Rhizobium nodulation gene nodD as a determinant of host specificity

Spaink, Herman P.; Wijffelman, C. A.; Pees, E.; Okker, R. J. H.; Lugtenberg, Ben

doi:10.1038/328337a0

Cited by 240 publications

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“…Results in Tables 1 and 2 extend the models by indicating that different NodD proteins in a single species probably have varying specificities for active flavonoids. This observation parallels NodD protein specificities shown previously with flavonoids from various host plants for NodD proteins from different species of rhizobia (27). In addition, a previously unpredicted possibility that luteolin binds with the NodD2 protein to form a complex incapable of inducing nod genes is suggested by the compet.…”

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Effects of alfalfa nod gene-inducing flavonoids on nodABC transcription in Rhizobium meliloti strains containing different nodD genes

et al. 1990

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Transcription of the nodulation genes nodABC in Rhizobium meliloti requires a plant flavonoid signal and nodD, a family of bacterial regulatory genes (nodDl, nodD2, and nodD3). Results from this study show that all previously identified nod gene inducers released by alfalfa seeds and roots induced nodABC-IacZ transcription in R. meliloti containing extra copies of nodDI, but only 4,4'-dihydroxy-2'-methoxychalcone gave high levels of induction with extra copies of nodD2. While mixtures of the methoxychalcone and luteolin showed a positive synergism with extra NodDl protein, they apparently competed for binding to the NodD2 protein.Rhizobium meliloti infect alfalfa (Medicago sativa L.) plants and induce the formation of root nodules that reduce N2 to ammonia. Several sets of bacterial genes are involved in the early stages of nodule formation. One well-described transcriptional unit, the nodABC genes, initiates cortical cell division (2, 26), root hair deformation (15), and production of a receptorlike protein (12,13). The nodABC genes in R. meliloti are expressed primarily in the presence of particular flavonoids exuded by alfalfa seeds or roots (7, 18, 21,23).Precisely how plant flavonoids induce transcription of nod genes in R. meliloti is not known, but a family of regulatory genes including nodDI, nodD2, and nodD3 is involved (4,5,9,22,25). Studies of the nodDi gene product (NodDl), nod gene-inducing flavonoids, and the promoter region of nod-ABC suggest that NodDl is a DNA-binding protein (3,8,16). Tests with crude seed exudates from different plant species nodulated by R. meliloti indicate that species-specific factors interact with different NodD proteins (5). In those tests, alfalfa seed exudate produced high levels of nod gene induction in the presence of nodDi, nodD2, and nodD3, but it could not be determined whether the same or separate (presumably flavonoid) factors functioned through different nodD genes.A series of flavonoids has now been identified as natural alfalfa nod gene inducers in R. meliloti 1021(pRmM57), which contains a cloned fragment with a nodDIABC-lacZ fusion (21). Luteolin (3',4',5,7-tetrahydroxyflavone; Fig. 1), which was first isolated from alfalfa seeds (23), was not found in root exudates of Moapa 69 alfalfa seedlings (18). However, the root exudates did contain three other nod gene inducers: 4,4'-dihydroxy-2'-methoxychalcone, 4',7-dihydroxyflavone, and 4',7-dihydroxyflavanone ( Fig. 1) (18). Seed rinses from the same alfalfa cultivar contained luteolin and chrysoeriol (3'-methoxyluteolin; Fig. 1) (7). The biological significance of this diversity of nod gene inducers is not clear, but at least three points are noteworthy. First, although luteolin probably is the most prevalent nod gene inducer in the soil around a germinating alfalfa seed (7), the methoxychalcone and chrysoeriol induce half-maximum transcriptional rates of nodABC-lacZ fusion at 10 and 25%, respectively, of the concentration required for luteolin (7, 18). Second, the 4',7 substitution pattern (flavone numberin...

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confidence: 59%

Effects of alfalfa nod gene-inducing flavonoids on nodABC transcription in Rhizobium meliloti strains containing different nodD genes

et al. 1990

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“…The NodD protein, which is required for activation of the other, inducible nod genes, is only active together with signal molecules, identified as flavonoids, which are exuded by the host plant roots (9,22,25,46). The NodD protein shows a certain flavonoid specificity, which restricts nod gene induction to plants that secrete flavonoids able to activate with the NodD protein (36). Besides the constitutive nodD promoter, four inducible nod promoters have been found in R. leguminosarum bv.…”

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A biovar-specific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene-inducing activity in root exudate of Vicia sativa subsp. nigra

