The importance of nitrate in ameliorating the effects of ammonium and urea nutrition on plant development: the relationships with free polyamines and plant proline contents
Fabrice Houdusse A , Angel M. Zamarreño A , Maria Garnica A B and Josemaria García-Mina A B CA Research and Development Department, Inabonos-Roullier Group, Poligono Arazuri-Orcoyen, C / C no. 32. 31160 Orcoyen (Navarra), Spain.
B Department of Chemistry and Soil Chemistry, Faculty of Sciences, University of Navarra, P.O. Box 273, 31080 Pamplona (Navarra), Spain.
C Corresponding author. Email: jgmina@inabonos.com
Functional Plant Biology 32(11) 1057-1067 https://doi.org/10.1071/FP05042
Submitted: 24 February 2005 Accepted: 7 June 2005 Published: 28 October 2005
Abstract
In order to investigate the possible involvement of free polyamines and proline in the mechanism underlying the action of nitrate in correcting the negative effects associated with ammonium and urea nutrition in certain plant species, we studied plant contents of free polyamines and proline associated with nitrogen nutrition involving different nitrogen forms (nitrate, ammonium, urea) in two plant species, wheat and pepper. The results showed that ammonium nutrition and, to a lesser extent, urea nutrition were associated with significant increases in plant putrescine content that were well correlated with reductions in plant growth. These negative effects of ammonium and urea nutrition were corrected by the presence of nitrate in the nutrient solution; the presence of nitrate was also related to a significant decrease in the plant putrescine content. These results are compatible with a specific effect of nitrate reducing ammonium accumulation through the improvement of ammonium assimilation. As for the plant proline content, in pepper a slight increase in this parameter was associated with ammonium and urea nutrition, but it was also decreased by the presence of nitrate in the nutrient solution. These changes, however, were not so clearly related to the variations in plant growth as in the case of putrescine content. These results are compatible with the hypothesis that putrescine biosynthesis might be related to proline degradation by a specific pathway related to ammonium detoxification.
Keywords: ammonium, nitrate, nitrogen nutrition, pepper, polyamines, proline, putrescine, spermidine, spermine, urea, wheat.
Acknowledgments
This research was founded by the Roullier Group and the Government of Navarra. Special thanks to David Rhymes for kindly improving the English of the manuscript.
Altman A, Levin N
(1993) Interactions of polyamines and nitrogen nutrition in plants. Physiologia Plantarum 89, 653–658.
| Crossref | GoogleScholarGoogle Scholar |
Aziz A, Larher F
(1995) Changes in polyamine titers associated with the proline response and osmotic adjustment of rape leaf discs submitted to osmotic stresses. Plant Science 112, 175–186.
| Crossref | GoogleScholarGoogle Scholar |
Balestrasse K,
Benavides MP,
Gallego SM, Tomaro ML
(2003) Effect of cadmium stress on nitrogen metabolism in nodules and roots of soybean plants. Functional Plant Biology 30, 57–64.
| Crossref | GoogleScholarGoogle Scholar |
Bates LS,
Waldren RP, Teare JD
(1973) Rapid determination of free proline for water stress studies. Plant and Soil 39, 205–207.
| Crossref | GoogleScholarGoogle Scholar |
Bouchereau A,
Aziz A,
Larher F, Martin-Tanguy J
(1999) Polyamines and environmental challenges: recent development. Plant Science 140, 103–125.
| Crossref | GoogleScholarGoogle Scholar |
Britto DT, Kronzucker HJ
(2002) NH4+ toxicity in higher plants: a critical review. Journal of Plant Physiology 159, 567–584.
| Crossref |
Britto DT, Kronzucker HJ
(2004) Bioengineering nitrogen acquisition in rice: can novel initiatives in rice genomics and physiology contribute to global food security? BioEssais 26, 683–692.
| Crossref | GoogleScholarGoogle Scholar |
Cadahia, C (1998).
