Rhizobium meliloti mutants that fail to succinylate their Calcofluor-binding exopolysaccharide are defective in nodule invasion

Leigh, John A.; Reed, Jason W.; Hanks, Joanna F.; Hirsch, Ann M.; Walker, Graham C.

doi:10.1016/0092-8674(87)90127-9

Cited by 223 publications

(204 citation statements)

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“…Possible roles for the rhizobial exopolysaccharides in the symbiosis have been suggested by a number of authors, e.g., Bauer (1 981), Halverson and Stacey (1986), Chen and Rolfe (1987), Djordjevic et al (1987), Leigh et al (1987), Long (1989), andGlazebrook andWalker (1989). These roles include recognition of susceptible root hairs, protection of rhizobia from plant defense, functioning as a carrier of extracellular enzymes, forming the infection thread matrix, and functioning as a signal to the plant.…”

Section: Discussion Lnfection Thread Formation Of Alfalfa Nodules 1smentioning

confidence: 99%

“…Thirty plants were inoculated by this method. All plantlets formed exclusively ineffective nodules, which showed the typical empty nodule morphology (Finan et al, 1985;Leigh et al, 1987;Niehaus and Puhler, 1988;Muller et al, 1988). These results indicated that the nodulation mutant above the filter was unable to assist the infection mutant to invade alfalfa nodules.…”

Section: The Formation Of Alfalfa Nodules Infected By Lnf~epsã Nd Nodmentioning

confidence: 99%

“…The nodulation and host specificity genes have been identified and located on megaplasmid 1, the symbiotic plasmid of R. meliloti (Banfalvi et al, 1981;Rosenberg et al, 1981). In the second class are infection mutants (Inf-) that are capable of nodule formation, although the typical infection threads do not form (Finan et al, 1985;Leigh et al, 1987;Müller et al, 1988;Niehaus and Pühler, 1988;Putnoky et al, 1988). These nodules are termed empty nodules because the central nodule tissue is devoid of bacteroids.…”

Section: Introductionmentioning

confidence: 99%

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Cooperative Action of Rhizobium meliloti Nodulation and Infection Mutants during the Process of Forming Mixed Infected Alfalfa Nodules.

et al. 1990

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Alfalfa plants co-inoculated with Rhizobium meliloti nodulation (Nod-) and infection mutants deficient in exopolysaccharide production (Inf-EPS) formed mixed infected nodules that were capable of fixing atmospheric nitrogen. The formation of infected nodules was dependent on close contact between the inoculation partners. When the partners were separated by a filter, empt) Fix-nodules were formed, suggesting that infection thread formation in alfalfa is dependent on signals from the nodulation and infection genes. In rnixed infected nodules, both nodulation and infection mutants colonized the plant cells and differentiated into bacteroids. The formation of bacteroids was not dependent on cell-to-cell contact between the mutants. Immunogold/silver staining revealed that the ratio of the two mutants varied considerably in colonized plant cells following mixed inoculation. The introduction of an additional niflfix mutation into one of the inoculation partners did not abolish nitrogen fixation in mixed infected nodules. The expression of nif D::lacZ fusions additionally demonstrated that mutations in the nodulation and infection genes did not prevent the nif genes from being expressed in the mutant bacteroids.

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Section: Discussion Lnfection Thread Formation Of Alfalfa Nodules 1smentioning

confidence: 99%

Section: The Formation Of Alfalfa Nodules Infected By Lnf~epsã Nd Nodmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Cooperative Action of Rhizobium meliloti Nodulation and Infection Mutants during the Process of Forming Mixed Infected Alfalfa Nodules.

et al. 1990

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“…ExoY initiates the synthesis of the repeating unit, by transferring the galactosyl residue to the lipid carrier on the cytoplasmic side of the inner membrane 148 , and sugar transferases encoded by exoA, exoL, exoM, exoO, exoU and exoW subsequently elongate the octasaccharide backbone 148 . ExoZ, ExoH and ExoV transfer succinyl (Succ), acetyl (Ac) and pyruvyl (pyr) groups, respectively, to the growing backbone 149,150 . The mature repeating unit (linked to the lipid carrier) is flipped to the periplasmic side of the inner membrane, and then transferred to the growing polymer of succinoglycan by ExoP, ExoQ and ExoT 148,149,151 .…”

