Symbiosis-specific expression of two Medicago truncatula nodulin genes, MtN1 and MtN13, encoding products homologous to plant defense proteins

Molecular Plant-Microbe Interactions

Volumn 11, Issue 5, 1998, Pages 393-403

  Gamas, Pascal ^a   De Billy, Françoise ^a   Truchet, Georges ^a  

^a CNRS   (France)

Author keywords

Gamma thionin

Indexed keywords

BACTERIAL INFECTION; CYSTEINE; GENE EXPRESSION; IDENTIFICATION; IN SITU HYBRIDIZATION; MEDICAGO TRUNCATULA; NODULIN; PATHOGENESIS; PLANT DEFENSE PROTEIN; RHIZOBIUM MELILOTI; SYMBIOSIS;

BACTERIA (MICROORGANISMS); EMBRYOPHYTA; MEDICAGO TRUNCATULA; PISUM SATIVUM; RHIZOBIUM; SINORHIZOBIUM MELILOTI;

EID: 0032078330     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.1998.11.5.393     Document Type: Article

References (61)

1. Allison, L. A., Kiss, G. B., Bauer, P., Poiret, M., Savouré, A., Kondorosi, E., and Kondorosi, A. 1993. Identification of two alfalfa early nodulin genes with homology to members of the pea Enod12 family. Plant Mol. Biol. 21:375-380.
2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Andersson, C., Ostergaard Jensen, E., Llewellyn, D., Dennis, E., and Peacock, W. J. 1996. A new hemoglobin gene from soybean: A role for hemoglobin in all plants. Proc. Natl. Acad. Sci. USA 93:5682-5687.
4. 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.
5. Barker, D. G., Bianchi, S., Blondon, F., Datté, Y., Duc, G., Flament, P., Gallusci, P., Génier, P., Guy, P., Muel, X., Tourneur, J., Dénarié, J., and Huguet, T. 1990. Medicago truncatula, a model plant for studying the molecular genetics of the Rhizobium-legume symbiosis. Plant Mol. Biol. Rep. 8:40-49.
6. Baron, C., and Zambriski, P. 1995. The plant response in pathogenesis, symbiosis, and wounding: Variations on a common theme? Annu. Rev. Genet. 29:107-129.
7. Benaben, V., Due, G., Lefebvre, V., and Huguet, T. 1995. TE7, an inefficient symbiotic mutant of Medicago truncatula Gaertn. cv Jemalong. Plant Physiol. 107:53-62.
8. Breda, C., Sallaud, C., El-Turk, J., Buffard, D., de Kosak, I., Esnault, R., and Kondorosi, A. 1996. Defense reaction in Medicago sativa: A gene encoding a class 10 PR protein is expressed in vascular bundles. Mol. Plant-Microbe Interact. 9:713-719.
9. Bufe, A., Spangfort, M. D., Kahlert, M., Schlaak, M., and Becker, W. M. 1996. The major birch pollen allergen, Bet v 1, shows ribonuclease activity. Planta 199:413-415.
10. Chiang, C. C., and Hadwiger, L. A. 1990. Cloning and characterization of a disease resistance response gene in pea inducible by Fusarium solani. Mol. Plant-Microbe Interact. 3:78-85.
11. Chiang, C. C., and Hadwiger, L. A. 1991. The Fusarium solani-induced expression of a pea gene family encoding high cysteine content proteins. Mol. Plant-Microbe Interact. 4:324-331.
12. Cook, D., Dreyer, D., Bonnet, D., Howell, M., Nony, E., and VandenBosch, K. 1995. Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. Plant Cell 7:43-55.
13. Corpet, F. 1988. Multiple sequence alignment with hierarchical cluster-ing. Nucleic Acids Res. 16:10881-10890.
14. Cutt, J. R., and Klessig, D. F. 1992. Genes involved in plant defense. Pages 20-243 in: Plant Gene Research Series. T. Boller and F. Meins, eds. Springer, Vienna.
15. de Billy, F., Barker, D., Gallusci, P., and Truchet, G. 1991. Leghaemoglobin gene transcription is triggered in a single cell layer in the indeterminate nitrogen-fixing root nodule of alfalfa. Plant J. 1:27-35.
16. De Jong, A. J., Cordewener, J., Lo Schiavo, F., Terzi, M., Vandekerckove, J., Van Kammen, A., and De Vries, S. C. 1992. A carrot somatic embryo mutant is rescued by chitinase. Plant Cell 4:425-433.
17. Debellé, F., Rosenberg, C., Vasse, J., Maillet, F., Martinez, E., Dénarié, J., and Truchet, G. 1986. Assignment of symbiotic developmental phenotypes to common and specific (nod) genetic loci of Rhizobium meliloti. J. Bacteriol. 168:1075-1086.
