Nodule-Specific Cysteine-Rich Peptides Negatively Regulate Nitrogen-Fixing Symbiosis in a Strain-Specific Manner in Medicago truncatula

Medicago truncatula shows a high level of specificity when interacting with its symbiotic partner Sinorhizobium meliloti. This specificity is mainly manifested at the nitrogen-fixing stage of nodule development, such that a particular bacterial strain forms nitrogen-fixing nodules (Nod+/Fix+) on one plant genotype but ineffective nodules (Nod+/Fix−) on another. Recent studies have just begun to reveal the underlying molecular mechanisms that control this specificity. The S. meliloti strain A145 induces the formation of Fix+ nodules on the accession DZA315.16 but Fix− nodules on Jemalong A17. A previous study reported that the formation of Fix− nodules on Jemalong A17 by S. meliloti A145 was conditioned by a single recessive allele named Mtsym6. Here we demonstrate that the specificity associated with S. meliloti A145 is controlled by multiple genes in M. truncatula, including NFS1 and NFS2 that encode nodule-specific cysteine-rich (NCR) peptides. The two NCR peptides acted dominantly to block rather than promote nitrogen fixation by S. meliloti A145. These two NCR peptides are the same ones that negatively regulate nitrogen-fixing symbiosis associated with S. meliloti Rm41.

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Inoculation with Efficient Nitrogen Fixing and Indoleacetic Acid Producing Bacterial Microsymbiont Enhance Tolerance of the Model LegumeMedicago truncatulato Iron Deficiency

BioMed Research International ◽

10.1155/2018/9134716 ◽

2018 ◽

Vol 2018 ◽

pp. 1-14 ◽

Cited By ~ 5

Author(s):

Nadia Kallala ◽

Wissal M’sehli ◽

Karima Jelali ◽

Zribi Kais ◽

Haythem Mhadhbi

Keyword(s):

Oxidative Stress ◽

Iron Deficiency ◽

Medicago Truncatula ◽

Sinorhizobium Meliloti ◽

Plant Biomass ◽

High Growth ◽

Fe Deficiency ◽

Nitrogen Fixing ◽

Bacterial Strains ◽

Negative Effect

The aim of this study was to assess the effect of symbiotic bacteria inoculation on the response ofMedicago truncatulagenotypes to iron deficiency. The present work was conducted on threeMedicago truncatulagenotypes: A17, TN8.20, and TN1.11. Three treatments were performed: control (C), direct Fe deficiency (DD), and induced Fe deficiency by bicarbonate (ID). Plants were nitrogen-fertilized (T) or inoculated with two bacterial strains:Sinorhizobium melilotiTII7 andSinorhizobium medicaeSII4. Biometric, physiological, and biochemical parameters were analyzed. Iron deficiency had a significant lowering effect on plant biomass and chlorophyll content in allMedicago truncatulagenotypes. TN1.11 showed the highest lipid peroxidation and leakage of electrolyte under iron deficiency conditions, which suggest that TN1.11 was more affected than A17 and TN8.20 by Fe starvation. Iron deficiency affected symbiotic performance indices of allMedicago truncatulagenotypes inoculated with bothSinorhizobiumstrains, mainly nodules number and biomass as well as nitrogen-fixing capacity. Nevertheless, inoculation withSinorhizobiumstrains mitigates the negative effect of Fe deficiency on plant growth and oxidative stress compared to nitrogen-fertilized plants. The highest auxin producing strain, TII7, preserves relatively high growth and root biomass and length when inoculated to TN8.20 and A17. On the other hand, both TII7 and SII4 strains improve the performance of sensitive genotype TN1.11 through reduction of the negative effect of iron deficiency on chlorophyll and plant Fe content. The bacterial inoculation improved Fe-deficient plant response to oxidative stress via the induction of the activities of antioxidant enzymes.

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MtBZR1 Plays an Important Role in Nodule Development in Medicago truncatula

International Journal of Molecular Sciences ◽

10.3390/ijms20122941 ◽

2019 ◽

Vol 20 (12) ◽

pp. 2941

Author(s):

Can Cui ◽

Hongfeng Wang ◽

Limei Hong ◽

Yiteng Xu ◽

Yang Zhao ◽

...

