Phosphate Role in the Rhizobium-Legume Symbiosis- A Review

Authors

  • Thamir S. Al-Niemi Department of Biology/Office of the Academic Affairs, King Faisal University, Al-Hassa, 31982, Kingdom of Saudi Arabia

Keywords:

Legumes, Nitrogen fixation, Phosphorus (P), Rhizobium, Symbiosis.

Abstract

The international emphasis on maintaining farming systems productivity and sustainability is focusing on the use of renewable plant nutrients resources. In case of nitrogen (N), biological N2 fixation via symbiosis is the most important input for agricultural systems sustainability.  Research studying the association between rhizobia and the host legume plants has enhanced our knowledge and understanding of this symbiosis process. Our current knowledge establishes that any interruption in the flow of nutrients between symbionts affects this association.  Since phosphorus (P) is one of the essential nutrients in Rhizobium-legume symbiosis, and its limitation affects every aspect of the symbiosis, it is important to understand its function in the symbiosis process. This review will emphasis on the role of P in nodulation and in the functional symbiosis between rhizobia and legumes. 

References

. Udvardi, M.K. and P.S. Poole. 2013. Transport and Metabolism in Legume-Rhizobia Symbioses. Ann. Rev. Plant Biol. 64:781-805.

. McDermott, T.R. Phosphorus assimilation and regulation in the rhizobia. pp. 529-548, In E.W. Triplett (ed.). Prokaryotic Nitrogen Fixation: A Model System for the Analysis of a Biological Process. Horizon Scientific Press. 1999.

. Vance C.P., Graham, P.H. and Allan, D.L. Biological nitrogen fixation: phosphorus a critical future need? pp. 509-514. In Pederosa, F.O., M Hungria, G. Yates, W.E. Newton (eds.). Nitrogen fixation: from molecules to crop productivity. Kluwer Academic. 2000. Dordrecht, the Netherlands.

. Rabalais N.N., Turner, R.E., Wiseman, W.J.J. 2002. Gulf of Mexico hypoxia, A.K.A. ‘The dead zone’. Annual Review of Ecology and Systematics. 33: 235–263.

. Abelson, P.H. 1999. A potential phosphate crisis. Science 283:2015.

. Al-Niemi, T.S., Kahn, M.L., and McDermott, T.R. 1997. P metabolism in the Rhizobium tropici - bean symbiosis. Plant Physiol. 113: 1233-1242.

. Deng, S., M.L. Kahn, and T.R. McDermott. 1998. Characterization and transposon mutagenesis of a nonspecific acid phosphatase cloned from Rhizobium meliloti. Arch. Microbiol. 170:18-26.

. Cassman, K.G., D.N. Munns, and D.P. Beck. 1981. Growth of Rhizobium strains at low concentrations of phosphate. Soil Sci. Soc. Am. J. 45:520-523.

. Johnson, J.F., Allen, D.L., and Vance, C.P. 1994. Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol. 104:657-665.

.Srere, P.A. 1967. Citrate synthase. Methods Enzymol. 13:3-11.

.Preiss, J. 1984. Starch, sucrose biosynthesis and partition of carbon in plants are regulated by orthophosphate and triose-phosphates. Trends Biochem. Sci. 9:24-27.

.Pereira, P.A.A. and Bliss, F.A. 1989. Selection of common bean (Phaseolus vulgaris L.) for N2 fixation at different levels of available phosphorus under field and environmentally controlled conditions. Plant and Soil. 115:75-82.

.Perotto, S., Donovan, N., Drobak, B.K., and Brewin, N.J. 1995. Differential expression of a glycosyl inositol phospholipid antigen on the peribacteroid membrane during pea nodule development. Mol. Plant-Microbe Inter. 8:560-568.

.Johnson, J.F., Allen, D.L., Vance, C.P., and Weiblen, G. 1996. Root carbon dioxide fixation by phosphorus-deficient Lupinus albus: Contribution to organic acid exudation by proteoid roots. Plant Physiol. 112:19-30.

.Ostergaard, J., Larsen, K., and Jochimsen, B.U. 1991. 5'-Nucleotidase from soybean (Glycine max) root nodules. Partial purification and characterization. Regulation in sterile tissue culture. J. Plant Physiol. 138:387-393.

