Abstract
Amino acid concentration in the rhizosphere results from fluxes between plant roots, soil and microorganisms. In this context, root amino acid exudation process, composed of both efflux and influx, remains unclear. One main issue is to understand the selectivity of amino acid exudation resulting mainly in high proportions of glycine and serine in exudates compared to low proportions inside the root. To reach this point, a quantitative analysis of exudation with dissociated measurements of efflux from influx is needed. We measured efflux and influx by supplying 15N-labelled glycine or serine for a short time of exposure at ecologically relevant concentrations to plants of white clover (Trifolium repens L.), perennial ryegrass (Lolium perenne L.), maize (Zea mays L.), oilseed rape (Brassica napus L.), tomato (Lycopersicon esculentum Mill.) and alfalfa (Medicago sativa L.). Efflux was estimated by the increase of 14N content of amino acids in root exudates and influx was estimated by the increase of 15N content in plant tissue. Glycine efflux exceeded influx for all six species and was much higher in Fabaceae than in Poaceae. Serine efflux exceeded influx in alfalfa, white clover and rape. We conclude that presence of glycine and serine in root bathing solutions results from high glycine and serine efflux rates, observed in all six species studied here. The physiological and ecological significances of these high efflux rates are discussed in the context of N metabolism and plant–soil–microorganisms interactions.
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References
Aslam M, Travis RL, Rains DW (1996) Evidence for substrate induction of a nitrate efflux system in barley roots. Plant Physiol 112:1167–1175
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Benizri E, Courtade A, Guckert A (1995) Fate of two microorganisms in maize simulated rhizosphere under hydroponic and sterile conditions. Soil Biol Biochem 27:71–77
Britto DT, Kronzucker HJ (2001) Can unidirectional influx be measured in higher plants? A mathematical approach using parameters from efflux analysis. New Phytol 150:37–47
Brophy LS, Heichel GH (1989) Nitrogen release from roots of alfalfa and soybean grown in sand culture. Plant Soil 116:77–84
Chiu JC, Brenner ED, DeSalle R, Nitabach MN, Holmes TC, Coruzzi GM (2002) Phylogenetic and expression analysis of the glutamate-receptor-like gene family in Arabidopsis thaliana. Mol Biol Evol 19:1066–1082
Cliquet JB, Murray PJ, Boucaud J (1997) Effect of the arbuscular mycorrhizal fungus Glomus fasciculatum on the uptake of amino nitrogen by Lolium perenne L. New Phytol 137:345–349
Dubos C, Huggins D, Grant GH, Knight MR, Campbell MM (2003) A role for glycine in the gating of plant NMDA-like receptors. Plant J 35:800–810
Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378
Hertenberger G, Wanek W (2004) Evaluation of methods to measure differential 15N labelling of soil and root N pools for studies of root exudation. Rapid Commun Mass Spectrom 18:2415–2425
Høgh-Jensen H, Schjoerring JK (2001) Rhizodeposition of nitrogen by red clover, white clover and ryegrass leys. Soil Biol Biochem 33:439–448
Høgh-Jensen H, Wollenweber B, Schjoerring JK (1997) Kinetics of nitrate and ammonium absorption and accompanying H+ fluxes in roots of Lolium perenne L. and N2-fixing Trifolium repens L. Plant Cell Environ 20:1184–1192
Jones DL, Darrah PR (1994) Amino-acid influx at the soil-root interface of Zea mays L and its implications in the rhizosphere. Plant Soil 163:1–12
Jones DL, Owen AG, Farrar JF (2002) Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biol Biochem 34:1893–1902
Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005) Dissolved organic nitrogen uptake by plants – an important N uptake pathway? Soil Biol Biochem 37:413–423
Kielland K (1995) Landscape patterns of free amino acids in Arctic tundra soils. Biogeochem 31:85–98
Lainé P, Ourry A, Macduff J, Boucaud J, Salette J (1993) Kinetic parameters of nitrate uptake by different catch crop species: effects of low temperatures or previous nitrate starvation. Physiol Plant 88:85–92
Lainé P, Bigot J, Ourry A, Boucaud J (1994) Effects of low temperature on nitrate uptake, and xylem and phloem flows of nitrogen, in Secale cereale L. and Brassica napus L. New Phytol 127:675–683
Lanfermeijer FC, van Oene MA, Borstlap AC (1992) Compartmental analysis of amino-acid release from attached and detached pea seed coats. Planta 187:75–82
Lipson DA, Raab TK, Schmidt SK, Monson RK (1999) Variation in competitive abilities of plants and microbes for specific amino acids. Biol Fertil Soils 29:257–261
Macduff JH, Jackson SB (1992) Influx and efflux of nitrate and ammonium in italian ryegrass and white clover roots: comparisons between effects of darkness and defoliation. J Exp Bot 43:525–535
