Depletion of the heaviest stable N isotope is associated with NH4+/NH3 toxicity in NH4+-fed plants

BMC Plant Biology

Volumn 11, Issue , 2011, Pages

  Ariz, Idoia ^a   Cruz, Cristina ^b   Moran, Jose F ^a   González Moro, María B ^c   García Olaverri, Carmen ^a   González Murua, Carmen ^c   Martins Loução, Maria A ^b   Aparicio Tejo, Pedro M ^a  

^a PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^b UNIVERSITY OF LISBON   (Portugal)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Ammonia uptake; Ammonium dissociation isotope factor; Ammonium ammonia; Low affinity ammonium transporters; Nitrogen isotopic signature

Indexed keywords

MIMOSA; PISUM SATIVUM; SPINACIA OLERACEA;

AMMONIA; CARRIER PROTEIN; NITRATE; NITROGEN; QUATERNARY AMMONIUM DERIVATIVE;

ANALYSIS OF VARIANCE; ARTICLE; BIOMASS; CROP; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PH; PLANT; PLANT ROOT; TRANSPORT AT THE CELLULAR LEVEL;

AMMONIA; ANALYSIS OF VARIANCE; BIOLOGICAL TRANSPORT; BIOMASS; CROPS, AGRICULTURAL; HYDROGEN-ION CONCENTRATION; MEMBRANE TRANSPORT PROTEINS; NITRATES; NITROGEN ISOTOPES; PLANT ROOTS; PLANT SHOOTS; QUATERNARY AMMONIUM COMPOUNDS;

EID: 79955911057     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-11-83     Document Type: Article

References (60)

