Release of Flavonoids by the Soybean Cultivars McCall and Peking and Their Perception as Signals by the Nitrogen-Fixing Symbiont<i>Sinorhizobium fredii</i>1

Pueppke, Steven G.; Bolaños-Vásquez, Maria Cristina; Werner, Dietrich; Bec-Ferté, Marie Pierre; Promé, J. C.; Krishnan, Hari B.

doi:10.1104/pp.117.2.599

Cited by 66 publications

(42 citation statements)

References 53 publications

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“…Consequently, this mutant, unlike the wild-type strain, was able to nodulate agronomically improved soybean cultivars, suggesting an important role for the Nops in regulating soybean cultivar specificity (27,30). To determine if the mutation in the gcv operon of USDA257 has any effect on Nops, we isolated extracellular proteins from USDA257 and the gcv mutant that were grown in either the presence or absence of apigenin, a potent inducer of the nod genes of USDA257 (21,37). SDS-PAGE analysis followed by silver staining of the gels revealed no major (Fig.…”

Section: Resultsmentioning

confidence: 99%

Disruption of the Glycine Cleavage System Enables Sinorhizobium fredii USDA257 To Form Nitrogen-Fixing Nodules on Agronomically Improved North American Soybean Cultivars

Lorio

Kim

Krishnan

et al. 2010

Appl Environ Microbiol

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The symbiosis between Sinorhizobium fredii USDA257 and soybean [Glycine max (L.) Merr.] exhibits a high degree of cultivar specificity. USDA257 nodulates primitive soybean cultivars but fails to nodulate agronomically improved cultivars such as McCall. In this study we provide evidence for the involvement of a new genetic locus that controls soybean cultivar specificity. This locus was identified in USDA257 by Tn5 transposon mutagenesis followed by nodulation screening on McCall soybean. We have cloned the region corresponding to the site of Tn5 insertion and found that it lies within a 1.5-kb EcoRI fragment. DNA sequence analysis of this fragment and an adjacent 4.4-kb region identified an operon made up of three open reading frames encoding proteins of deduced molecular masses of 41, 13, and 104 kDa, respectively. These proteins revealed significant amino acid homology to glycine cleavage (gcv) system T, H, and P proteins of Escherichia coli and other organisms. Southern blot analysis revealed the presence of similar sequences in diverse rhizobia. Measurement of ␤-galactosidase activity of a USDA257 strain containing a transcriptional fusion of gcvT promoter sequences to the lacZ gene revealed that the USDA257 gcvTHP operon was inducible by glycine. Inactivation of either gcvT or gcvP of USDA257 enabled the mutant to nodulate several agronomically improved North American soybean cultivars. These nodules revealed anatomical features typical of determinate nodules, with numerous bacteroids within the infected cells. Unlike for the previously characterized soybean cultivar specificity locus nolBTUVW, inactivation of the gcv locus had no discernible effect on the secretion of nodulation outer proteins of USDA257.Sinorhizobium fredii USDA257 is a fast-growing rhizobium that forms nitrogen-fixing nodules on Glycine max, Glycine soja, Neonotonia wightii, Phaseolus vulgaris, and several other legumes (24, 36). The symbiotic relationship between S. fredii USDA257 (here called USDA257) and soybean is of particular scientific and economic interest because this bacterium nodulates soybean in a cultivar-specific manner (13,19). USDA257 effectively nodulates the primitive soybean cultivar Beijing but fails to nodulate agronomically improved cultivars such as McCall (2, 13). Histological studies have shown that USDA257 is able to infect McCall root hairs and induce cortical cell divisions but fails to form infection threads (5).Previously, we have demonstrated the presence of negatively acting nodulation genes by creating Tn5 mutants (14). In one of the mutants (DH4) the Tn5 insertion was located in sym plasmid, while in the second mutant (DH5), the mutation was located in the bacterial chromosome. In DH4, the Tn5 insertion was located in an 8.0-kb EcoRI fragment which harbors the nolXWBTUV locus (34). Disruption of any these genes expands the host range of S. fredii USDA257. Subsequent studies have demonstrated that this locus is part of a USDA257 type III secretion system (T3SS) (27,34). Both DH4 and DH5 were able to form ...