et al. 1990

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Flavonoids in root exudate of leguminous plants activate the transcription of Rhizobium genes involved in the formation of root nodules (nod genes). We report that inoculation with the homologous symbiont R. kguminosarum bv. viciae results in an increased nod gene-inducing activity (Ini) in root exudate of V. sativa subsp. nigra, whereas inoculation with heterologous Rhizobium strains results in exudates with nod geneinducing activity comparable to that of uninfected plants. Ini can be demonstrated by using either of the isogenic indicator strains containing an inducible nod promoter fused to the Escherichia coli lacZ reporter gene and the regulatory nodD gene of R. leguminosarum bv. viciae, R. leguminosarum bv. trifolii, or R. meliloti. The presence of genes nodDABCEL of R. leguminosarum bv. viciae appeared to be essential for induction of Ini. Mutation of the genes nodI and nodJ causes a delay of Ini, whereas gene nodF appears to be required for both the timely appearance and the maximum level of Ini activity. The nodE gene is responsible for the biovar specificity of induction of Ini by Rhizobium spp. Ini is caused by a soluble heat-stable factor of rhizobial origin. This Rhizobium-produced Ini factor has an apparent molecular weight between 1,000 and 10,000 and does not originate from flavonoid precursors.Induction by Rhizobium bacteria of symbiotic nitrogenfixing root nodules on leguminous plants is a host-specific process; e.g., R. leguminosarum bv. viciae nodulates common vetch, pea, sweet pea, and lentil but not clover or bean, whereas R. leguminosarum bv. trifolii nodulates only clover. Many genes required for root nodule formation (nod genes) by Rhizobium species, including those of R. leguminosarum, are located on a symbiosis (Sym) plasmid. In R. leguminosarum three types of nod genes have been distinguished: (i) a regulatory gene, nodD; (ii) the common nod genes, nodAB-CIJ; and (iii) the genes nodFELMNTO, of which the nodE gene is a host-specific gene which determines whether R. leguminosarum is able to nodulate Vicia or Trifolium plants (3-5, 14, 19, 27, 33). The NodD protein, which is required for activation of the other, inducible nod genes, is only active together with signal molecules, identified as flavonoids, which are exuded by the host plant roots (9,22,25,46 (22,25,46). However, in nature root exudate is not sterile, and we therefore extended our studies to exudate of plants that had been inoculated with Rhizobium spp. (coculture exudate). In this paper, we report that inoculation of Vicia sativa subsp. nigra plants with R. leguminosarum bv. viciae results in significantly increased nod gene-inducing activity (Ini) in coculture exudate. We show that this effect is induced by a biovar-specific extracellular signal of R. leguminosarum bv. viciae. The production of this signal, which is not a flavonoid, requires induction of specific nod genes. MATERIALS AND METHODSBacterial strains, plasmids, and growth conditions. Rhizobium strains and plasmids used in this study are listed in Table 1. Plas...

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“…Rhizobia sense flavonoids secreted by seeds and by the host plant root, which activate the constitutively expressed nodD gene product (reviewed by Schlaman et al, 1992). This step is a determinant of host plant specificity in some Rhizobium-host plant combinations (Horvath et al, 1987; Spaink et al, 1987). Transcription of structural nod genes is under the control of NodD and results in production and secretion of specific lipochitin oligosaccharides (Nod factors), which act as host plant-specific inducers of nodule morphogenesis (reviewed by Dénarié and Cullimore, 1993;Spaink et al, 1993).…”

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Sugar-Binding Activity of Pea Lectin Expressed in White Clover Hairy Roots

et al. 1995

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Dénarié et al., 1992). Nodulation is regulated by a two-way exchange of plant and bacterial signal molecules (Fisher and Long, 1992;Spaink et al., 1993). Signal exchange begins in the rhizosphere. Rhizobia sense flavonoids secreted by seeds and by the host plant root, which activate the constitutively expressed nodD gene product (reviewed by Schlaman et al., 1992). This step is a determinant of host plant specificity in some Rhizobium-host plant combinations (Horvath et al., 1987; Spaink et al., 1987). Transcription of structural nod genes is under the control of NodD and results in production and secretion of specific lipochitin oligosaccharides (Nod factors), which act as host plant-specific inducers of nodule morphogenesis (reviewed by Dénarié and Cullimore, 1993;Spaink et al., 1993). Most probably, Nod factors constitute the primary determinants of host-plant specificity of nodulation.Root lectins are plant factors involved in nodulation. Lectins are nonenzymatic sugar-binding (g1yco)proteins characterized by sugar-binding specificity. For example, root PSL is Glc/Man specific (Díaz et al., 1990) and white clover root lectin is 2-deoxyglucose specific (Sherwood et al., 1984). In general, the interaction between RI uiciae and white clover does not proceed beyond root hair curling, and these bacteria are not able to penetrate host plant cells by infection thread formation (Yao and Vincent, 1969;Djordjevic et al., 1986;Huang et al., 1993). However, RI viciae is able to induce infection thread formation and nodulation in a significant percentage of white clover plants with roots transformed with the psl gene, as reported by Díaz et al. (1989Díaz et al. ( , 1995. This heterologous nodulation does not take place when a psl mutant, which encodes a non-sugar-binding protein, is used for transformation of white clover roots (Van Eijsden et al., 1992. These results strongly suggest that (a) PSL is functionally expressed in transgenic white clover roots, (b) conservation of the sugar-binding activity of PSL is necessary for infection of white clover by RI viciae, and (c) root lectin helps to break a host plant-specific barrier for nodulation. The relationship between Nod factor recognition by host plants and Rhizobium recognition by host lectin is not yet clear.PSL is an ellipsoidal, nonglycosylated dimeric lectin with two sugar-binding sites, each located near the top of two identical monomers (Einspahr et al., 1988). PSL is encoded by a single gene (Gatehouse et al., 1987;Kaminski et al., 1987) and is synthesized as a single translation product, a prolectin with a molecular mass of 28 kD. Posttranslational modifications result in a protein that dissociates into two p subunits (18 kD each) and two 01 subunits (6 kD each, Higgins et al., 1983)

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Rhizobium nodulation gene nodD as a determinant of host specificity

Cited by 240 publications

References 0 publications

Effects of alfalfa nod gene-inducing flavonoids on nodABC transcription in Rhizobium meliloti strains containing different nodD genes

Effects of alfalfa nod gene-inducing flavonoids on nodABC transcription in Rhizobium meliloti strains containing different nodD genes

A biovar-specific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene-inducing activity in root exudate of Vicia sativa subsp. nigra

Sugar-Binding Activity of Pea Lectin Expressed in White Clover Hairy Roots

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