1. Owen AG, Jones DL. Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biol Biochem 2001, 33(4-5):651-657.
2. Britto DT, Kronzucker HJ. NH4+ toxicity in higher plants: A critical review. J Plant Physiol 2002, 159(6):567-584.
3. Handley LL, Raven JA. The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant, Cell Environ 1992, 15(9):965-985.
4. Werner RA, Schmidt H. The in vivo nitrogen isotope discrimination among organic plant compounds. Phytochemistry 2002, 61(5):465-484. 10.1016/S0031-9422(02)00204-2, 12409013.
5. Denton TM, Schmidt S, Critchley C, Stewart GR. Natural abundance of stable carbon and nitrogen isotopes in Cannabis sativa reflects growth conditions. Funct Plant Biol 2001, 28(10):1005-1012.
6. Evans RD. Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 2001, 6(3):121-126. 10.1016/S1360-1385(01)01889-1, 11239611.
7. Yoneyama T, Matsumaru T, Usui K, Engelaar WMHG. Discrimination of nitrogen isotopes, during absorption of ammonium and nitrate at different nitrogen concentrations by rice (Oryza sativa L.) plants. Plant Cell Environ 2001, 24(1):133-139.
8. Forde BG, Clarkson DT. Nitrate and ammonium nutrition of plants: Physiological and molecular perspectives. Adv Bot Res 1999, 30:1-90.
9. Li B-, Merrick M, Li S-, Li H-, Zhu S-, Shi W-, Su Y-. Molecular basis and regulation of ammonium transporter in rice. Rice Sci 2009, 16(4):314-322.
10. Loqué D, von Wirén N. Regulatory levels for the transport of ammonium in plant roots. J Exp Bot 2004, 55(401):1293-1305. 10.1093/jxb/erh147, 15133056.
11. Ludewig U, Von Wiren N, Frommer WB. Uniport of NH4+ by the root hair plasma membrane ammonium transporter LeAMT1;1. J Biol Chem 2002, 277(16):13548-13555. 10.1074/jbc.M200739200, 11821433.
12. Ludewig U, Wilken S, Wu B, Jost W, Obrdlik P, El Bakkoury M, Marini A-, André B, Hamacher T, Boles E, Von Wirén N, Frommer WB. Homo- and Hetero-oligomerization of ammonium transporter-1 NH4+ uniporters. J Biol Chem 2003, 278(46):45603-45610. 10.1074/jbc.M307424200, 12952951.
13. Mayer M, Ludewig U. Role of AMT1;1 in NH4+ acquisition in Arabidopsis thaliana. Plant Biol 2006, 8(4):522-528. 10.1055/s-2006-923877, 16917981.
14. Neuhäuser B, Dynowski M, Ludewig U. Channel-like NH3 flux by ammonium transporter AtAMT2. FEBS Lett 2009, 583(17):2833-2838. 10.1016/j.febslet.2009.07.039, 19635480.
15. Guether M, Neuhäuser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P. A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 2009, 150(1):73-83. 10.1104/pp.109.136390, 2675747, 19329566.
16. Howitt SM, Udvardi MK. Structure, function and regulation of ammonium transporters in plants. Biochim Biophys Acta Biomembr 2000, 1465(1-2):152-170.
17. Soupene E, He L, Yan D, Kustu S. Ammonia acquisition in enteric bacteria: Physiological role of the ammonium/methylammonium transport B (AmtB) protein. Proc Natl Acad Sci USA 1998, 95(12):7030-7034. 10.1073/pnas.95.12.7030, 22728, 9618533.
18. Sanz-Cobena A, Misselbrook TH, Arce A, Mingot JI, Diez JA, Vallejo A. An inhibitor of urease activity effectively reduces ammonia emissions from soil treated with urea under Mediterranean conditions. Agric Ecosyst Environ 2008, 126(3-4):243-249.
19. Harrison R, Webb J. A review of the effect of N fertilizer type on gaseous emissions. Adv Agron 2001, 73:65-108.
20. Hermes JD, Weiss PM, Cleland WW. Use of nitrogen-15 and deuterium isotope effects to determine the chemical mechanism of phenylalanine ammonia-lyase. Biochem 1985, 24(12):2959-2967.
21. Waser NAD, Harrison PJ, Nielsen B, Calvert SE, Turpin DH. Nitrogen isotope fractionation during the uptake and assimilation of nitrate, nitrite, ammonium, and urea by a marine diatom. Limnol Oceanogr 1998, 43(2):215-224.
22. Cruz C, Bio AFM, Domínguez-Valdivia MD, Aparicio-Tejo PM, Lamsfus C, Martins-Loução MA. How does glutamine synthetase activity determine plant tolerance to ammonium?. Planta 2006, 223(5):1068-1080. 10.1007/s00425-005-0155-2, 16292661.
23. Cruz C, Soares MIM, Martins-Loucção MA, Lips SH. Nitrate reduction in carob (Ceratonia siliqua L.) seedlings. New Phytol 1991, 119:413-419.