Cantera, R ,
Urdaniz, A ,
Lerga, J ,
and
García-Mina, JM (1999). Acidifying product as a source of stabilized ammonia nitrogen under greenhouse conditions. In ‘Soils with Mediterranean type of climate’. pp. 233–235. (UB Publicaciones: Barcelona)
Capell T,
Bassie L, Christou P
(2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proceedings of the National Academy of Sciences USA 101, 9909–9914.
| Crossref | GoogleScholarGoogle Scholar |
Chattopadhayay MK,
Tiwari BS,
Chattopadhyay G,
Bose A,
Sengupt DN, Ghosh B
(2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiologia Plantarum 116, 192–199.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chen JG,
Cheng SH,
Cao WX, Zhou X
(1998) Involvement of endogenous plant hormones in the effect of mixed nitrogen source on growth and tillering of wheat. Journal of Plant Nutrition 21, 87–97.
Chen SJ, Kao CH
(1996) Polyamines in relation to ammonium-inhibited growth in suspension-cultured rice cells. Botanic Bulletin Academia Sinica 37, 197–200.
Claussen W
(2002) Growth, water use efficiency, and proline content of hydroponically grown tomato plants as affected by nitrogen source and nutrient concentration. Plant and Soil 247, 199–209.
| Crossref | GoogleScholarGoogle Scholar |
Cruz, C ,
Castillo, M ,
Domínguez, CN ,
Juanarena, N ,
Aparicio-Tejo, P ,
Lamsfus, C ,
Botella, MA ,
and
Martins-Louçao, MA (2003). The importance of nitrate signalling in plant ammonium tolerance: spinach as a case study. In ‘Actas XV reunión de la Sociedad Española de Fisiología Vegetal y VIII congreso Hispano-Luso’. pp. 297. (Sociedad Española de Fisiología Vegetal: Palma de Mallorca)
Cuevas JC,
Sanchez DH,
Marina M, Ruiz OA
(2004) Do polyamines modulated the Lotus glaber NADPH oxidation activity induced by the herbicide methyl violagen? Functional Plant Biology 31, 921–928.
| Crossref | GoogleScholarGoogle Scholar |
El-Shintinawy F
(2000) Photosynthesis in two wheat cultivars differing in salt susceptibility. Photosynthetica 38, 615–620.
| Crossref | GoogleScholarGoogle Scholar |
Flores, HE (1991). Changes in polyamine metabolism in response to abiotic stress. In ‘Biochemistry and physiology of polyamines in plants’. (CRC Press: Boca Raton)
Frechilla S,
Lasa B,
Ibarretxe L,
Lamsfus C, Aparicio-Tejo P
(2001) Pea responses to saline stress is affected by the source of nitrogen nutrition (ammonium or nitrate). Plant Growth Regulation 35, 171–179.
| Crossref | GoogleScholarGoogle Scholar |
Gerendás J, Sattelmacher B
(1997a) Significance of Ni supply for growth, urease activity and the concentrations of urea, amino acids and mineral nutrients of urea-grown plants. Plant and Soil 190, 153–162.
| Crossref | GoogleScholarGoogle Scholar |
Gerendás J, Sattelmacher B
(1997b) Significance of N source (urea vs NH4NO3) and Ni supply for growth, urease activity and nitrogen metabolism of zucchini (Cucurbita pepo convar. Giromontiina). Plant and Soil 196, 217–222.
| Crossref | GoogleScholarGoogle Scholar |
Gerendás J,
Zhu Z,
Bendixen R,
Ratcliffe RG, Sattelmacher B
(1997) Physiological and biochemical processes related to ammonium toxicity in plants. Zeitschrift für Pflanzenernährung und Bodenkunde 160, 239–251.
Goicoechea N,
Aguirreolea J,
Cenoz S, Garcia-Mina JM
(2000)
Verticillium dahliae modifies the concentration of proline, soluble sugars, starch, soluble protein and abscisic acid in pepper plants. European Journal of Plant Pathology 106, 19–25.
| Crossref | GoogleScholarGoogle Scholar |
Hare PD, Cress WA
(1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation 21, 79–102.
| Crossref | GoogleScholarGoogle Scholar |
Hauck, RD (1985). Slow-release and bioinhibitor-amended nitrogen fertilizers. In ‘Fertilizer technology and use’. pp. 293–322. (Soil Science Society of America: Madison)
Hohlt HE,
Maynard DN, Barker AV
(1970) Studies on the ammonium tolerance of some cultivated Solanaceae. Journal of the American Society for Horticultural Science 95, 345–348.
