Journal articles: 'Rhizobium leguminosarum Molecular aspects'

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Chalifour, François-P., and Nicole Benhamou. "Indirect evidence for cellulase production by Rhizobium in pea root nodules during bacteroid differentiation: cytochemical aspects of cellulose breakdown in rhizobial droplets." Canadian Journal of Microbiology 35, no. 9 (September 1, 1989): 821–29. http://dx.doi.org/10.1139/m89-138.

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Cytochemical localization of cellulosic β-(1–4) glucans in pea (Pisum sativum L.) nodules at different stages of infection by an effective isolate of Rhizobium leguminosarum biovar viceae was studied using a gold-complexed exoglucanase. Cellulose subunits were present in great amounts in root cell walls, as shown by intense and regular labeling by gold particles. Labeling was unevenly distributed over the thin walls of emerging infection threads. In more developed infection threads, labeling was more intense and evenly distributed than in emerging threads, although slightly altered, unlabeled wall areas were frequently observed at the growing tips. Droplets containing rhizobia, which originated from infection threads, were surrounded by labeled wall-like material. Rhizobial droplets were either single- or multi-celled, and were sometimes separated by inner, unevenly labeled compartments. The surrounding wall-like material was irregularly labeled, and unlabeled wall areas, neighbouring intensely labeled ones, were observed frequently. There was an absence of labeling ahead of the rhizobia that escaped from the droplets, but degenerating wall-like material was present around the escaping rhizobia, mainly on their sides. At more advanced stages of development, labeling was present only over the outermost wall layers of rhizobial droplets, indicating that inner portions were degraded first. These observations suggest that a hydrolytic enzyme is involved in the sequence of events from infection thread formation through rhizobial release in the host cell cytoplasm, and that the hydrolytic enzyme is of rhizobial origin.Key words: Rhizobium–Pisum symbiosis, root nodules, rhizobial droplets, cellulose, colloidal gold.

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Russo, Daniela M., Alan Williams, Anne Edwards, Diana M. Posadas, Christine Finnie, Marcelo Dankert, J. Allan Downie, and Angeles Zorreguieta. "Proteins Exported via the PrsD-PrsE Type I Secretion System and the Acidic Exopolysaccharide Are Involved in Biofilm Formation by Rhizobium leguminosarum." Journal of Bacteriology 188, no. 12 (June 15, 2006): 4474–86. http://dx.doi.org/10.1128/jb.00246-06.

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ABSTRACT The type I protein secretion system of Rhizobium leguminosarum bv. viciae encoded by the prsD and prsE genes is responsible for secretion of the exopolysaccharide (EPS)-glycanases PlyA and PlyB. The formation of a ring of biofilm on the surface of the glass in shaken cultures by both the prsD and prsE secretion mutants was greatly affected. Confocal laser scanning microscopy analysis of green-fluorescent-protein-labeled bacteria showed that during growth in minimal medium, R. leguminosarum wild type developed microcolonies, which progress to a characteristic three-dimensional biofilm structure. However, the prsD and prsE secretion mutants were able to form only an immature biofilm structure. A mutant disrupted in the EPS-glycanase plyB gene showed altered timing of biofilm formation, and its structure was atypical. A mutation in an essential gene for EPS synthesis (pssA) or deletion of several other pss genes involved in EPS synthesis completely abolished the ability of R. leguminosarum to develop a biofilm. Extracellular complementation studies of mixed bacterial cultures confirmed the role of the EPS and the modulation of the biofilm structure by the PrsD-PrsE secreted proteins. Protein analysis identified several additional proteins secreted by the PrsD-PrsE secretion system, and N-terminal sequencing revealed peptides homologous to the N termini of proteins from the Rap family (Rhizobium adhering proteins), which could have roles in cellular adhesion in R. leguminosarum. We propose a model for R. leguminosarum in which synthesis of the EPS leads the formation of a biofilm and several PrsD-PrsE secreted proteins are involved in different aspects of biofilm maturation, such as modulation of the EPS length or mediating attachment between bacteria.

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Figueira, Etelvina Maria de Almeida Paula, Ana Isabel Gusmão Lima, and Sofia Isabel Almeida Pereira. "Cadmium tolerance plasticity in Rhizobium leguminosarum bv. viciae: glutathione as a detoxifying agent." Canadian Journal of Microbiology 51, no. 1 (January 1, 2005): 7–14. http://dx.doi.org/10.1139/w04-101.

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Rhizobium leguminosarum bv. viciae strains expressing different degrees of tolerance to metal stress were used in this work to study the basic mechanisms underlying heavy metal tolerance. We used various parameters to evaluate this response. The strains' growth responses under different Cd2+ concentrations were determined and we reported variation in Cd2+ tolerance. Total soluble protein content decreased drastically, revealing the toxic effects that intracellular Cd2+ imposes on cellular metabolism, but this decrease in protein content was particularly evident in sensitive and moderately tolerant strains. Tolerant strains presented the highest intracellular and wall-bound Cd2+ concentrations. Cd2+ induced increases in the expression of some specific proteins, which were identical in all tolerant strains. Glutathione levels remained unaltered in the sensitive strain and increased significantly in tolerant and moderately tolerant strains, suggesting the importance of glutathione in coping with metal stress. This work suggests that efflux mechanisms may not be the only system responsible for dealing with heavy metal tolerance. A clear correlation between glutathione levels and Cd2+ tolerance is reported, thus adding a novel aspect in bacteria protection against heavy metal deleterious effects.Key words: glutathione, heavy metal, protein expression, rhizobia, thiol quantification.

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Shahzad, Farood, Muhammad Kamran Taj, Ferhat Abbas, Muhammad Shafee, Safed Ahmed Essote, Imran Taj, and Abdul Manan Achakzai. "Microbiological studies on Rhizobium leguminosarum isolated from pea (Pisum sativum L.)." Bangladesh Journal of Botany 48, no. 4 (December 31, 2019): 1223–29. http://dx.doi.org/10.3329/bjb.v48i4.49079.

