Roles for azorhizobial nod factors and surface polysaccharides in intercellular invasion and nodule penetration, respectively

Molecular Plant-Microbe Interactions

Volumn 11, Issue 10, 1998, Pages 999-1008

  D'Haeze, Wim ^a   Gao, Mengsheng ^a   De Rycke, Riet ^a   Van Montagu, Marc ^a   Engler, Gilbert ^b   Holsters, Marcelle ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

GUS; LCO

Indexed keywords

BACTERIAL COLONIZATION; BACTERIAL INFECTION; INOCULATION; MUTANT; NODULATION; NODULATION FACTOR; POLYSACCHARIDE;

AZORHIZOBIUM CAULINODANS; BACTERIA (MICROORGANISMS); ROSTRATA; SESBANIA ROSTRATA;

EID: 0031687727     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.1998.11.10.999     Document Type: Article

References (45)

1. Bauer, W. D. 1981. Infection of legumes by rhizobia. Annu. Rev. Plant Physiol. 32:407-449.
2. Cedergren, R. A., Lee, J., Ross, K. L., and Hollingsworth, R. I. 1995. Common links in the structure and cellular localization of Rhizobium chitolipooligosaccharides and general Rhizobium membrane phospholipid and glycolipid components. Biochemistry 34:4467-4477.
3. Chandler, M. R., Date, R. A., and Roughley, R. J. 1982. Infection and root-nodule development in Stylosanthes species by Rhizobium. J. Exp. Bot. 33:47-57.
4. De Block, M., and Debrouwer, D. 1992. In-situ enzyme histochemistry on plastic-embedded plant material. The development of an artefact-free β-glucuronidase assay. Plant J. 2:261-266.
5. Dénarié, J., Debellé, F., and Promé, J.-C. 1996. Rhizobium lipochitooligosaccharide nodulation factors: Signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65: 503-535.
6. Ditta, G., Stanfield, S., Corbin, D., and Helinski, D. R. 1980. Broad host range DNA cloning system for Gram-negative bacteria: Construction of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 77: 7347-7351.
7. Duhoux, E. 1984. Ontogénèse des nodules caulinaires du Sesbania rostrata (légumineuses). Can. J. Bot. 62:982-994.
8. Fischer, H.-M. 1994. Genetic regulation of nitrogen fixation in rhizobia. Microbiol. Rev. 58:352-386.
9. Forsberg, L. S., and Reuhs, B. L. 1997. Structural characterization of the K antigens from Rhizobium fredii USDA257: Evidence for a common structural motif, with strain-specific variation, in the capsular polysaccharides of Rhizobium spp. J. Bacteriol. 179:5366-5371.
10. Freiberg, C., Fellay, R., Bairoch, A., Broughton, W. J., Rosenthal, A., and Perret, X. 1997. Molecular basis of symbiosis between Rhizobium and legumes. Nature (London) 387:394-401.
11. Gage, D. J., Bobo, T., and Long, S. R. 1996. Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J. Bacteriol. 178:7159-7166.
12. Geremia, R. A., Mergaert, P., Geelen, D., Van Montagu, M., and Holsters, M. 1994. The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminyltransferase. Proc. Natl. Acad. Sci. USA 91: 2669-2673.
13. Goethals, K., Gao, M., Tomekpe, K., Van Montagu, M., and Holsters, M. 1989. Common nodABC genes in Nod locus 1 of Azorhizobium caulinodans: Nucleotide sequence and plant-inducible expression. Mol. Gen. Genet. 219:289-298.
14. Goethals, K., Leyman, B., Van den Eede, G., Van Montagu, M., and Holsters, M. 1994. An Azorhizobium caulinodans ORS571 locus involved in lipopolysaccharide production and nodule formation on Sesbania rostrata stems and roots. J. Bacteriol. 176:92-99.
15. Goormachtig, S., Alves-Ferreira, M., Van Montagu, M., Engler, G., and Holsters, M. 1997. Expression of cell cycle genes during Sesbania rostrata stem nodule development. Mol. Plant-Microbe Interact. 10: 316-325.
16. Goormachtig, S., Valerio-Lepiniec, M., Szczyglowski, K., Van Montagu, M., Holsters, M., and de Bruijn, F. J. 1995. Use of differential display to identify novel Sesbania rostrata genes enhanced by Azorhizobium caulinodans infection. Mol. Plant-Microbe Interact. 8:816-824.
17. Gough, C., Galera, C., Vasse, J., Webster, G., Cocking, E. C., and Dénarié, J. 1997. Specific flavonoids promote intercellular root colonization of Arabidopsis thaliana by Azorhizobium caulinodans ORS571. Mol. Plant-Microbe Interact. 10:560-570.
18. Heidstra, R., and Bisseling, T. 1996. Nod factor-induced host responses and mechanisms of Nod factor perception. New Phytol. 133:25-43.
19. Heidstra, R., Geurts, R., Franssen, H., Spaink, H. P., van Kammen, A., and Bisseling, T. 1994. Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol. 105:787-797.
