Abstract
It is well established that nitrate is a potent inhibitor of nodulation and nitrogen fixation in legumes. The objective of this study was to demonstrate the relative insensitivity of these processes to nitrate with Calopogonium mucunoides, a tropical South American perennial legume, native to the cerrado (savannah) region. It was found that nodule number was reduced by about half in the presence of high levels of nitrate (15 mM) but nodule growth (total nodule mass per plant) and nitrogen fixation (acetylene reduction activity and xylem sap ureide levels) were not affected. Other sources of N (ammonium and urea) were also without effect at these concentrations. At even higher concentrations (30 mM), nitrate did promote significant inhibition (ca. 50%) of acetylene reduction activity, but no significant reduction in xylem sap ureides was found. The extraordinary insensitivity of nodulation and N2 fixation of C. mucunoides to nitrate suggests that this species should be useful in studies aimed at elucidating the mechanisms of nitrate inhibition of these processes.
Similar content being viewed by others
References
Amarante L, Lima JD, Sodek L (2006) Growth and stress conditions cause similar changes in xylem amino acids for different legume species. Environ Exp Bot 58:123–129
Betts JH, Herridge DF (1987) Isolation of soybean lines capable of nodulation and nitrogen fixation under high levels of nitrate supply. Crop Sci 27:1156–1161
Bielski LR, Turner NA (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Anal Biochem 17:278–293
Bollman MI, Vessey JK (2006) Differential effects of nitrate and ammonium supply on nodule initiation, development, and distribution on roots of pea (Pisum sativum). Can J Bot 84:893–903
Buttery BR, Park SJ (1990) Effects of nitrogen, inoculation and grafting on expression of supernodulation in a mutant of Phaseolus vulgaris L. Can J Plant Sci 70:375–381
Carroll BJ, McNeil DL, Gresshoff PM (1985a) A supernodulation and nitrate-tolerant symbiotic (nts) soybean mutant. Plant Physiol 78:34–40
Carroll BJ, McNeil DL, Gresshoff PM (1985b) Isolation and properties of soybean [Glycine max (L.) Merr.] mutants that nodulate in the presence of high nitrate concentrations. Proc Natl Acad Sci USA 82:4162–4166
Dakora FD (1998) Nodule function in symbiotic Bambara Groundnut (Vigna subterranea L.) and Kersting’s Bean (Macrotyloma geocarpum L.) is tolerant of nitrate in the root medium. Ann Bot 82:687–690
Dakora FD (2000) Commonality of root nodulation signals and nitrogen assimilation in tropical grain legumes belonging to the tribe Phaseoleae. Aust J Plant Physiol 27:885–892
Dart PJ, Wildon DC (1970) Nodulation and nitrogen fixation by Vigna sinensis and Vicia atropurpurea: influence of concentration, form, and site of application of combined nitrogen. Aust J Agric Res 21:45–56
Day DA, Carroll BJ, Delves AC, Gresshoff PM (1989) Relationship between autoregulation and nitrate inhibition of nodulation in soybeans. Physiol Plant 75:37–42
Evans J (1982) Response of soybean-Rhizobium symbioses to mineral nitrogen. Plant Soil 66:439–442
Forde BG (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53:203–224
Furley PA, Ratter JA (1988) Soil resources and plant communities of the central Brazilian cerrado and their development. J Biogeogr 15:97–108
Gan YB, Stulen I, van Keulen H, Kuiper PJC (2004) Low concentrations of nitrate and ammonium stimulate nodulation and N2 fixation while inhibiting specific nodulation (nodule DW g−1 root dry weight) and specific N2 fixation (N2 fixed g−1 root dry weight) in soybean. Plant Soil 258:281–292
Gibson AH, Harper JE (1985) Nitrate effect on nodulation of soybean by Bradyrhizobium japonicum. Crop Sci 25:497–501
Glyan’ko AK, Vasil’eva GG, Mitanova NB, Ishchenko AA (2009) The influence of mineral nitrogen on legume-rhizobium symbiosis. Biol Bull 36:250–258
Gremaud MF, Harper JE (1989) Selection and initial characterization of partially nitrate tolerant nodulation mutants of soybean. Plant Physiol 89:169–173
Gulden RH, Vessey JK (1998) Low concentrations of ammonium inhibit specific nodulation (nodule number g−1 root DW) in soybean (Glycine max [L.] Merr.). Plant Soil 198:127–136
Guo R, Silsbury JH, Graham RD (1992) Effect of four nitrogen compounds on nodulation and nitrogen fixation in faba bean, white lupin and medic plants. Aust J Plant Physiol 19:501–508
Hansen AP, Peoples MB, Gresshoff PM, Atkins CA, Pate JS, Carroll BL (1989) Symbiotic performance of supernodulating soybean (Glycine max (L.) Merrill) mutants during development on different nitrogen regimes. J Exp Bot 40:715–724