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Rhizobia are the true bacteria that establish symbiotic relationship leading to the development of new root nodules. This study has been designed to evaluate the microbiological aspects of Rhizobium leguminosarum in target area. A total of 1000 (200 from each site) roots were collected from five different agriculture fields (Quetta, Pishin, Killa Abdulla, Kuchlak and Hanna Urak) and screened through different standard microbiological procedures. Results revealed that 665/1000 (66.5%) roots samples were positive for Rhizobium leguminosarum. The highest percentage was from Pishin 180/200 (18%) and Killa Abdullah 160/200 (16%). A remarkable growth of Rhizobium leguminosarum was noted at 28 to 30°C whereas, less growth was recorded at 24, 34 and 42°C. Similarly, Rhizobium leguminosarum showed growth at pH 5 to 10, but superlative pH values for the growth of Rhizobium leguminosarum were from 6 to 8 pH. The PCR reconfirmed 1300 bp band of 16S rRNA gene of Rhizobium leguminosarum. The organism was further applied as biofertilizer and showed promising results in subjected plants. Medicinal plants application showed that Rhizobium leguminosarum was sensitive to different plants. However, the effects of insecticides showed that Cypermethrin exhibited least zone of inhibition 10 and 11 mm, while Chlorpyrifos showed least zone of inhibition 14 and 17 mm by using disc and well method with (1: 16) dilution. These findings ensure the devastation of microbiota in rhizosphere with rational use of these pesticides that may result in adverse effects over crop productions in the region.

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Enibukun, Jesupemi Mercy, and Bolatito Esther Boboye. "Molecular characterization and evaluation of crude oil remediation potential of some rhizobia isolated from plant root nodules." Nova Biotechnologica et chimica 19, no. 1 (June 30, 2020): 80–88. http://dx.doi.org/10.36547/nbc.v19i1.580.

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This study aimed to determine the molecular identities and genetic relatedness of rhizobia isolated from pigeon pea and pinto beans, and assess their remediation potential in the presence of 1 %, 3 % and 5 % (w/v) crude oil in minimal medium for 7 days incubation period. Standard microbiological and molecular methods which include amplification and purification of 16S rRNA, agarose gel electrophoresis, and sequencing. Results showed molecular identities of six rhizobia from pigeon peas as Bradyrhizobium diazoefficiens USDA122, Rhizobium leguminosarum WSM2304, Bradyrhizobium japonicum N61, Rhizobium leguminosarum N741, Rhizobium leguminosarum BIHIB1217, and Bradyrhizobium japonicum E109; and three rhizobia obtained from pinto beans were Rhizobium leguminosarum N871, Bradyrhizobium diazoefficiens USDA110 and Bradyrhizobium japonicum SEMIA5079. All tested rhizobia (9) showed petroleum degradation ability, as they all grew in the 1, 3 and 5 % (w/v) crude oil minimal medium under laboratory conditions. B. diazoefficiens USDA122 showed the highest optical density (OD) value of 1.184 ± 0.05 on 7th day at 1 % (w/v) crude oil contamination, while R. leguminosarum N741 has the lowest OD value of 0.372 ± 0.02 at 5 % (w/v) crude oil on 7th day. For all the rhizobia, increase occurred throughout incubation period at 1, 3 and 5 % (w/v) except Rhizobium leguminosarum N741 and R. leguminosarum BIHIB1217. In conclusion, the association of R. leguminosarum BIHIB1217 and R. leguminosarum N871 from pigeon pea and pinto beans respectively, were found most effective in crude oil degradation and thus they are recommended as a promising association for remediation of crude oil spilled soils.

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Soberón-Chávez, Gloria, and Rebeca Nájera. "Isolation from soil of Rhizobium leguminosarum lacking symbiotic information." Canadian Journal of Microbiology 35, no. 4 (April 1, 1989): 464–68. http://dx.doi.org/10.1139/m89-071.

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Bacteria resembling Rhizobium leguminosarum, but lacking symbiotic information, were isolated from soil of two different geographical origins. One of these bacteria belongs to a previously described Rhizobium leguminosarum bv. phaseoli somatic serogroup, is fully complemented for nodulation and nitrogen fixation by an R. leguminosarum bv. phaseoli symbiotic plasmid, and is able to compete for bean nodulation with indigenous R. leguminosarum bv. phaseoli strains. This is the first report giving evidence for persistence in soil of Rhizobium lacking symbiotic information.Key words: Rhizobium ecology, symbiotic plasmid, nodulation, plasmid transfer.

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Laguerre, Gisèle, Marc Bardin, and Noëlle Amarger. "Isolation from soil of symbiotic and nonsymbiotic Rhizobium leguminosarum by DNA hybridization." Canadian Journal of Microbiology 39, no. 12 (December 1, 1993): 1142–49. http://dx.doi.org/10.1139/m93-172.

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A procedure based upon DNA hybridization was developed for the specific detection of Rhizobium leguminosarum and its different biovars among bacteria isolated from soil. DNA colony hybridization and restriction fragment length polymorphism analysis with a R. leguminosarum chromosomal probe were found to be species specific for R. leguminosarum and Rhizobium etli. By using R. leguminosarum nod gene probes, biovar specificity was obtained. Of 302 soil isolates screened for their inability to grow on Luria-Bertani agar medium, 13 strains could be assigned to the R. leguminosarum species on the basis of DNA homology to the chromosomal probe and antibiotic resistance tests. Of these strains, three and two were assigned by colony hybridization and subsequent plant host specificity tests, respectively, to R. leguminosarum biovars viciae and trifolii. The eight other R. leguminosarum soil isolates lacked symbiotic information but were able to gain nodulation capacity with the acquisition of a conjugative symbiotic plasmid. They were thus considered as nonsymbiotic R. leguminosarum.Key words: Rhizobium leguminosarum, DNA hybridization, soil, symbiotic genes.

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Rioux, Clément R., D. Carlyle Jordan, and James B. M. Rattray. "Anthranilate-promoted iron uptake in Rhizobium leguminosarum." Archives of Biochemistry and Biophysics 248, no. 1 (July 1986): 183–89. http://dx.doi.org/10.1016/0003-9861(86)90415-7.

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Velázquez, Encarna, Esperanza Martı́nez-Romero, Dulce Nombre Rodrı́guez-Navarro, Martha E. Trujillo, Antonio Daza, Pedro F. Mateos, Eustoquio Martı́nez-Molina, and Peter van Berkum. "Characterization of Rhizobial Isolates of Phaseolus vulgaris by Staircase Electrophoresis of Low-Molecular-Weight RNA." Applied and Environmental Microbiology 67, no. 2 (February 1, 2001): 1008–10. http://dx.doi.org/10.1128/aem.67.2.1008-1010.2001.