.Mullen, M.D., Israel, D.W., and Wollum II, A.G. 1988. Effects of Bradyrhizobium japonicum and soybean (Glycine max (L) Merr.) phosphorus nutrition on nodulation and dinitrogen fixation. Appl. Environ. Microbiol. 54:2387-2392.

.Fredeen, A.L., Raab, T.K., Rao, I.M., and Terry, N. 1990. Effects of phosphorus nutrition on photosynthesis in Glycine max (lL) Merr. Planta. 181:399-405.

.Goldstein, A.H. Phosphate starvation inducible enzymes and proteins in higher plants. pp 25-44. In J.L. Wray (ed.) Inducible Plant Proteins, Society for Experimental Biology Seminar Series 49, Cambridge University Press. 1992.

.Redgwell, P.J. 1980. Fractionation of plant extracts using ion-exchange sephadex. Anal. Biochem. 107:44-50.

.Drevon, J.J. and Hartwig U.A. 1997. Phosphorus deficiency increases the argon-induced decline of nodule nitrogenase activity in soybean and alfalfa. Planta. 201:463-469.

.Roest, H.P., Roo, L.G., Wijffelman, C.A., de Maagd, R.A., and Lugtenberg, B.J.J. 1995. Outer membrane protein changes during bacteroid development are independent of nitrogen fixation and differ between indeterminate and determinate nodulating host plants of Rhizobium leguminosarum. Mol. Plant Microb. Int. 8:14-22.

.Rolin, D.B., Pfeffer, P.E., Boswell, R.T., Schmidt, J.H., and Tu, S.I. 1989. In vivo 31P NMR spectroscopic studies of soybean Bradyrhizobium symbiosis. FEBS Lett. 254:203-206.

.Johnson, J.F., Vance, C.P., and Allen, D.L. 1996. Phosphorus deficiency in Lupinus albus: Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol. 112:31-41.

.Kahn, M.L., McDermott, T.R., and Udvardi, M.L. Carbon and nitrogen metabolism in the Rhizobiaceae. pp. 461-484. In H.P. Spaink (ed.). The Rhizobiaceae. Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers. 1998. Dordrecht. The Netherlands.

.Al-Niemi, T.S., Summers, M.L., Elkins, J.G., Khan, M.L., and McDermott, T.R. 1997. Regulation of the phosphate stress response in Rhizobium meliloti by PhoB. Appl. Environ. Microbiol. 63: 4978-4981.

.Powell, C.L. 1977. Mycorrhizas in hill country soils. III Effect of inoculation on clover growth in unsterile soils. N.Z. J. Agric. Res. 20:343-348.

.Theodorou, M.E., Elrifi, I.R., Turpin, D.H., and Plaxton, W.C. 1991. Effects of phosphorus limitation on respiratory metabolism in green alga Selenastrum minutum. Plant Physiol. 95:1089-1095.

.Simonsen, A.C.W. and Rosendahl, L. 1999. Origin of de novo synthesized proteins in the different compartments of pea-Rhizobium sp. symbiosomes. Mol. Plant-Microbe Int. 12:319-327.

.Itoh, S. 1987. Characteristics of phosphorus uptake of chickpea in comparison with pigeon pea, soybean and maize. Soil Sci. Plant Nutr. 33:417-422.

.Al-Niemi, T.S., Kahn, M.L., and McDermott, T.R. 1998. Bean nodule phosphorus uptake. Plant and Soil. 198:71-78.

.Sharfstein, S. T., and Keasling, J. D. 1994. Polyphosphate Metabolism in Escherichia Coli. Annals of the New York Academy of Sciences. 745:77-91.

.Rao, N. N., Liu, S., and Kornberg, A. 1998. Inorganic Polyphosphate in Escherichia Coli: the Phosphate Regulon and the Stringent Response. J. Bacteriol. 180:2186-2193.

.Mellor, R.B. 1988. Distribution of trehalase in soybean root nodule cells: implications for trehalose metabolism. J. Plant Physiol. 133:173-177.

.Theodorou, M.E. and Plaxton, W.C. 1993. Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol. 101:339-344.