24. Domínguez-Valdivia MD, Aparicio-Tejo PM, Lamsfus C, Cruz C, Martins-Loução MA, Moran JF. Nitrogen nutrition and antioxidant metabolism in ammonium-tolerant and - sensitive plants. Physiol Plant 2008, 132(3):359-369. 10.1111/j.1399-3054.2007.01022.x, 18275467.
25. Ariz I, Esteban R, García-Plazaola JI, Becerril JM, Aparicio-Tejo PM, Moran JF. High irradiance induces photoprotective mechanisms and a positive effect on NH4+ stress in Pisum sativum L. J Plant Physiol 2010, 167(13):1038-1045. 10.1016/j.jplph.2010.02.014, 20434233.
26. Cruchaga S, Artola E, Lasa B, Ariz I, Irigoyen I, Moran JF, Aparicio-Tejo PM. Short term physiological implications of NBPT application on the N metabolism of Pisum sativum and Spinacea oleracea. J Plant Physiol 2011, 168(4):329-336. 10.1016/j.jplph.2010.07.024, 20932600.
27. Ariz I, Artola E, Asensio AC, Cruchaga S, Aparicio-Tejo PM, Moran JF. High irradiance increases NH4+ tolerance in Pisum sativum: Higher carbon and energy availability improve ion balance but not N assimilation. J Plant Physiol 2011, 168(10):1009-1015. 10.1016/j.jplph.2010.11.022, 21371777.
28. Labhilili M, Joudrier P, Gaultier M. Characterization of cDNA encoding Triticum durum dehydrins and their expression patterns in cultivars that differ in drought tolerance. Plant Sci 1995, 112:219-230.
29. Levene H. Robust tests for equality of variances. Contributions to Probability and Statistic: essays in honor of Harold Hotelling 1960, 278-292. Stanford University Press, Ingram Olkin ea.
30. Dunnett CW. Pairwise multiple comparisons in the unequal variance case. J Am Statist Assoc 1980, 75(372):796-800.
31. Szczerba MW, Britto DT, Balkos KD, Kronzucker HJ. Alleviation of rapid, futile ammonium cycling at the plasma membrane by potassium reveals K+-sensitive and - insensitive components of NH 4+ transport. J Exp Bot 2008, 59(2):303-313. 10.1093/jxb/erm309, 18203690.
32. Gierth M, Mäser P. Potassium transporters in plants - Involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett 2007, 581(12):2348-2356. 10.1016/j.febslet.2007.03.035, 17397836.
33. Doyle DA, Cabral JM, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R. The structure of the potassium channel: Molecular basis of K+ conduction and selectivity. Science 1998, 280(5360):69-77. 10.1126/science.280.5360.69, 9525859.
34. Kohl DH, Shearer G. Isotopic fractionation associated with symbiotic N2 fixation and uptake of NO3- by plants. Plant Physiol 1980, 66:51-56. 10.1104/pp.66.1.51, 440529, 16661392.
35. Kolb KJ, Evans RD. Influence of nitrogen source and concentration on nitrogen isotopic discrimination in two barley genotypes (Hordeum vulgare L.). Plant Cell Environ 2003, 26(9):1431-1440.
36. Mattsson M, Schjoerring JK. Ammonia emission from young barley plants: Influence of N source, light/dark cycles and inhibition of glutamine synthetase. J Exp Bot 1996, 47(297):477-484.
37. Mattsson M, Husted S, Schjoerring JK. Influence of nitrogen nutrition and metabolism on ammonia volatilization in plants. Nutr Cycl Agroecosyst 1998, 51(1):35-40.
38. Schjoerring JK, Husted S, Mäck G, Nielsen KH, Finnemann J, Mattsson M. Physiological regulation of plant-atmosphere ammonia exchange. Plant Soil 2000, 221(1):95-102.
39. Massad R-, Tuzet A, Loubet B, Perrier A, Cellier P. Model of stomatal ammonia compensation point (STAMP) in relation to the plant nitrogen and carbon metabolisms and environmental conditions. Ecol Model 2010, 221(3):479-494.
40. O'Deen WA. Wheat volatilized ammonia and resulting nitrogen isotopic fractionation. Agron J 1989, 81:980-985.
41. Yoneyama T, Kamachi K, Yamaya T, Mae T. Fractionation of nitrogen isotopes by glutamine synthetase isolated from spinach leaves. Plant Cell Physiol 1993, 34:489-491.
42. Högberg P, Högberg MN, Quist ME, Ekblad A, Näsholm T. Nitrogen isotope fractionation during nitrogen uptake by ectomycorrhizal and non-mycorrhizal Pinus sylvestris. New Phytol 1999, 142(3):569-576.
43. Li Q, Li B-, Kronzucker HJ, Shi W-. 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 2010, 33(9):1529-1542.
44. Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ. Futile transmembrane NH4+ cycling: A cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 2001, 98(7):4255-4258. 10.1073/pnas.061034698, 31212, 11274450.
45. Qin C, Qian W, Wang W, Wu Y, Yu C, Jiang X, Wang D, Wu P. GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana. Proc Natl Acad Sci USA 2008, 105(47):18308-18313. 10.1073/pnas.0806168105, 2587558, 19011088.
46. Barth C, Gouzd ZA, Steele HP, Imperio RM. A mutation in GDP-mannose pyrophosphorylase causes conditional hypersensitivity to ammonium, resulting in Arabidopsis root growth inhibition, altered ammonium metabolism, and hormone homeostasis. J Exp Bot 2010, 61(2):379-394. 10.1093/jxb/erp310, 2803207, 20007685.
47. Mook WG. Introduction: Theory, Methods and Review. Environmental isotopes in the hydrological cycle, principes and applications IHP-V 2000, 1:31-48. Paris: UNESCO/IAEA, Mook WG, 39.
48. Rothe J, Gleixner G. Application of stable nitrogen isotopes to investigate food-web development in regenerating ecosystems. Assembly Rules and Restoration Ecology - Bridging the Gap Between Theory and Practice 2004, 245-264. Island Press, Temperton VM, Hobbs RJ, Nuttle T, Halle S.
49. Kosegarten H, Grolig F, Esch A, Glüsenkamp K-, Mengel K. Effects of NH4+, NO3- and HCO3-on apoplast pH in the outer cortex of root zones of maize, as measured by the fluorescence ratio of fluorescein boronic acid. Planta 1999, 209(4):444-452. 10.1007/s004250050747, 10550625.
50. Kosegarten H, Grolig F, Wieneke J, Wilson G, Hoffmann B. Differential ammonia-elicited changes of cytosolic pH in root hair cells of rice and maize as monitored by 2',7'-bis-(2-carboxyethyl)-5 (and -6)-carboxyfluorescein-fluorescence ratio. Plant Physiol 1997, 113(2):451-461. 158160, 12223619.
51. Lasa B, Frechilla S, Aparicio-Tejo PM, Lamsfus C. Role of glutamate dehydrogenase and phosphoenolpyruvate carboxylase activity in ammonium nutrition tolerance in roots. Plant Physiol Biochem 2002, 40(11):969-976.
52. Khademi S, O'Connell J, Remis J, Robles-Colmenares Y, Miercke LJW, Stroud RM. Mechanism of ammonia transport by Amt/MEP/Rh: Structure of AmtB at 135 Å. Science 2004, 305(5690):1587-1594. 10.1126/science.1101952, 15361618.
53. Zheng L, Kostrewa D, Bernèche S, Winkler FK, Li X-. The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli. Proc Natl Acad Sci USA 2004, 101(49):17090-17095. 10.1073/pnas.0406475101, 535379, 15563598.
54. Jahn TP, Møller ALB, Zeuthen T, Holm LM, Klærke DA, Mohsin B, Kühlbrandt W, Schjoerring JK. Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 2004, 574(1-3):31-36. 10.1016/j.febslet.2004.08.004, 15358535.
55. Giglioli-Guivarc'h N, Pierre J-, Brown S, Chollet R, Vidal J, Gadal P. The light- dependent transduction pathway controlling the regulatory phosphorylation of C4 phosphoenolpyruvate carboxylase in protoplasts from Digitaria sanguinalis. Plant Cell 1996, 8(4):573-586. 161121, 12239393.
56. Britto DT, Kronzucker HJ. Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: New views on old paradigms. Plant Cell Environ 2005, 28(11):1396-1409.
57. Lukowitz W, Nickle TC, Meinke DW, Last RL, Conklin PL, Somerville CR. Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc Natl Acad Sci USA 2001, 98(5):2262-2267. 10.1073/pnas.051625798, 30126, 11226227.
58. Hoopen FT, Cuin TA, Pedas P, Hegelund JN, Shabala S, Schjoerring JK, Jahn TP. Competition between uptake of ammonium and potassium in barley and Arabidopsis roots: Molecular mechanisms and physiological consequences. J Exp Bot 2010, 61(9):2303-2315. 10.1093/jxb/erq057, 2877888, 20339151.
59. Uozumí N, Gassmann W, Cao Y, Schroeder JI. Identification of strong modifications in cation selectivity in an Arabidopsis inward rectifying potassium channel by mutant selection in yeast. J Biol Chem 1995, 270(41):24276-24281. 10.1074/jbc.270.41.24276, 7592636.
60. White PJ. The permeation of ammonium through a voltage-independent K+ channel in the plasma membrane of rye roots. J Membr Biol 1996, 152(1):89-99. 10.1007/s002329900088, 8660414.