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ABSTRACT Low-molecular-weight (LMW) RNA molecules were analyzed to characterize rhizobial isolates that nodulate the common bean growing in Spain. Since LMW RNA profiles, determined by staircase electrophoresis, varied across the rhizobial species nodulating beans, we demonstrated that bean isolates recovered from Spanish soils presumptively could be characterized as Rhizobium etli,Rhizobium gallicum, Rhizobium giardinii,Rhizobium leguminosarum bv. viciae and bv. trifolii, andSinorhizobium fredii.

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Kucey, R. M. N., and M. F. Hynes. "Populations of Rhizobium leguminosarum biovars phaseoli and viceae in fields after bean or pea in rotation with nonlegumes." Canadian Journal of Microbiology 35, no. 6 (June 1, 1989): 661–67. http://dx.doi.org/10.1139/m89-107.

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Populations of Rhizobium leguminosarum bv. phaesoli and bv. viceae in southern Alberta soils were measured over a period of 4 years using a most probable number method. Five fields cropped to bean (Phaseolus vulgaris L.), five fields cropped to pea (Pisum sativum L.), and two fields cropped to wheat were used as test sites. Legume crops had received appropriate legume inoculants. Fields were sampled in the fall of the crop year and in the spring of the following 3 years during which fields were cropped to nonlegumes or left fallow. Numbers of R. leguminosarum bv. phaseoli were 100 to 1000 times higher in fields that had been planted to bean than in fields that had been planted to pea or wheat. Fields that had been planted to pea maintained populations of R. leguminosarum bv. viceae 10 to 100 times higher than fields that had been planted to bean or wheat. Wheat fields, which had never had legumes grown in them, contained between 1 and 100 rhizobia per gram of soil of both biovars of R. leguminosarum, indicating that both biovars are native to southern Alberta soils. The numbers of rhizobia did not decrease in proportion to the population of other bacteria in the soil over the duration of the experiment. Plasmid profiles of soil Rhizobium isolates obtained in the last year of the experiment showed that none of the isolates had plasmid profiles similar to those of strains added as inoculants in the 1st year of the experiment. These results show that fields cropped to legumes and receiving rhizobial inoculants in this study maintained high populations of rhizobia for several years after harvest of the legume crop.Key words: Rhizobium leguminosarum bv. phaseoli, Rhizobium leguminosarum bv. viceae, nodule, plasmid profiles, inoculum potential, rhizobium competition.

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Moreno, S., E. J. Patriarca, M. Chiurazzi, R. Meza, R. Defez, A. Lamberti, A. Riccio, M. Iaccarino, and G. Espin. "Phenotype of a Rhizobium leguminosarum ntrC mutant." Research in Microbiology 143, no. 2 (January 1992): 161–71. http://dx.doi.org/10.1016/0923-2508(92)90005-9.

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Noel, T. C., C. Sheng, C. K. Yost, R. P. Pharis, and M. F. Hynes. "Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce." Canadian Journal of Microbiology 42, no. 3 (March 1, 1996): 279–83. http://dx.doi.org/10.1139/m96-040.

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Early seedling root growth of the nonlegumes canola (Brassica campestris cv. Tobin, Brassica napus cv. Westar) and lettuce (Lactuca saliva cv. Grand Rapids) was significantly promoted by inoculation of seeds with certain strains of Rhizobium leguminosarum, including nitrogen- and nonnitrogen-fixing derivatives under gnotobiotic conditions. The growfh-promotive effect appears to be direct, with possible involvement of the plant growth regulators indole-3-acetic acid and cytokinin. Auxotrophic Rhizobium mutants requiring tryptophan or adenosine (precursors for indole-3-acetic acid and cytokinin synthesis, respectively) did not promote growth to the extent of the parent strain. The findings of this study demonstrate a new facet of the Rhizobium–plant relationship and that Rhizobium leguminosarum can be considered a plant growth-promoting rhizobacterium (PGPR).Key words: Rhizobium, plant growth-promoting rhizobacteria, PGPR, indole-3-acetic acid, cytokinin, roots, auxotrophic mutants.

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Brito, Belén, Rosa-Isabel Prieto, Ezequiel Cabrera, Marie-Andrée Mandrand-Berthelot, Juan Imperial, Tomás Ruiz-Argüeso, and José-Manuel Palacios. "Rhizobium leguminosarum hupE Encodes a Nickel Transporter Required for Hydrogenase Activity." Journal of Bacteriology 192, no. 4 (December 18, 2009): 925–35. http://dx.doi.org/10.1128/jb.01045-09.

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ABSTRACT Synthesis of the hydrogen uptake (Hup) system in Rhizobium leguminosarum bv. viciae requires the function of an 18-gene cluster (hupSLCDEFGHIJK-hypABFCDEX). Among them, the hupE gene encodes a protein showing six transmembrane domains for which a potential role as a nickel permease has been proposed. In this paper, we further characterize the nickel transport capacity of HupE and that of the translated product of hupE2, a hydrogenase-unlinked gene identified in the R. leguminosarum genome. HupE2 is a potential membrane protein that shows 48% amino acid sequence identity with HupE. Expression of both genes in the Escherichia coli nikABCDE mutant strain HYD723 restored hydrogenase activity and nickel transport. However, nickel transport assays revealed that HupE and HupE2 displayed different levels of nickel uptake. Site-directed mutagenesis of histidine residues in HupE revealed two motifs (HX5DH and FHGX[AV]HGXE) that are required for HupE functionality. An R. leguminosarum double mutant, SPF22A (hupE hupE2), exhibited reduced levels of hydrogenase activity in free-living cells, and this phenotype was complemented by nickel supplementation. Low levels of symbiotic hydrogenase activity were also observed in SPF22A bacteroid cells from lentil (Lens culinaris L.) root nodules but not in pea (Pisum sativum L.) bacteroids. Moreover, heterologous expression of the R. leguminosarum hup system in bacteroid cells of Rhizobium tropici and Mesorhizobium loti displayed reduced levels of hydrogen uptake in the absence of hupE. These data support the role of R. leguminosarum HupE as a nickel permease required for hydrogen uptake under both free-living and symbiotic conditions.

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Richardson, Jason S., Xavi Carpena, Jack Switala, Rosa Perez-Luque, Lynda J. Donald, Peter C. Loewen, and Ivan J. Oresnik. "RhaU of Rhizobium leguminosarum Is a Rhamnose Mutarotase." Journal of Bacteriology 190, no. 8 (December 21, 2007): 2903–10. http://dx.doi.org/10.1128/jb.01120-07.

