska-Bugajska M, Borysiuk K, Tarnowska A, Jakubiak M, Burian M, Rasmusson AG, Szal B (2018) Suppression of external NADPH dehydrogenase-NDB1 in Arabidopsis thaliana confers improved tolerance to ammonium toxicity via efficient glutathione/redox metabolism. Int J Mol Sci 19:1412. https://doi.org/10.3390/ijms19051412

    Article  CAS  PubMed Central  Google Scholar 

  • Poucet T, González-Moro MB, Cabasson C, Beauvoit B, Gibon Y, Dieuaide-Noubhani M, Marino D (2021) Ammonium supply induces differential metabolic adaptive responses in tomato according to leaf phenological stage. J Exp Bot 72(8):3185–3199

    Article  CAS  PubMed  Google Scholar 

  • Roosta HR, Schjoerring JK (2008a) Effects of nitrate and potassium on ammonium toxicity in cucumber plants. J Plant Nutr 31(7):1270–1283

    Article  CAS  Google Scholar 

  • Roosta HR, Schjoerring JK (2008b) Root carbon enrichment alleviates ammonium toxicity in cucumber plants. J Plant Nutr 31:941–958. https://doi.org/10.1080/0190416080204327

    Article  CAS  Google Scholar 

  • Setién I, Fuertes-Mendizabal T, González A, Aparicio-Tejo PM, González-Murua C, González-Moro MB, Estavillo JM (2013) High irradiance improves ammonium tolerance in wheat plants by increasing N assimilation. J Plant Physiol 170:758–771

    Article  PubMed  CAS  Google Scholar 

  • Setién I, Vega-Mas I, Celestino N, Calleja-Cervantes ME, González-Murua C, Estavillo JM, González-Moro MB (2014) Root phosphoenolpyruvate carboxylase and NAD-malic enzymes activity increase the ammonium assimilating capacity in tomato. J Plant Physiol 171:49–63

    Article  PubMed  CAS  Google Scholar 

  • Shi D, Zhuang K, Chen Y, Xu F, Hu Z, Shen Z (2020) Effects of excess ammoniacal nitrogen (NH4+-N) on pigments, photosynthetic rates, chloroplast ultrastructure, proteomics, formation of reactive oxygen species and enzymatic activity in submerged plant Hydrilla verticillata (Lf) Royle. Aqua Toxicol 226:105585

    Article  CAS  Google Scholar 

  • Situmorang A (2018) Elucidation of the ammonium major facilitator (AMF) family in plants (Doctoral dissertation).

  • Sun L, Di D, Li G, Kronzucker HJ, Shi W (2017) Spatio-temporal dynamics in global rice gene expression (Oryza sativa L.) in response to high ammonium stress. J Plant Physiol 212:94–104. https://doi.org/10.1016/j.jplph.2017.02.006

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Di DW, Li G, Kronzucker HJ, Wu X, Shi W (2020) Endogenous ABA alleviates rice ammonium toxicity by reducing ROS and free ammonium via regulation of the SAPK9-bZIP20 pathway. J Exp Bot 71(15):4562–4577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun D, Fang X, Xiao CZM, Huang X, Su J, Li J, Wang J, Wang S, Luan S, He K (2021) Kinase SnRK1.1 regulates nitrate channel SLAH3 engaged in nitrate-dependent alleviation of ammonium toxicity. Plant Physiol 186:731–749. https://doi.org/10.1093/plphys/kiab057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szczerba MW, Britto DT, Kronzucker HJ (2006) Rapid, futile K+ cycling and pool-size dynamics define low-affinity potassium transport in barley. Plant Physiol 141:1494–1507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szczerba MW, Britto DT, Balkos KD, Kronzucker HJ (2008) Alleviation of rapid, futile ammonium cycling at the plasma membrane by potassium reveals K+-sensitive and -insensitive components of NH4+ transport. J Exp Bot 59:303–313

    Article  CAS  PubMed  Google Scholar 

  • Ten Hoopen F, Cuin TA, Pedas P, Hegelund JN, Shabala S, Schjoerring JK, Jahn TP (2010) Competition between uptake of ammonium and potassium in barley and Arabidopsis roots: molecular mechanisms and physiological consequences. J Exp Bot 61:2303–2315

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tian WH, Ye JY, Cui MQ, Chang JB, Liu Y, Li GX, Wu YR, Xu JM, Harberd NP, Mao CZ, Jin CW, Ding ZJ, Zheng SJ (2021) A transcription factor STOP1-centered pathway coordinates ammonium and phosphate acquisition in Arabidopsis. Mol Plant 14:1554–1568

