Nodule parenchyma-specific expression of the Sesbania rostrata early nodulin gene SrEnod2 is mediated by its 3' untranslated region

Plant Cell

Volumn 10, Issue 10, 1998, Pages 1585-1602

  Chen, Rujin ^a,b,d   Silver, David L ^a,e   De Bruijn, Frans J ^a,b,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c University of Wisconsin ^*  (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EMBRYOPHYTA; GLYCINE MAX; LOTUS CORNICULATUS; RHIZOBIACEAE; ROSTRATA; SESBANIA ROSTRATA;

EID: 0031795690     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.10.10.1585     Document Type: Article

References (84)

1. Allen, T., Raja, S., and Dunn, K. (1991). Cells expressing Enod2 show differential spatial organization during the development of alfalfa root nodules. Mol. Plant-Microbe Interact. 2, 139-146.
2. An, G., Mitra, A., Choi, H.K., Costa, M.A., An, K., Thornburg, R.W., and Ryan, C.A. (1989). Functional analysis of the 3′ control region of the potato wound-inducible proteinase inhibitor II gene. Plant Cell 1, 115-122.
3. Arora, N., Skoog, F., and Allen, O.N. (1959). Kinetin-induced pseudonodules on tobacco roots. Am. J. Bot. 46, 610-613.
4. Averyhart-Fullard, V., Datta, K., and Marcus, A. (1988). A hydroxy-proline-rich protein in the soybean cell wall. Proc. Natl. Acad. Sci. USA 85, 1082-1085.
5. Benfey, P.N., Ren, L., and Chua, N.-H. (1989). The CaMV 35S enhancer contains at least two domains which can confer developmental and tissue-specific expression patterns. EMBO J. 8, 2195-2202.
6. Binder, R., Horowitz, J.A., Basilion, J.P., Koeller, D.M., Klausner, R.D., and Harford, J.B. (1994). Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3′ UTR and does not involve poly(A) tail shortening. EMBO J. 13, 1969-1980.
7. Bodine, D.M., and Ley, T.J. (1987). An enhancer element lies 3′ to the human Aγ globin gene. EMBO J. 6, 2997-3004.
8. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
9. Chen, F.Y., Amara, F.M., and Wright, J.A. (1993). Mammalian ribonucleotide reductase R1 mRNA stability under normal and phorbol ester stimulating conditions: Involvement of a cis-trans interaction at the 3′ untranslated region. EMBO J. 12, 3977-3986.
10. Chen, R. (1996). Structure, Function and Regulation of Early Nodulin Gene Enod2 from Legume Plants. PhD Dissertation (East Lansing, MI: Michigan State University).
11. Choi, O.-R., and Engel, J.D. (1986). A 3′ enhancer is required for temporal and tissue-specific transcriptional activation of the chicken adult β-globin gene. Nature 323, 731-734.
12. Cooper, J.B., and Long, S.R. (1994). Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6, 215-225.
13. Cox, K.H., and Goldberg, R.B. (1988). Analysis of plant gene expression. In Plant Molecular Biology: A Practical Approach, C.H. Shaw, ed (Oxford, UK: IRL Press), pp. 1-34.
14. Dean, C., Favreau, M., Bond-Nutter, D., Bedbrook, J., and Dunsmuir, P. (1989). Sequences downstream of translation start regulate quantitative expression of two petunia rbcS genes. Plant Cell 1, 201-208.
15. De Block, M., and DeBrouwer, D. (1992). In-situ enzyme histochemistry on plastic embedded plant material: The development of an artifact-free β-glucuronidase assay. Plant J. 2, 261-266.
16. De Block, M., and DeBrouwer, D. (1993). RNA-RNA in-situ hybridization using digoxigenin labeled probes: The use of high molecular weight polyvinylalcohol in the alkaline phosphatase indoxyl-nitroblue-tetrazolium reaction. Anal. Biochem. 215, 86-89.
17. de Bruijn, F.J. (1989). The unusual symbiosis between the diazotrophic stem-nodulating bacterium Azorhizobium caulinodans ORS571 and its host, the tropical legume Sesbania rostrata. In Plant-Microbe Interactions: Molecular and Genetic Perspectives, Vol. 3, T. Kosuge and E. Nester, eds (New York: McGraw Hill), pp. 457-504.
18. de Bruijn, F.J., and Schell, J. (1992). Regulation of plant genes specifically induced in developing and mature nitrogen-fixing nodules: cis-Acting elements and trans-acting factors. In Control of Plant Gene Expression, D.P.S. Verma, ed (Boca Raton, FL: CRC Press), pp. 241-258.