Keyword(s):

Medicago Truncatula ◽

Sinorhizobium Meliloti ◽

Normal Growth ◽

Dry Mass ◽

Growth Conditions ◽

Nodule Development ◽

Functional Study ◽

Loss Of Function ◽

Wild Type

Brassinosteroid (BR) is an essential hormone in plant growth and development. The BR signaling pathway was extensively studied, in which BRASSINAZOLE RESISTANT 1 (BZR1) functions as a key regulator. Here, we carried out a functional study of the homolog of BZR1 in Medicago truncatula R108, whose expression was induced in nodules upon Sinorhizobium meliloti 1021 inoculation. We identified a loss-of-function mutant mtbzr1-1 and generated 35S:MtBZR1 transgenic lines for further analysis at the genetic level. Both the mutant and the overexpression lines of MtBZR1 showed no obvious phenotypic changes under normal growth conditions. After S. meliloti 1021 inoculation, however, the shoot and root dry mass was reduced in mtbzr1-1 compared with the wild type, caused by partially impaired nodule development. The transcriptomic analysis identified 1319 differentially expressed genes in mtbzr1-1 compared with wild type, many of which are involved in nodule development and secondary metabolite biosynthesis. Our results demonstrate the role of MtBZR1 in nodule development in M. truncatula, shedding light on the potential role of BR in legume–rhizobium symbiosis.

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Plant Nitrate Reductases Regulate Nitric Oxide Production and Nitrogen-Fixing Metabolism During the Medicago truncatula–Sinorhizobium meliloti Symbiosis

Frontiers in Plant Science ◽

10.3389/fpls.2020.01313 ◽

2020 ◽

Vol 11 ◽

Cited By ~ 2

Author(s):

Antoine Berger ◽

Alexandre Boscari ◽

Natasha Horta Araújo ◽

Mickaël Maucourt ◽

Mohamed Hanchi ◽

...

Keyword(s):

Nitric Oxide ◽

Medicago Truncatula ◽

Sinorhizobium Meliloti ◽

Nitric Oxide Production ◽

Nitrogen Fixing ◽

Oxide Production ◽

Nitrate Reductases

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Sinorhizobium meliloti Controls Nitric Oxide–Mediated Post-Translational Modification of a Medicago truncatula Nodule Protein

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-05-15-0118-r ◽

2015 ◽

Vol 28 (12) ◽

pp. 1353-1363 ◽

Cited By ~ 21

Author(s):

Pauline Blanquet ◽

Liliana Silva ◽

Olivier Catrice ◽

Claude Bruand ◽

Helena Carvalho ◽

...

Keyword(s):

Nitric Oxide ◽

Nitrogen Fixation ◽

Medicago Truncatula ◽

Sinorhizobium Meliloti ◽

Molecular Mechanisms ◽

Root Nodules ◽

Plant Protein ◽

Post Translational Modification ◽

Model Legume ◽

Bacterial Mutants

Nitric oxide (NO) is involved in various plant-microbe interactions. In the symbiosis between soil bacterium Sinorhizobium meliloti and model legume Medicago truncatula, NO is required for an optimal establishment of the interaction but is also a signal for nodule senescence. Little is known about the molecular mechanisms responsible for NO effects in the legume-rhizobium interaction. Here, we investigate the contribution of the bacterial NO response to the modulation of a plant protein post-translational modification in nitrogen-fixing nodules. We made use of different bacterial mutants to finely modulate NO levels inside M. truncatula root nodules and to examine the consequence on tyrosine nitration of the plant glutamine synthetase, a protein responsible for assimilation of the ammonia released by nitrogen fixation. Our results reveal that S. meliloti possesses several proteins that limit inactivation of plant enzyme activity via NO-mediated post-translational modifications. This is the first demonstration that rhizobia can impact the course of nitrogen fixation by modulating the activity of a plant protein.