Meyerhoff O, Müller K, Roelfsema MRG, Latz A, Lacombe B, Hedrich R, Dietrich P, Becker D (2005) AtGLR3.4, a glutamate receptor channel-like gene is sensitive to touch and cold. Planta 222:418–427
Miller AE, Bowman WD (2003) Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen. Plant Soil 250:283–292
Morgan MA, Volk RJ, Jackson WA (1973) Simultaneous influx and efflux of nitrate during uptake by perennial ryegrass. Plant Physiol 51:267–272
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497
Murray PJ, Hatch DJ, Cliquet JB (1996) Impact of insect root herbivory on the growth and nitrogen and carbon contents of white clover (Trifolium repens) seedlings. Can J Bot 74:1591–1595
Näsholm T, Huss-Danell K, Högberg P (2001) Uptake of glycine by field grown wheat. New Phytol 150:59–63
Ofosu-Budu KG, Fujita K, Ogata S (1990) Excretion of ureide and other nitrogenous compounds by the root system of soybean at different growth stages. Plant Soil 128:135–142
Ortiz-Lopez A, Chang HC, Bush DR (2000) Amino acid transporters in plants. Biochim Biophys Acta Biomembr 1465:275–280
Paynel F, Murray PJ, Cliquet JB (2001) Root exudates: a pathway for short-term N transfer from clover and ryegrass. Plant Soil 229:235–243
Persson J, Näsholm T (2002) Regulation of amino acid uptake in conifers by exogenous and endogenous nitrogen. Planta 215:639–644
Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894
Qi Z, Nicholas NR, Spalding EP (2006) Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol 142:963–971
Raab TK, Lipson DA, Monson RK (1996) Non-mycorrhizal uptake of amino acids by roots of the alpine sedge Kobresia myosuroides: implications for the alpine nitrogen cycle. Oecologia 108:488–494
Rroço E, Kosegarten H, Mengel K (2002) Importance of plasmalemma H+-ATPase activity for N losses from intact roots of spring wheat (Triticum aestivum L.). Eur J Agron 16:187–196
Schobert C, Komor E (1987) Amino acid uptake by Ricinus communis roots: characterization and physiological significance. Plant Cell Environ 10:493–500
Shepherd T, Davies HV (1994) Patterns of short-term amino acid accumulation and loss in the root-zone of liquid-cultured forage rape (Brassica napus L.). Plant Soil 158:99–109
Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23
Sokal RR, Rohlf FJ (1995) Biometry; the Principles and practice of Statistics in biology research, 3rd edn. W.H. Freeman and Company, New York, pp 897
Streeter TC, Bol R, Bardgett RD (2000) Amino acids as a nitrogen source in temperate upland grasslands: the use of dual labelled (13C, 15N) glycine to test for direct uptake by dominant grasses. Rapid Commun Mass Spectrom 14:1351–1355
Sundin P, Valeur A, Olsson S, Odham G (1990) Interactions between bacteria-feeding nematodes and bacteria in the rape rhizosphere: effects on root exudation and distribution of bacteria. FEMS Microbiol Ecol 73:13–22
Svenningsson H, Sundin P, Liljenberg C (1990) Lipids, carbohydrates and amino acids exuded from the axenic roots of rape seedlings exposed to water-deficit stress. Plant Cell Environ 13:155–162
Szajdak L, Jezierski A, Cabrera ML (2003) Impact of conventional and no-tillage management on soil amino acids, stable and transient radicals and properties of humic and fulvic acids. Org Geochem 34:693–700
Ta TC, Faris MA (1987) Species variation in the fixation and transfer of nitrogen from legumes to associated grasses. Plant Soil 98:265–274
Ta TC, Macdowall FDH, Faris MA (1986) Excretion of nitrogen assimilated from N2 fixed by nodulated roots of alfalfa (Medicago sativa). Can J Bot 64:2063–2067
Taylor AFS, Gebauer G, Read DJ (2004) Uptake of nitrogen and carbon from double-labelled (15N and 13C) glycine by mycorrhizal pine seedlings. New Phytol 164:383–388
Thornton B (2001) Uptake of glycine by non-mycorrhizal Lolium perenne. J Exp Bot 52:1315–1322
Thornton B, Robinson D (2005) Uptake and assimilation of nitrogen from solutions containing multiple N sources. Plant Cell Environ 28:813–821
Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Ann Bot 97:875–881
Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51
Wyse RE, Komor E (1984) Mechanism of amino acid uptake by sugarcane suspension cells. Plant Physiol 76:865–870
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We thank Dr. MC Roland and Dr. PJ Murray for critical comments and advice on the manuscript. We are grateful to Alexandra Bré for technical assistance on amino acid analyses.
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Lesuffleur, F., Paynel, F., Bataillé, MP. et al. Root amino acid exudation: measurement of high efflux rates of glycine and serine from six different plant species. Plant Soil 294, 235–246 (2007). https://doi.org/10.1007/s11104-007-9249-x
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DOI: https://doi.org/10.1007/s11104-007-9249-x