20. Jefferson, R. A. 1987. Assaying chimeric genes in plants: The GUS gene fusion system. Plant Mol. Biol. Rep. 5:387-405.
21. Jefferson, R. A., Kavanagh, T. A., and Bevan, M. W. 1987. GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6:3901-3907.
22. Kapp, D., Niehaus, K., Quandt, J., Müller, P., and Pühler, A. 1990. Co-operative action of Rhizobium meliloti nodulation and infection mutants during the process of forming mixed infected alfalfa nodules. Plant Cell 2:139-151.
23. Kijne, J. W. 1992. The Rhizobium infection process. Pages 349-398 in: Biological Nitrogen Fixation. G. Stacey, R. H. Burris, and H. J. Evans, eds. Chapman & Hall, New York.
24. Klein, S., Hirsch, A. M., Smith, C. A., and Signer, E. R. 1988. Interaction of nod and exo Rhizobium meliloti in alfalfa nodulation. Mol. Plant-Microbe Interact. 1:94-100.
25. Leong, S. A., Williams, P. H., and Ditta, G. S. 1985. Analysis of the 5′ regulatory region of the gene for δ-aminolevulinic acid synthetase of Rhizobium meliloti. Nucleic Acids Res. 13:5965-5976.
26. Long, S. R. 1996. Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885-1898.
27. Mergaert, P., D'Haeze, W., Geelen, D., Promé, D., Van Montagu, M., Promé, J.-C., and Holsters, M. 1995. Biosynthesis of Azorhizobium caulinodans Nod factors. Study of the activity of the NodABCS proteins by expression of the genes in Escherichia coli. J. Biol. Chem. 270:29217-29223.
28. Mergaert, P., Ferro, M., D'Haeze, W., Van Montagu, M., Holsters, M., and Promé, J.-C. 1997a. Nod factors of Azorhizobium caulinodans strain ORS571 can be glycosylated with an arabinosyl group, a fucosyl group, or both. Mol. Plant-Microbe Interact. 10:683-687.
29. Mergaert, P., Van Montagu, M., and Holsters, M. 1997b. Molecular mechanisms of Nod factor diversity. Mol. Microbiol. 25:811-817.
30. Mergaert, P., Van Montagu, M., Promé, J.-C., and 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.
31. Mylona, P., Pawlowski, K., and Bisseling, T. 1995. Symbiotic nitrogen fixation. Plant Cell 7:869-885.
32. O'Brien, T. P, Feder, N., and McCully, M. E. 1964. Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59: 367-373.
33. O'Callaghan, K. J., Davey, M. R., and Cocking, E. 1997. Xylem colonization of the legume Sesbania rostrata by Azorhizobium caulinodans. Proc. R. Soc. Lond. B 264:1821-1826.
34. Relić, B., Perret, X., Estrada-García, M. T, Kopcinska, J., Golinowski, W., Krishnan, H. B., Pueppke, S. G., and Broughton, W. J. 1994. Nod factors of Rhizobium are a key to the legume door. Mol. Microbiol. 13:171-178.
35. Sambrook, J., Fritsch, E. F., and Maniatis, T. A. 1989. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
36. Schlaman, H. R. M., Horvath, B., Vijgenboom, E., Okker, R. J. H., and Lugtenberg, B. J. J. 1991. Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar viciae. J. Bacteriol. 173:4277-4287.
37. Schultze, M., Kondorosi, É., Ratet, P., Buiré, M., and Kondorosi, Á. 1994. Cell and molecular biology of Rhizobium-plant interactions. Int. Rev. Cytol. 156:1-75.
38. Sharma, S. B., and Signer, E. R. 1990. Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA. Genes Dev. 4:344-356.
39. Spaink, H. P. 1996. Regulation of plant morphogenesis by lipo-chitin oligosaccharides. Crit. Rev. Plant Sci. 15:559-582.
40. Sprent, J. I., and de Faria, S. M. 1988. Mechanisms of infection of plants by nitrogen fixing organisms. Plant Soil 110:157-165.
41. Timmers, A. C. J., Auriac, M.-C, de Billy, F., and Truchet, G. 1998. Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development 125:339-349.
42. Tsien, H. C., Dreyfus, B. L., and Schmidt, E. L. 1983. Initial stages in the morphogenesis of nitrogen-fixing stem nodules of Sesbania rostrata. J. Bacteriol. 156:888-897.
43. Van den Eede, G., Deblaere, R., Goethals, K., Van Montagu, M., and Holsters, M. 1992. Broad host range and promoter selection vectors for bacteria that interact with plants. Mol. Plant-Microbe Interact. 5: 228-234.
44. Van den Eede, G., Dreyfus, B., Goethals, K., Van Montagu, M., and Holsters, M. 1987. Identification and cloning of nodulation genes from the stem-nodulating bacterium ORS571. Mol. Gen. Genet. 206: 291-299.
45. van Workum, W. A. T., van Brussel, A. A. N., Tak, T, Wijffelman, C. A., and Kijne, J. W. 1995. Ethylene prevents nodulation of Vicia sativa ssp. nigra by exopolysaccharide-deficient mutants of Rhizobium leguminosarum bv. viciae. Mol. Plant-Microbe Interact. 8:278-285.