    Article  CAS  PubMed  Google Scholar 

  • Uenishi Y, Nakabayashi Y, Tsuchihira A, Takusagawa M, Hashimoto K, Maeshima M, Sato-Nara K (2014) Accumulation of TIP2;2 aquaporin during dark adaptation is partially PhyA dependent in roots of Arabidopsis seedlings. Plants 3:177–195

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vega-Mas I, Marino D, Sanchez-Zabala J, Gonzalez-Murua C, Estavillo JM, González-Moro MB (2015) CO2 enrichment modulates ammonium nutrition in tomato adjusting carbon and nitrogen metabolism to stomatal conductance. Plant Sci 241:32–44

    Article  CAS  PubMed  Google Scholar 

  • Vega-Mas I, Pérez-Delgado CM, Marino D, Fuertes-Mendizábal T, González-Murua C, Márquez AJ, Betti M, Estavillo JM, González-Moro MB (2017) Elevated CO2 induces root defensive mechanisms in tomato plants when dealing with ammonium toxicity. Plant Cell Physiol 58(12):2112–2125

    Article  CAS  PubMed  Google Scholar 

  • Viciedo DO, de Mello PR, Toledo RL, dos Santos LCN, Hurtado AC, Nedd LLT, Gonzalez LC (2019) Silicon supplementation alleviates ammonium toxicity in sugar beet (Beta vulgaris L.). J Soil Sci Plant Nutr 19(2):413–419

    Article  CAS  Google Scholar 

  • Wang MY, Siddiqi MY, Ruth TJ, Glass ADM (1993) Ammonium uptake by rice roots II. Kinetics of 13NH4+ influx across the plasmalemma. Plant Physiol 103:1259–1267. https://doi.org/10.1104/pp.103.4.1259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17:458–467

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Gao J, Liu Y, Tian Z, Muhammad A, Zhang Y, Jiang D, Cao W, Dai T (2016) Higher ammonium transamination capacity can alleviate glutamate inhibition on winter wheat (Triticum aestivum L.) root growth under high ammonium stress. PLoS ONE 11(8):e0160997. https://doi.org/10.1371/journal.pone.0160997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Gao J, Shi S, He X, Dai T (2019a) Impaired electron transfer accounts for the photosynthesis inhibition in wheat seedlings (Triticum aestivum L) subjected to ammonium stress. Physiol Plant 167(2):159–172. https://doi.org/10.1111/ppl.12878

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Xu S, Sun H, Feng S, Jiang C, Zhou S, Wu S, Zhuang G, Chen B, Bai Z, Zhuang X (2019b) Complex regulatory network allows Myriophyllum aquaticum to thrive under high-concentration ammonia toxicity. Sci Rep 9(1):1–13

    CAS  Google Scholar 

  • Wang B, Wei H, Zhang H, Zhang WH (2020) Enhanced accumulation of gibberellins rendered rice seedlings sensitive to ammonium toxicity. J Exp Bot 71:1514–1526. https://doi.org/10.1093/jxb/erz492

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Li A, Zhang Z, Chu C (2021) Post-translational modifications: regulation of nitrogen utilization and signaling. Plant Cell Physiol 62:543–552. https://doi.org/10.1093/pcp/pcab008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weil S, Barker AV, Zandvakili OR, Etemadi F (2021) Plant growth and calcium and potassium accumulation in lettuce under different nitrogen regimes of ammonium and nitrate nutrition. J Plant Nutr 44(2):270–281. https://doi.org/10.1080/01904167.2020.1806313

    Article  CAS  Google Scholar 

  • Weng L, Zhang M, Wang K, Chen G, Ding M, Yuan W, Zhu Y, Xu W, Xu F (2020) Potassium alleviates ammonium toxicity in rice by reducing its uptake through activation of plasma membrane H+-ATPase to enhance proton extrusion. Plant Physiol Biochem 151:29–437. https://doi.org/10.1016/j.plaphy.2020.03.040

    Article  CAS  Google Scholar 

  • Xiao C, Sun D, Liu B, Fang X, Li P, Jiang Y, He M, Li J, Luan S, He K (2022) Nitrate transporter NRT1.1 and anion channel SLAH3 form a functional unit to regulate nitrate-dependent alleviation of ammonium toxicity. J Integr Plant Biol 64:942–957