Section: Sinorhizobium Meliloti Succinoglycan Biosynthesismentioning

confidence: 99%

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

et al. 2007

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Nitrogen-fixing rhizobial bacteria and leguminous plants have evolved complex signal exchange mechanisms that allow a specific bacterial species to induce its host plant to form invasion structures through which the bacteria can enter the plant root. Once the bacteria have been endocytosed within a host-membrane-bound compartment by root cells, the bacteria differentiate into a new form that can convert atmospheric nitrogen into ammonia. Bacterial differentiation and nitrogen fixation are dependent on the microaerobic environment and other support factors provided by the plant. In return, the plant receives nitrogen from the bacteria, which allows it to grow in the absence of an external nitrogen source. Here, we review recent discoveries about the mutual recognition process that allows the model rhizobial symbiont Sinorhizobium meliloti to invade and differentiate inside its host plant alfalfa (Medicago sativa) and the model host plant barrel medic (Medicago truncatula).The recent completion of the Sinorhizobium meliloti genome sequence, and the progress towards the completion of the Medicago truncatula genome sequence, have led to a surge in the molecular characterization of the determinants that are involved in the development of the symbiosis between rhizobial bacteria and leguminous plants. Aromatic compounds from legumes called flavonoids first signal the rhizobial bacteria to produce lipochitooligosaccharide compounds called Nod factors 1 . Nod factors that are secreted by the bacteria activate multiple responses in the host plant that prepare the plant to receive the invading bacteria. Nod factors and symbiotic exopolysaccharides induce the plant to form infection threads, which are thin tubules filled with bacteria that penetrate into the plant cortical tissue and deliver the bacteria to their target cells. Plant cells in the inner cortex internalize the invading bacteria in host-membrane-bound compartments that mature into structures known Correspondence to G.C.W. gwalker@mit.edu. Competing interests statementThe authors declare no competing financial interests. DATABASES Invasion of plant rootsAlthough plant roots are exposed to various micro-organisms in the soil, their cell walls form a strong protective barrier against most harmful species. The early steps in the invasion of barrel medic (M. truncatula) and alfalfa (Medicago sativa) roots by S. meliloti are characterized by the reciprocal exchange of signals that allow the bacteria to use the plant root hair cells as a means of entry. Initial signal exchangeFlavonoid compounds (2-phenyl-1,4-benzopyrone derivatives) produced by leguminous plants are the first signals to be exchanged by host-rhizobial symbiont pairs 1 (FIG. 1). Flavonoids bind bacterial NodD proteins, which are members of the LysR family of transcriptional regulators, and activate these proteins to induce the transcription of rhizobial genes 1,2 . For example, the M. sativa-derived flavonoid luteolin stimulates binding of an active form of NodD1 to an S. meliloti 'nod-box' p...

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“…We also wanted to find a gene that could serve as an early genetic marker for studies on signal exchange between R. meliloti and its host. Alfalfa offers the advantage that it has been well studied with regard to points of nodule arrest following inoculation with various invasion-defective R. meliloti mutants, especially the exopolysaccharide ( e m ) mutants (Finan et al, 1985;Leigh et al, 1987;Yang et al, 1992). It also can be transformed using Agrobacterium-derived vectors (Deak et al, 1986).…”

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confidence: 99%

A Gene That Encodes a Proline-Rich Nodulin with Limited Homology to PsENOD12 Is Expressed in the Invasion Zone of Rhizobium meliloti-Induced Alfalfa Root Nodules

Löbler

Hirsch

1993

Plant Physiol.

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~ ~~~To define the early stages of the interaction between Rhizobium and host legumes, we have cloned and characterized three early nodulin-encoding sequences from an alfalfa (Medicago sativa 1.) cDNA library by probing with a fragment of a cDNA clone for PsENOD12, an infection-related nodulin from pea (Pisum sativum 1.). Although the coding regions of the three clones are 95 to 98% homologous to each other, they are only 43% homologous to the pea clone. However, the putative signal peptide encoded by the alfalfa cDNA clones is 100% homologous to the PsENOD12 signal peptide. The spatial and temporal expression patterns of PsENODl2 and the alfalfa clones were compared. In situ hybridization experiments detected RNA transcripts in the invasion zone of mature nitrogen-fixing nodules, the same site where PsENODl2 mRNAs are found. Transcripts were also found by in situ hybridization in cells of Rhizobium meliloti exoH mutant-induced nodules penetrated by infection threads, but northern analysis did not detect transcripts in Inf-(infection thread minus) nodules elicited by R. meliloti ex06 nodules or in pseudonodules elicited by treatment with the auxin transport inhibitor N-1-(naphthy1)phthalamic acid. In addition, the alfalfa gene represented by these cDNA clones exhibited a temporal expression pattern that differed from that of PsENOD12, which is transiently expressed. These data, plus information derived from Southern blot analysis, indicate that we have isolated cDNA clones for a novel early nodulin, which we have designated MsENODlO (Medicago sativa Early Nodulin 10).

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Rhizobium meliloti mutants that fail to succinylate their Calcofluor-binding exopolysaccharide are defective in nodule invasion

Cited by 223 publications

References 26 publications

Cooperative Action of Rhizobium meliloti Nodulation and Infection Mutants during the Process of Forming Mixed Infected Alfalfa Nodules.

Cooperative Action of Rhizobium meliloti Nodulation and Infection Mutants during the Process of Forming Mixed Infected Alfalfa Nodules.

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

A Gene That Encodes a Proline-Rich Nodulin with Limited Homology to PsENOD12 Is Expressed in the Invasion Zone of Rhizobium meliloti-Induced Alfalfa Root Nodules

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