Houdusse, F ,
Urdaniz, A ,
Zamarreño, AM ,
Cantera, R-G ,
and
García-Mina, JM (2002). Efecto comparativo de diferentes formas de nitrógeno – ureico, amoniacal y nítrico – sobre el desarrollo y nutrición de plantas de trigo cultivadas en medio hidropónico. In ‘Avances en el metabolismo del nitrógeno: de la biología molecular a la agronomía’. pp. 419–425. (Universidad Pública de Navarra: Pamplona)
Houdusse, F ,
Zamarreño, AM ,
Garnica, M ,
and
Garcia-Mina, JM (2004). La urea como fuente eficiente de nitrógeno para diferentes especies de plantas cultivadas en hidroponía. In ‘Nutriçao mineral: causas e consequências da dependência da fertilizaçao’. pp. 28–31. (Facultade de Ciencias da Universidad de Lisboa: Lisboa)
Kevers, C ,
Bisbis, B ,
Franck, T ,
Le Dily, F ,
Huault, C ,
Billard, JP ,
Fiodart, JM ,
and
Gaspar, TH (1997). On the possible causes of polyamine accumulation in in vitro plant tissues under neoplasic progression. In ‘Travelling shot on plant development.’ pp. 63–71. (University of Geneva: Geneva)
Klein H,
Priebe A, Jager HJ
(1979) Putrescine and spermidine in peas: effects and nitrogen source and potassium supply. Physiologia Plantarum 45, 497–499.
Kronzucker HJ,
Siddiqi MY,
Glass ADM, Kirk GJD
(1999) Nitrate-ammonium synergism in rice. A subcellular flux analysis. Plant Physiology 119, 1041–1045.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Larher F,
Aziz A,
Deleu C,
Lemesle P,
Ghaffar A,
Bouchard F, Plasman M
(1998) Suppression of the osmoinduced proline response of rapeseed leaf discs by polyamines. Physiologia Plantarum 102, 139–147.
| Crossref | GoogleScholarGoogle Scholar |
Le Rudulier D, Goas G
(1974) Devenir de l’hornitine 14C-5 dans les jeunes plantes de Soja hispida Moench. privées de leurs cotylédons et cultivées en présence de chlorure d’ammonium et de nitrates. Comptes Rendus de l’Académie des Sciences 278, 1039–1042.
Le Rudulier D, Goas G
(1975) Influence des ions ammonium et potassium sur l’accumulation de la putrescine chez les jeunes plantes de Soja hispida Moench. privées de leurs cotylédons. Physiolgie Vegetale 13, 125–136.
Le Rudulier D, Goas G
(1977) La diamine oxydase dans les jeunes plantes de Glycine max. Phytochemistry 16, 509–512.
| Crossref | GoogleScholarGoogle Scholar |
Leidi EO,
Silberbush M, Lips SH
(1991a) Wheat growth as affected by nitrogen type, pH and salinity. I. Biomass production and mineral nutrition. Journal of Plant Nutrition 14, 235–246.
Leidi EO,
Silberbush M, Lips SH
(1991b) Wheat growth as affected by nitrogen type, pH and salinity. II. Photosynthesis and transpiration. Journal of Plant Nutrition 14, 247–256.
Leidi EO,
Silberbush M,
Soares M, Lips SH
(1992) Salinity and nitrogen nutrition studies on peanut and cotton plants. Journal of Plant Nutrition 15, 591–604.
Lewis OAM,
Leidi EO, Lips SH
(1989) Effect on nitrogen source on growth response to salinity stress in maize and wheat. New Phytologist 111, 155–160.
Macadam XMB,
del Prado A,
Merino P,
Estavillo JM,
Pinto M, Gonzalez-Murua C
(2003) Dicyandiamide and 3,4-dimethyl pyrazole phosphate decrease N2O emissions from grassland but dicyandiamide produces deleterious effects in clover. Journal of Plant Physiology 160, 1517–1523.
| Crossref |
PubMed |
Mansour MMF
(2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biologia Plantarum 43, 491–500.
| Crossref | GoogleScholarGoogle Scholar |
Marschner, H (1995).
