Factors Determining Host Recognition in the Clover-Rhizobium Symbiosis

Djordjevic, M. A.; Weinman, J. J.

doi:10.1071/pp9910543

Cited by 28 publications

(22 citation statements)

References 42 publications

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“…Compounds with these structures are themselves potential nod gene inducers and could be involved in interactions with the nodD gene product. Chalcones especially have been reported to serve as more potent nod gene inducers than other flavonoid molecules (9), and this feature has largely been attributed to their open C-ring system (7), which offers increased spatial flexibility during interactions with NodD proteins (5). Chalcones emerging from an initial C-ring fission in the inducer flavonoid may provide additional conformational flexibility during binding to NodD proteins, thereby increasing transcriptional activation of other nod genes.…”

Section: Discussionmentioning

confidence: 99%

Rhizobia catabolize nod gene-inducing flavonoids via C-ring fission mechanisms

1994

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Gas chromatographic and mass spectrometric analyses of derivatized culture medium extracts were used to identify the products of flavonoid metabolism by rhizobia. A number ofRhizobium species and biovars degraded their nod gene-inducing flavonoids by mechanisms which originated in a cleavage of the C-ring of the molecule and which yielded conserved A-and B-ring products among the metabolites. In contrast, Pseudomonas putida degraded quercetin via an initial fission in its A-ring, and Agrobacterium tumefaciens displayed a nonspecific mode of flavonoid degradation which yielded no conserved A-or B-ring products. When incubated with rhizobia, flavonoids with OH substitutions at the 5 and 7 positions yielded phloroglucinol as the conserved A-ring product, and those with a single OH substitution at the 7 position yielded resorcinol. A wider range of structures was found among the B-ring derivatives, including p-coumaric, p-hydroxybenzoic, protocatechuic, phenylacetic, and caffeic acids. The isoflavonoids genistein and daidzein were also degraded via C-ring fission by Rhizobium fredii and Rhizobium sp. strain NGR234, respectively. Partially characterized aromatic metabolites with potential nod gene-inducing activity were detected among the products of naringenin degradation by Rhizobium leguminosarum bv. viciae. The initial structural modification of nod gene-inducing flavonoids by rhizobia can generate chalcones, whose open C-ring system may have implications for the binding of inducers to the nodD gene product.Flavonoids are polyphenolic secondary metabolites which are synthesized by plants via the expression of two multigeneencoded enzymes: phenylalanine ammonia lyase and chalcone synthase. Subgroups of compounds such as chalcones, flavanones, flavones, flavonols, and isoflavonoids occur in legume tissues, and they can be released (15) from roots into the rhizosphere, where some of them act as molecular signals to trigger the establishment of symbioses with bacteria in the family Rhizobiaceae (18,19). Their principal function is to interact with the nodD gene products of rhizobia and the subsequent transcriptional activation of other nod genes (17). Other effects of flavonoids on rhizobia include promotion of chemotactic responses (1) and stimulation of growth rate by unspecified mechanisms (8).Although rhizobia are known to utilize various aromatic compounds as carbon and/or energy sources by degrading them to catechol and protocatechuate and channelling these products after further enzymatic cleavage into the tricarboxylic acid cycle via the 0-ketoadipate pathway (3, 16), their capacity to degrade flavonoids has received little attention. Only two examples have been reported: the utilization of catechin by a Rhizobium sp. isolated from Leucaena leucocephala, with attendant formation of phloroglucinol carboxylic acid and protocatechuate (6), and a novel form of C-ring cleavage in a pentahydroxy flavone, quercetin, by Rhizobium loti (20). One report (4) has described an alteration in the types and amounts of formon...

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Section: Discussionmentioning

confidence: 99%

Rhizobia catabolize nod gene-inducing flavonoids via C-ring fission mechanisms

1994

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“…Purified BF-7 was dried, resuspended in nitrogen-free (NF) plant growth medium (13) (12,54). Interestingly, several orcinol-positive components in different fractions from the silica column chromatography were shown by TLC to fulfill the criteria specified above.…”

Section: Methodsmentioning

confidence: 99%

“…symbiosis, the bacterial symbiont expresses several nodulation (nod) genes located on its symbiotic plasmid (pSym) (12,27). The action of certain pSym nod genes is correlated with the production of specific molecules capable of acting as signals to elicit various symbiosis-related morphological responses in the plant root, including root hair deformations (Had), induction of foci of cortical cell divisions (Ccd), and a thick, short root (Tsr) (reviewed in references 2, 3, and 16).…”

