Abstract
Combined forms of nitrogen negatively influence rhizobia-legume symbiosis. The effects of combined nitrogen are known for nodulation and dinitrogen (N2) fixation, but little is known about the effect on preinfection events. Here, we studied the effects of combined nitrogen on the adhesion of Rhizobium etli to common bean (Phaseolus vulgaris L.) roots. When potassium nitrate (KNO3) or sodium glutamate was added to an incubation mixture of rhizobia and plants that were previously grown in nitrogen-free solution, rhizobial adhesion to roots was stimulated. However, the rhizobial adhesion to bean roots that were previously grown with 10 mM KNO3 was reduced by half. A fraction of the bean root exudates, which is thermolabile and has molecular mass larger than 12 kDa stimulated rhizobial adhesion, but this stimulatory activity was lost in root exudates obtained with 10 mM KNO3. Thus, the inhibition of symbiosis in response to combined nitrogen may be controlled by the plant at the preinfection stage as well.
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Althabegoiti MJ, López-García SL, Piccinetti C, Mongiardini EJ, Pérez-Giménez J, Quelas JI, Perticari A, Lodeiro AR (2008) Strain selection for improvement of Bradyrhizobium japonicum competitiveness for nodulation of soybean. FEMS Microbiol Lett 282:115–123
Ausmees N, Jonsson H, Höglund S, Ljunggren H, Lindberg M (1999) Structural and putative regulatory genes involved in cellulose synthesis in Rhizobium leguminosarum bv. trifolii. Microbiology 145:1253–1262
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681
Bueno E, Gómez-Hernández N, Girard L, Bedmar EJ, Delgado MJ (2005) Function of the Rhizobium etli CFN42 nirK gene in nitrite metabolism. Biochem Soc Trans 33:162–163
Caetano-Anollés G, Favelukes G (1986) Quantitation of adsorption of rhizobia in low numbers to small legume roots. Appl Environ Microbiol 52:371–376
Caetano-Anollés G, Lagares A, Favelukes G (1989) Adsorption of Rhizobium meliloti to alfalfa roots: dependence on divalent cations and pH. Plant Soil 117:67–74
Calderón-Flores A, Du Pont G, Huerta-Saquero A, Merchant-Larios H, Servín-González L, Durán S (2005) The stringent response is required for amino acid and nitrate utilization, nod factor regulation, nodulation, and nitrogen fixation in Rhizobium etli. J Bacteriol 187:5075–5083
Dazzo FB, Hubbell HD (1975) Cross-reactive antigens and lectins as determinats of symbiotic specificity in the Rhizobium-clover association. Appl Microbiol 30:1017–1033
Dazzo FB, Truchet GL, Sherwood JE, Hrabak EM, Abe M, Pankratz SH (1984) Specific phases of root hair attachment in the Rhizobium trifolii-clover symbiosis. Appl Environ Microbiol 48:1140–1150
Díaz CL, Melchers LS, Hooykaas PJJ, Lugtenberg BJJ (1989) Root lectin as a determinant of host-plant specificity in the Rhizobium-legume symbiosis. Nature 338:579–581
Dusha I, Austin S, Dixon R (1999) The upstream region of the nodD3 gene of Sinorhizobium meliloti carries enhancer sequences for the transcriptional activator NtrC. FEMS Microbiol Lett 179:491–499
Fåhraeus G (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16:374–381
Fujishige NA, Lum MR, De Hoff PL, Whitelegge JP, Faull KF, Hirsch AM (2008) Rhizobium common nod genes are required for biofilm formation. Mol Microbiol 67:504–515
Gay-Fraret J, Ardissone S, Kambara K, Broughton WJ, Deakin WJ, Le Quéré A (2012) Cyclic-β-glucans of Rhizobium (Sinorhizobium) sp. strain NGR234 are required for hypo-osmotic adaptation, motility, and efficient symbiosis with host plants. FEMS Microbiol Lett 333:28–36
Ho S-C, Wang JL, Schindler M (1990) Carbohydrate binding activities of Bradyrhizobium japonicum. II. Isolation and characterization of a galactose-specific lectin. J Cell Biol 111:1639–1643
Laus MC, Logman TJ, Van Brussel AA, Carlson RW, Azadi P, Gao MY, Kijne JW (2004) Involvement of exo5 in production of surface polysaccharides in Rhizobium leguminosarum and its role in nodulation of Vicia sativa subsp. nigra. J Bacteriol 186:6617–6625
Laus MC, Logman TJ, Lamers GE, Van Brussel AAN, Carlson RW, Kijne JW (2006) A novel polar surface polysaccharide from Rhizobium leguminosarum binds host plant lectin. Mol Microbiol 59:1704–1713
Lodeiro AR, Lagares A, Martínez EN, Favelukes G (1995) Early interactions of Rhizobium leguminosarum bv phaseoli and bean roots: specificity in the process of adsorption and its requirement of Ca2+ and Mg2+ ions. Appl Environ Microbiol 61:1571–1579
Lodeiro AR, López-García SL, Vázquez TE, Favelukes G (2000) Stimulation of adhesiveness, infectivity, and competitiveness for nodulation of Bradyrhizobium japonicum by its treatment with soybean seed lectin. FEMS Microbiol Lett 188:177–184