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ABSTRACT Of the nine genes comprising the l-rhamnose operon of Rhizobium leguminosarum, rhaU has not been assigned a function. The construction of a ΔrhaU strain revealed a growth phenotype that was slower than that of the wild-type strain, although the ultimate cell yields were equivalent. The transport of l-rhamnose into the cell and the rate of its phosphorylation were unaffected by the mutation. RhaU exhibits weak sequence similarity to the formerly hypothetical protein YiiL of Escherichia coli that has recently been characterized as an l-rhamnose mutarotase. To characterize RhaU further, a His-tagged variant of the protein was prepared and subjected to mass spectrometry analysis, confirming the subunit size and demonstrating its dimeric structure. After crystallization, the structure was refined to a 1.6-Å resolution to reveal a dimer in the asymmetric unit with a very similar structure to that of YiiL. Soaking a RhaU crystal with l-rhamnose resulted in the appearance of β-l-rhamnose in the active site.

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Sprout, Sharon L., Louise M. Nelson, and James J. Germida. "Influence of metribuzin on the Rhizobium leguminosarum–lentil (Lens culinaris) symbiosis." Canadian Journal of Microbiology 38, no. 4 (April 1, 1992): 343–49. http://dx.doi.org/10.1139/m92-058.

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The effects of the triazine herbicide metribuzin (Sencor) on the lentil (Lens culinaris Medic.) - Rhizobium leguminosarum biovar viciae symbiosis were studied in Leonard jars and growth pouches. Lentils inoculated with Rhizobium leguminosarum strain 128C54 or 128C84, and noninoculated lentils grown in plant nutrient solution supplemented with 5 mM KNO3, had metribuzin applied to the plants at either 8 or 13 days after planting. When sprayed at 8 days, metribuzin had a significant (p ≤ 0.05) negative effect on plant weight, number of nodules, taproot growth, and acetylene reduction activity. Five to 10 days after spraying, the plants began to recover from the inhibitory effects. When spraying was delayed to 13 days after planting, metribuzin had little effect on plant growth. The R. leguminosarum strain used as inoculant affected the degree of inhibition of lentil growth and the rate of plant recovery. Less than 0.2% of foliarly applied metribuzin was translocated to the root. Thus the detrimental effects of metribuzin application to lentils were mainly due to direct effects on the plant, which resulted in indirect effects on nodulation and nitrogen fixation. Key words: Rhizobium leguminosarum, lentil, metribuzin.

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Karunakaran, Ramakrishnan, Andreas F. Haag, Alison K. East, Vinoy K. Ramachandran, Jurgen Prell, Euan K. James, Marco Scocchi, Gail P. Ferguson, and Philip S. Poole. "BacA Is Essential for Bacteroid Development in Nodules of Galegoid, but not Phaseoloid, Legumes." Journal of Bacteriology 192, no. 11 (April 2, 2010): 2920–28. http://dx.doi.org/10.1128/jb.00020-10.

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ABSTRACT BacA is an integral membrane protein, the mutation of which leads to increased resistance to the antimicrobial peptides bleomycin and Bac71-35 and a greater sensitivity to SDS and vancomycin in Rhizobium leguminosarum bv. viciae, R. leguminosarum bv. phaseoli, and Rhizobium etli. The growth of Rhizobium strains on dicarboxylates as a sole carbon source was impaired in bacA mutants but was overcome by elevating the calcium level. While bacA mutants elicited indeterminate nodule formation on peas, which belong to the galegoid tribe of legumes, bacteria lysed after release from infection threads and mature bacteroids were not formed. Microarray analysis revealed almost no change in a bacA mutant of R. leguminosarum bv. viciae in free-living culture. In contrast, 45 genes were more-than 3-fold upregulated in a bacA mutant isolated from pea nodules. Almost half of these genes code for cell membrane components, suggesting that BacA is crucial to alterations that occur in the cell envelope during bacteroid development. In stark contrast, bacA mutants of R. leguminosarum bv. phaseoli and R. etli elicited the formation of normal determinate nodules on their bean host, which belongs to the phaseoloid tribe of legumes. Bacteroids from these nodules were indistinguishable from the wild type in morphology and nitrogen fixation. Thus, while bacA mutants of bacteria that infect galegoid or phaseoloid legumes have similar phenotypes in free-living culture, BacA is essential only for bacteroid development in indeterminate galegoid nodules.

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Karunakaran, R., K. Ebert, S. Harvey, M. E. Leonard, V. Ramachandran, and P. S. Poole. "Thiamine Is Synthesized by a Salvage Pathway in Rhizobium leguminosarum bv. viciae Strain 3841." Journal of Bacteriology 188, no. 18 (September 15, 2006): 6661–68. http://dx.doi.org/10.1128/jb.00641-06.

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ABSTRACT In the absence of added thiamine, Rhizobium leguminosarum bv. viciae strain 3841 does not grow in liquid medium and forms only “pin” colonies on agar plates, which contrasts with the good growth of Sinorhizobium meliloti 1021, Mesorhizobium loti 303099, and Rhizobium etli CFN42. These last three organisms have thiCOGE genes, which are essential for de novo thiamine synthesis. While R. leguminosarum bv. viciae 3841 lacks thiCOGE, it does have thiMED. Mutation of thiM prevented formation of pin colonies on agar plates lacking added thiamine, suggesting thiamine intermediates are normally present. The putative functions of ThiM, ThiE, and ThiD are 4-methyl-5-(β-hydroxyethyl) thiazole (THZ) kinase, thiamine phosphate pyrophosphorylase, and 4-amino-5-hydroxymethyl-2-methyl pyrimidine (HMP) kinase, respectively. This suggests that a salvage pathway operates in R. leguminosarum, and addition of HMP and THZ enabled growth at the same rate as that enabled by thiamine in strain 3841 but elicited no growth in the thiM mutant (RU2459). There is a putative thi box sequence immediately upstream of the thiM, and a gfp-mut3.1 fusion to it revealed the presence of a promoter that is strongly repressed by thiamine. Using fluorescent microscopy and quantitative reverse transcription-PCR, it was shown that thiM is expressed in the rhizosphere of vetch and pea plants, indicating limitation for thiamine. Pea plants infected by RU2459 were not impaired in nodulation or nitrogen fixation. However, colonization of the pea rhizosphere by the thiM mutant was impaired relative to that of the wild type. Overall, the results show that a thiamine salvage pathway operates to enable growth of Rhizobium leguminosarum in the rhizosphere, allowing its survival when thiamine is limiting.

