Functions of Rhizobial Nodulation Genes

Downie, J. A.

doi:10.1007/978-94-011-5060-6_20

Cited by 75 publications

(57 citation statements)

References 162 publications

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“…Specialized secretion systems for NF delivery have been proposed (Downie, 1998), that could account for the ability of live bacteria to elicit host responses not seen with purified NF. Several candidate secretory proteins have been identified in Rhizobium.…”

Section: The Sensitivity Of Calcium Spiking Led To the Detection Of Dmentioning

confidence: 99%

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Structure-Function Analysis of Nod Factor-Induced Root Hair Calcium Spiking in Rhizobium-Legume Symbiosis

Wais¹,

Keating

Long

2002

Plant Physiology

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In the Rhizobium-legume symbiosis, compatible bacteria and host plants interact through an exchange of signals: Host compounds promote the expression of bacterial biosynthetic nod (nodulation) genes leading to the production of a lipochito-oligosaccharide signal, the Nod factor (NF). The particular array of nod genes carried by a given species of Rhizobium determines the NF structure synthesized and defines the range of legume hosts by which the bacterium is recognized. Purified NF can induce early host responses even in the absence of live Rhizobium One of the earliest known host responses to NF is an oscillatory behavior of cytoplasmic calcium, or calcium spiking, in root hair cells, initially observed in Medicago spp. and subsequently characterized in four other genera (D.W. Ehrhardt, R. Wais, S.R. Long [1996] Cell 85: 673-681; S.A. Walker, V. Viprey, J.A. Downie [2000] Proc Natl Acad Sci USA 97: 13413-13418; D.W. Ehrhardt, J.A. Downie, J. Harris, R.J. Wais, and S.R. Long, unpublished data). We sought to determine whether live Rhizobium trigger a rapid calcium spiking response and whether this response is NF dependent. We show that, in the Sinorhizobium melilotiMedicago truncatula interaction, bacteria elicit a calcium spiking response that is indistinguishable from the response to purified NF. We determine that calcium spiking is a nod gene-dependent host response. Studies of calcium spiking in M. truncatula and alfalfa (Medicago sativa) also uncovered the possibility of differences in early NF signal transduction. We further demonstrate the sufficiency of the nod genes for inducing calcium spiking by using Escherichia coli BL21 (DE3) engineered to express 11 S. meliloti nod genes.The Rhizobium-legume interaction initiates the development of a novel organ on the root of the host plant, the nodule, and its colonization by the bacteria, resulting in a nitrogen-fixing symbiosis. Within the first 12 to 24 h, bacteria trigger a series of microscopically visible morphological changes. In the epidermis, altered growth of root hair cells (root hair deformation) is followed by root hair curling. Bacteria concurrently induce renewed cortical cell division that will lead to the formation of a root nodule. Invasion structures, called infection threads, initiate within curled root hairs and grow into the developing nodule. Bacteria are eventually released from infection threads into the cells of the nodule, where they begin fixing nitrogen. Thus, in a compatible interaction, Rhizobium elicits root hair deformation and curling, infection thread development, and cell division in the root cortex leading to nodule formation. These morphological responses are considered to be the hallmarks of nodulation.Nodulation occurs only when compatible species of legumes and Rhizobium come into contact. Thus, Sinorhizobium meliloti interacts with Medicago spp. but not Vicia spp., which in turn form nodules in the presence of Rhizobium leguminosarum bv viciae. The specificity of the interaction is based on a reciprocal exchange of sig...

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Section: The Sensitivity Of Calcium Spiking Led To the Detection Of Dmentioning

confidence: 99%

“…Several candidate secretory proteins have been identified in Rhizobium. Mutation of genes such as nodIJ in R. leguminosarum species can cause delayed nodulation (Downie, 1998). Similar mutations in S. meliloti, however, have no effect on nodulation kinetics (Jacobs et al, 1985).…”

Section: The Sensitivity Of Calcium Spiking Led To the Detection Of Dmentioning

confidence: 99%

Structure-Function Analysis of Nod Factor-Induced Root Hair Calcium Spiking in Rhizobium-Legume Symbiosis