18. 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.
19. Esnault, R., Buffard, D., Breda, C., Sallaud, C., El Turk, J., and Kondorosi, A. 1993. Pathological and molecular characterizations of alfalfa interactions with compatible and incompatible bacteria, Xanthomonas campestris pv. alfalfae and Pseudomonas syringae pv. pisi. Mol. Plant-Microbe Interact. 6:655-664.
20. Faucher, C., Camut, S., Dénarié, J., and Truchet, G. 1989. The nodH and nodQ host range genes of Rhizobium meliloti behave as avirulence genes in R. leguminosarum bv. viciae and determine changes in the production of plant-specific extracellular signals. Mol. Plant-Microbe Interact. 2:291-300.
21. Florack, D. E. A., and Stiekema, W. J. 1994. Thionins: Properties, possible biological roles and mechanisms of action. Plant Mol. Biol. 26:25-37.
22. Gallusci, P., Dedieu, A., Journet, E. P., Huguet, T., and Barker, D. G. 1991. Synchronous expression of leghaemoglobin genes in Medicago truncatula during nitrogen-fixing root nodule development and response to exogenously supplied nitrate. Plant Mol. Biol. 17:335-349.
23. Gamas, P., de Carvalho Niebel, F., Lescure, N., and Cullimore, J. V. 1996. Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. Mol. Plant-Microbe Interact. 9:233-242.
24. Gu, Q., Kawata, E. E., Morse, M.-J., Wu, H.-M., and Cheung, A. 1992. A flower-specific cDNA encoding a novel thionin in tobacco. Mol. Gen. Genet. 234:89-96.
25. Hirsch, A. 1992. Developmental biology of legume nodulation. Tansley Review No. 40. New Phytol. 122:211-237.
26. Jackson, A. D., and Larkins, B. A. 1976. Influence of ionic strength, pH, and chelation of divalent metals on isolation of polyribosomes from tobacco leaves. Plant Physiol. 57:5-10.
27. Kado, C. I., and Heskett, M. G. 1970. Selective media for isolation of Agrobacterium, Corynebacterium, Erwinia, Pseudomonas, and Xanthomonas. Phytopathology 60:969-976.
28. Kijne, J. 1992. The Rhizobium infection process. Pages 348-397 in: Biological Nitrogen Fixation. G. Stacey, H. Evans, and R. Burris, eds. Chapman and Hall, London.
29. King, E. O., Ward, M. K., and Rancy, D. E. 1954. Two simple media for the demonstration of phycocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
30. Kragh, K. M., Nielsen, J. E., Nielsen, K. K., Dreboldt, S., and Mikkelsen, J. D. 1995. Characterization and localization of new antifungal cysteine-rich proteins from Beta vulgaris. Mol. Plant-Microbe Interact. 8:424-434.
31. Kyte, J., and Doolittle, R. F. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
32. Löbler, M., and Hirsch, A. M. 1993. A gene that encodes a proline-rich nodulin with limited homology to PsENOD 12 is expressed in the invasion zone of Rhizobium meliloti-induced alfalfa root nodules. Plant Physiol. 103:21-30.
33. Long, S. 1996. Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885-1898.
34. Lotan, T., Ori, N., and Fluhr, R. 1989. Pathogenesis-related proteins are developmentally regulated in tobacco flowers. Plant Cell 1:881-887.
35. McKhann, H. I., and Hirsch, A. M. 1994. Does Rhizobium avoid the host response? Pages 139-162 in: Bacterial Pathogenesis of Plants and Animals. J. L. Dangl, ed. Springer-Verlag, Berlin.
36. Milligan, S. B., and Gasser, C. S. 1995. Nature and regulation of pistil-expressed genes in tomato. Plant Mol. Biol. 28:691-711.
37. Moiseyev, G., Beintema, J., Fedoreyeva, L., and Yakovlev, G. 1994. High sequence similarity between a ribonuclease from ginseng calluses and fungus-elicited proteins from parsley indicates that intra-cellular pathogenesis-related proteins are ribonucleases. Planta 193:470-472.
38. Mylona, P., Moerman, M., Yang, W.-C., Gloudemans, T., Vandekerckove, J., Van Kammen, A., Bisseling, T., and Franssen, H. J. 1994. The root epidermis-specific pea gene RH2 is homologous to a pathogenesis-related gene. Plant Mol. Biol. 26:39-50.