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Nadler, K. D., A. W. Johnston, J. W. Chen, and T. R. John. "A Rhizobium leguminosarum mutant defective in symbiotic iron acquisition." Journal of Bacteriology 172, no. 2 (1990): 670–77. http://dx.doi.org/10.1128/jb.172.2.670-677.1990.

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Schlaman, H. R., R. J. Okker, and B. J. Lugtenberg. "Subcellular localization of the Rhizobium leguminosarum nodI gene product." Journal of Bacteriology 172, no. 9 (1990): 5486–89. http://dx.doi.org/10.1128/jb.172.9.5486-5489.1990.

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Parke, D., F. Rynne, and A. Glenn. "Regulation of phenolic catabolism in Rhizobium leguminosarum biovar trifolii." Journal of Bacteriology 173, no. 17 (1991): 5546–50. http://dx.doi.org/10.1128/jb.173.17.5546-5550.1991.

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Brom, S., A. García de los Santos, M. de Lourdes Girard, G. Dávila, R. Palacios, and D. Romero. "High-frequency rearrangements in Rhizobium leguminosarum bv. phaseoli plasmids." Journal of Bacteriology 173, no. 3 (1991): 1344–46. http://dx.doi.org/10.1128/jb.173.3.1344-1346.1991.

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Zhang, Xue-Xian, Bob Kosier, and Ursula B. Priefer. "Symbiotic Plasmid Rearrangement in Rhizobium leguminosarum bv. viciae VF39SM." Journal of Bacteriology 183, no. 6 (March 15, 2001): 2141–44. http://dx.doi.org/10.1128/jb.183.6.2141-2144.2001.

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ABSTRACT A rearrangement between the symbiotic plasmid (pRleVF39d) and a nonsymbiotic plasmid (pRleVF39b) in Rhizobium leguminosarumbv. viciae VF39 was observed. The rearranged derivative showed the same plasmid profile as its parent strain, but hybridization to nod, fix, and nif genes indicated that most of the symbiotic genes were now present on a plasmid corresponding in size to pRleVF39b instead of pRleVF39d. On the other hand, some DNA fragments originating from pRleVF39b now hybridized to the plasmid band at the position of pRleVF39d. These results suggest that a reciprocal but unequal DNA exchange between the two plasmids had occurred.

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Mazurier, Sylvie-Isabelle, and Gisele Laguerre. "Unusual localization of nod and nif genes in Rhizobium leguminosarum bv. viciae." Canadian Journal of Microbiology 43, no. 4 (April 1, 1997): 399–402. http://dx.doi.org/10.1139/m97-056.

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Genomic DNA from seven strains of Rhizobium leguminosarum bv. viciae isolated from nodules of field-grown lentils showed homology to nod and nif gene probes, whereas plasmid DNA did not hybridize with these probes. The results suggest that symbiotic genes could be located on the chromosome or perhaps on a very large plasmid that could not be resolved in Eckhardt gels. Each strain contained one plasmid that hybridized with a pSym isolated from a R. leguminosarum strain of the same field population. This finding led us to hypothesize that the nod and nif genes of the seven strains might have originated from a Sym plasmid and have been integrated into another replicon. The ability to nodulate vetch was confirmed for all of the seven strains. Thus, wild strains of R. leguminosarum bv. viciae that nodulate vetch carry nod and nif genes either on the chromosome or on an extrachromosomal replicon of size much larger than the pSyms hitherto described.Key words: Rhizobium leguminosarum, nod genes, nif genes, chromosome, symbiotic plasmid, megaplasmid.

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Jiang, J., B. H. Gu, L. M. Albright, and B. T. Nixon. "Conservation between coding and regulatory elements of Rhizobium meliloti and Rhizobium leguminosarum dct genes." Journal of Bacteriology 171, no. 10 (1989): 5244–53. http://dx.doi.org/10.1128/jb.171.10.5244-5253.1989.

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Hardy, Kimberly, and J. Diane Knight. "Evaluation of biochars as carriers for Rhizobium leguminosarum." Canadian Journal of Microbiology 67, no. 1 (January 2021): 53–63. http://dx.doi.org/10.1139/cjm-2020-0416.

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Peat is the standard carrier material used for commercial microbial inoculants produced in Canada and the United States. Peat is a slowly renewable resource and its production is extremely vulnerable to variable weather conditions. Furthermore, it may not be widely available in all countries. We investigated the potential to develop biochar as a carrier material. Our goal was to evaluate if different biochars perform comparably in supporting rhizobial survival, and what characteristics contribute to their ability to support rhizobial survival. Evaluation included characterization of the biochars, assessment of biochar phytotoxicity, survival of Rhizobium on biochars, and growth chamber evaluation of two biochars as Rhizobium carriers for inoculating pea. Of the original nine biochars evaluated, six supported Rhizobium leguminosarum for 84 days at 4 °C; of this six, two supported numbers >1 × 106 cfu·(g biochar)−1. The only characteristics that correlated with survival were C/N ratio and percent C. The two biochars evaluated delivered R. leguminosarum to pea that initiated nodulation, biomass production, and biomass N at levels higher than a noninoculated control and heat-killed inoculated biochars. We demonstrate that there is considerable potential to develop biochar as a carrier for rhizobial inoculants.

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Tambalo, Dinah D., Christopher K. Yost, and Michael F. Hynes. "Characterization of swarming motility in Rhizobium leguminosarum bv. viciae." FEMS Microbiology Letters 307, no. 2 (April 13, 2010): 165–74. http://dx.doi.org/10.1111/j.1574-6968.2010.01982.x.

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Wolff, Andreas B., and Dietrich Werner. "Defence Reactions in Rhizobium-Legume Symbiosis: Phytoalexin Concentration in Vicia faba Nodules is Affected by the Host Plant Genotype." Zeitschrift für Naturforschung C 45, no. 9-10 (October 1, 1990): 958–62. http://dx.doi.org/10.1515/znc-1990-9-1006.

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Abstract In the Vicia faba-Rhizobium leguminosarum symbiosis defence reactions are established by a variable phytoalexin concentration in the nodules. No differences were observed between effective (fix+) and ineffective (fix- ) nodules. In nodules of field grown plants the average phytoalexin concentration was about 3 times higher than that from sterile pot-cultured plants infected with different Rhizobium leguminosarum strains. A great variability of phytoalexin accumulation in nodules of single plants was observed. In field grown plants about 60% of the nodules of each plant had very low levels (< 50 µg wyerone g nodule fresh weight-1) the other 40% had levels between 100 and 600 µig w yerone-g nodule fresh weight-1 indicating different defence reactions in the nodules distributed over the root system of one plant. Phytoalexin accumulation was more affected by the cultivar of the host plant than by the infecting Rhizobium strain. Two inbred lines had the lowest concentration in nodules

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Perrine, Francine M., Joko Prayitno, Jeremy J. Weinman, Frank B. Dazzo, and Barry G. Rolfe. "Rhizobium plasmids are involved in the inhibition or stimulation of rice growth and development." Functional Plant Biology 28, no. 9 (2001): 923. http://dx.doi.org/10.1071/pp01046.

