Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa

Development

Volumn 125, Issue 3, 1998, Pages 339-349

  Timmers, Antonius C J ^a   Auriac, Marie Christine ^a   De Billy, Françoise ^a   Truchet, Georges ^a  

^a CNRS   (France)

Author keywords

Alfalfa; Microtubular cytoskeleton; Nod factors; Nodule differentiation; Rhizobium meliloti

Indexed keywords

TUBULIN;

ALFALFA; ARTICLE; CYTOSKELETON; DEVELOPMENTAL GENETICS; DIFFERENTIATION; INTERNALIZATION; NONHUMAN; ONTOGENY; PLANT GROWTH; POLYPLOIDY; PRIORITY JOURNAL; SOIL MICROFLORA; SYMBIOSIS;

CELL DIFFERENTIATION; CYTOPLASM; MEDICAGO SATIVA; MICROTUBULE PROTEINS; MICROTUBULES; ORGANELLES; PLANT ROOTS; RHIZOBIUM;

BACTERIA (MICROORGANISMS); MEDICAGO SATIVA; RHIZOBIUM; SINORHIZOBIUM MELILOTI;

EID: 0031913138     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. + currents and on cytoskeletal behavior. In Advances in Molecular Genetics of Plant-Microbe Interactions (ed. M. J. Daniels, J. A. Downie and A. E. Osbourn), Vol. 3, pp. 107-113. Kluwer Academic Publishers, Dordrecht.
2. Ardourel, M., Demont, N., Debellé, F., Maillet, F., De Billy, F., Promé, J.-C., Dénarié, J. and Truchet, G. (1994). Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6, 1357-1374.
3. Bakhuizen, R. (1988). The plant cytoskeleton in the Rhizobium-legume symbiosis. Ph.D. thesis. Leiden University, The Netherlands.
4. Bakhuizen, R., Van Spronsen, P. C., Sluiman-Den Hertog, F. A. J., Venverloo, C. J. and Goosen-De Roo, L. (1985). Nuclear envelope radiating microtubules in plant cells during interphase mitosis transition. Protoplasma 128, 43-51.
5. Baluska, F., Parker, J. S. and Barlow, P. W. (1992). Specific patterns of cortical and endoplasmic microtubules associated with cell growth and tissue differentiation in roots of maize (Zea mays L.). J. Cell Sci. 103, 191-200.
6. Bershadsky, A., Chausovsky, A., Becker, E., Lyubimova, A. and Geiger, B. (1996). Involvement of microtubules in the control of adhesion-dependent signal transduction. Curr. Biol. 6, 1279-1289.
7. Blanchard, V., Raisman-Vozari, R., Savasta, M., Hirsch, E., Javoy-Agid, F., Feuerstein, C. and Agid, Y. (1993). Cellular quantification of tyrosine hydroxylase in the rat brain by immunoautoradioaraphy. J. Neurochem. 61, 617-626.
8. Bono, J.-J., Riond, J., Nicolaou, K. C., Bockovich, N. J., Estevez, V. A., Cullimore, J. V. and Ranjeva, R. (1995). Characterization of a binding site for chemically synthesized lipo-oligosaccharidic NodRm factors in particulate fractions prepared from roots. Plant J. 7, 253-260.
9. Brewin, N. J. (1991). Development of the legume root nodule. Ann. Rev. Cell Biol. 7, 191-226.
10. Brown, R. C., Lemmon, B. E. and Olsen, O.-A. (1994). Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell 6, 1241-1252.
11. Callaham, D. A. and Torrey, J. G. (1981). The structural basis for infection of root hairs of Trifolium repens by Rhizobium. Can. J. Bot. 59, 1647-1664.
12. Cole, N. B. and Lippincott-Schwartz, J. (1995). Organization of organelles and membrane traffic by microtubules. Curr. Opin. Cell Biol. 7, 55-64.
13. Crossin, K. L. and Carney, D. H. (1981). Evidence that microtubule depolymerization early in the ceil cycle is sufficient to initiate DNA synthesis. Cell 23, 61-71.
14. Cyr, R. J. (1994) Microtubules in plant morphogenesis: role of the cortical array. Ann. Rev. Cell Biol. 10, 153-180.
15. Cyr, R. J. and Palevitz, B. A. (1995). Organization of cortical microtubules in plant cells. Curr. Opin. Cell Biol. 7, 65-71.
16. Dénarié, J., Debellé, F. and Promé, J.-C. (1996). Rhizobium lipochitooligosaccharide nodulation factors: Signaling molecules mediating recognition and morphogenesis. Ann. Rev. Biochem. 65, 503-535.