Martin-Tanguy J
(2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regulation 34, 135–148.
| Crossref | GoogleScholarGoogle Scholar |
Minocha R,
Long S,
Magill AH,
Aber J, McDowell WH
(2000) Foliar free polyamine and inorganic ion content in relation to soil and soil solution chemistry in two fertilized forest stands at the Harvard Forest, Massachusetts. Plant and Soil 222, 119–137.
| Crossref | GoogleScholarGoogle Scholar |
Minocha R,
Lee JS,
Long S,
Bhatnagar P, Minocha SC
(2004) Physiological responses of wild type and putrescine-overproducing transgenic cells of poplar to variations in the form and concentration of nitrogen in the medium. Tree Physiology 24, 551–560.
| PubMed |
Redinbaugh MG, Campbell WH
(1993) Glutamine synthetase and ferredoxin-dependent glutamate synthase expression in the maize (Zea mays) root primary response to nitrate. Plant Physiology 101, 1249–1255.
| PubMed |
Römheld V
(2000) The chlorosis paradox: Fe inactivation as a secondary event in chlorotic leaves in grapevine. Journal of Plant Nutrition 23, 1629–1643.
Santa-Cruz A,
Acosta M,
Pérez-Afocea F, Bolarin C
(1997) Changes in free polyamine levels induced by salt stress in leaves of cultivated and wild tomato species. Physiologia Plantarum 101, 341–346.
| Crossref | GoogleScholarGoogle Scholar |
Smith MA, Davies PJ
(1985) Separation and quantification of polyamines in plant tissues by high performance liquid chromatography of their dansyl derivatives. Plant Physiology 78, 89–91.
Speer M, Kaiser WM
(1994) Replacement of nitrate by ammonium as the nitrogen source increases the salt sensitivity of pea plants. II. Inter- and intracellular solute compartmentation in leaflets. Plant, Cell & Environment 17, 1223–1231.
Speer M,
Brune A, Kaiser WM
(1994) Replacement of nitrate by ammonium as the nitrogen source increases the salt sensitivity of pea plants. I. Ion concentration in roots and leaves. Plant, Cell & Environment 17, 1215–1221.
Sung H-I,
Liu LF, Kao CH
(1994) Putrescine accumulation is associated with growth inhibition in suspension-cultured rice cells under potassium deficiency. Plant & Cell Physiology 35, 313–316.
Tan XW,
Ikeda H, Oda M
(2000) The absorption, translocation, and assimilation of urea, nitrate and ammonium in tomato plants at different plant growth stages in hydroponic culture. Scientia Horticulturae 84, 275–283.
| Crossref | GoogleScholarGoogle Scholar |
Tiburcio, AF ,
Kaur Sawhney, R ,
and
Galston, AW (1990). Polyamine metabolism. In ‘Stress response in plants: adaptation and acclimation mechanism’. pp. 283–325. (Wiess-Liss: New York)
Tonon G,
Kevers C,
Faivre-Rampant O,
Graziani M, Gaspar T
(2004) Effect of NaCl and mannitol iso-osmotic stresses on proline and free polyamine levels in embryogenic Fraxinus angustifolia callus. Journal of Plant Physiology 161, 701–708.
| Crossref |
PubMed |
Wilson MR,
O’Donoghue SL, Walker NA
(1988) The transport and metabolism of urea in Chara australis. III. Two specific transport systems. Journal of Experimental Botany 39, 763–774.
Witte C-P,
Tiller S,
Taylor M, Davies H
(2002) Leaf urea metabolism in potato. Urease activity profile and patterns of recovery and distribution of 15N after foliar urea application in wild-type and urease-antisense transgenics. Plant Physiology 128, 1129–1136.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yamamoto A,
Shim IS,
Fujihara S,
Yoneyama T, Usui K
(2004) Effect of difference in nitrogen media on salt-stress response and contents of nitrogen compounds in rice seedlings. Soil Science and Plant Nutrition 50, 85–93.
Yanai J,
Robinson D,
Young IM,
Kyuma K, Kosaki T
(1998) Effects of the chemical form of inorganic nitrogen fertilizers on the dynamics of the soil solution composition and on nutrient uptake in wheat. Plant and Soil 202, 263–270.
| Crossref | GoogleScholarGoogle Scholar |