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This paper originates from an address at the 8th International Symposium on Nitrogen Fixation with Non-Legumes, Sydney, NSW, December 2000 We examined growth responses of rice seedlings (Oryza sativaL. cv. Pelde) to specific Rhizobium strains and their mutants, to investigate the molecular basis of colonization and the stimulation or inhibition of rice growth and development by rhizobia. Inoculation experiments with rice seedlings showed that specific Rhizobium isolates of these rice-associated and legume-associated rhizobia could either promote, inhibit, or have no influence on rice plant growth. There are genes on certain plasmids of Rhizobium leguminosarum bv. trifolii and R. leguminosarum bv. viciae that affect the growth and development of rice root morphology. Additionally, we found that bacteria can intimately associate with, and enter into, rice seedling roots by alternative mechanisms to those encoded by the symbiotic (pSym) and the tumour-inducing (Ti) plasmids. Investigations suggest an involvement of the phytohormone auxin, and possibly nitrate, in this complex rice–Rhizobium interaction.

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Sivakumaran, S., B. D. W. Jarvis, and P. J. Lockhart. "Identification of soil bacteria expressing a symbiotic plasmid from Rhizobium leguminosarum bv. trofolii." Canadian Journal of Microbiology 43, no. 2 (February 1, 1997): 164–77. http://dx.doi.org/10.1139/m97-022.

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A hundred strains of non-nodulating, Gram-negative, rod-shaped bacteria were isolated from clover–ryegrass pastures on three different soil types and from a sandy loam under lupins. When crossed with Escherichia coli PN200 containing the cointegrate plasmid pPN1, 11 transconjugants gained the ability to form nodules on the roots of white clover (Trifolium repens cv. Grasslands Huia). A nodA probe indicated that they had gained nodulation genes. The identities of these 11 strains and 4 others derived from earlier work on non-nodulating root nodule bacteria, were determined by ribotyping, DNA – DNA hybridization, and partial 16S rRNA sequencing. Good agreement was obtained between the three methods, and 11 of the strains were identified as Rhizobium leguminosarum (6), Rhizobium loti (2), Rhizobium etli (1), Rhizobium tropici (1), and Sinorhizobium meliloti (1). DNA –DNA hybridization indicated that the remaining four strains were related to the Rhizobium leguminosarum reference strains. The existence of several species of non-nodulating rhizobia in pasture soil, including species for which the normal host plant was absent, is discussed in relation to the fate of symbiotic plasmids from Rhizobium seed inoculants. It is also suggested that new species should be named for the geographical region from which they are first isolated rather than the host plant.Key words: Rhizobium, non-nodulating, nonsymbiotic, isolation, identification.

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Fenton, M., and B. D. W. Jarvis. "Expression of the symbiotic plasmid from Rhizobium leguminosarum biovar trifolii in Sphingobacterium multivorum." Canadian Journal of Microbiology 40, no. 10 (October 1, 1994): 873–79. http://dx.doi.org/10.1139/m94-138.

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An inoculant strain of Rhizobium leguminosarum biovar trifolii containing a Tn5 marked symbiotic plasmid transferred this plasmid by conjugation to Sphingobacterium multivorum, an organism that can be found in soil. The transconjugant bacteria nodulated the roots of white clover (Trifolium repens) seedlings but did not fix atmospheric nitrogen. Microscopic examination revealed abnormal nodule structures. Bacteria isolated from the nodules were shown to be closely related to the recipient S. multivorum and Southern blots of genomic digests probed with nodA DNA confirmed that the transconjugants contained symbiotic genes. This is the first report of the spontaneous transfer, by conjugation, of a symbiotic plasmid from R. leguminosarum biovar trifolii to S. multivorum.Key words: Rhizobium, Sphingobacterium, nodulation, nod gene transfer.

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Selbitschka, Werner, Walter Arnold, Ursula B. Priefer, Thomas Rottschäfer, Michael Schmidt, Reinhard Simon, and Alfred Pühler. "Characterization of recA genes and recA mutants of Rhizobium meliloti and Rhizobium leguminosarum biovar viciae." Molecular and General Genetics MGG 229, no. 1 (September 1991): 86–95. http://dx.doi.org/10.1007/bf00264217.

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32

Garg, Nisha, and H. S. Nainawatee. "Reductant and energy level of bacteroids of Rhizobium leguminosarum." Phytochemistry 28, no. 11 (January 1989): 2913–15. http://dx.doi.org/10.1016/0031-9422(89)80252-3.

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33

George, M. L. C., J. P. W. Young, and D. Borthakur. "Genetic characterization of Rhizobium sp. strain TAL1145 that nodulates tree legumes." Canadian Journal of Microbiology 40, no. 3 (March 1, 1994): 208–15. http://dx.doi.org/10.1139/m94-034.

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Rhizobium sp. strain TALI 145 nodulates Leucaena ieucocephaia and Phaseolus vulgaris, in addition to a wide range of tropical tree legumes. Six overlapping clones that complemented nodulation defects in leucaena and bean rhizobia were isolated and a 40-kb map of the symbiosis region was constructed. The common nod and nifA genes were situated approximately 17 kb apart, with the nodlJ genes in between. These clones enabled a derivative of TAL1145 carrying a partially deleted pSym to form ineffective nodules on both leucaena and bean, and a similar derivative of Rhizobium etli TAL182 to form ineffective nodules on bean. When two representative clones, pUHR9 and pUHR114, were each transferred to wild-type rhizobial strains, they allowed ineffective nodulation by Rhizobium meliloti on both leucaena and bean and by Rhizobium leguminosarum bv. viciae on bean. Transconjugants of R. leguminosarum bv. trifolii formed effective nodules on leucaena and ineffective nodules on bean. Tn5 mutagenesis of the symbiosis region resulted in a variety of nodulation and fixation phenotypes on leucaena and bean. On the basis of 16S rRNA sequences, TAL1145 was found to be distinct from both R. tropici and NGR234, the two groups of leucaena symbionts that were previously described.Key words: Rhizobium, Leucaena leucocephala, nodulation, nitrogen fixation.

