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PubMed2004

Control of nodule number by the phytohormone abscisic Acid in the roots of two leguminous species.

The effects of the phytohormone abscisic acid (ABA) on plant growth and root nodule formation were analyzed in Trifolium repense (white clover) and Lotus japonicus, which form indeterminate and determinate nodules, respectively. In T. repense, although the number of nodules formed after inoculation with Rhizobium leguminosarum bv. trifolii strain 4S (wild type) was slightly affected by exogenous ABA, those formed by strain H1(pC4S8), which forms ineffective nodules, were dramatically reduced 28 days after inoculation (DAI). At 14 and 21 DAI, the number of nodules formed with the wild-type strain was decreased by exogenous ABA. In L. japonicus, the number of nodules was also reduced by ABA treatment. Thus, exogenous ABA inhibits root nodule formation after inoculation with rhizobia. Observation of root hair deformation revealed that ABA blocked the step between root hair swelling and curling. When the ABA concentration in plants was decreased by using abamine, a specific inhibitor of 9-cis-epoxycarotenoid dioxygenase, the number of nodules on lateral roots of abamine-treated L. japonicus increased dramatically, indicating that lower-than-normal concentrations of endogenous ABA enhance nodule formation. We hypothesize that the ABA concentration controls the number of root nodules.

Abscisic Acid↗

PubMed1987

Rhizobium Population Genetics: Enzyme Polymorphism in Rhizobium leguminosarum from Plants and Soil in a Pea Crop.

A population of Rhizobium leguminosarum biovar viceae symbiotic on the roots of a commercial pea (Pisum sativum cv. Maro) crop was sampled by extracting a total of 249 isolates from root nodules on nine plants. Another 104 isolates were obtained by using soil from the same site to inoculate test plants, and a further 86 isolates were similarly obtained from soil 20 m distant within the crop. Each isolate was characterized for mobility variants of the enzymes glucose-6-phosphate dehydrogenase, superoxide dismutase, and beta-galactosidase by polyacrylamide gel electrophoresis. All three enzymes were polymorphic, and there was a strong disequilibrium among them. Of the 15 observed combinations of alleles (electrophoretic types [ETs]), 12 were indistinguishable from those previously described for isolates from a site 25 km distant. ET frequencies were significantly different among isolates from nodules on primary roots as opposed to lateral roots. The population on each individual plant was very diverse, but ET frequencies were similar from plant to plant. The ETs nodulating the primary roots were almost, although not perfectly, mixed, since the incidence of the same ETs in adjacent nodules was only about twice that expected by chance. The two samples derived from soil had the same ET frequencies but were significantly different from the field nodule sample, although the level of diversity was similar and there were no new ETs.

Journal Article↗

PubMed1977

Ultrastructural and immunological demonstration of the nodulation of the European Alnus glutinosa (L.) Gaertn. host plant by the North-American Alnus crispa var. mollis Fern. root nodule endophyte.

The inoculation of the European Alnus glutinosa (L.) Gaertn. host plant by a crushed-nodule inoculum, prepared with the North-American Alnus crispa var. mollis Fern. root nodule, was successful. Fluorescein- and ferritin-labelled antibodies, specific against the A. crispa var. mollis root nodule endophyte (Lalonde et al. 1975), demonstrated the idenity of this endophyte in the resulting nodules. The nodulation process of this abnormal host-endophyte system was studied by light and electron microscopy. An excretion of host blebs containing electron-dense polysaccharide material, resulting in the formation of exo-encapsulation threads containing presumptive endophytic bacterial cells, was associated with deformed root hairs. Originating from an exoencapsulation thread, the endophyte penetrates the root hair cell and then migrates as a hypha toward the cortical cells of the root. Its migration in the cortical cells of the primary nodule results in the induction of a lateral root which develops as the true nodule. The ultrastructure of the A. crispa var. mollis endophyte developing in the primary and true nodule of the abnormal A. glutinosa host was similar to the one induced inside its normal A. crispa var. mollis host. The actinomycetal intruder was a branched and septate hypha able to produce septate vesicles. The endophyte was always encapsulated in an electron-dense polysaccharide material surrounded by a host plasma membrane envelope. However, in this abnormal host-endophyte system, the number of primary nodules formed per root system was drastically reduced, and their appearance was delayed by 1 to 2 weeks. The delayed nodules were effective in fixing nitrogen and able to support satisfactory plant growth in a nitrogen-free medium.

