Abstract
At the base of adventitious root primordia, located on the stem of the tropical legume Sesbania rostrata, nitrogen-fixing nodules are formed upon inoculation with the microsymbiont Azorhizobium caulinodans. This pattern of nodule development presents features of indeterminate and determinate nodules in early and later stages, respectively. A S. rostrata cDNA clone homologous to early nodulin ENOD40 genes was isolated from a cDNA library of developing stem nodules. SrENOD40-1 contained the conserved regions I and II of other ENOD40 genes. By reverse transcriptase PCR, enhanced SrENOD40-1 expression was observed in the adventitious root primordia between 4 and 8 h after inoculation with A. caulinodans. In situ hybridization showed that SrENOD40-1 transcripts, present around the central vascular bundle of the uninfected root primordia, were strongly enhanced upon induction of nodule development. De novo SrENOD40-1 expression was observed in the initiating and growing nodule primordia and around vascular bundles. When cell type specification sets in, the expression became pronounced in cells derived from the meristematic regions. In other parts of the plant, weak SrENOD40-1 expression was associated with vascular bundles and was observed in leaf and stipule primordia.
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References
Asad S, Fang Y, Wycoff KL, Hirsch AM: Isolation and characterization of cDNA and genomic clones of MsENOD40; transcripts are detected in meristematic cells of alfalfa. Protoplasma 183: 10–23 (1994).
Charon C, Johansson C, Kondorosi E, Kondorosi A, Crespi M: enod40 induces dedifferentiation and division of root cortical cells in legumes. Proc Natl Acad Sci USA 94: 8901–8906 (1997).
Cox K, DeLeon DV, Angerer LM, Angerer RC: Detection of mRNAs in sea urchin embryos by in situ hybridization using asymmetric RNA probes. Devel Biol 101: 485–502 (1984).
Crespi M, Jurkevitch E, Poiret M, d'Aubenton-Carafa Y, Petrovics G, Kondorosi E, Kondorosi A: enod40, a gene expressed during nodule organogenesis, codes for a nontranslatable RNA involved in plant growth. EMBO J 13: 5099–5112 (1994).
Crespi M, Charon C, Johansson C, Frugier F, Coba T, Bauer P, Fehér A, Lodeiro A, Poirier S, Brown S, Ratet P, Staehelin C, Trinh TH, Schultze M, Kondorosi E, Felle HH, Kondorosi A: Control of nodule organogenesis in Medicago. In: Stacey G, Mullin B, Gresshoff PM (eds), Biology of Plant-Microbe Interactions, pp. 363–368. International Society for Molecular Plant-Microbe Interactions, St. Paul, MN (1996).
Dreyfus B, Garcia JL, Gillis M: Characterization of Azorhizobium caulinodans gen. nov, sp. nov, a stem-nodulating nitrogen-fixing bacterium isolated from Sesbania rostrata. Int J Syst Bacteriol 38: 89–98 (1988).
Duhoux E: Ontogénèse des nodules caulinaires du Sesbania rostrata (légumineuses). Can J Bot 62: 982–994 (1984).
Goethals K, Gao M, Tomekpe K, VanMontagu M, Holsters M: Common nodABC genes in Nod locus 1 of Azorhizobium caulinodans: nucleotide sequence and plant-inducible expression. Mol Gen Genet 219: 289–298 (1989).
Goethals K, Leyman B, Van den Eede G, Van Montagu M, Holsters M: An Azorhizobium caulinodans ORS571 locus involved in lipopolysaccharide production and nodule formation on Sesbania rostrata stems and roots. J Bacteriol 176: 92–99 (1994).
Goormachtig S, Valerio-Lepiniec M, Szczyglowski K, Van Montagu M, Holsters M, de Bruijn FJ: Use of differential display to identify novel Sesbania rostrata genes enhanced by Azorhizobium caulinodans infection. Mol Plant-Microbe Interact 8: 816–824 (1995).
Goormachtig S, Alves-Ferreira M, Van Montagu M, Engler G, Holsters M: Expression of cell cycle genes during Sesbania rostrata stem nodule development. Mol Plant-Microbe Interact 10: 316–325 (1997).
Kouchi H, Hata S: Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238: 106–119 (1993).