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Martínez, Marta, José M. Palacios, Juan Imperial, and Tomás Ruiz-Argüeso. "Symbiotic Autoregulation of nifA Expression in Rhizobium leguminosarum bv. viciae." Journal of Bacteriology 186, no. 19 (October 1, 2004): 6586–94. http://dx.doi.org/10.1128/jb.186.19.6586-6594.2004.

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ABSTRACT NifA is the general transcriptional activator of nitrogen fixation genes in diazotrophic bacteria. In Rhizobium leguminosarum bv. viciae UPM791, the nifA gene is part of a gene cluster (orf71 orf79 fixW orf5 fixABCX nifAB) separated by 896 bp from an upstream and divergent truncated duplication of nifH (ΔnifH). Symbiotic expression analysis of genomic nifA::lacZ fusions revealed that in strain UPM791 nifA is expressed mainly from a σ54-dependent promoter (P nifA1 ) located upstream of orf71. This promoter contains canonical NifA upstream activating sequences located 91 bp from the transcription initiation site. The transcript initiated in P nifA1 spans 5.1 kb and includes nifA and nifB genes. NifA from Klebsiella pneumoniae was able to activate transcription from P nifA1 in a heterologous Escherichia coli system. In R. leguminosarum, the P nifA1 promoter is essential for effective nitrogen fixation in symbiosis with peas. In its absence, partially efficient nitrogen-fixing nodules were produced, and the corresponding bacteroids exhibited only low levels of nifA gene expression. The basal level of nifA expression resulted from a promoter activity originating upstream of the fixX-nifA intergenic region and probably from an incomplete duplication of P nifA1 located immediately upstream of fixA.

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Schlaman, H. R., H. P. Spaink, R. J. Okker, and B. J. Lugtenberg. "Subcellular localization of the nodD gene product in Rhizobium leguminosarum." Journal of Bacteriology 171, no. 9 (1989): 4686–93. http://dx.doi.org/10.1128/jb.171.9.4686-4693.1989.

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36

Leyva, A., J. M. Palacios, T. Mozo, and T. Ruiz-Argüeso. "Cloning and characterization of hydrogen uptake genes from Rhizobium leguminosarum." Journal of Bacteriology 169, no. 11 (1987): 4929–34. http://dx.doi.org/10.1128/jb.169.11.4929-4934.1987.

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37

Tao, H., N. J. Brewin, and K. D. Noel. "Rhizobium leguminosarum CFN42 lipopolysaccharide antigenic changes induced by environmental conditions." Journal of Bacteriology 174, no. 7 (1992): 2222–29. http://dx.doi.org/10.1128/jb.174.7.2222-2229.1992.

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38

Breedveld, M. W., H. C. Cremers, M. Batley, M. A. Posthumus, L. P. Zevenhuizen, C. A. Wijffelman, and A. J. Zehnder. "Polysaccharide synthesis in relation to nodulation behavior of Rhizobium leguminosarum." Journal of Bacteriology 175, no. 3 (1993): 750–57. http://dx.doi.org/10.1128/jb.175.3.750-757.1993.

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39

Ercolano, R., R. Mirabella, M. Chiurazzi, and M. Merrick. "The Rhizobium leguminosarum glnB gene is down-regulated during symbiosis." Molecular and General Genetics MGG 264, no. 5 (January 2001): 555–64. http://dx.doi.org/10.1007/s004380000333.

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40

Chakrabarti, S. K., A. K. Mishra, and P. K. Chakrabartty. "DNA homology studies of rhizobia from Cicer arietinum L." Canadian Journal of Microbiology 32, no. 6 (June 1, 1986): 524–27. http://dx.doi.org/10.1139/m86-096.

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The taxonomic status of rhizobia which infect Cicer arietinum is poorly defined. Historically these organisms have been placed under Rhizobium leguminosarum; however, later reports suggested that they be treated as a separate cross-inoculation group. Therefore, DNA homology tests were carried out with various rhizobia. The data indicate that rhizobia from Cicer cannot be placed under any of the recognised species of Rhizobium.

41

Abd EL- Basit, Howaida, Amina Hassan, M. Youssef, and M. Amin. "MOLECULAR AND GENETIC CHARACTERIZATION OF SOME Rhizobium leguminosarum bv. vicieae isolates." Journal of Plant Production 32, no. 6 (June 1, 2007): 4515–32. http://dx.doi.org/10.21608/jpp.2007.208779.

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42

Brink, B. A., J. Miller, R. W. Carlson, and K. D. Noel. "Expression of Rhizobium leguminosarum CFN42 genes for lipopolysaccharide in strains derived from different R. leguminosarum soil isolates." Journal of Bacteriology 172, no. 2 (1990): 548–55. http://dx.doi.org/10.1128/jb.172.2.548-555.1990.

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43

García-de los Santos, Alejandro, Alejandro Morales, Laura Baldomá, Scott R. D. Clark, Susana Brom, Christopher K. Yost, Ismael Hernández-Lucas, Juan Aguilar, and Michael F. Hynes. "TheglcBlocus ofRhizobium leguminosarumVF39 encodes an arabinose-inducible malate synthase." Canadian Journal of Microbiology 48, no. 10 (October 1, 2002): 922–32. http://dx.doi.org/10.1139/w02-091.

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In the course of a study conducted to isolate genes upregulated by plant cell wall sugars, we identified an arabinose-inducible locus from a transcriptional fusion library of Rhizobium leguminosarum VF39, carrying random insertions of the lacZ transposon Tn5B22. Sequence analysis of the locus disrupted by the transposon revealed a high similarity to uncharacterized malate synthase G genes from Sinorhizobium meliloti, Agrobacterium tumefaciens, and Mesorhizobium loti. This enzyme catalyzes the condensation of glyoxylate and acetyl-CoA to yield malate and CoA and is thought to be a component of the glyoxylate cycle, which allows microorganisms to grow on two carbon compounds. Enzyme assays showed that a functional malate synthase is encoded in the glcB gene of R. leguminosarum and that its expression is induced by arabinose, glycolate, and glyoxylate. An Escherichia coli aceB glcB mutant, complemented with the R. leguminosarum PCR-amplified gene, recovered malate synthase activity. A very similar genome organization of the loci containing malate synthase and flanking genes was observed in R. leguminosarum, S. meliloti, and A. tumefaciens. Pea plants inoculated with the glcB mutant or the wild-type strain showed no significant differences in nitrogen fixation. This is the first report regarding the characterization of a mutant in one of the glyoxylate cycle enzymes in the rhizobia.Key words: Rhizobium, malate synthase, glyoxylate cycle, arabinose metabolism.