Antigens, Bacterial↗

PubMed2026

Mesorhizobium bavaricum sp. nov. and Mesorhizobium monacense sp. nov., two novel Lotus-associated species harbouring symbiotic plasmids.

Legumes establish a mutualistic interaction with nitrogen-fixing rhizobia. Lotus japonicus is a model for studying this symbiosis; however, only a limited number of rhizobial species nodulating this host have been taxonomically described. Here, we characterise four Mesorhizobium strains (DC-1.1T, Qj1B1, DC-1.5T, and Qj2B2) isolated from root nodules of Lotus japonicus and Lotus burttii. Multi-locus phylogeny and phylogenomic analyses resolved these isolates into two well-supported monophyletic clades. Genome-based comparisons supported their classification as distinct taxa, with strains DC-1.1T and Qj1B1 showing 95.2% average nucleotide identity (ANI) and 62.9-63.5% digital DNA-DNA hybridisation (dDDH) values relative to Mesorhizobium newzealandense ICMP 19545T, whereas DC-1.5T and Qj2B2 exhibited 92.5-92.8% ANI and 49.9-50.5% dDDH compared with Mesorhizobium waimense ICMP 19557T. Together with chemotaxonomic and physiological traits, these data support the proposal of two novel species, Mesorhizobium bavaricum sp. nov. (DC-1.1T and Qj1B1) and Mesorhizobium monacense sp. nov. (DC-1.5T and Qj2B2). Metagenomic analyses predicted high environmental prevalence for these novel taxa, particularly within soil habitats. Isolates DC-1.1T, Qj1B1, and DC-1.5T effectively nodulated Lotus burttii and significantly promoted plant growth, whereas Qj2B2 neither nodulated nor enhanced growth. Comparative genomic analysis revealed that the nodulating isolates harbour symbiotic genes (nod, fix, and nif) on symbiotic plasmids, a rare feature in Mesorhizobium strains, whereas Qj2B2 lacks essential nod and nif genes. Consistent with these genomic features, symbiotaxonomic analysis assigned the nodulating isolates to symbiovar loti. These results highlight the potential of these isolates as models for comparative analyses of symbiotic plasmid evolution and horizontal gene transfer.

Mesorhizobium↗

PubMed2004

[Recent advances in research and application of associated nitrogen-fixation with graminaceous plants].

The category, characteristic of diazotrophs isolated from inside and/or rhizosphere of graminaceous plants in recent year and the mechanism of the promoting effects on their host plant were reviewed in this paper. The current status of application of associative nitrogen-fixation inoculants and the problems in inoculation were discussed. It was indicated that the main factors influencing the effects of inoculants include the competition of indigenous micro-organism with inoculants for nutritions and energy, difference of host plant genotypes in associative relationship, and variance of environmental conditions such as the concentration of ammonium in soil solution and the oxygen partial pressure in soil air. The trends of future research in this field were prospected, for example, to isolate and identify the high nitrogen fixing efficiency strains with wider environmental adaptability, to create associative nitrogen fixing bacteria strain which is able to bear or endure higher concentration of ammonium by gene engineering technique, to induce graminaceous plant forming root nodule for nitrogen fixation and to exert the predominance of endophytic diazotrophs.

Acetobacter↗

PubMed1995

Uridine, a cell division factor in pea roots.

Nodulation (root nodule formation) in legume roots is initiated by the induction of cell divisions and formation of root nodule primordia in the plant root cortex, usually in front of the protoxylem ridges of the central root cylinder. We isolated a factor from the central cylinder (stele) of pea roots which enhances hormone-induced cell proliferation in root cortex explants at positions similar to those of nodule primordia. The factor was identified as uridine. Uridine may act as a morphogen in plant roots at picomolar concentrations.