17. Djordjevic, M. A., Schofield, P. R. and Rolfe, B. G. (1985). Tn5 mutagenesis of Rhizobium trifolii host-specific nodulation genes result in mutants with altered host-range ability. Mol. Gen. Genet. 200, 463-471.
18. Ehrhardt, D. W., Atkinson, E. M. and Long, S. R. (1992). Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256, 998-1000.
19. Ehrhardt, D. W., Wais, R. and Long, S. R. (1996). Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85, 673-681.
20. Engvall, E. and Perlmann, P. (1971). Enzyme-linked immunosorbent assay (ELISA). Quantitative assay of immunoglobulin G. Immunochem. 8, 871-874.
21. Felle, H. H., Kondorosi, E. and Kondorosi, A. (1995). Nod-signal induced plasma membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipochito-oligosaccharide. Plant J. 7, 939-947.
22. Foussard, M., Garnerone, A.-M., Ni, F., Soupène, E., Boistard, P. and Batut, J. (1997). Negative autoregulation of the Rhizobium meliloti fixK gene is indirect and requires a newly identified regulator. FixT. Mol. Microbiol. 25, 27-37.
23. Giddings, T. H. Jr. and Staehelin, L. A. (1991). Microtubule-mediated control of microfibril deposition: a re-examination of the hypothesis. In The Cytoskeletal Basis of Plant Growth and Form (ed. C. W. Lloyd), pp. 85-99. Academic Press, London.
24. Goddard, R. H., Wick, S. W., Silflow, C. D. and Sunstad, D. P. (1994) Microtubule components of the plant cell cytoskeleton. Plant Physiol. 104, 1-6.
25. Hirsch, A. M. (1992). Developmental biology of legume nodulation. New. Phytol. 122, 211-237.
26. Kijne, J. W. (1992). The rhizobium infection process. In Biological Nitrogen Fixation (ed. G. Stacey, R. H. Burris and H. J. Evans), pp. 349-398. Chapmann and Hall, New York.
27. Lambert, A.-M. (1993). Microtubule-organizing centers in higher plants. Curr. Opin. Cell Biol. 5, 116-122.
28. Leigh, J. A., Signer, E. R. and Walker, G. C. (1985). Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc. Natl. Acad. Sci. USA 82, 6231-6235.
29. Lewin, A., Cervantes, E., Wong, C.-H. and Broughton, W. J. (1990). nodSU, two new nod genes of the broad host range Rhizobium strain NGR234 encode host-specific nodulation of the tropical tree Leucaena leucocephala. Mol. Plant-Microbe Interact. 3, 317-326.
30. Long, S. R. (1996). Rhizobium symbiosis: Nod factors in perspective. Plain Cell 8, 1885-1898.
31. Liu, B., Joshi, H. C., Wilson, T. J., Silflow, C. D., Palevitz, B. A. and Snustad, D. P. (1994). γ-Tubulin in Arabidopsis: Gene sequence, immunoblot, and immunofluorescence studies. Plant Cell 6, 303-314.
32. Martinez-Romero, E. and Cabballero-Mellado, J. (1996). Rhizobium phylogenies and bacterial genetic diversity. Crit. Rev. Plant Sci. 15, 113-140.
33. Newcomb, W. (1981). Nodule morphogenesis and differentiation. In Biology of the Rhizobiaceae (ed. K. L. Giles and A. G. Atherly), Int. Rev. Cytol., suppl. 13. pp. 247-298. Academic Press, New York.
34. Niebel, A., Bono, J.-J., Ranjeva, R. and Cullimore, J. V. (1997). Identification of a high affinity binding site for lipo-oligosaccharidic NodRm factors in the microsomal fraction of Medicago cell suspension cultures. Mol. Plant-Microb. Interact. 10, 132-134.
35. Panteris, E., Apostolakos, P. and Galatis, B. (1995). Telophase-interphase transition in taxol-treated Triticum root cells: cortical microtubules appear without the prior presence of a radial perinuclear array. Protoplasma 188, 78-84.
36. Philip-Hollingsworth, S., Dazzo, F. B. and Hollingsworth, R. (1997). Structural requirements of Rhizobium chitolipooligosaccharides for uptake and bioactivity in legume roots as revealed by synthetic analogs and fluorescent probes. J. Lipid Res. 38, 1229-1241.
