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. 1991 Jun;173(11):3492–3499. doi: 10.1128/jb.173.11.3492-3499.1991

Early recognition in the Rhizobium meliloti-alfalfa symbiosis: root exudate factor stimulates root adsorption of homologous rhizobia.

L G Wall 1, G Favelukes 1
PMCID: PMC207963  PMID: 2045369

Abstract

Adsorption of Rhizobium meliloti to alfalfa roots before their infection and nodule formation shows the specificity of the symbiotic association (G. Caetano-Anollés and G. Favelukes, Appl. Environ. Microbiol. 52:377-382, 1986). The time course of specific adsorption of R. meliloti (10(3) to 10(4) cells per ml) to roots shows an initial lag period of 3 h, suggesting that either or both symbionts must become conditioned for the adsorption process. Preincubation of R. meliloti L5-30 for 3 h with dialyzed alfalfa root exudate (RE) markedly increased early adsorption of rhizobia to alfalfa roots. The activity in RE was linked to a nondialyzable, thermolabile, trypsin-sensitive factor(s), very different from the root-exuded flavonoid compounds also involved in early Rhizobium-legume interactions. The lack of activity in the RE from plants grown in 5 mM NO3- suggested its negative regulation by the nitrogen nutritional status of the plant. Preincubation of R. meliloti with heterologous clover RE did not stimulate adsorption of rhizobial cells to roots. A short pretreatment of RE with homologous (but not heterologous) strains eliminated the stimulatory activity from solution. The stimulation of adsorption of R. meliloti to alfalfa roots was strongly dependent on the growth phase of the rhizobia, being greater at the late exponential stage. Nevertheless, the capacity of R. meliloti L5-30 to eliminate from solution the stimulatory activity in RE appeared to be constitutive in the rhizobia. The low concentration of rhizobial cells used in these experiments was critical to detect the stimulation of adsorption. The early interaction of spontaneously released alfalfa root macromolecular factor(s) and free-living R. meliloti, which shows the specificity and regulatory properties characteristic of infection and nodulation, would be an initial recognition event in the rhizosphere which triggers the process of symbiotic association.