Cell Division↗

PubMed2025

Nodules-associated Klebsiella oxytoca complex: genomic insights into plant growth promotion and health risk assessment.

The swift emergence of antibiotic resistance genes (ARGs) across interconnected One Health compartments poses a significant global threat. Although plant growth-promoting (PGP) bacteria possess numerous attributes beneficial to host plants, many of these bacteria also harbor ARGs, necessitating a focused assessment of their negative implications. In this context, here we performed whole genome sequencing of 14 PGP endophytic strains isolated from root nodules of faba beans, belonging to three Klebsiella oxytoca species complex (KoSC): K. grimontii (n = 5), K. michiganensis (n = 5), and K. pasteurii (n = 4). We performed comparative genomics, molecular typing, and pangenome analyses on these strains. We identified significant diversity within the KoSC population, classifying the strains into five sequence types (STs), three of which are novel to this study (ST-542, ST-569, and ST-629). Phylogenomic analysis revealed that the bacterial strains clustered more closely by ST than by their source of isolation. Annotation of gene clusters indicated that all assembled genomes are enriched with genes involved in PGP activities, alongside a robust array of genes conferring tolerance to abiotic stresses. Importantly, our findings disclosed that the 14 assembled genomes harbored multiple ARGs, conferring resistance to various antibiotic classes, with 71% of the population classified as multidrug-resistant based on the in vitro antibiotic susceptibility assay. Furthermore, all genomes contained an array of virulence factors critical for survival, pathogenesis, biofilm formation, and root colonization. In conclusion, this study substantiates the hypothesis that certain PGP bacteria may serve as potential reservoirs of multidrug resistance, posing significant public health risks. Thus, the future advancement of bacteria-based biofertilizers should integrate environmental considerations and monitor their impact on antibiotic resistance dissemination in soil ecosystems.

Klebsiella oxytoca↗

PubMedDate not supplied

[Evolution and phylogeny of rhizobia].

Nitrogen fixation an ancient process that may is have originated in the archaean Eon under the primitive atmosphere anoxygenic conditions. Diazotrophy is an exclusive process of prokaryotes, only Euryarchaeota and 6 of 54 Bacteria phyla have diazotrophs lineages. Some of them coevolved with flowering plants for the establishment of molecular bases of a mutualistic symbiosis relationship. In rhizobia, the nitrogen fixation occurs inside the nodules, special structures on the roots or stems of legumes. Nodule organogenesis starts with the bacterial nodulation factors (Nod factors) codified in large plasmids or symbiotic islands in the bacterial genomes. Nodulation genes had more recent origin than the nitrogen fixation ones because the origin of the nod gene is associated with the origin of the hosts. The 16S rRNA phylogeny groups rhizobia in 7 genuses of the alpha-Proteobacteria: Bradyrhizobium, Mesorhizobium, Rhizobium, Sinorhizobium, Methylobacterium and Devosia, and two genuses recently described in f-Proteobacteria: Burkholderia and Wautersia. The phylogenies obtained with other chromosomal genes are similar at the genus level, but it is incongruent with the symbiotic gene (nif & nod) phylogeny, because horizontal gene transfer has allowed their evolution in function to the legume host fitness.

Biodiversity↗

PubMed1991

The exoD gene of Rhizobium meliloti encodes a novel function needed for alfalfa nodule invasion.

During the symbiotic interaction between alfalfa and the nitrogen-fixing bacterium Rhizobium meliloti, the bacterium induces the formation of nodules on the plant roots and then invades these nodules. Among the bacterial genes required for nodule invasion are the exo genes, involved in production of an extracellular polysaccharide, and the ndv genes, needed for production of a periplasmic cyclic glucan. Mutations in the exoD gene result in altered exopolysaccharide production and in a nodule invasion defect. In this work we show that the stage of symbiotic arrest of exoD mutants is similar to that of other exo and ndv mutants. However, the effects of exoD mutations on exopolysaccharide production and growth on various media are different from the effects of other exo and ndv mutations. Finally, exoD mutations behave differently from other exo mutations in their ability to be suppressed or complemented extracellularly. The results suggest that exoD represents a new class of Rhizobium genes required for nodule invasion, distinct from the other exo genes and the ndv genes. We discuss models for the function of exoD.