37. Ridge, R. W. (1992). A model of legume root hair growth and Rhizobium infection. Symbiosis 14, 359-373.
38. Ridge, R. W. and Rolfe, B. G. (1985) Rhizobium sp. degradation of legume root hair cell wall at the site of infection thread origin. Appl. Envtl. Microbiol. 50, 717-720.
39. Roche, P., Debellé, F., Maillet, F., Lerouge, P., Faucher, C., Truchet, G., Dénarié, J. and Promé, J.-C. (1991). Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sultation of lipo-oligosaccharide signals. Cell 67, 1131-1143.
40. Roth, L. E. and Stacey, G. (1989). Bacterium release into host cells of nitrogen-fixing soybean nodules: The symbiosome membrane comes from three sources. Eur. J. Cell Biol. 49, 13-23.
41. Roth, L. E. and Stacey, G. (1991). Rhizobium-legume symbiosis. In Microbial Cell-Cell Interactions (ed. M. Dworkin), pp. 255-301. American Society of Microbiology, Washington D. C.
42. 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 bv. viciae. J. Bacteriol. 173, 4277-4287.
43. Schultze, M. and Kondorosi, A. (1996). The role of lipooligosaccharides in root nodule organogenesis and plant cell growth. Curr. Opin. Genet. Devel. 6, 631-638.
44. Seagull, R. W. (1989). The plant cytoskeleton. CRC Crit. Rev. Plant Sci. 8, 131-167.
45. Spaink, H. P. (1996). Regulation of plant morphogenesis by lipo-chitin oligosaccharides. Crit. Rev. Plant Sci. 15, 559-582.
46. Truchet, G. (1978). Sur l'tat diploide des cellules du meristme des nodules radiculaires des Lgumineuses. Ann. Sci. Nat. Bot. Biol. Vg. 19, 3-38.
47. Truchet, G., Barker, D. G., Camut, S., De Billy, F., Vasse, J. and Huguet, T. (1989). Alfalfa nodulution in the absence of Rhizobium. Mol. Gen. Genet. 219, 65-68.
48. Truchet, G. and Coulomb, P. (1973). Mise en évidence et évolution du système phytolysosomal dans les cellules des différentes zones de nodules radiculaires de pois (Pisum sativum L.). Notion d'hétérophagie. J. Ultrastruct. Res. 43, 36-57.
49. Truchet, G., Roche, P., Lcrouge, P., Vasse, J., Camut, S., De Billy, F., Promé, J.-C. and Dénarié, J. (1991). Sulfated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351, 670-673.
50. Van Brussel, A. A. N., Bakhuizen, R., Van Spronsen, P. C., Spaink, H. P., Tak, T., Lugtenberg, B. J. J. and Kijne, J. W. (1992). Induction of preinfection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium. Science 2547, 70-72.
51. Van Brussel, A. A. N., Zaat, S. A. J., Canter Cremers, H. C. J., Wijfellman, C. A., Pees, E., Tak, T. and 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.
52. Van Spronsen, P. C., Van Brussel, A. A. N. and Kijne, J. W. (1995). Nod factors produced by Rhizobium leguminosarum biovar viciae induce ethylene-related changes in root cortical cells of Vicia sativa ssp. nigra. Eur. J. Cell Biol. 68, 463-469.
53. Vasse, J., de Billy, F., Camut, S. and Truchet, G. (1990). Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J. Bacteriol. 172, 4295-4306.
54. Warren, G. and Wickner, W. (1996). Organelle inheritance. Cell 84, 395-400.
55. Williamson, R. E. (1991). Orientation of cortical microtubules in interphase plant cells. Int. Rev. Cytol. 129, 135-206.
56. Yaffe, M. P., Harata, D., Verde, F, Eddison, M., Toda, T. and Nurse P. (1996). Microtubules mediate mitochondrial distribution in fission yeast. Proc. Natl. Acad. Sci. USA 93, 11664-11668.
57. Yang, W.-C., De Blank, C., Meskiene, I., Hirt, H., Bakker, J., Van Kammen, A., Franssen, H. and Bisseling, T. (1994). Rhizobium Nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. Plant Cell 6, 1415-1426,