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confidence: 99%

Flavone-enhanced accumulation and symbiosis-related biological activity of a diglycosyl diacylglycerol membrane glycolipid from Rhizobium leguminosarum biovar trifolii

et al. 1994

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Rhizobium leguminosarum bv. trifolii is the bacterial symbiont which induces nitrogen-fixing root nodules on the leguminous host, white clover (Trifolium repens L.). In this plant-microbe interaction, the host plant excretes a flavone, 4',7-dihydroxyflavone (DHF), which activates expression of nodulation genes, enabling the bacterial symbiont to elicit various symbiosis-related morphological changes in its roots. We have investigated the accumulation of a diglycosyl diacylglycerol (BF-7) in wild-type R. kguminosarum bv. trifolii ANU843 when grown with DHF and the biological activities of this glycolipid bacterial factor on host and nonhost legumes. In vivo labeling stud-ies indicated that wild-type ANU843 cells accumulate BF-7 in response to DHF, and this flavone-enhanced alteration in membrane glycolipid composition was suppressed in isogenic nod4::TnS and nodD::TnS mutant derivatives. Seedling bioassays performed under microbiologically controlled conditions indicated that subnanomolar concentrations of purified BF-7 elicit various symbiosis-related morphological responses on white clover roots, including thick short roots, root hair deformation, and foci of cortical cell divisions. Roots of the nonhost legumes alfalfa and vetch were much less responsive to BF-7 at these low concentrations. A structurally distinct diglycosyl diacylglycerol did not induce these responses on white clover, indicating structural constraints in the biological activity of BF-7 on this legume host. In bioassays using aminoethoxyvinylglycine to suppress plant production of ethylene, BF-7 elicited a meristematic rather than collaroid type of mitogenic response in the root cortex of white clover. These results indicate an involvement of flavone-activated nod expression in membrane accumulation of BF-7 and a potent ability of this diglycosyl diacylglycerol glycolipid to perform as a bacterial factor enabling R. leguminosarum bv. trifolii to activate segments of its host's symbiotic program during early development of the root nodule symbiosis.At early stages in development of the Rhizobium-legume symbiosis, the bacterial symbiont expresses several nodulation (nod) genes located on its symbiotic plasmid (pSym) (12, 27). The action of certain pSym nod genes is correlated with the production of specific molecules capable of acting as signals to elicit various symbiosis-related morphological responses in the plant root, including root hair deformations (Had), induction of foci of cortical cell divisions (Ccd), and a thick, short root (Tsr) (reviewed in references 2, 3, and 16). The functions of Nod proteins are necessary for bacterium-plant signaling that enables rhizobia to successfully infect and nodulate the host legume, leading to establishment of a nitrogen-fixing symbiosis (10, 48).Recent studies have described a family of Rhizobium noddependent chitolipooligosaccharides, first reported by Lerouge et al. (26) Rhizobium lipopolysaccharides, which are released from the bacteria into the external root environment and modulate primary infe...

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“…Previous research on this topic suggests that molecules from the host plant are required for the expression of symbiotic fungal genes (Koske, 1982;Elias and Safir, 1987;Mosse, 1988; Bécard and Piché, 1989b; GianinazziPearson et al, 1989; Bécard and Piché, 1990; Paula and Siquiera, 1990). In particular, the hypothesis that plant phenolics could play a role as signal molecules in plant-AM fungus interactions, as in plant-Rhizobium interactions (Firmin et al, 1986;Kosslak et al, 1987;Rolfe, 1988;Djordjevic and Weinman, 1991;Hartwig and Phillips, 1991;Hungria et al, 1991), has been investigated. The isoflavonoids formononetin and biochanin A, identified in clover roots, have been shown to increase AM infection in white clover Siqueira et al, 1991) and the flavonoids hesperitin, naringenin and apigenin have been reported to stimulate Gigaspora margarita hyphal growth in vitro (Gianinazzi-Pearson et al, 1989), as has the widely occurring flavone quercetin in the presence of CO 2 (Bécard et al, 1992) Knowing that AM infection can increase the accumulation of phytoalexins and associated isoflavonoids in soybean roots (Morandi et al, 1984;Morandi and Gianinazzi-Pearson, 1986;Morandi, 1989) and that these compounds are generally exuded into the rhizosphere (D'Arcy-Lameta, 1984), we tested the effect of 2 soybean isoflavonoids (glyceollin I and coumestrol) and quercetin on in vitro spore germination, hyphal growth and vesicle formation of Gigaspora margarita.…”

Section: Introductionmentioning

confidence: 99%