19. de Bruijn, F.J., Szabados, L., and Schell, J. (1990). Chimeric genes and transgenic plants are used to study the regulation of genes involved in symbiotic plant-microbe interactions. Dev. Genet. 11, 182-196.
20. de Bruijn, F.J., Chen, R.C., Fujimoto, S.Y., Pinaev, A., Silver, D., and Szczyglowski, K. (1994). Regulation of nodulin gene expression. Plant Soil 161, 59-68.
21. Dehio, C., and de Bruijn, F.J. (1992). The early nodulin gene SrEnod2 from Sesbania rostrata is inducible by cytokinin. Plant J. 2, 117-128.
22. Depicker, A., Stachel, S., Dhaese, P., Zambryski, P., and Goodman, H.M. (1982). Nopaline synthase: Transcript mapping and DNA sequence. J. Mol. Appl. Genet. 1, 561-573.
23. Dickstein, R.T., Bisseling, T., Reinhold, V.N., and Ausubel, F.M. (1988). Expression of nodule-specific genes in alfalfa root nodules blocked at an early stage of development. Genes Dev. 2, 677-678.
24. Dietrich, R.A., Radke, S.E., and Harada, J.J. (1992). Downstream DNA sequences are required to activate a gene expressed in the root cortex of embryos and seedlings. Plant Cell 4, 1371-1382.
25. Dreyfus, B.L., and Dommergues, Y.R. (1981). Nitrogen-fixing nodules induced by Rhizobium on the stem of the tropical legume Sesbania rostrata. FEMS Microbtol. Lett. 10, 313-317.
26. Ebert, P., Ha, S.B., and An, G. (1987). Identification of an essential upstream element in the nopaline synthase promoter by stable and transient assays. Proc. Natl. Acad. Sci. USA 84, 5745-5749.
27. Finan, T.M., Hirsch, A.M., Leigh, J.A., Johansen, E., Kuldau, G.A., Deegan, S., Walker, G.C., and Signer, E.R. (1985). Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation. Cell 40, 869-877.
28. Fisher, R.F., and Long, S.R. (1992). Rhizobium-plant signal exchange. Nature 357, 655-660.
29. Franck, A., Guilley, H., Jonard, G., Richards, K., and Hirth, L. (1980). Nucleotide sequence of cauliflower mosaic virus DNA. Cell 21, 285-294.
30. Franssen, H.J., Nap, J.-P., Gloudemans, T., Stiekema, W., Van Dam, H., Govers, F., Louwerse, J., Van Kammen, A., and Bisseling, T. (1987). Characterization of cDNA for nodulin-75 of soybean: A gene product involved in early stages of root nodule development. Proc. Natl. Acad. Sci. USA 84, 4495-4499.
31. Fu, H., Kim, S.Y., and Park, W.D. (1995a). High-level tuber expression and sucrose inducibility of a potato Sus4 sucrose synthase gene require 5′ and 3′ flanking sequences and the leader intron. Plant Cell 7, 1387-1394.
32. Fu, H., Kim, S.Y., and Park, W.D. (1995b). A potato Sus3 sucrose synthase gene contains a context-dependent 3′ element and a leader intron with both positive and negative tissue-specific effects. Plant Cell 7, 1395-1403.
33. Gloudemans, T., and Bisseling, T. (1989). Plant gene expression in early stages of Rhizobium-legume symbiosis. Plant Sci. 65, 1-4.
34. Govers, F., Franssen, H.J., Pieterse, C., Wilmer, J., and Bisseling, T. (1990). Function and regulation of the early nodulin gene ENOD2. In Genetic Engineering of Crop Plants, G.W. Lycett and D.W. Grierson, eds (London: Butterworths), pp. 259-269.
35. Hall, T.C., Ma, Y., Buchbinder, B.U., Pyne, J.W., Sun, S.M., and Bliss, F.A. (1978). Messenger RNA for G1 protein of French bean seeds: Cell-free translation and product characterization. Proc. Natl. Acad. Sci. USA 75, 3196-3200.
36. Hirsch, A.M. (1992). Developmental biology of legume nodulation. New Phytol. 122, 211-237.
37. Hirsch, A.M., Bhuvaneswari, T.V., Torrey, J.G., and Bisseling, T. (1989). Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc. Natl. Acad. Sci. USA 86, 1244-1248.
38. Hirsch, A.M., Assad, S., Fang, Y., Wycoff, K., and Loebler, M. (1993). Molecular interactions during nodule development. In New Horizons in Nitrogen Fixation, R. Palacios, J. Moira, and W.E. Newton, eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 291-296.