39. Nakai, K., and Kanehisa, M. 1992. A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14:897-911.
40. Neale, A. D., Wahleithner, J. A., Lund, M., Bonnett, H. T., Kelly, A., Meeks-Wagner, D. R., Peacock, W. J., and Dennis, E. S. 1990. Chitinase, β-1,3-glucanase, osmotin, and extensin are expressed in tobacco explants during flower formation. Plant Cell 2:673-684.
41. Niehaus, K., Kapp, D., and Pühler, A. 1993. Plant defense and delayed infection of alfalfa pseudonodules induced by an exopolysaccharide (EPS I)-deficient Rhizobium meliloti mutant. Planta 190:415-425.
42. Noel, K. D., VandenBosch, K. A., and Kulpaca, B. 1986. Mutations in Rhizobium phaseoli that lead to arrested development of infection threads. J. Bacteriol. 168:1392-1401.
43. Pawlowski, K., and Bisseling, T. 1996. Rhizobial and actinorhizal symbioses: What are the shared features? Plant Cell 8:1899-1913.
44. Pichon, M., Journet, E. P., Dedieu, A., de Billy, F., Truchet, G., and Barker, D. G. 1992. Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell 4:1199-1211.
45. 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 sulfation of lipo-oligosaccharide signals. Cell 67:1131-1143.
46. 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.
47. Scheres, B., Van Engelen, F., Van der Knaap, E., Van de Wiel, C., Van Kammen, A., and Bisseling, T. 1990. Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell 2:687-700.
48. 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.
49. Spaink, H. P. 1996. Regulation of plant morphogenesis by lipo-chitin oligosaccharides. Crit. Rev. Plant Sci. 15:559-582.
50. Staehelin, C., Schultze, M., Kondorosi, E., Mellor, R. B., Boller, T., and Kondorosi, A. 1994. Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases. Plant J. 5:319-330.
51. Swoboda, I., Hoffmann-Sommergruber, K., O'Riordain, G., Scheiner, O., Heberle-Bors, E., and Vicente, O. 1996. Bet v 1 proteins, the major birch pollen allergens and members of conserved pathogenesis-related proteins, show ribonuclease activity in vitro. Physiol. Plant. 96:433-438.
52. Swoboda, I., Scheiner, O., Heberle-Bors, E., and Vicente, O. 1995. cDNA cloning and characterization of three birch genes, members of the bet v 1 gene family of pollen allergens, that encode pathogenesis-related proteins. Plant Cell Environ. 18:865-874.
53. Truchet, G., Barker, D. G., Camut, S., de Billy, F., Vasse, J., and Huguet, T. 1989. Alfalfa nodulation in the absence of Rhizobium. Mol. Gen. Genet. 219:65-68.
54. Truesdell, G., and Dickman, M. 1997. Isolation of pathogen/stress-inducible cDNAs from alfalfa by mRNA differential display. Plant Mol. Biol. 33:737-743.
55. Van de Wiel, C., Norris, J., Bochenek, B., Dickstein, R., Bisseling, T., and Hirsch, A. 1990. Nodulin gene expression and ENOD2 localization in effective, nitrogen-fixing and ineffective, bacteria-free nodules of alfalfa. Plant Cell 2:1009-1017.
56. Van Kammen, A. 1984. Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Mol. Biol. Rep. 2:43-45.
57. Van Loon, L. C., Pierpoint, W. S., Boller, T., and Conejero, V. 1994. Recommendations for naming plant pathogenesis-related proteins. Plant Mol. Biol. Rep. 12:245-264.
58. 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.
59. Vasse, J., de Billy, F., and Truchet, G. 1993. Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. Plant J. 4:555-566.
60. Wilson, R. C., Long, F., Maruoka, E. M., and Cooper, J. C. 1994. A new proline-rich early nodulin from Medicago truncatula is highly expressed in nodule meristematic cells. Plant Cell 6:1265-1275.
61. Yang, C., Signer, E. R., and Hirsch, A. M. 1992. Nodules initiated by Rhizobium meliloti exopolysaccharide mutants lack a discrete, persistent nodule meristem. Plant Physiol. 98:143-151.