.Cassman, K.G., D.N. Munns, and D.P. Beck. 1981. Phosphorus nutrition of Rhizobium japonicum: strain differences in phosphate storage and utilization. Soil Sci. Soc. Am J. 45:517-520.

.LeVier, K., Day, D.A., and Guerinot, M.L. 1996. Iron uptake by symbiosomes from soybean root nodules. Plant Physiol. 111:893-900.

.Bassarab, S., R.B. Mellor, and D. Werner. 1986. Evidence for two types of Mg++-ATPase in the peribacteroid membrane from Glycine max root nodules. Endocyt. Cell Res. 3:189-196.

.McKay, I.A. and Djordjevic, M.A. 1993. Production and excretion of nod metabolites by Rhizobium leguminosarum bv. trifolii are disrupted by the same environmental factors that reduce nodulation in the field. Appl. Environ. Microbiol. 59:3385-3392.

.Bal, A.K. and Wong, P.P. 1982. Infection process and sloughing off of rhizobial outer membrane in effective nodules of lima bean. Can. J. Microbiol. 28:890-896.

.Summers, M.L., Botero, L.M., Busse, S.C., and McDermott, T.R. 2000. The Sinorhizobium meliloti Lon protease is involved in regulating exopolysaccharide synthesis and is required for symbiosis. J. Bacteriol. 182:2551-2558.

.Botero, L.M., T.S. Al-Niemi, and T.R. McDermott. 2000. Characterization of two inducible phosphate transport systems in Rhizobium tropici. Appl. Environ. Microbiol. 66:15-22.

.Bardin, S.D., Dan, S., Osteras, M., and Finan, T.M. 1996. A phosphate transport system is required for symbiotic nitrogen fixation by Rhizobium meliloti. J. Bacteriol. 178:4540-4547.

.Salminen, S.O. and Streeter, J.G. 1987. Uptake and metabolism of carbohydrates by Bradyrhizobium japonicum bacteroids. Plant Physiol. 83:535-540.

.Sun, J.S., Simpson, R.J., and Sands, R. 1992. Nitrogenase activity of two genotypes of Acacia mangium as affected by phosphorus nutrition. Plant Soil. 144:51-58.

.Fredeen, A.L., Rao, I.M., and Terry, N. 1989. Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiol. 89:225-230.

.Kinzig, A.P. and Socolow, R.H. 1994. Human impacts on the nitrogen cycle. Physics today. 47:24-35.

.Beck, D.P. and D.N. Munns. 1984. Phosphate nutrition of Rhizobium spp. Appl. Environ. Microbiol. 47:278-282.

.Voegele, R.T., Bardin, S., and Finan, T.M. 1997. Characterization of the Rhizobium (Sinorhizobium) meliloti high- and low-affinity phosphate uptake systems. J. Bacteriol. 179:7226-7232.

.Bardin, S.D. and Finan, T.M. 1998. Regulation of phosphate assimilation in Rhizobium (Sinorhizobium) meliloti. Genetics. 148:1689-1700.

.Deng, S., Elkins, J.G., Da, L.H., Botero, L.M. and McDermott, T.R. 2001. Cloning and Characterization of a second acid phosphatase from Sinorhizobium melilotistrain 104A14. Arch Microbiol. 176:255-263.

.Liu, C. M., McLean, P.A., Sookdeo, C.C., and Cannon, F.C. 1991. Degradation of the herbicide glyphosate by members of the family Rhizobiaceae. Appl. Environ. Microbiol. 57:1799-1804.

.Ruberg, S., Puhler, A. & Becker, A. (1999). Biosynthesis of the exopolysaccharide galactoglucan in Sinorhizobium meliloti is subject to a complex control by the phosphate-dependent regulator PhoB and the proteins ExpG and MucR. Microbiology 145, 603–611.

.Bhat, U.R. and R.W. Carlson. 1992. Chemical characterization of pH-dependent structural epitopes of lipopolysaccharides from Rhizobium leguminosarum biovar phaseoli. J. Bacteriol. 174:2230-2235.

.Kinnback, A. and Werner, D. 1991. Glucosidases (α,β) and trehalase (α) in the peribacteroid space and the bacteroid periplasm of Glycine max root nodules. Plant Sci. 77:47-55.

