Abstract
The (Brady)rhizobium nodulation gene products synthesize lipo-oligosaccharide (LOS) signal molecules that induce nodule primordia on legume roots. Previously, nodule primordia had been induced by LOS on several legumes, but the induction of a complete nodule structure by LOS had only been shown on alfalfa. Since alfalfa can spontaneously form nodules at a low frequency, it has been unclear whether LOS molecules are sufficient to induce morphologically complete nodules on plants that do not spontaneously form nodules. In this study, we isolated LOS from Bradyrhizobium elkanii previously Bradyrhizobium japonicum group II; (Kuykendall et al. 1992, Can. J. Microbiol. 38, 501–505) strain USDA61 and determined their biological activity on Glycine soja. When spot-inoculated onto G. soja roots, these LOS induced a morphologically complete nodule structure showing many features similar to root nodules induced by rhizobia. These features include a broad mitotically active nodule primordium in the root outer cortex and a vascular bundle that emanates from the pericycle and bifurcates to surround the mitotically active cells. From this work it can be concluded that LOS are sufficient to induce a structurally complete nodule on plants that form determinate nodules.
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Abbreviations
- LOS:
-
lipo-oligosaccharide(s)
References
Allen, O.N., Allen, E.K. (1981) The Leguminosae. Macmillan Publishers Ltd, London
Bhuvaneswari, T.V., Bhagwat, A.A., Bauer, W.D. (1981) Transient susceptibility of root cells in four common legumes to nodulation by rhizobia. Plant Physiol. 68, 1144–1149
Bulawa, C.E. (1992) CSD2, CSD3 and CSD4, genes required for chitin synthesis in Saccharomyces cerevisiae: the CSD2 gene product is related to chitin synthases and to developmentally regulated proteins in Rhizobium species and Xenopus laevis. Mol. Cell Biol. 12, 1764–1776
Calvert, H.E., Pence, M.K., Pierce, M., Malik, N.S.A., Bauer, W.D. (1984) Anatomical analysis of the development and distribution of Rhizobium infections in soybean roots. Can. J. Bot. 62, 2375–2384
Carlson, R.W., Sanjuan, J., Bhatt, U.R., Glushka, J., Spaink, H.P., Wijfjes, A.H.M., van Brussel, A.A.N., Stokkermans, T.J.W., Peters, N.K., Stacey, G. (1993) The structure and biological activities of the lipo-oligosaccharide nodulation signals produced by type I and type II strains of Bradyrhizobium japonicum. J. Biol. Chem. 268, 18372–18381
De Jong, A.J., Heidstra, R., Spaink, H.P., Hartog, M.V., Meijer, E.A., Hendriks, T., Lo Shiaovo, F., Terzi, M., Bisseling, T., Van Kammen, A., De Vries, S.C. (1993) Rhizobium lipo-oligosaccharides rescue a carrot somatic embryo mutant. Plant Cell 5, 615–620
Dudley, M.E., Jacobs, T.W., Long, S.R. (1987) Microscopic studies of cell divisions induced in alfalfa roots by Rhizobium meliloti. Planta 171, 289–301
Ehrhardt, D.W., Atkinson, E.M., Long, S.R. (1992) Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti nod factors. Science 256, 998–1000
Kuykendall, L.D., Saxena, B., Devine, T.E., Udell, S.E. (1992) Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can. J. Microbiol. 38, 501–505
Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Promé, J.C., Dénarié, J. (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344, 781–784
Martinez, E., Poupot, R., Promé, J.C., Prado, M.A., Segovia, L., Truchet, G., Dénarié, J. (1993) Chemical signalling of Rhizobium nodulating bean. In: New horizons in nitrogen fixation, pp. 171–175, Palacios, R., Mora, J., Newton, W.E., eds. Kluwer Academic Publishers, Boston
Maxwell, C.A., Hartwig, U.A., Joseph, C.M., Phillips, D.A. (1989) A chalcone and 2 related flavonoids released from alfalfa roots induce nod genes of Rhizobium meliloti. Plant Physiol. 91, 842–847
Mergaert, P., Van Montagu, M., Promé, J.C., Holsters, M. (1993) Three unusual modifications, a d-arabinosyl, an N-methyl, and a carbamoyl group, are present on the Nod factors of Azorhizobium caulinodans strain ORS571. Proc. Natl. Acad. Sci. USA 90, 1551–1555
Newcomb, W., Sippell, D., Peterson, R.L. (1979) The early morphogenesis of Glycine max and Pisum sativum root nodules. Can. J. Bot. 57, 2603–2616
Peters, N.K., Long, S.R. (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233, 977–980