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Section: Resultsmentioning

confidence: 99%

Disruption of the Glycine Cleavage System Enables Sinorhizobium fredii USDA257 To Form Nitrogen-Fixing Nodules on Agronomically Improved North American Soybean Cultivars

Lorio

Kim

Krishnan

et al. 2010

Appl Environ Microbiol

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“…The results, shown in Table 3, indicate that the best flavonoid inducers for ttsI were coumestrol, genistein and daidzein (all released by roots of soybeans McCall and Peking; Pueppke et al, 1998), apigenin and morin. Coumestrol was the most potent inducer among these five flavonoids.…”

Section: Regulation Of Ttsi By Flavonoids and Phmentioning

confidence: 99%

Regulation and symbiotic significance of nodulation outer proteins secretion in Sinorhizobium fredii HH103

et al. 2008

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In this work we show that the Sinorhizobium fredii HH103 ttsI gene is essential for the expression of the tts genes and secretion of nodulation outer proteins (Nops). Moreover, we demonstrate for the first time, to our knowledge, that the nod box preceding ttsI is necessary for Nops secretion. TtsI is responsible for the transcriptional activation of nopX, nopA, rhcJ and rhcQ. We confirm that the S. fredii HH103 ttsI gene is activated by NodD1 and repressed by NolR. In contrast, NodD2 is not involved in the regulation of ttsI expression. Despite the dependence of expression of both ttsI and nodA on NodD1 and flavonoids, clear differences in the capacity of some flavonoids to activate these genes were found. The expression of the ttsI and nodA genes was also sensitive to differences in the pH of the media. Secretion of Nops in the ttsI mutant could not be complemented with a DNA fragment containing the ttsI gene and its nod box, but it was restored when a plasmid harbouring the ttsI, rhcC2 and y4xK genes was transferred to the mutant strain. The symbiotic effect of Nops secretion was host-dependent but independent of the type of nodule formed by the host legume. Nops are beneficial in the symbiosis with Glycine max and Glycyrrhiza uralensis, and detrimental in the case of the tropical legume Erythrina variegata.

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“…Interestingly, R. etli strains belonging to each of the lineages are able to nodulate beans from the different centers of diversity and domestication, arguing against a situation of restricted nodulation such as is found with certain soybeans, peas, and beans. For instance, Sinorhizobium fredii strain USDA191 forms nodules on the soybean cultivars McCall and Peking, but S. fredii strain USDA257 nodulates only cultivar Peking (32). The Afghanistan pea cultivar is resistant to nodulation by European R. leguminosarum strains but is efficiently nodulated by strains isolated from Israel (29).…”

Section: Distribution Of Prevalence Among Wild and Cultivated Common mentioning

confidence: 99%

Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification

Aguilar

Riva

Peltzer

2004

Proc. Natl. Acad. Sci. U.S.A.

135

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Common beans (Phaseolus vulgaris) comprise three major geographic genetic pools, one in Mexico, Central America, and Colombia, another in the southern Andes, and a third in Ecuador and northern Peru. Species Rhizobium etli is the predominant rhizobia found symbiotically associated with beans in the Americas. We have found polymorphism in the common nodulation gene nodC among R. etli strains from a wide range of geographical origins, which disclosed three nodC types. The different nodC alleles in American strains show varying predominance in their regional distributions in correlation with the centers of bean genetic diversification (BD centers). By cross-inoculating wild common beans from the three BD centers with soils from Mexico, Ecuador, Bolivia, and Northwestern Argentina, the R. etli populations from nodules originated from Mexican soil again showed allele predominance that was opposite to those originated from Bolivian and Argentinean soil, whereas populations from Ecuadorian soil were intermediate. These results also indicated that the preferential nodulation of beans by geographically related R. etli lineages was independent of the nodulating environment. Coinoculation of wild common beans from each of the three BD centers with an equicellular mixture of R. etli strains representative of the Mesoamerican and southern Andean lineages revealed a host-dependent distinct competitiveness: beans from the Mesoamerican genetic pool were almost exclusively nodulated by strains from their host region, whereas nodules of beans from the southern Andes were largely occupied by the geographically cognate R. etli lineages. These results suggest coevolution in the centers of host genetic diversification.Phaseolus vulgaris-rhizobia coevolution ͉ Rhizobium etli lineages ͉ symbiotic interaction ͉ nodC gene

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Release of Flavonoids by the Soybean Cultivars McCall and Peking and Their Perception as Signals by the Nitrogen-Fixing SymbiontSinorhizobium fredii1

Cited by 66 publications

References 53 publications

Disruption of the Glycine Cleavage System Enables Sinorhizobium fredii USDA257 To Form Nitrogen-Fixing Nodules on Agronomically Improved North American Soybean Cultivars

Disruption of the Glycine Cleavage System Enables Sinorhizobium fredii USDA257 To Form Nitrogen-Fixing Nodules on Agronomically Improved North American Soybean Cultivars

Regulation and symbiotic significance of nodulation outer proteins secretion in Sinorhizobium fredii HH103

Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification

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