39. Ingelbrecht, I.L.W., Herman, L.M.F., Dekeyser, R.A., Van Montagu, M.C., and Depicker, A.G. (1989). Different 3′ end regions strongly influence the level of gene expression in plant cells. Plant Cell 1, 671-680.
40. Jefferson, R.A. (1987). Assaying chimeric genes in plants: The GUS gene fusion system. Plant Mol. Biol. Rep. 5, 387-405.
41. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: β-Glucuronidase as sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
42. Kijne, J.W. (1992). The Rhizobium infection process. In Biological Nitrogen Fixation, G. Stacey, R.H. Burris, and H.J. Evans, eds (New York: Chapman and Hall), pp. 349-398.
43. Kunkel, T.A. (1985). Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82, 488-498.
44. Larkin, J.C., Oppenheimer, D.G., Pollock, S., and Marks, M.D. (1993). Arabidopsis GLABROUS1 gene requires downstream sequences for function. Plant Cell 5, 1739-1748.
45. Lauridsen, P., Franssen, H., Stougaard, J., Bisseling, T., and Marker, K.A. (1993). Conserved regulation of the soybean early nodulin ENOD2 gene promoter in determinate and indeterminate transgenic root nodules. Plant J. 3, 483-492.
46. 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 sulfated and acylated glucosamine oligosaccharide signal. Nature 344, 781-784.
47. Libbenga, K.R., Van Iren, F., Bogers, R.J., and Schraag-Lamers, M.F. (1973). The role of hormones and gradients in the initiation of cortex proliferation and nodule formation in Pisum sativum L. Planta 114, 29-39.
48. Long, S.R. (1989). Rhizobium-legume nodulation: Life together in the underground. Cell 56, 203-214.
49. Maniatis, T., Fritsch, E.F., and Sambrook, J. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
50. Mylona, P., Pawlowski, K., and Bisseling, T. (1995). Symbiotic nitrogen fixation. Plant Cell 7, 869-885.
51. Nap, J.-P., and Bisseling, T. (1990). Developmental biology of a plant-prokaryote symbiosis: The legume root nodule. Science 250, 948-954.
52. Ndoye, I., de Billy, F., Vasse, J., Dreyfus, B., and Truchet, G. (1994). Root nodulation of Sesbania rostrata. J. Bacteriol. 176, 1060-1068.
53. Odell, J.T., Nagy, F., and Chua, N.-H. (1985). Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313, 810-812.
54. Owen, D., and Kuhn, L.C. (1987). Noncoding 3′ sequences of the transferrin receptor gene are required for mRNA regulation by iron. EMBO J. 6, 1287-1293.
55. Pankhurst, C.E., Broughton, W.J., and Wieneke, U. (1983). Transfer of an indigenous plasmid of Rhizobium loti to other rhizobia and Agrobacterium tumefaciens. J. Gen. Microbiol. 129, 2535-2543.
56. Pawlowski, K., Klosse, U., and de Bruijn, F.J. (1991). Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism. Mol. Gen. Genet. 231, 124-138.
57. Pietrzak, M., Shillito, R.D., Hohn, T., and Potrykus, I. (1986). Expression in plants of two bacterial antibiotic resistance genes after protoplast transformation with a new plant expression vector. Nucleic Acids Res. 14, 5857-5868.
58. Pingret, J.-L., Journet, E.-P., and Barker, D.G. (1998). Rhizobium Nod factor signaling: Evidence for a G protein-mediated transduction mechanism. Plant Cell 10, 659-672.
59. Ramlov, K.B., Laursen, N.B., Stougaard, J., and Marcker, K.A. (1993). Site-directed mutagenesis of the organ-specific element in the soybean leghemoglobin lbc3 gene promoter. Plant J. 4, 577-580.
60. Sanders, P.R., Winter, J.A., Barnason, A.R., Rogers, S.G., and Fraley, R.T. (1987). Comparison of cauliflower mosaic virus 35S and nopaline synthase promoters in transgenic plants. Nucleic Acids Res. 15, 1543-1558.
61. Silver, D.L. (1996). The Sesbania rostrata Early Nodulin Gene SrEnod2 as a Marker for Cytokinin Signal Transduction. PhD Dissertation (East Lansing, MI: Michigan State University).
62. Silver, D.L., Pinaev, A., Chen, R., and de Bruijn, F.J. (1996). Post-transcriptional regulation of the Sesbania rostrata early nodulin gene SrEnod2 by cytokinin. Plant Physiol. 112, 559-567.