.Minder, A.C., Narberhaus, F., Fischer, H.-M., and Henneke, H. 1998. The Bradyrhizobium japonicum phoB gene is required for phosphate-limited growth but not for symbiotic nitrogen fixation. FEMS Microbiol. Lett. 161:47-52.

.Rosendaul, L., Vance, C.P., and Pedersen, W.B. 1990. Products of dark CO2 fixation in pea root nodules support bacteroid metabolism. Plant Physiol. 93:12-19.

.Udvardi, M.K. and Day, D.A. 1997. Metabolite transport across symbiotic membranes of legume nodules. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:493-523.

.Smart, J.B., Dilworth, M.J., and Robson, A.D. 1984. Effect of phosphorus supply on phosphate uptake and alkaline phosphatase activity in rhizobia. Arch. Microbiol. 140:281-286.

.Penheiter, A.R., Duff, S.M.G., and Sarath, G. 1997. Soybean root nodule acid phosphatase. Plant Physiol. 114:597-604.

.Pena-Cabriales, J.J., Grageda-Cabrera, O.A., Kola, V., and Hardarson, G. 1993. Time course of N2 fixation in common bean (Phaseolus vulgaris L.) Plant and Soil. 152:115-121.

.Bardin, S.D., Voegele, R.T., and Finan, T.M. 1998. Phosphate assimilation in Rhizobium (Sinorhizobium) meliloti: identification of a pit-like gene. J. Bacteriol. 180:4219-4226.

.Bassarab, S. and Werner, D. 1989. Mg2+ -dependent pyrophosphatase, a tonoplast enzyme in the peribacteroid membrane of Glycine max root nodules. Symbiosis. 7:81-94.

.Udvardi, M.K., Yang, Young, L.O, S., and Day, D.A. 1990. Sugar and amino acid transport across symbiotic membranes from soybean nodules. Mol. Plant Microbe Interact. 3:334-340.

.Streeter, J.G. 1987. Carbohydrate, organic acid, and amino acid composition of bacteroids and cytosol from soybean nodules. Plant Physiol. 85:768-773.

.Bieleski, R.L. 1973. Phosphate pools, phosphate transport, and phosphate availability. Ann. Rev. Plant Physiol. 24:225-252.

.Drobak, B.K. 1993. Plant phosphoinositides and intracellular signaling. Plant Physiol. 102:705-709.

.Charles, T.C., W. Newcomb, and T.M. Finan. 1991. ndvF, a novel locus located on megaplasmid pRmeSU47b (pEXO) of Rhizobium meliloti, is required for normal nodule development. J. Bacteriol. 173:3981-3992.

.Summers M. L., Elkins J. G., Elliot B., McDermott T. R. (1998) Expression and regulation of phosphate starvation inducible genes in Rhizobium meliloti. Mol. Plant-Microbe Interact. 11:1094–1101.

.Summers, M.L., Denton, M.C., and McDermott, T.R. 1999. Genes coding for phosphotransacetylase and acetate kinase in Sinorhizobium meliloti are part of an operon that is controlled by phosphate availability and PhoB. J. Bacteriol. 181:2217-2224.

.Wanner, B.L. Phosphorus assimilation and control of the phosphate regulon. pp. 1357-1381. In F.C. Neidhardt et al (eds.). Escherichia coli and Salmonella. Cellular and molecular biology.. ASM Press. 1996. Washington, D.C.

.Oresnik, I.J., Charles, T.C., and Finan, T.M. 1994. Second site mutations specifically suppress the Fix- phenotype of Rhizobium meliloti ndvF mutations on alfalfa: identification of a conditional ndvF-dependent mucoid colony phenotype. Genetics. 136:1233-1243.

Downloads

Published

2017-12-21

How to Cite

S. Al-Niemi, T. (2017). Phosphate Role in the Rhizobium-Legume Symbiosis- A Review. International Journal of Sciences: Basic and Applied Research (IJSBAR), 36(8), 178–191. Retrieved from https://www.gssrr.org/index.php/JournalOfBasicAndApplied/article/view/8553

Issue

Section

Articles