Mongiardini EJ, Ausmees N, Pérez-Giménez J, Julia Althabegoiti M, Quelas JI, López-García SL, Lodeiro AR (2008) The rhizobial adhesion protein RapA1 is involved in adsorption of rhizobia to plant roots but not in nodulation. FEMS Microbiol Ecol 65:279–288
Mortier V, Holsters M, Goormachtig S (2012) Never too many? How legumes control nodule numbers. Plant Cell Environ 35:245–258
Noel KD, Forsberg LS, Carlson RW (2000) Varying the abundance of O-antigen in Rhizobium etli and its effect on symbiosis with Phaseolus vulgaris. J Baceriol 182:5317–5324
Oldroyd GE, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144
Patriarca EJ, Tatè R, Ferraioli S, Iaccarino M (2004) Organogenesis of the legume root nodules. Int Rev Cytol 234:201–262
Pérez-Giménez J, Mongiardini EJ, Althabegoiti MJ, Covelli J, Quelas JI, López-García SL, Lodeiro AR (2009) Soybean lectin enhances biofilm formation by Bradyrhizobium japonicum in the absence of plants. Int J Microbiol 2009:719367
Quelas JI, Mongiardini EJ, Casabuono A, López-García SL, Althabegoiti MJ, Covelli JM, Pérez-Giménez J, Couto A, Lodeiro AR (2010) Lack of galactose or galacturonic acid in Bradyrhizobium japonicum USDA 110 exopolysaccharide leads to different symbiotic responses in soybean. Mol Plant-Microbe Interact 23:1592–1604
Reid DE, Ferguson BJ, Hayashi S, Lin Y-H, Gresshoff PM (2011) Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108:789–795
Robledo M, Jiménez-Zurdo JI, Velázquez E, Trujillo ME, Zurdo-Piñeiro JL, Ramírez-Bahena MH, Ramos B, Díaz-Minguez JM, Dazzo F, Martínez-Molina E, Mateos PF (2008) Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots. Proc Natl Acad Sci USA 105:7064–7069
Robledo M, Rivera LP, Jiménez-Zurdo JI, Rivas R, Dazzo FB, Velázquez E, Martínez-Molina E, Hirsch AM, Mateos PF (2012) Role of Rhizobium endoglucanase CelC2 in cellulose biosynthesis and biofilm formation on plant roots and abiotic surfaces. Microb Cell Fact 11:125
Schubert S (1995) Nitrogen assimilation by legumes –processes and ecological limitations. Fert Res 42:99–107
Smit G, Kijne JW, Lugtenberg BJJ (1987) Involvement of both cellulose fibrils and a Ca2+-dependent adhesin in the attachment of Rhizobium leguminosarum to pea root hair tips. J Bacteriol 169:4294–4301
Smit G, Logman TJJ, Boerrigter M, Kijne JW, Lugtenberg BJJ (1989) Purification and partial characterization of the Rhizobium leguminosarum biovar viciae Ca2+-dependent adhesin, which mediates the first step in attachment of cells of the family Rhizobiaceae to plant root hair tips. J Bacteriol 171:4054–4062
Stacey G, So JS, Roth LE, Lakshmi SKB, Carlson RW (1991) A lipopolysaccharide mutant of Bradyrhizobium japonicum that uncouples plant from bacterial differentiation. Mol Plant-Microbe Interact 4:332–340
van Rhijn P, Goldberg RB, Hirsch AM (1998) Lotus corniculatus nodulation specificity is changed by the presence of a soybean lectin gene. Plant Cell 10:1233–1249
van Workum WAT, van Slageren S, van Brussel AAN, Kijne JW (1998) Role of exopolysaccharides of Rhizobium leguminosarum bv. viciae as host plant-specific molecules required for infection thread formation during nodulation of Vicia sativa. Mol Plant-Microbe Interact 11:1233–1241
Vincent JM (1970) A manual for the practical study of the root nodule bacteria. IBP Handbook No. 15. Blackwell Scientific Publications, Oxford
Wall LG, Favelukes G (1991) Early recognition in the Rhizobium meliloti-alfalfa symbiosis: root exudate factor stimulates root adsorption of homologous rhizobia. J Bacteriol 173:3492–3499
Williams A, Wilkinson A, Krehenbrink M, Russo DM, Zorreguieta A, Downie JA (2008) Glucomannan-mediated attachment of Rhizobium leguminosarum to pea root hairs is required for competitive nodule infection. J Bacteriol 190:4706–4715
Acknowledgments
This work was supported by Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, Argentina). JPG is researcher at Universidad Nacional de La Plata and ARL is member of the Scientific Career of Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), both of Argentina. The authors are grateful to Paula Giménez, Silvana Tongiani, Abel Bortolameotti and Bernabé Castillo for their excellent technical assistance.
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Pérez-Giménez, J., Lodeiro, A.R. Two effects of combined nitrogen on the adhesion of Rhizobium etli to bean roots. Symbiosis 59, 157–163 (2013). https://doi.org/10.1007/s13199-013-0229-z
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DOI: https://doi.org/10.1007/s13199-013-0229-z