Interactions Between Genotypes of Soybeans and Genotypes of Nodulating Bacteria<sup>1</sup>

Johnson, H. W.; Means, Ura Mae

doi:10.2134/agronj1960.00021962005200110012x

Cited by 30 publications

(14 citation statements)

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“…However, in some instances, this symbiosis takes on characteristics of a parasitic association and is characterized by foliar chlorosis. This parasitic association occurs between certain combinations of bradyrhizobia and cultivars of soybean and is highly dependent upon the host genotype (8,16). This phenomenon illustrates an interesting situation in which the genotype of the host determines whether the association with the bacteria will be mutualistic or parasitic.…”

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confidence: 99%

Isolation and characterization of rhizobitoxine mutants of Bradyrhizobium japonicum

Ruan

Peters

1992

J Bacteriol

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To explore the role of rhizobitoxine in Bradyrhizobium-legume symbiosis, 11 rhizobitoxine mutants of B. japonicum USDA61 were isolated on the basis of their inability to synthesize the toxin in culture. Each mutant is prototrophic and symbiotically effective on soybean, cowpea, siratro, and Glycine soja. The rhizobitoxine mutants differ in their chlorosis phenotypes and rhizobitoxine production in planta. As expected, one group of mutants fails to make toxin in planta, resulting in the absence of chlorosis. Another group of mutants causes severe chlorosis on all cultivars of soybean tested. Surprisingly, this group of mutants makes more rhizobitoxine in soybean nodules than the wild-type strain does. This phenotype is only observed on soybean and not on other hosts such as cowpea, siratro, or G. soja. The remaining mutants all produce rhizobitoxine in planta but vary in the amount of toxin they produce and the severity of chlorosis they induce in soybean plants. Biochemical analysis of mutants demonstrates that one mutant.is unable to synthesize serinol, a molecule hypothesized to be an intermediate in rhizobitoxine biosynthesis. By using these mutants, it was found that rhizobitoxine plays no apparent role in the nodulation of rjl soybeans. Recently, it was found that inhibition of ethylene biosynthesis allows Rhizobium meliloti to overcome nitrate inhibition of nodule formation on alfalfa. Because rhizobitoxine also inhibits ethylene biosynthesis, we tested the ability of mutants which accumulate high levels of toxin in planta to overcome nitrate inhibition of nodule formation on soybean plants and found that the nodule formation induced by the wild type and that induced by mutant strains were equally suppressed in the presence of nitrate.There are three types of symbiosis: commensalistic, parasitic, and mutualistic. The symbiotic association of Bradyrhizobium species with host legumes is considered to be a mutualistic relationship because both symbionts benefit from the interaction. In this mutualistic symbiosis, the bacteria invade the host root, inducing the formation of a nodule by synthesis of specific lipo-oligosaccharides (22, 38). The bacteria infect specific plant nodule cells where they differentiate into nitrogen-reducing bacteroids. The bacteria provide the plant host with reduced nitrogen, and the plant in turn provides a suitable environment and energy source for reduction of atmospheric nitrogen. However, in some instances, this symbiosis takes on characteristics of a parasitic association and is characterized by foliar chlorosis. This parasitic association occurs between certain combinations of bradyrhizobia and cultivars of soybean and is highly dependent upon the host genotype (8,16). This phenomenon illustrates an interesting situation in which the genotype of the host determines whether the association with the bacteria will be mutualistic or parasitic.The bradyrhizobia that cause foliar chlorosis synthesize the phytotoxin rhizobitoxine (30, 31). Strains which synthesize the toxin are a dis...

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Isolation and characterization of rhizobitoxine mutants of Bradyrhizobium japonicum

Ruan

Peters

1992

J Bacteriol

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“…G. max cv. Lee is a soybean cultivar that is susceptible to chlorosis caused by rhizobitoxine (12). Plants inoculated with USDA94 showed foliar chlorosis on newly forming leaves from 20 days after inoculation, and by 30 days after inoculation these symptoms had worsened (Fig.…”

Section: Resultsmentioning

confidence: 99%

Bradyrhizobium elkanii rtxC Gene Is Required for Expression of Symbiotic Phenotypes in the Final Step of Rhizobitoxine Biosynthesis

