A carbonic anhydrase gene is induced in the nodule primordium and its cell-specific expression is controlled by the presence of Rhizobium during development

Plant Journal

Volumn 11, Issue 3, 1997, Pages 407-420

  De la Peña, Teodoro Coba ^a,b   Frugier, Florian ^a   McKhann, Heather I ^a,d   Bauer, Petra ^a,e   Brown, Spencer ^a   Kondorosi, Adam ^a,c   Crespi, Martin ^a  

^a CNRS   (France)

^b UNIVERSITY OF VIGO   (Spain)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d UTRECHT UNIVERSITY   (Netherlands)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

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

EID: 0031105327     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.1997.11030407.x     Document Type: Article

References (59)

1. 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.
2. Asad, S., Fang, Y., Wycoff, K.L. and Hirsch, A.M. (1994) Isolation and characterization of cDNA and genomic clones of Msenod40; transcripts are detected in meristematic cells of alfalfa. Protoplasma, 183, 10-23.
3. Atkins, C.A. (1974) Occurrence and some properties of carbonic anhydrases from legume root nodules. Phytochemistry, 13, 93-98.
4. Badger, M.R. and Price, G.D. (1994) The role of carbonic anhydrase in photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 369-392.
5. Bauer, P., Ratet, P., Crespi, M.D. and Kondorosi, A. (1996) Nod factors and cytokinins induce similar cortical cell division, amyloplast deposition and MsEnod12A expression patterns in alfalfa roots. Plant J. 10, 91-105.
6. Bradford, M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
7. Burnell, J.N., Gibbs, M.J. and Mason, J.G. (1990) Spinach chloroplastic carbonic anhydrase: nucleotide sequence analysis of cDNA. Plant Physiol. 92, 37-40.
8. Cooper, J.B. and Long, S.R. (1994) Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell, 6, 215-225.
9. Crespi, M.D., Jurkevitch, E., Poiret, M., D'Aubenton-Carafa, Y., Petrovics, G., Kondorosi, E. and Kondorosi, A. (1994). enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO J. 13, 5099-5112.
10. Day, D.A. and Copeland, L. (1991). Carbon metabolism and compartmentation in nitrogen-fixing legume nodules. Plant Physiol. Biochem. 29, 185-201.
11. Deak, M., Kiss, G.B., Koncz, C. and Dudits, D. (1986) Transformation of Medicago by Agrobacteriunn mediated gene transfer. Plant Cell Rep. 5, 97-100.
12. Drevon, J.J., Deransart, C., Fleurat-Lessard, P., Jaillard, B., Ndjiondjop, M.N., Payre, H., Ribet, J., Roy, G. and Serraj, R. (1995) Is the symbiotic nitrogen fixation osmoregulated by reversible contraction of cells in the legume-nodule inner-cortex? In Nitrogen Fixation: Fundamentals and Applications (Tikhonovich, Provorov, Romanov and Newton, eds). Dordrecht, The Netherlands: Kluwer Academic, p. 598.
13. Fett, J. and Coleman, J. (1994) Characterization and expression of two cDNAs encoding carbonic anhydrase in Arabidopsis thaliana. Plant Physiol. 105, 707-713.
14. Franssen, H.J., Vijn, I., Yang, W.C. and Bisseling, T. (1992) Developmental aspects of the Rhizobium-legume symbiosis. Plant Mol. Biol. 19, 89-107.
15. Furbank, R.T. and Taylor, W.C. (1995) Regulation of photosynthesis in C3 and C4 plants: a molecular approach. Plant Cell, 7, 797-807.
16. Gibson, A.H. and Nutman, P.S. (1960) Studies on the physiology of nodule formation. VII. A reappraisal of the effect of preplanting. Ann. Bot. 24, 420-433.
17. Glazebrook, J., Ichige, A. and Walker, G.C. (1993) A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Devel. 7, 1485-1497.
