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. 1992 Jun 15;89(12):5625–5629. doi: 10.1073/pnas.89.12.5625

Specific oligosaccharide form of the Rhizobium meliloti exopolysaccharide promotes nodule invasion in alfalfa.

L Battisti 1, J C Lara 1, J A Leigh 1
PMCID: PMC49345  PMID: 1608972

Abstract

Rhizobium meliloti strain SU47 produces both high molecular weight (HMW) and low molecular weight (LMW) forms of an acidic exopolysaccharide, succinoglycan. Genetic studies have shown that succinoglycan is required for alfalfa root nodule invasion. We found that LMW succinoglycan, when applied exogenously to alfalfa roots, restored nodule invasion to exoA, exoB, exoF, and exoH mutants. Nodule initiation signals were not involved, since LMW succinoglycan from R. meliloti nodD1D2D3 and nodA mutants and from luteolin-induced wild-type cultures elicited effects similar to LMW succinoglycan from the uninduced wild-type strain. In contrast, LMW fractions from an exoA mutant, nonsuccinylated LMW succinoglycan, and HMW succinoglycan did not promote invasion, nor did LMW exopolysaccharides from R. leguminosarum bv. trifolii and Rhizobium sp. strain NGR234. LMW succinoglycan could be separated by anion-exchange chromatography into several distinct subfractions differing in repeating subunit multiplicities (monomer, trimer, and tetramer) and charge. When tested singly, only the most charged, tetrameric form was active. These results show that a specific oligosaccharide form of succinoglycan promotes nodule invasion in alfalfa. The implications for the mode of action of succinoglycan are discussed.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Chakravorty A. K., Zurkowski W., Shine J., Rolfe B. G. Symbiotic nitrogen fixation: molecular cloning of Rhizobium genes involved in exopolysaccharide synthesis and effective nodulation. J Mol Appl Genet. 1982;1(6):585–596. [PubMed] [Google Scholar]
  2. De Vos G. F., Walker G. C., Signer E. R. Genetic manipulations in Rhizobium meliloti utilizing two new transposon Tn5 derivatives. Mol Gen Genet. 1986 Sep;204(3):485–491. doi: 10.1007/BF00331029. [DOI] [PubMed] [Google Scholar]
  3. Djordjevic S. P., Chen H., Batley M., Redmond J. W., Rolfe B. G. Nitrogen fixation ability of exopolysaccharide synthesis mutants of Rhizobium sp. strain NGR234 and Rhizobium trifolii is restored by the addition of homologous exopolysaccharides. J Bacteriol. 1987 Jan;169(1):53–60. doi: 10.1128/jb.169.1.53-60.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Glazebrook J., Walker G. C. A novel exopolysaccharide can function in place of the calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti. Cell. 1989 Feb 24;56(4):661–672. doi: 10.1016/0092-8674(89)90588-6. [DOI] [PubMed] [Google Scholar]
  5. Gray J. X., Zhan H. J., Levery S. B., Battisti L., Rolfe B. G., Leigh J. A. Heterologous exopolysaccharide production in Rhizobium sp. strain NGR234 and consequences for nodule development. J Bacteriol. 1991 May;173(10):3066–3077. doi: 10.1128/jb.173.10.3066-3077.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Honma M. A., Ausubel F. M. Rhizobium meliloti has three functional copies of the nodD symbiotic regulatory gene. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8558–8562. doi: 10.1073/pnas.84.23.8558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Leigh J. A., Lee C. C. Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules. J Bacteriol. 1988 Aug;170(8):3327–3332. doi: 10.1128/jb.170.8.3327-3332.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Leigh J. A., Reed J. W., Hanks J. F., Hirsch A. M., Walker G. C. Rhizobium meliloti mutants that fail to succinylate their calcofluor-binding exopolysaccharide are defective in nodule invasion. Cell. 1987 Nov 20;51(4):579–587. doi: 10.1016/0092-8674(87)90127-9. [DOI] [PubMed] [Google Scholar]
  9. Leigh J. A., Signer E. R., Walker G. C. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6231–6235. doi: 10.1073/pnas.82.18.6231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lerouge P., Roche P., Faucher C., Maillet F., Truchet G., Promé J. C., Dénarié J. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature. 1990 Apr 19;344(6268):781–784. doi: 10.1038/344781a0. [DOI] [PubMed] [Google Scholar]
  11. Long S. R. Rhizobium-legume nodulation: life together in the underground. Cell. 1989 Jan 27;56(2):203–214. doi: 10.1016/0092-8674(89)90893-3. [DOI] [PubMed] [Google Scholar]
  12. Olivera B. M., Rivier J., Clark C., Ramilo C. A., Corpuz G. P., Abogadie F. C., Mena E. E., Woodward S. R., Hillyard D. R., Cruz L. J. Diversity of Conus neuropeptides. Science. 1990 Jul 20;249(4966):257–263. doi: 10.1126/science.2165278. [DOI] [PubMed] [Google Scholar]
  13. Peters N. K., Frost J. W., Long S. R. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science. 1986 Aug 29;233(4767):977–980. doi: 10.1126/science.3738520. [DOI] [PubMed] [Google Scholar]
  14. Tolmasky M. E., Staneloni R. J., Leloir L. F. Lipid-bound saccharides in Rhizobium meliloti. J Biol Chem. 1982 Jun 25;257(12):6751–6757. [PubMed] [Google Scholar]
  15. Yang C., Signer E. R., Hirsch A. M. Nodules Initiated by Rhizobium meliloti Exopolysaccharide Mutants Lack a Discrete, Persistent Nodule Meristem. Plant Physiol. 1992 Jan;98(1):143–151. doi: 10.1104/pp.98.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Zhan H. J., Levery S. B., Lee C. C., Leigh J. A. A second exopolysaccharide of Rhizobium meliloti strain SU47 that can function in root nodule invasion. Proc Natl Acad Sci U S A. 1989 May;86(9):3055–3059. doi: 10.1073/pnas.86.9.3055. [DOI] [PMC free article] [PubMed] [Google Scholar]

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