Peters, N.K., Long, S.R. (1988) Alfalfa root exudates and compounds which promote or inhibit induction of Rhizobium meliloti nodulation genes. Plant Physiol. 88, 396–400
Price, N.P.J., Relíc, B., Talmont, F., Lewin, A., Promé, D., Pueppke, S.G., Maillet, F., Dénarié, J., Promé, J.-C., Broughton, W.J. (1992) Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated and sulphated. Mol. Microbiol. 6, 3575–3584
Rossbach, S., Gloudemans, T., Bisseling, T., Studer, D., Kaluza, B., Ebeling, S., Hennecke, H. (1989) Genetic and physiologic characterization of a Bradyrhizobium japonicum mutant defective in early bacteroid development. Mol. Plant Microbe Interact. 2, 233–250
Sanjuan, J., Carlson, R.W., Spaink, H.P., Bhat, U.R., Barbour, W.M., Glushka, J., Stacey, G. (1992) A novel sugar moiety is present in the lipo-oligisaccharide signal of Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. USA 89, 8789–8793
Schiefelbein, J.W., Benfey, P.N. (1991) The development of plant roots: New approaches to underground problems. Plant Cell 3, 1147–1154
Schmidt, J., Röhrig, H., John, M., Wieneke, U., Stacey, G., Koncz, C., Schell, J. (1993) Alteration of plant growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules. Plant J. 4, 651–658
Spaink, H.P., Sheeley, D.M., van Brussel, A.A.N., Glushka, J., York, V.N., Lugtenberg, B.J.J. (1991) A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354, 125–129
Spaink, H.P., Wijfjes, A.H.M, Geiger, O., Van Bloemberg, G.V., Ritsema, T., Lugtenberg, B.J.J. (1993) The function of the rhizobial nodABC and nodFEL operons in the biosynthesis of the lipo-oligosaccharides. In: New horizons in nitrogen fixation, pp. 165–170, Palacios, R., Mora, J., Newton, W.E., eds. Kluwer Academic Publishers, Dordrecht, the Netherlands
Truchet, G., Camut, S., de Billy, F., Odorico, R., Vasse, J. (1989) The Rhizobium-legume symbiosis. Two methods to discriminate between nodules and other root-derived structures. Protoplasma 149, 82–88
Truchet, G., Roche, P., Lerouge, P., Vasse, J., Camut, S., de Billy, F., Promé, J.C., Dénarié, J. (1991) Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351, 670–673
Turgeon, B.G., Bauer, W.D. (1982) Early events in the infection of soybean by Rhizobium japonicum. Time course and cytology of the initial process. Can. J. Bot. 60, 152–161
van Brussel, A.A.N., Bakhuizen, R., van Spronsen, P.C., Spaink, H.P., Tak, T., Lugtenberg, B.J.J., Kijne, J.W. (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257, 70–72
van Brussel, A.A.N., Recourt, K., Pees, E., Spaink, H.P., Tak, T., Wijffelman, C.A., Kijm, J.W., Lugtenberg, B.J.J. (1990) A biovaspecific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene-inducing activity in root exudate of Vicia sativa ssp. nigra. J. Bacteriol. 172, 5394–5401
van Brussel, A.A.N., Zaat, S.A.J., Canter-Cremers, H.C.J., Wijffelman, C.A., Pees, E., Tak, T., Lugtenberg, B.J.J. (1986) Role of plant root exudate and sym plasmid-localized nodulation genes in the synthesis by Rhizobium leguminosarum of Tsr factor which causes thick and short roots on common vetch. J. Bacteriol. 165, 517–522
Verma, D.P.S. (1992) Signals in root nodule organogenesis and endocytosis of Rhizobium. Plant Cell 4, 373–382
Vesper, S.J., Bauer, W.D. (1985) Characterization of Rhizobium attachment of soybean roots. Symbiosis 1, 139–162
Vijn, I., das Neves, L., van Kammen, A., Franssen, H., Bisseling, T. (1993) Nod factors and nodulation in plants. Science 260, 1764–1765
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We thank Drs. Leslie Wanner (Ohio State Biotechnology Center) and Desh Pal Verma for critical reading of this manuscript and Doug Hughes for his help in preparation of the photomicrographs. This work was supported by National Science Foundation grant IBN 9291878 awarded to N. K. P. This is publication 179-93 of the Ohio Agricultural Research and Development Center.
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Stokkermans, T.J.W., Peters, N.K. Bradyrhizobium elkanii lipo-oligosaccharide signals induce complete nodule structures on Glycine soja Siebold et Zucc.. Planta 193, 413–420 (1994). https://doi.org/10.1007/BF00201821
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DOI: https://doi.org/10.1007/BF00201821