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Wielbo, Jerzy, Andrzej Mazur, Jarosław E. Król, Małgorzata Marczak, and Anna Skorupska. "Environmental modulation of the pssTNOP gene expression in Rhizobium leguminosarum bv. trifolii." Canadian Journal of Microbiology 50, no. 3 (March 1, 2004): 201–11. http://dx.doi.org/10.1139/w04-004.

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Exopolysaccharide production by Rhizobium leguminosarum bv. trifolii is required for successful establishment of nitrogen-fixing symbiosis with clover (Trifolium pratense L.). Using plasmid-borne transcriptional fusions of promoters of pss genes with promoterless lacZ the effect of root exudate, phosphate, and ammonia on expression of pssT, pssN, pssO, and pssP genes in wild-type strain RtTA1 background was determined. A stimulating effect of these environmental factors on pssO and pssP gene expression was observed. The putative pssO gene promoter was determined to be a strong promoter within which the divergent nod-box element was identified. The pssO promoter was slightly inducible in a flavonoid-dependent manner in wild-type R. leguminosarum bv. trifolii strains RtTA1 and ANU843 and very weakly active in a mutant of strain ANU843 that lacks the regulatory nodD gene. The expression of pssO and pssP genes in planta was investigated using plasmid-borne pssO–gusA and pssP–gusA fusions under different phosphate availability to clover. The level of pssO–gusA fusion expression was shown to be dependent on phosphate concentration in the plant growth medium.Key words: Rhizobium leguminosarum, exopolysaccharide, nod box, transcriptional fusion.

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Skorupska, A., and M. Deryło. "Homology of genes for exopolysaccharide synthesis in Rhizobium leguminosarum and effect of cloned exo genes on nodule formation." Acta Biochimica Polonica 40, no. 4 (December 31, 1993): 477–82. http://dx.doi.org/10.18388/abp.1993_4787.

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A 5.4 kb BamHI fragment of R. leguminosarum bv. trifolii TA1 was found to carry genes involved in exopolysaccharide synthesis (exo genes). This fragment was strongly hybridized to the total DNA from R. l. bv. viciae and bv. phaseoli digested with EcoRI. No homology was found with total DNA of R. meliloti and Rhizobium sp. NGR 234. The exo genes from R. l. bv. trifolii TA1 conjugally introduced into R. l. bv. viciae 1302 considerably affected the symbiosis: the nodules induced on vetch were abortive and did not fix nitrogen. On the other hand, Phaseolus beans infected with R. l. bv. phaseoli harbouring R. l. bv. trifolii exo genes formed the nitrogen-fixing nodules. It can be concluded that additional copies of exo genes introduced into wild type Rhizobium leguminosarum strains can disturb the synthesis of acidic exopolysaccharides and affect symbiosis of the plants forming indeterminate nodules, but do not affect symbiosis of the plants forming the determinate nodules.

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Leyva, A., J. M. Palacios, J. Murillo, and T. Ruiz-Argüeso. "Genetic organization of the hydrogen uptake (hup) cluster from Rhizobium leguminosarum." Journal of Bacteriology 172, no. 3 (1990): 1647–55. http://dx.doi.org/10.1128/jb.172.3.1647-1655.1990.

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47

Girard, M. L., M. Flores, S. Brom, D. Romero, R. Palacios, and G. Dávila. "Structural complexity of the symbiotic plasmid of Rhizobium leguminosarum bv. phaseoli." Journal of Bacteriology 173, no. 8 (1991): 2411–19. http://dx.doi.org/10.1128/jb.173.8.2411-2419.1991.

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48

Dowling, D. N., U. Samrey, J. Stanley, and W. J. Broughton. "Cloning of Rhizobium leguminosarum genes for competitive nodulation blocking on peas." Journal of Bacteriology 169, no. 3 (1987): 1345–48. http://dx.doi.org/10.1128/jb.169.3.1345-1348.1987.

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49

Vedam, Vinata, Elmar L. Kannenberg, Janine G. Haynes, D. Janine Sherrier, Anup Datta, and Russell W. Carlson. "A Rhizobium leguminosarum AcpXL Mutant Produces Lipopolysaccharide Lacking 27-Hydroxyoctacosanoic Acid." Journal of Bacteriology 185, no. 6 (March 15, 2003): 1841–50. http://dx.doi.org/10.1128/jb.185.6.1841-1850.2003.

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ABSTRACT The structure of the lipid A from Rhizobium etli and Rhizobium leguminosarum lipopolysaccharides (LPSs) lacks phosphate and contains a galacturonosyl residue at its 4′ position, an acylated 2-aminogluconate in place of the proximal glucosamine, and a very long chain ω-1 hydroxy fatty acid, 27-hydroxyoctacosanoic acid (27OHC28:0). The 27OHC28:0 moiety is common in lipid A's among members of the Rhizobiaceae and also among a number of the facultative intracellular pathogens that form chronic infections, e.g., Brucella abortus, Bartonella henselae, and Legionella pneumophila. In this paper, a mutant of R. leguminosarum was created by placing a kanamycin resistance cassette within acpXL, the gene which encodes the acyl carrier protein for 27OHC28:0. The result was an LPS containing a tetraacylated lipid A lacking 27OHC28:0. A small amount of the mutant lipid A may contain an added palmitic acid residue. The mutant is sensitive to changes in osmolarity and an increase in acidity, growth conditions that likely occur in the nodule microenvironment. In spite of the probably hostile microenvironment of the nodule, the acpXL mutant is still able to form nitrogen-fixing root nodules even though the appearance and development of nodules are delayed. Therefore, it is possible that the acpXL mutant has a host-inducible mechanism which enables it to adapt to these physiological changes.

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Prell, J., G. Mulley, F. Haufe, J. P. White, A. Williams, R. Karunakaran, J. A. Downie, and P. S. Poole. "The PTSNtr system globally regulates ATP-dependent transporters in Rhizobium leguminosarum." Molecular Microbiology 84, no. 1 (March 2, 2012): 117–29. http://dx.doi.org/10.1111/j.1365-2958.2012.08014.x.

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Journal articles on the topic 'Rhizobium leguminosarum Molecular aspects'

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