Hansen AP, Martin P, Buttery BR, Park SJ (1992) Nitrate inhibition of N2 fixation in Phaseolus vulgaris L. cv OAC Rico and a supernodulating mutant. New Phytol 122:611–615
Harborne JB, Boulter D, Turner BL (1971) Chemotaxonomy of the Leguminosae. Academic Press, New York, 612 pp
Harper JE, Gibson AH (1984) Differential nodulation tolerance to nitrate among legume species. Crop Sci 24:797–801
Herridge, D.F., and Peoples, M.B (1990) Ureide assay for measuring nitrogen fixation by nodulated soybean calibrated by 15N methods. Plant Physiol 93:495–503
Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. California Agricultural Experimental Station Bulletin, 347
Imsande J (1986) Inhibition of nodule development in soybean by nitrate or reduced nitrogen. J Exp Bot 37:348–355
Izaguirre-Mayoral ML, Vivas AI (1996) Symbiotic N2-fixation in tropical legume species growing at high geographic elevation. Symbiosis 21:49–60
Jacobsen E, Feenstra WJ (1984) A new pea mutant with efficient nodulation in the presence of nitrate. Plant Sci Lett 33:337–344
Jarret HW, Cooksy KD, Ellis B, Anderson JM (1986) The separation of o-phthalaldehyde derivatives of amino acids by reverse-phase chromatrography on octylsilica columms. Anal Biochem 153:189–198
Lucinski R, Polcyn W, Ratajczac L (2002) Nitrate reduction and nitrogen fixation in symbiotic association Rhizobium-legumes. Acta Biochim Pol 49:537–546
Magalhães JR, Silva FLIM, Salgado I, Ferrarese-Filho O, Rockel P, Kaiser WM (2002) Nitric oxide and nitrate reductase in higher plants. Physiol Molelcular Biol Plants 8:11–17
Manhart JR, Wong PP (1980) Nitrate effect on nitrogen fixation (acetylene reduction). Plant Physiol 65:502–505
McCullough H (1967) Determination of ammonia in whole blood by a direct colorimetric method. Clin Chim Acta 17:297–304
McNeil DL (1982) Variations in ability of Rhizobium leguminosarum strains to nodulate soybeans and maintain fixation in the presence of nitrate. Appl Environ Microbiol 44:647–652
Puiatti M, Sodek L (1999) Waterlogging affects nitrogen transport in the xylem of soybean. Plant Physiol Biochem 37:767–773
Radin JW (1973) In vivo assay of nitrate reductase in cotton leaf discs. Plant Physiol 51:332–336
Rice CF, Lukaszewski KM, Walker S, Blevins DG, Winkler RG, Randall DD (1990) Changes in ureide synthesis, transport and assimilation following ammonium nitrate fertilization of nodulated soybeans. J Plant Nutr 13:1539–1553
Serraj R, Drevon JJ, Obaton M, Vidal A (1992) Variation in nitrate tolerance of nitrogen fixation in soybean (Glycine max)—Bradyrhizobium symbiosis. J Plant Physiol 140:366–371
Silva DM, Sodek L (1997) Effect of aluminum on soybean nodulation and nodule activity in a vertical split-root system. J Plant Nutr 20:963–974
Sodek L, Silva DM (1996) Nitrate inhibits soybean nodulation and nodule activity when applied to root regions distant from the nodulation sites. Rev Bras Fisiol Veg 8:187–191
Streeter JG (1981) Effect of nitrate in the rooting medium on carbohydrate composition of soybean nodules. Plant Physiol 68:840–844
Streeter JG (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. CRC Crit Rev Plant Sci 7:1–23
Svenning MM, Junttila O, MacDuff JH (1996) Differential rates of inhibition of N2 fixation by sustained low concentrations of NH +4 and NO −3 in northern ecotypes of white clover (Trifolium repens L.). J Exp Bot 47:729–738
Unkovich M, Herridge D, Peoples M, Cadisch G, Boddey B, Giller K, Alves B, Chalk P (2008) Measuring plant-associated nitrogen fixation in agricultural systems. ACIAR Monograph No. 136, Canberra, Australia, 258 pp
Vessey JK, Waterer J (1992) In search of the mechanism of nitrate inhibition of nitrogenase activity in legume nodules: recent developments. Physiol Plant 84:171–176
Vogels GD, Van Der Drift C (1970) Differential analysis of glyoxylate derivatives. Anal Biochem 33:143–157
Wang RC, Xing XJ, Crawford N (2007) Nitrite acts as a transcriptome signal molecule at micromolar concentrations in Arabidopsis roots. Plant Physiol 145:1735–1745
Wu S, Harper JE (1990) Nitrogen fixation of nodulation mutants of soybean as affected by nitrate. Plant Physiol 92:1142–1147
Yemm EW, Cocking EC (1955) The determination of amino acids with ninhydrin. Analyst 80:209–213
Acknowledgements
One of us (LSC) wishes to acknowledge the scholarship received from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Camargos, L.S., Sodek, L. Nodule growth and nitrogen fixation of Calopogonium mucunoides L. show low sensitivity to nitrate. Symbiosis 51, 167–174 (2010). https://doi.org/10.1007/s13199-010-0063-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-010-0063-5