    Article  CAS  PubMed  Google Scholar 

  • Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182

    Article  CAS  PubMed  Google Scholar 

  • Yamashita K, Kasai M, Ezaki B, Shibasaka M, Yamamoto Y, Matsumoto H, Sasakawa H (1995) Stimulation of H+ extrusion and plasma membrane H+-ATPase activity of barley roots by ammonium-treatment. Soil Sci Plant Nutr 41(1):133–140

    Article  CAS  Google Scholar 

  • Yang S, Hao D, Jin M, Li Y, Liu Z, Huang Y, Chen T, Su Y (2020) Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice. BMC Plant Biol 20:143. https://doi.org/10.1186/s12870-020-02363-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan GX, Cao T, Fu H, Ni LY, Zhang XL, Li W, Song X, Xie P, Jeppesen E (2013) Linking carbon and nitrogen metabolism to depth distribution of submersed macrophytes using high ammonium dosing tests and a lake survey. Freshw Biol 58:2532–2540. https://doi.org/10.1111/fwb.12230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan GX, Fu H, Zhong JY, Cao T, Ni LY, Zhu TS, Li W, Song X (2015) Nitrogen/carbon metabolism in response to NH4+ pulse for two submersed macrophytes. Aquat Bot 121:76–82. https://doi.org/10.1016/j.aquabot.2014.12.001

    Article  CAS  Google Scholar 

  • Yuan GX, Fu H, Li W, Zhong JY, Feng Q, Ni LY, Xie P, Cao T, Guo CJ, Lou Q (2017) The C/N metabolic responses to water depth gradients and seasons in natural macrophyte populations. Ecol Eng 104:195–204. https://doi.org/10.1016/j.ecoleng.2017.04.003

    Article  Google Scholar 

  • Zhang L, Song H, Li B, Wang M, Di D, Lin X, Kronzucker HJ, Shi W, Li G (2021a) Induction of S-nitrosoglutathione reductase protects root growth from ammonium toxicity by regulating potassium homeostasis in Arabidopsis and rice. J Exp Bot 72(12):4548–4564

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang YX, Lü X, Du W, Feng B, Li H, Wang Z, Xia H, Fan S, Kong LA (2021b) Study on physiological mechanism of NO3- alleviating NH4+ stress in wheat. Plant Physiol J 57(2):480–492. https://doi.org/10.13592/j.cnki.ppj.2020.0219

    Article  CAS  Google Scholar 

  • Zhao P, Wang Y, Lin Z, Zhou J, Chai H, He Q, Li Y, Wang J (2019) The alleviative effect of exogenous phytohormones on the growth, physiology and gene expression of Tetraselmis cordiformis under high ammonia-nitrogen stress. Bioresource Technol 282:339–347

    Article  CAS  Google Scholar 

  • Zheng X, He K, Kleist T, Chen F, Luan S (2015) Anion channel SLAH3 functions in nitrate dependent alleviation of ammonium toxicity in Arabidopsis. Plant Cell Environ 38:474–486

    Article  CAS  PubMed  Google Scholar 

  • Zhong YQW, Yan WM, Chen J, Shangguan ZP (2014) Net ammonium and nitrate fluxes in wheat roots under different environmental conditions as assessed by scanning ion-selective electrode technique. Sci Rep 4:7223–7223. https://doi.org/10.1038/srep07223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou T, Hua Y, Yue C, Huang J, Zhang Z (2021) Physiologic, metabolomic, and genomic investigations reveal distinct glutamine and mannose metabolism responses to ammonium toxicity in allotetraploid rapeseed genotypes. Plant Sci 310:110963

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Huang X, Hao Y, Su W, Liu H, Sun G, Chen R, Song S (2020) Ammonium transporter (BcAMT1.2) mediates the interaction of ammonium and nitrate in Brassica campestris. Front Plant Sci 10:1776. https://doi.org/10.3389/fpls.2019.01776

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Qi B, Hao Y, Liu H, Sun G, Chen R, Song S (2021) Appropriate NH4+/NO3- ratio triggers plant growth and nutrient uptake of flowering Chinese cabbage by optimizing the pH value of nutrient solution. Front Plant Sci 12:656144. https://doi.org/10.3389/fpls.2021.656144

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the Natural Science Foundation of Shandong Province (ZR2020MC087), the National Natural Science Foundation of China (31801282), and the Shandong Modern Agricultural Technology and Industry System (SDAIT-01-06).

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Kong, L., Zhang, Y., Zhang, B. et al. Does energy cost constitute the primary cause of ammonium toxicity in plants?. Planta 256, 62 (2022). https://doi.org/10.1007/s00425-022-03971-7

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