63. Stougaard, J., Sandal, N.N., Gron, A., Kühle, A., and Marcker, K.A. (1987). 5′-Analysis of the soybean leghemoglobin lbc3 gene: Regulatory elements required for promoter activity and organ specificity. EMBO J. 6, 3565-3569.
64. Szabados, L., Ratet, P., Grunenberg, B., and de Bruijn, F.J. (1990). Functional analysis of the Sesbania rostrata leghemoglobin glb3 gene 5′-upstream region in transgenic Lotus corniculatus and Nicotiana tabacum plants. Plant Cell 2, 973-986.
65. Szczyglowski, K., and Legocki, A.B. (1990). Isolation and nucleotide sequence of a cDNA clone encoding nodule-specific (hydroxy) proline-rich protein LEnod2 from yellow lupin. Plant Mol. Biol. 15, 361-363.
66. Szczyglowski, K., Szabados, L., Fujimoto, S.F., Silver, D., and de Bruijn, F.J. (1994). Site-specific mutagenesis of the nodule-infected cell expression (NICE) element and the AT-rich element ATRE-BS2* of the Sesbania rostrata leghemoglobin glb3 promoter. Plant Cell 6, 317-332.
67. Taylor, C.B., Bariola P.A., Del Cardayre, S.B., Raines, R.T., and Green, P.J. (1993). RNS2: A senescence-associated RNase of Arabidopsis that diverged from the S-RNases before speciation. Proc. Natl. Acad. Sci. USA 90, 5118-5122.
68. Tempe, J., and Casse-Delbart, F. (1989). Plant gene vectors and genetic transformation: Agrobacterium Ri plasmids. In Cell Culture and Somatic Cell Genetics of Plants, Vol. 6, J. Schell and I.K. Vasil, eds (San Diego, CA: Academic Press), pp. 25-49.
69. Thimann, K.V. (1936). On the physiology of the formation of nodules on legume roots. Proc. Natl. Acad. Sci. USA 22, 511-515.
70. Thornburg, R.W., An, G., Cleveland, T.E., Johnson, R., and Ryan, C.A. (1987). Wound-inducible expression of a potato inhibitor II-chloramphenicol acetyltransferase gene fusion in transgenic tobacco plants. Proc. Natl. Acad. Sci. USA 84, 744-748.
71. Tjepkema, J.D., and Yocum, C.S. (1974). Measurement of oxygen partial pressure within soybean nodules by oxygen microelectrodes. Planta 119, 351-360.
72. Trainor, C.D., Stamler, S.J., and Engel, J.D. (1987). Erythroid-specific transcription of the chicken histone H5 gene is directed by a 3′ enhancer. Nature 328, 827-830.
73. Truchet, G., Roche, P., Lerouge, P., Vasse, J., Camut, S., de Billy, F., Promé, J.C., and Dénarié, J. (1991). Sulphated lipooligosaccharide signals from Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351, 670-673.
74. 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.
75. Van de Wiel, C., Scheres, B., Franssen, H., Van Lierop, M.J., Van Lammeren, A., Van Kammen, A., and Bisseling, T. (1990a). The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO J. 9, 1-7.
76. Van de Wiel, C., Norris, J.H., Bochenek, B., Dickstein, R., Bisseling, T., and Hirsch, A.M. (1990b). Nodulin gene expression and ENOD2 localization in effective, nitrogen-fixing and ineffective, bacteria-free nodules of alfalfa. Plant Cell 2, 1009-1017.
77. Van Kammen, A. (1984). Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Mol. Biol. Rep. 2, 43-45.
78. Varma, D.P.S. (1992). Signals in root nodule organogenesis and endocytosis of Rhizobium. Plant Cell 4, 373-382.
79. Verma, D.P.S., and Delauney, A.J. (1988). Root nodule symbiosis: Nodulins and nodulin genes. In Temporal and Spatial Regulation of Plant Genes, R.B. Goldberg and D.P.S. Verma, eds (New York: Springer-Verlag), pp. 169-199.
80. Verwoerd, T.C., Dekker, B.M.M., and Hoekema, A. (1989). A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 17, 2362.
81. Vijn, I., das Neves, L., Van Kammen, A., Franssen, H., and Bisseling, T. (1993). Nod factors and nodulation in plants. Science 260, 1764-1765.
82. Weiss, I.M., and Liebhaber, S.A. (1995). Erythroid cell-specific mRNA stability elements in the α2-globin 3′ nontranslated region. Mol. Cell. Biol. 15, 2457-2465.
83. Witty, J.F., Minchin, F.R., Skot, L., and Sheehy, J.E. (1986). Nitrogen fixation and oxygen in legume nodules. Oxford Surv. Plant Mol. Cell Biol. 3, 275-314.
84. 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.