18. Hatch, M.D. and Burnell, J.N. (1990) Carbonic anhydrase activity in leaves and its role in the first step of C4 photosynthesis. Plant Physiol. 93, 825-828.
19. Hedrich, R. (1994) Voltage-dependent chloride channels in plant cells: identification, characterization, and regulation of a guard cell anion channel. Curr. Top. Memb. 42, 1-33.
20. 2 sensor to guard cells. EMBO J., 12, 897-901.
21. Hirsch, A.M. (1992) Developmental biology of legume nodulation. New Phytol. 122, 211-237.
22. Hirsch, A.M. and Fang, Y. (1994) Plant hormones and nodulation: what's the connection? Plant Mol. Biol. 26, 5-9.
23. Horvath, B., Heidstra, R., Lados, M., Moerman, M., Spaink, H.P., Prome, J.C., Kammen, A. V. and Bisseling, T. (1993) Lipooligosaccharides of Rhizobium induce infection-related early nodulin gene expression in pea root hairs. Plant J. 4, 727-733.
24. Hunt, S. and Layzell, D.B. (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu. Rev. Plant Mol. Biol. 44, 483-511.
25. Joshi, P.A., Caetano-Anolles, G., Graham, E.T. and Gresshoff, P.M. (1991) Ontogeny and ultrastructure of spontaneous nodules in alfalfa (Medicago sativa). Protoplasma, 162, 1-11.
26. Kereszt, A., Slaska-Kiss, K., Putnoky, P., Banfalvi, Z. and Kondorosi, A. (1995) The cycHJKL genes of Rhizobium meliloti involved in cytochrome c biogenesis are required for 'respiratory' nitrate reduction ex planta and for nitrogen fixation during symbiosis. Mol. Gen. Genet. 247, 39-47.
27. Kiss, G.B., Vincze, E., Kalman Z., Forrai, T. and Kondorosi, A. (1979) Genetic and biochemical analysis of mutants affected in nitrate reduction in Rhizobium meliloti. J. Gen. Microbiol. 113, 105-118.
28. Kondorosi, E., Banfalvi, Z. and Kondorosi, A. (1984) Physical and genetic analysis of a symbiotic region of Rhizobium meliloti: identification of nodulation genes. Mol. Gen. Genet, 193, 445-452.
29. Kurkdjian, A. and Guern, J. (1989) Intracellular pH: measurement and importance in cell activity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 271-303.
30. Küster, H., Frühling, M., Perlick, A. M. and Pühler, A. (1993) The sucrose synthase gene is predominantly expressed in the root nodule tissue of Vicia faba. Am. Phytopath. Soc. 6, 507-514.
31. Lerouge, P., Roche, P., Faucher, C., Maillet F., Truchet, G., Promé, J.C. and Dénarié, J. (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature, 344, 781-784.
32. McKhann, H.I. and Hirsch, A.M. (1993) In situ localization of specific mRNAs in plant tissues. In Experimental Procedures in Plant Molecular Biology and Biotechnology (Glick, B.R. and Thompson, J.E. eds). Boca Raton, FL: CRC Press, pp. 179-205.
33. Majeau, N., Arnoldo, M.A. and Coleman, J.R. (1994) Modification of carbonic anhydrase activity by antisense and over-expression constructs in transgenic tobacco. Plant Mol. Biol. 25, 377-385.
34. Majeau, N. and Coleman, J.R. (1991) Isolation and characterization of a cDNA coding for pea chloroplastic carbonic anhydrase. Plant Physiol. 95, 264-268.
35. Majeau, N. and Coleman, J.R. (1994) Correlation of carbonic anhydrase and ribulose-1,5-bisphosphate carboxylase/oxygenase expression in pea. Plant Physiol. 104, 1393-1399.
36. Miller, S.S., Boylan, K.L.M. and Vance, C.P. (1987) Alfalfa root nodule carbon dioxide fixation. III. Immunological studies of nodule phosphoenolpyruvate carboxylase. Plant Physiol. 84, 501-508.
37. Orosz, L., Svab, Z., Kondorosi, A. and Sik, T. (1973) Genetic studies on Rhizobiophage 16-3 T; genes and function on the chromosome. Mol. Gen. Genet. 125, 341-350.