Chromosomes, Bacterial↗

PubMed1998

Fusions between green fluorescent protein and beta-glucuronidase as sensitive and vital bifunctional reporters in plants.

By fusing the genes encoding green fluorescent protein (GFP) and beta-glucuronidase (GUS) we have created a set of bifunctional reporter constructs which are optimized for use in transient and stable expression studies in plants. This approach makes it possible to combine the advantage of GUS, its high sensitivity in histochemical staining, with the advantages of GFP as a vital marker. The fusion proteins were functional in transient expression studies in tobacco using either DNA bombardment or potato virus X as a vector, and in stably transformed Arabidopsis thaliana and Lotus japonicus plants. The results show that high level of expression does not interfere with efficient stable transformation in A. thaliana and L. japonicus. Using confocal laser scanning microscopy we show that the fusion constructs are very suitable for promoter expression studies in all organs of living plants, including root nodules. The use of these reporter constructs in the model legume L. japonicus offers exciting new possibilities for the study of the root nodulation process.

Arabidopsis↗

PubMed1993

Soybean nodulin-26 gene encoding a channel protein is expressed only in the infected cells of nodules and is regulated differently in roots of homologous and heterologous plants.

Nodulin-26 (N-26) is a major peribacteroid membrane protein in soybean root nodules. The gene encoding this protein is a member of an ancient gene family conserved from bacteria to humans. N-26 is specifically expressed in root nodules, while its homolog, soybean putative channel protein, is expressed in vegetative parts of the plant, with its highest level in the root elongation zone. Analysis of the soybean N-26 gene showed that its four introns mark the boundaries between transmembrane domains and the surface peptides, suggesting that individual transmembrane domains encoded by a single exon act as functional units. The number and arrangement of introns between N-26 and its homologs differ, however. Promoter analysis of N-26 was conducted in both homologous and heterologous transgenic plants. The cis-acting elements of the N-26 gene are different from those of the other nodulin genes, and no nodule-specific cis-acting element was found in this gene. In transgenic nodules, the expression of N-26 was detected only in the infected cells; no activity was found in nodule parenchyma and uninfected cells of the symbiotic zone. The N-26 gene is expressed in root meristem of transgenic Lotus corniculatus and tobacco but not in untransformed and transgenic soybean roots, suggesting the possibility that this nodulin gene is controlled by a trans-negative regulatory mechanism in homologous plants. This study demonstrates how a preexisting gene in the root may have been recruited for symbiotic function and brought under nodule-specific developmental control.

Amino Acid Sequence↗

PubMed2006

Siderophore cross-utilization amongst nodule isolates of the cowpea miscellany group and its effect on plant growth in the presence of antagonistic organisms.

Nodule isolates from the cowpea miscellany group of legumes produced varying concentrations of catecholate and hydroxamate types of siderophores under iron-limiting conditions. The nodule isolates differed with respect to siderophore cross-utilizing abilities; some were proficient at using siderophores of other nodule isolates (homologous siderophores) while others could utilize siderophores produced by other rhizospheric bacteria (heterologous siderophores). Utilization of siderophore of rhizospheric bacterium PsB, a plant pathogen, benefited the nodule isolate G11 in terms of growth under iron-limiting laboratory conditions, while PsB was clearly inhibited in the presence of G11. Plate assays showed that siderophore of G11 could withhold iron from PsB and hence PsB was inhibited in the presence of G11. Isolates G11 and PsB when applied simultaneously to peanut seedlings under sterile soil conditions, provided a clear advantage to the plant in terms of reduction in the inhibitory effect of PsB. The count of the nodule isolate G11 increased in the soil when co-inoculated with PsB, as compared to when inoculated alone. Thus, the increased growth of the plant can be attributed to the iron sequestration and plant growth promoting properties of G11. The isolate G11 could utilize the siderophores produced by many other rhizospheric isolates while the siderophore of G11 was not being utilized by these rhizospheric isolates.

