Metabolic changes of rhizobia in legume nodules

Prell, Jürgen; Poole, Philip S.

doi:10.1016/j.tim.2006.02.005

Cited by 248 publications

(214 citation statements)

References 61 publications

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“…In indeterminate nodules, the internalized bacteria and the symbiosome membrane divide concomitantly before bacteroid differentiation, whereas in determinate nodules, bacteria divide within the membrane compartment and form a small mass of cells 88 . Surprisingly, plants that form indeterminate nodules impose a programme of genomic endoreduplication on the invading bacterial cells 65 .…”

Section: Lps and Rhizobial Survivalmentioning

confidence: 99%

Section: Box 3 Host Invasion Parallels Between Rhizobia and Animal Pamentioning

confidence: 99%

“…Once secreted, it is thought to be taken up by the plant through NH 4 + channels that have been detected in the peribacteroid membrane and then assimilated 88,102 . A complex amino-acid cycling system between plant cells and bacteroids might prevent the bacteroids from assimilating NH 4 + , and allow NH 4 + to be secreted for uptake by the plant 88,101,103,104 . Metabolite analysis and RNAi depletion experiments suggest that NH 4 + assimilation by plant cells occurs primarily through glutamine and asparagine synthetases [105][106][107] .…”

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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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Section: Lps and Rhizobial Survivalmentioning

confidence: 99%

Section: Box 3 Host Invasion Parallels Between Rhizobia and Animal Pamentioning

confidence: 99%

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How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

et al. 2007

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“…In nodules of galegoid legumes (a clade in the subfamily Papilionoideae, such as Medicago, Pisum, or Vicia), bacteria undergo dramatic increases in size, shape, and DNA content (3) before they start to reduce N 2 . Plants provide differentiated bacteria (bacteroids) with dicarboxylic acids, which energize N 2 reduction to ammonium for secretion back to the plant (4).…”

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confidence: 99%

Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids

Prell

White

Bourdès

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

175

160

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One of the largest contributions to biologically available nitrogen comes from the reduction of N 2 to ammonia by rhizobia in symbiosis with legumes. Plants supply dicarboxylic acids as a carbon source to bacteroids, and in return they receive ammonia. However, metabolic exchange must be more complex, because effective N 2 fixation by Rhizobium leguminosarum bv viciae bacteroids requires either one of two broad-specificity amino acid ABC transporters (Aap and Bra). It was proposed that amino acids cycle between plant and bacteroids, but the model was unconstrained because of the broad solute specificity of Aap and Bra. Here, we constrain the specificity of Bra and ectopically express heterologous transporters to demonstrate that branched-chain amino acid (LIV) transport is essential for effective N 2 fixation. This dependence of bacteroids on the plant for LIV is not due to their known down-regulation of glutamate synthesis, because ectopic expression of glutamate dehydrogenase did not rescue effective N 2 fixation. Instead, the effect is specific to LIV and is accompanied by a major reduction in transcription and activity of LIV biosynthetic enzymes. Bacteroids become symbiotic auxotrophs for LIV and depend on the plant for their supply. Bacteroids with aap bra null mutations are reduced in number, smaller, and have a lower DNA content than wild type. Plants control LIV supply to bacteroids, regulating their development and persistence. This makes it a critical control point for regulation of symbiosis.mutualism ͉ nitrogen fixation ͉ peas ͉ symbiosis T he largest input of available nitrogen in the biosphere comes from biological reduction of atmospheric N 2 to ammonium (1). Most of this comes from legume-Rhizobium symbioses, arising from infection of host plants and resulting in root structures called nodules (2). These symbioses are initiated by plant-released flavonoids and related compounds, which elicit synthesis of lipochitooligosaccharide Nod factors by rhizobia. Bacteria are trapped by curling root hairs that they enter via infection threads. These grow into the root cortex, into a zone of newly induced meristematic cells forming the origin of the nodule. Bacteria are released from infection threads by endocytosis and are surrounded by a plant-derived symbiosome membrane. In nodules of galegoid legumes (a clade in the subfamily Papilionoideae, such as Medicago, Pisum, or Vicia), bacteria undergo dramatic increases in size, shape, and DNA content (3) before they start to reduce N 2 . Plants provide differentiated bacteria (bacteroids) with dicarboxylic acids, which energize N 2 reduction to ammonium for secretion back to the plant (4).A simple exchange of dicarboxylates and ammonium is the classical model of nutrient exchange in nodules, but amino acid transport by bacteroids has also been shown to be essential (5). Rhizobium leguminosarum mutated in 2 broad-specificity amino acid ABC transporters (Aap and Bra) formed N 2 -fixing pea bacteroids that appeared morphologically normal in electron micrographs,...

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“…It is within the symbiosomes that the bacteria fix nitrogen in the form of ammonia, which is then released to the host plant (Brewin, 1991). In addition, it has been proposed that nitrogen fixation requires the cycling of amino acids between the bacteroid and plant compartments (Lodwig et al, 2003;Prell & Poole, 2006). However, more recently, Prell et al (2009) have emphasized that plants control branched-chain amino acid (BCAA) supply to bacteroids, regulating their development and persistence, at least in the symbioses of Rhizobium leguminosarum with Pisum sativum and Phaseolus vulgaris (Prell et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Biosynthesis of branched-chain amino acids is essential for effective symbioses between betarhizobia and Mimosa pudica

et al. 2012

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ROCBurkholderia phymatum STM815 and Cupriavidus taiwanensis LMG19424 are betaproteobacterial strains that can effectively nodulate several species of the large legume genus Mimosa. A Tn5 mutant, derived from B. phymatum STM815 (KM60), and another derived from C. taiwanensis LMG19424 (KM184-55) induced Fix " nodules on Mimosa pudica. The Tn5-interrupted genes of the mutants showed strong homologies to ilvE, which encodes a branchedchain amino acid aminotransferase, and leuC, which encodes the large subunit of isopropylmalate isomerase. Both enzymes are known to be involved in the biosynthetic pathways for branchedchain amino acids (BCAAs) (leucine, valine and isoleucine). The B. phymatum ilvE mutant, KM60, was not auxotrophic for BCAAs and could grow well on minimal medium with pyruvate as a carbon source and ammonia as a nitrogen source. However, it grew less efficiently than the wildtype (WT) strain when ammonia was substituted with valine or isoleucine as a nitrogen source. The BCAA aminotransferase activity of KM60 was significantly reduced relative to the WT strain, especially with isoleucine and valine as amino group donors. The C. taiwanensis leuC mutant, KM184-55, could not grow on a minimal medium with pyruvate as a carbon source and ammonia as a nitrogen source, but its growth was restored when leucine was added to the medium. The isopropylmalate isomerase activity of KM184-55 was completely lost compared with the WT strain. Both mutants recovered their respective enzyme activities after complementation with the WT ilvE or leuC genes and were subsequently able to grow as well as their parental strains on minimal medium. They were also able to form nitrogen-fixing nodules on M. pudica. We conclude that the biosynthesis of BCAAs is essential for the free-living growth of betarhizobia, as well as for their ability to form effective symbioses with their host plant.

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Metabolic changes of rhizobia in legume nodules

Cited by 248 publications

References 61 publications

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids

Biosynthesis of branched-chain amino acids is essential for effective symbioses between betarhizobia and Mimosa pudica

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