38. Pathirana, S.M., Vance, C.P., Miller, S.S. and Gantt, S. (1992) Alfalfa root nodule phosphoenolpyruvate carboxylase: characterization of the cDNA and expression in effective and plant-controlled ineffective nodules. Plant Mol. Biol. 20, 437-450.
39. Pay, A., Heberle-Bors, E. and Hirt, H. (1992) An alfalfa cDNA encodes a protein with homology to translationally controlled human tumor protein. Plant. Mol. Biol. 19, 501-503.
40. Phillips, D.A. (1980) Efficiency of symbiotic nitrogen fixation in legumes. Annu. Rev. Plant Physiol. 31, 29-49.
41. Pichon, M., Journet, E.-P., de Billy, F., Dedieu, A., Huguet, T., Truchet, G. and Barker, D.G. (1994) ENOD12 gene expression as a molecular marker for comparing Rhizobium-dependent and -independent nodulation in alfalfa. Mol. Plant-Microbe Interact. 7, 740-747.
42. 2 assimilation. Planta, 193, 331-340.
43. Provart, N.J., Majeau, N. and Coleman, J.R. (1993) Characterization of pea chloroplastic carbonic anhydrase. Expression in Escherichia coli and site-directed mutagenesis. Plant Mol. Biol. 22, 937-943.
44. Putnoky, P., Grosskopf, E., Cam Ha, D.T., Kiss, G.B. and Kondorosi, A. (1988) Rhizobium fix genes mediate at least two communication steps in symbiotic nodule development. J. Cell Biol. 106, 597-607.
45. 2 on mRNA levels. Plant Mol. Biol. 20, 1143-1148.
46. Ridge, R.W., Ride, K.M. and Rolfe, B.G. (1993) Nodule-like structures induced on the roots of rice seedlings by addition of the synthetic auxin 2,4-dichlorophenoxyacetic acid. Aust. J. Plant Physiol. 20, 705-717.
47. 2 fixation in pea root nodules support bacteroid metabolism. Plant Physiol. 93, 12-19.
48. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
49. Sharma, P., Tripathi, A. and Bisht S. (1995) Zinc requirement for stomatal opening in Cauliflower. Plant Physiol. 107, 751-756.
50. Spaink, H.P., Sheeley, D.M., Van Brussel, A.A.N., Glushka, J., York, W.S., Tak, T., Geiger, O., Kennedy, E.P., Reinhold, V.N. and Lugtenberg, B.J.J. (1991) A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature, 354, 125-130.
51. Stokkermans, T.J.W. and Peters, N.K. (1994) Bradyrhizobium elkanii lipo-oligosaccharide signals induce complete nodule structures on Glycine soja Siebold et Zucc. Planta, 193, 413-420.
52. Sugiharto, B., Burnell J.N. and Sugiyama, T. (1992) Cytokinin is required to induce the nitrogen-dependent accumulation of mRNAs for phosphoenolpyruvate carboxylase and carbonic anhydrase in detached maize leaves. Plant Physiol. 100, 153-156.
53. Truchet, G., Barker, D.G., Camut, S., Billy, F.D., Vasse, J. and Huguet, T. (1989) Alfalfa nodulation in the absence of Rhizobium. Mol. Gen. Genet. 219, 65-68.
54. Truchet, G., Roche, P., Lerouge, P., Vasse, J., Camut S., de Billy, F., PromÁ, J.-C. and DÁnariÁ, J. (1991) Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature, 351, 670-673.
55. Van Kammen, A. (1984) Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Mol. Biol. Rep. 2, 43-45.
56. Vance, C.P. and Gantt, J.S. (1992) Control of nitrogen and carbon metabolism in root nodules. Physiol. Plant 85, 266-274.
57. Vance, C.P., Gregerson, R.G., Robinson, D.L., Miller, S.S. and Gantt, J.S. (1994) Primary assimilation of nitrogen in alfalfa nodules: molecular features of the enzymes involved. Plant Sci. 101, 51-64.
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. Williams, T. and Colman, B. (1993) Identification of distinct internal and external isozymes of carbonic anhydrase in Chlorella saccharofila. Plant Physiol. 103, 943-948.