Bacteria↗

PubMed2000

Characterizing the interaction between fire ants (Hymenoptera: Formicidae) and developing soybean plants.

This research characterizes the interaction between the fire ants Solenopsis invicta Buren and developing soybean plants. Phagostimulant studies showed that fire ant foraging on soybean seeds increased once the seeds imbibed water. During seedling development over a 5-d germination period, fire ant foraging shifted from the stem/cotyledons to the roots, despite continual increases in fresh weights for each region, and the fact that stem/cotyledon tissue contained the majority of food reserves. Carbohydrate analysis showed that although 2-d-old seedlings had higher concentrations of phagostimulant carbohydrates, especially sucrose, than tissues of mature plants, all tissues analyzed had enough of these sugars to induce a phagostimulant response. Fire ant association with seeds/seedlings germinated in soil resulted in reduced seedling vigor, as determined by a doubling of seedling emergence time, a threefold increase in malformed seedlings, and visible damage to cotyledons. Seeds germinated and grown to mature plants in association with fire ants, allocated 43% more assimilate into pods, but produced 28% less root dry matter, 11% less total dry matter, and there was an 81% reduction in the number of root nodules compared with control plants. We propose that reduced root development and inhibitions of nodule formation would be major yield limiting factors under field conditions. This work demonstrates that fire ant damage to soybeans is not limited to seedling establishment and that more research should be directed at the subterranean activities of the fire ant.

Animals↗

PubMed1999

A plant regulator controlling development of symbiotic root nodules.

Symbiotic nitrogen-fixing root nodules on legumes are founded by root cortical cells that de-differentiate and restart cell division to establish nodule primordia. Bacterial microsymbionts invade these primordia through infection threads laid down by the plant and, after endocytosis, membrane-enclosed bacteroids occupy cells in the nitrogen-fixing tissue of functional nodules. The bacteria excrete lipochitin oligosaccharides, triggering a developmental process that is controlled by the plant and can be suppressed. Nodule inception initially relies on cell competence in a narrow infection zone located just behind the growing root tip. Older nodules then regulate the number of nodules on a root system by suppressing the development of nodule primordia. To identify the regulatory components that act early in nodule induction, we characterized a transposon-tagged Lotus japonicus mutant, nin (for nodule inception), arrested at the stage of bacterial recognition. We show that nin is required for the formation of infection threads and the initiation of primordia. NIN protein has regional similarity to transcription factors, and the predicted DNA-binding/dimerization domain identifies and typifies a consensus motif conserved in plant proteins with a function in nitrogen-controlled development.

Amino Acid Sequence↗

PubMed2001

Effect of inoculation and leaf litter amendment on establishment of nodule-forming Frankia populations in soil.

High-N(2)-fixing activities of Frankia populations in root nodules on Alnus glutinosa improve growth performance of the host plant. Therefore, the establishment of active, nodule-forming populations of Frankia in soil is desirable. In this study, we inoculated Frankia strains of Alnus host infection groups I, IIIa, and IV into soil already harboring indigenous populations of infection groups (IIIa, IIIb, and IV). Then we amended parts of the inoculated soil with leaf litter of A. glutinosa and kept these parts of soil without host plants for several weeks until they were spiked with [(15)N]NO(3) and planted with seedlings of A. glutinosa. After 4 months of growth, we analyzed plants for growth performance, nodule formation, specific Frankia populations in root nodules, and N(2) fixation rates. The results revealed that introduced Frankia strains incubated in soil for several weeks in the absence of plants remained infective and competitive for nodulation with the indigenous Frankia populations of the soil. Inoculation into and incubation in soil without host plants generally supported subsequent plant growth performance and increased the percentage of nitrogen acquired by the host plants through N(2) fixation from 33% on noninoculated, nonamended soils to 78% on inoculated, amended soils. Introduced Frankia strains representing Alnus host infection groups IIIa and IV competed with indigenous Frankia populations, whereas frankiae of group I were not found in any nodules. When grown in noninoculated, nonamended soil, A. glutinosa plants harbored Frankia populations of only group IIIa in root nodules. This group was reduced to 32% +/- 23% (standard deviation) of the Frankia nodule populations when plants were grown in inoculated, nonamended soil. Under these conditions, the introduced Frankia strain of group IV was established in 51% +/- 20% of the nodules. Leaf litter amendment during the initial incubation in soil without plants promoted nodulation by frankiae of group IV in both inoculated and noninoculated treatments. Grown in inoculated, amended soils, plants had significantly lower numbers of nodules infected by group IIIa (8% +/- 6%) than by group IV (81% +/- 11%). On plants grown in noninoculated, amended soil, the original Frankia root nodule population represented by group IIIa of the noninoculated, nonamended soil was entirely exchanged by a Frankia population belonging to group IV. The quantification of N(2) fixation rates by (15)N dilution revealed that both the indigenous and the inoculated Frankia populations of group IV had a higher specific N(2)-fixing capacity than populations belonging to group IIIa under the conditions applied. These results show that through inoculation or leaf litter amendment, Frankia populations with high specific N(2)-fixing capacities can be established in soils. These populations remain infective on their host plants, successfully compete for nodule formation with other indigenous or inoculated Frankia populations, and thereby increase plant growth performance.