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Rhizobium meliloti exopolysaccharides: genetic analyses and symbiotic importance

Biochemical Society Transactions ◽

10.1042/bst0190636 ◽

1991 ◽

Vol 19 (3) ◽

pp. 636-644 ◽

Cited By ~ 9

Author(s):

T. Lynne Reuber ◽

Jason Reed ◽

Jane Glazebrook ◽

M. Alexandra Glucksmann ◽

Dianne Ahmann ◽

...

Keyword(s):

Rhizobium Meliloti ◽

Nodule Development ◽

Nitrogen Fixing ◽

Free Living ◽

Genetic Analyses ◽

Living State ◽

Meliloti Strain

Summary Genetic experiments have indicated that succinoglycan (EPS I), the acidic Calcofluor-binding exopolysaccharide, of the nitrogen-fixing bacterium Rhizobium meliloti strain Rm1021 is required for nodule invasion and possibly for later events in nodule development on alfalfa and other hosts. Fourteen exo loci on the second megaplasmid have been identified that are required for, or affect, the synthesis of EPS I. Mutations in certain of these loci completely abolish the production of EPS I and result in mutants that form empty Fix- nodules. We have identified two loci, exoR and exoS, that are involved in the regulation of EPS I synthesis in the free-living state. Certain exo mutations which completely abolish EPS I production are lethal in an exoR95 or exoS96 background. Histochemical analyses of the expression of exo genes during nodulation using exo :: TnphoA fusions have indicated that the exo genes are expressed most strongly in the invasion zone. In addition, we have discovered that R. meliloti has a latent capacity to synthesize a second exopolysaccharide (EPS II) that can substitute for the role(s) of EPS I in nodulation of alfalfa but not of other hosts. Possible roles for exopolysaccharides in symbiosis are discussed.

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Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain

Journal of Experimental Botany ◽

10.1093/jxb/erp140 ◽

2009 ◽

Vol 60 (11) ◽

pp. 3097-3107 ◽

Cited By ~ 148

Author(s):

C. Bianco ◽

R. Defez

Keyword(s):

Acetic Acid ◽

Salt Tolerance ◽

Medicago Truncatula ◽

Sinorhizobium Meliloti ◽

Meliloti Strain ◽

Indole 3 Acetic Acid

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Evidence that nano-TiO2 induces acute cytotoxicity to the agronomically beneficial nitrogen fixing bacteria Sinorhizobium meliloti

Canadian Journal of Microbiology ◽

10.1139/cjm-2021-0124 ◽

2021 ◽

Author(s):

Jieping Wang ◽

Yu Jia ◽

Joann K. Whalen ◽

Heather McShane ◽

Brian T. Driscoll ◽

...

Keyword(s):

Reactive Oxygen Species ◽

Sinorhizobium Meliloti ◽

Ultra Violet ◽

Oxygen Species ◽

Light Conditions ◽

Nitrogen Fixing ◽

Nano Tio2 ◽

Aqueous Dispersions ◽

Acute Cytotoxicity ◽

Meliloti Strain

When nano-sized titanium dioxide (nano-TiO2) absorbs ultra-violet (UV-A) radiation, it produces reactive oxygen species that can be toxic to bacteria. We used the agronomically beneficial nitrogen-fixing bacterium Sinorhizobium meliloti strain 1021 as a model microorganism to detect nano-TiO2 toxicity. S. meliloti was exposed to aqueous dispersions of micrometer-sized TiO2 (micron-TiO2, 44 μm) or nanometer-sized TiO2 (nano-TiO2, 21 nm) at nominal concentrations of 0, 100, 300, 600, 900 and 1800 mg TiO2/L. There were fewer viable S. meliloti after exposure to nano-TiO2 under dark and UV-A light conditions. Nano-TiO2 was more toxic to S. meliloti with UV-A irradiation (100% mortality at 100 mg TiO2/L) than under dark conditions (100% mortality at 900 mg TiO2/L). Micron-TiO2 concentrations less than 300 mg TiO2/L had no effect on the S. meliloti viability under dark or UV-A light conditions. Exposure to 600 mg/L or more of micron-TiO2 under UV-A light could also photo-kill S. meliloti cells (100% mortality). Further study is needed to ascertain whether nano-TiO2 interferes with the growth of N2-fixing microorganisms in realistic agricultural environments.

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