Okazaki

Sugawara

Minamisawa

2004

Appl Environ Microbiol

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We disrupted the rtxC gene on the chromosome of Bradyrhizobium elkanii USDA94 by insertion of a nonpolar aph cartridge. The rtxC mutant, designated ⌬rtxC, produced serinol and dihydrorhizobitoxine but no rhizobitoxine, both in culture and in planta. The introduction of cosmids harboring the rtxC gene into the ⌬rtxC mutant complemented rhizobitoxine production, suggesting that rtxC is involved in the final step of rhizobitoxine biosynthesis in B. elkanii USDA94. Glycine max cv. Lee inoculated with ⌬rtxC or with a null mutant, ⌬rtx::⍀1, showed no foliar chlorosis, whereas the wild-type strain USDA94 caused severe foliar chlorosis. The two mutants showed significantly less nodulation competitiveness than the wild-type strain on Macroptilium atropurpureum. These results indicate that dihydrorhizobitoxine, the immediate precursor of the oxidative form of rhizobitoxine, has no distinct effect on nodulation phenotype in these legumes. Thus, desaturation of dihydrorhizobitoxine by rtxC-encoded protein is essential for the bacterium to show rhizobitoxine phenotypes in planta. In addition, complementation analysis of rtxC by cosmids differing in rtxC transcription levels suggested that rhizobitoxine production correlates with the amount of rtxC transcript.Recent studies have suggested that rhizobia adopt at least two strategies to reduce the amount of ethylene synthesized by their host legumes and thus decrease the negative effect of ethylene on nodulation (15). 1-Aminocyclopropane-1-carboxylate (ACC) deaminase, which degrades ACC (an immediate precursor of ethylene) into ammonia and ␣-ketobutyrate, has been found and well characterized in plant growth-promoting rhizobacteria (9, 36). The ACC deaminase of plant growthpromoting rhizobacteria reduces the amount of ACC in associated roots and promotes root elongation via the reduction of ethylene production (8). Genes encoding ACC deaminase have also been found in some rhizobia, including Rhizobium leguminosarum, Mesorhizobium loti, and Bradyrhizobium japonicum (17). In R. leguminosarum bv. viciae, ACC deaminase has been confirmed to enhance nodulation of Pisum sativum (16).Another strategy used by some strains of rhizobia to lower ethylene is the production of rhizobitoxine [2-amino-4-(2-amino-3-hydropropoxy)-trans-but-3-enoic acid] (27). Thus far, Bradyrhizobium elkanii and the plant pathogen Burkholderia andropogonis are known as rhizobitoxine-producing bacteria (18,22). The biochemical action of rhizobitoxine is to inhibit ACC synthase (39) and ␤-cystathionase (31). Rhizobitoxine is regarded as a phytotoxin because it induces chlorosis in a variety of plants (13,25). However, recent studies have shown that it has a positive role in the symbiosis between B. elkanii strains and their host legumes. Enhanced nodulation and competitiveness by rhizobitoxine production in B. elkanii have been reported so far for three legumes: Amphicarpaea edgeworthii (28), Vigna radiata (4), and Macroptilium atropurpureum (41).The biosynthetic genes of rhizobitoxine have been identified for B....

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“…Research by JOHNSON & MEANS (1960) indicated a range of variation in Rhizobium japonicum for the propensity to induce the rhizobitoxine syndrome and a range of variation in the soybean host for susceptibility to expression of rhizobitoxine symptoms . Thirty-four percent of a random sample of 70 strains of Rm japonicum produced chlorotic symptoms on at least one of four test cultivars of soybeans .…”

Section: Discussionmentioning

confidence: 99%

“…Strains 83, 84, 85, and 86, reported by CLARK (1957) and confirmed by our tests as infective on rj1 rj 1 , were tested in Leonard jar culture for their ability to induce rhizobitoxine symptoms on the cultivars `Clark', `Peking', and 'Hawkeye', and an experimental line, N53-3494 . 'Hawkeye' and N53-3494 were reported to be acutely sensitive in the expression of rhizobial-induced chlorosis (JOHNSON & MEANS, 1960) . Strains 76 and 94, known rhizobitoxine producers, and strain 110, never observed to produce rhizobitoxine symptoms in our experience, were included for reference .…”

Section: Experiments IIImentioning

confidence: 99%

Genetic specificity of nodulation

Devine

Weber

1977

Euphytica

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Interactions Between Genotypes of Soybeans and Genotypes of Nodulating Bacteria¹

Cited by 30 publications

References 4 publications

Isolation and characterization of rhizobitoxine mutants of Bradyrhizobium japonicum

Isolation and characterization of rhizobitoxine mutants of Bradyrhizobium japonicum

Bradyrhizobium elkanii rtxC Gene Is Required for Expression of Symbiotic Phenotypes in the Final Step of Rhizobitoxine Biosynthesis

Genetic specificity of nodulation

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Interactions Between Genotypes of Soybeans and Genotypes of Nodulating Bacteria1

Cited by 30 publications

References 4 publications

Isolation and characterization of rhizobitoxine mutants of Bradyrhizobium japonicum

Isolation and characterization of rhizobitoxine mutants of Bradyrhizobium japonicum

Bradyrhizobium elkanii rtxC Gene Is Required for Expression of Symbiotic Phenotypes in the Final Step of Rhizobitoxine Biosynthesis

Genetic specificity of nodulation

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Interactions Between Genotypes of Soybeans and Genotypes of Nodulating Bacteria¹