Actinomycetales↗

PubMed2006

Nitrogen-fixing sinorhizobia with Medicago laciniata constitute a novel biovar (bv. medicaginis) of S. meliloti.

Sixty-eight new rhizobial isolates were obtained from root-nodules of Medicago laciniata and from Mediterranean soils in Tunisia and France. All of them were identified as Sinorhizobium meliloti on the basis of PCR-RFLP analyses of 16S rDNA and the intergenic spacer sequence between 16S and 23S rDNAs. DNA/DNA hybridization, phenotypic characterization and 16S rRNA gene sequencing led to the conclusion that they belong the same taxon. All new isolates shared the ability to nodulate and fix nitrogen with M. laciniata except 11 of them not capable of fixing nitrogen with this plant and originating from French soils containing no efficiently adapted symbionts with M. laciniata. The nitrogen-fixing rhizobia on M. laciniata differed markedly from the other S. meliloti or Sinorhizobium medicae isolates and references in their symbiotic traits such as nifDK RFLP diversity, nodA sequences and nitrogen effectiveness with tree other different annual Medicago species (M. truncatula, M. polymorpha and M. sauvagei). Two infrasubspecific (biovar) divisions are therefore proposed within S. meliloti: bv. medicaginis for Sinorhizobium efficient on M. laciniata and bv. meliloti for the classically known S. meliloti group represented by the strains ATCC9930(T) and RCR 2011 efficient on M. sativa.

Acyltransferases↗

PubMed1998

Fusions between green fluorescent protein and beta-glucuronidase as sensitive and vital bifunctional reporters in plants.

Arabidopsis↗

PubMed2002

The Sinorhizobium meliloti stringent response affects multiple aspects of symbiosis.

Sinorhizobium meliloti and host legumes enter into a nitrogen-fixing, symbiotic relationship triggered by an exchange of signals between bacteria and plant. S. meliloti produces Nod factor, which elicits the formation of nodules on plant roots, and succinoglycan, an exopolysaccharide that allows for bacterial invasion and colonization of the host. The biosynthesis of these molecules is well defined, but the specific regulation of these compounds is not completely understood. Bacteria control complex regulatory networks by the production of ppGpp, the effector molecule of the stringent response, which induces physiological change in response to adverse growth conditions and can also control bacterial development and virulence. Through detailed analysis of an S. meliloti mutant incapable of producing ppGpp, we show that the stringent response is required for nodule formation and regulates the production of succinoglycan. Although it remains unknown whether these phenotypes are connected, we have isolated suppressor strains that restore both defects and potentially identify key downstream regulatory genes. These results indicate that the S. meliloti stringent response has roles in both succinoglycan production and nodule formation and, more importantly, that control of bacterial physiology in response to the plant and surrounding environment is critical to the establishment of a successful symbiosis.

Bacterial Proteins↗