Long SR: Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8: 1885–1898 (1996).
Matvienko M, van de Sande K, Yang WC, van Kammen A, Bisseling T, Franssen H: Comparison of soybean and pea ENOD40 cDNA clones representing genes expressed during both early and late stages of nodule development. Plant Mol Biol 26: 487–493 (1994).
Matvienko M, van de Sande K, Pawlowski K, van Kammen A, Franssen H, Bisseling T: Nicotiana tabacum SR1 contains two ENOD40 homologs. In: Stacey G, Mullin B, Gresshoff PM (eds) Biology of Plant-Microbe Interactions, pp. 387–391. International Society for Molecular Plant-Microbe Interactions, St. Paul, MN (1996).
Mergaert P, Van Montagu M, Promé JC, Holsters M: 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 (1993).
Minami E, Kouchi H, Cohn JR, Ogawa T, Stacey G: Expression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules. Plant J 10: 23–32 (1996).
Mylona P, Pawlowski K, Bisseling T: Symbiotic nitrogen fixation. Plant Cell 7: 869-885 (1995).
Papadopoulou K, Roussis A, Katinakis P: Phaseolus ENOD40 is involved in symbiotic and non-symbiotic organogenetic processes: expression during nodule and lateral root development. Plant Mol Biol 30: 403–417 (1996).
Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Sanger F, Nicklen S, Coulson, AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).
Spencer-Barreto MM, Cottignies A, Chamel A, Duhoux E: Caractéristiques physiologiques des ébauches racinaires adventives de la tige de Sesbania rostrata Brem (Leguminosae). Acta Bot Gall 142: 763–771 (1995).
Tsien HC, Dreyfus BL, Schmidt EL: Initial stages in the morphogenesis of nitrogen-fixing stem nodules of Sesbania rostrata. J Bacteriol 156: 888–897 (1983).
van de Sande K, Pawlowski K, Czaja I, Wieneke U, Schell J, Schmidt J, Walden R, Matvienko M, Wellink J, van Kammen A, Franssen H, Bisseling T: Modification of phytohormone response by a peptide encoded by ENOD40 of legumes and a nonlegume. Science 273: 370–373 (1996).
van Rhijn P, Fang Y, Galili S, Shaul O, Atzmon N, Wininger S, Eshed Y, Lum M, Li Y, To V, Fujishige N, Kapulnik Y, Hirsch AM: Expression of early nodulin genes in alfalfa mycorrhizae indicates that signal transduction pathways used in forming arbuscular mycorrhizae and Rhizobium-induced nodules may be conserved. Proc Natl Acad Sci USA 94: 5467–5472 (1997).
Vijn I, Martinez-Abarca F, Yang W-C, das Neves L, van Brussel A, van Kammen A, Bisseling T: Early nodulin gene expression during Nod factorinduced processes in Vicia sativa. Plant J 8: 111–119 (1995).
Vijn I, Yang W-C, Pallisgård N, Jensen EØ, van Kammen A, Bisseling T: VsENOD5, VsENOD12 and VsENOD40 expressing during Rhizobium-induced nodule formation on Vicia sativa roots. Plant Mol Biol 28: 1111–1119 (1995).
Watts FZ, Moore AL: Nucleotide sequence of a full length cDNA clone encoding a polyubiquitin gene from Pisum sativum. Nucl Acids Res 17: 10100 (1989).
Yang W-C, Katinakis P, Hendriks P, Smolders A, de Vries F, Spee J, van Kammen A, Bisseling T, Franssen H: Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant J 3: 573–585 (1993).
Yang WC, van de Sande K, Pawlowski K, Schmidt J, Walden R, Matvienko M, Franssen H, Bisseling T: ENOD40 expression precedes cell division and affects phytohormone perception at the onset of nodulation. In: Legocki A, Bothe H, Pühler A (eds) Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture (NATO ASI Series, Vol G39), pp. 51–53. Springer Verlag, Berlin (1997).
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Corich, V., Goormachtig, S., Lievens, S. et al. Patterns of ENOD40 gene expression in stem-borne nodules of Sesbania rostrata . Plant Mol Biol 37, 67–76 (1998). https://doi.org/10.1023/A:1005925607793
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DOI: https://doi.org/10.1023/A:1005925607793