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Selected References

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  1. Badenoch-Jones J., Flanders D. J., Rolfe B. G. Association of Rhizobium Strains with Roots of Trifolium repens. Appl Environ Microbiol. 1985 Jun;49(6):1511–1520. doi: 10.1128/aem.49.6.1511-1520.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bergman K., Gulash-Hoffee M., Hovestadt R. E., Larosiliere R. C., Ronco P. G., 2nd, Su L. Physiology of behavioral mutants of Rhizobium meliloti: evidence for a dual chemotaxis pathway. J Bacteriol. 1988 Jul;170(7):3249–3254. doi: 10.1128/jb.170.7.3249-3254.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bhagwat A. A., Thomas J. Legume-Rhizobium interactions: cowpea root exudate elicits faster nodulation response by Rhizobium species. Appl Environ Microbiol. 1982 Apr;43(4):800–805. doi: 10.1128/aem.43.4.800-805.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bhuvaneswari T. V., Mills K. K., Crist D. K., Evans W. R., Bauer W. D. Effects of culture age on symbiotic infectivity of Rhizobium japonicum. J Bacteriol. 1983 Jan;153(1):443–451. doi: 10.1128/jb.153.1.443-451.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Caetano Anollés G., Favelukes G. Host-Symbiont Specificity Expressed during Early Adsorption of Rhizobium meliloti to the Root Surface of Alfalfa. Appl Environ Microbiol. 1986 Aug;52(2):377–382. doi: 10.1128/aem.52.2.377-382.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Caetano Anollés G., Favelukes G. Quantitation of adsorption of rhizobia in low numbers to small legume roots. Appl Environ Microbiol. 1986 Aug;52(2):371–376. doi: 10.1128/aem.52.2.371-376.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Caetano-Anollés G., Crist-Estes D. K., Bauer W. D. Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacteriol. 1988 Jul;170(7):3164–3169. doi: 10.1128/jb.170.7.3164-3169.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Caetano-Anollés G., Wall L. G., De Micheli A. T., Macchi E. M., Bauer W. D., Favelukes G. Role of Motility and Chemotaxis in Efficiency of Nodulation by Rhizobium meliloti. Plant Physiol. 1988 Apr;86(4):1228–1235. doi: 10.1104/pp.86.4.1228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Currier W. W., Strobel G. A. Chemotaxis of Rhizobium spp. to a Glycoprotein Produced by Birdsfoot Trefoil Roots. Science. 1977 Apr 22;196(4288):434–436. doi: 10.1126/science.196.4288.434. [DOI] [PubMed] [Google Scholar]
  10. Dazzo F. B., Napoli C. A., Hubbell D. H. Adsorption of bacteria to roots as related to host specificity in the Rhizobium-clover symbiosis. Appl Environ Microbiol. 1976 Jul;32(1):166–171. doi: 10.1128/aem.32.1.166-171.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dazzo F. B., Truchet G. L., Sherwood J. E., Hrabak E. M., Abe M., Pankratz S. H. Specific phases of root hair attachment in the Rhizobium trifolii-clover symbiosis. Appl Environ Microbiol. 1984 Dec;48(6):1140–1150. doi: 10.1128/aem.48.6.1140-1150.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dazzo F. B., Truchet G. L., Sherwood J. E., Hrabak E. M., Gardiol A. E. Alteration of the Trifoliin A-Binding Capsule of Rhizobium trifolii 0403 by Enzymes Released from Clover Roots. Appl Environ Microbiol. 1982 Aug;44(2):478–490. doi: 10.1128/aem.44.2.478-490.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. FAHRAEUS G. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol. 1957 Apr;16(2):374–381. doi: 10.1099/00221287-16-2-374. [DOI] [PubMed] [Google Scholar]
  14. Faucher C., Maillet F., Vasse J., Rosenberg C., van Brussel A. A., Truchet G., Dénarié J. Rhizobium meliloti host range nodH gene determines production of an alfalfa-specific extracellular signal. J Bacteriol. 1988 Dec;170(12):5489–5499. doi: 10.1128/jb.170.12.5489-5499.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Halverson L. J., Stacey G. Effect of lectin on nodulation by wild-type Bradyrhizobium japonicum and a nodulation-defective mutant. Appl Environ Microbiol. 1986 Apr;51(4):753–760. doi: 10.1128/aem.51.4.753-760.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Halverson L. J., Stacey G. Host recognition in the Rhizobium-soybean symbiosis : evidence for the involvement of lectin in nodulation. Plant Physiol. 1985 Mar;77(3):621–625. doi: 10.1104/pp.77.3.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Halverson L. J., Stacey G. Host recognition in the Rhizobium-soybean symbiosis: detection of a protein factor in soybean root exudate which is involved in the nodulation process. Plant Physiol. 1984 Jan;74(1):84–89. doi: 10.1104/pp.74.1.84. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Halverson L. J., Stacey G. Signal exchange in plant-microbe interactions. Microbiol Rev. 1986 Jun;50(2):193–225. doi: 10.1128/mr.50.2.193-225.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Honma M. A., Asomaning M., Ausubel F. M. Rhizobium meliloti nodD genes mediate host-specific activation of nodABC. J Bacteriol. 1990 Feb;172(2):901–911. doi: 10.1128/jb.172.2.901-911.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Maxwell C. A., Hartwig U. A., Joseph C. M., Phillips D. A. A Chalcone and Two Related Flavonoids Released from Alfalfa Roots Induce nod Genes of Rhizobium meliloti. Plant Physiol. 1989 Nov;91(3):842–847. doi: 10.1104/pp.91.3.842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Peters N. K., Long S. R. Alfalfa Root Exudates and Compounds which Promote or Inhibit Induction of Rhizobium meliloti Nodulation Genes. Plant Physiol. 1988 Oct;88(2):396–400. doi: 10.1104/pp.88.2.396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Smit G., Kijne J. W., Lugtenberg B. J. Involvement of both cellulose fibrils and a Ca2+-dependent adhesin in the attachment of Rhizobium leguminosarum to pea root hair tips. J Bacteriol. 1987 Sep;169(9):4294–4301. doi: 10.1128/jb.169.9.4294-4301.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Stacey G., Paau A. S., Brill W. J. Host recognition in the Rhizobium-soybean symbiosis. Plant Physiol. 1980 Oct;66(4):609–614. doi: 10.1104/pp.66.4.609. [DOI] [PMC free article] [PubMed] [Google Scholar]

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