Wais¹,

Keating

Long

2002

Plant Physiology

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“…M. ciceri failed to give an amplification product, while M. loti and M. tianshanense produced an expected 800 bp PCR product (data not shown). This indicates that M. ciceri may not have an intS adjacent to a phenylalanine tRNA as found in the Biserrula mesorhizobia.The nodulation gene nodA determines the type of N-acyl substitution transferred onto the oligosaccharide backbone of Nod factor and thus plays a significant role in determining the symbiotic specificity of root-nodule bacteria (Downie, 1998). A 567 bp intragenic fragment of nodA was sequenced for Biserrula mesorhizobial strains WSM1271, WSM1283, WSM1284 and WSM1497 (Nandasena et al, 2006), and there was <78.6 % sequence similarity between the nodA sequences of Biserrula mesorhizobia and that of the type strain of M. ciceri.…”

mentioning

confidence: 99%

Mesorhizobium ciceri biovar biserrulae, a novel biovar nodulating the pasture legume Biserrula pelecinus L.

Nandasena

O’Hara

Tiwari

et al. 2007

International Journal of Systematic and Evolutionary Microbiology

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Biserrula pelecinus L. is a pasture legume species that forms a highly specific nitrogen-fixing symbiotic interaction with a group of bacteria that belong to Mesorhizobium. These mesorhizobia have >98.8 % sequence similarity to Mesorhizobium ciceri and Mesorhizobium loti for the 16S rRNA gene (1440 bp) and >99.3 % sequence similarity to M. ciceri for the dnaK gene (300 bp), and strain WSM1271 has 100 % sequence similarity to M. ciceri for GSII (600 bp). Strain WSM1271 had 85 % relatedness to M. ciceri LMG 14989 T and 50 % relatedness to M. loti LMG 6125 T when DNA-DNA hybridization was performed. WSM1271 also had a similar cellular fatty acid profile to M. ciceri. These results are strong evidence that the Biserrula mesorhizobia and M. ciceri belong to the same group of bacteria. Significant differences were revealed between the Biserrula mesorhizobia and M. ciceri in growth conditions, antibiotic resistance and carbon source utilization. The G+C content of the DNA of WSM1271 was 62.7 mol%, compared to 63-64 mol% for M. ciceri. The Biserrula mesorhizobia contained a plasmid (~500 bp), but the symbiotic genes were detected on a mobile symbiosis island and considerable variation was present in the symbiotic genes of Biserrula mesorhizobia and M. ciceri. There was <78.6 % sequence similarity for nodA and <66.9 % for nifH between Biserrula mesorhizobia and M. ciceri. Moreover, the Biserrula mesorhizobia did not nodulate the legume host of M. ciceri, Cicer arietinum, and M. ciceri did not nodulate B. pelecinus. These significant differences observed between Biserrula mesorhizobia and M. ciceri warrant the proposal of a novel biovar for Biserrula mesorhizobia within M. ciceri. The name Mesorhizobium ciceri biovar biserrulae is proposed, with strain WSM1271 (=LMG 23838=HAMBI 2942) as the reference strain.Biserrula pelecinus L. is an annual herbaceous legume suited to arid land, which is rapidly gaining popularity as a forage species in Australia (Howieson et al., 1995(Howieson et al., , 2000Loi et al., 2005). The Mediterranean basin is the centre of origin of this monospecific genus (Allen & Allen, 1981). B. pelecinus forms a highly specific nitrogen-fixing symbiotic association with bacteria that have been classified within the genus Mesorhizobium (Howieson et al., 1995; Nandasena et al., 2001 Nandasena et al., , 2004 The locus dnaK encodes a highly conserved chaperone protein with multiple cellular functions, and this gene has proven to be a useful diagnostic tool for root-nodule bacteria (Stepkowski et al., 2003;Eardly et al., 2005). A 300 bp intragenic fragment from the variable region of dnaK was amplified and sequenced using the primers TSdnaK2 and TSdnaK3 (Stepkowski et al., 2003 and WSM1540) differed by only 1 or 2 bp. These Biserrula mesorhizobia had >99.3 % sequence similarity to M. ciceri and <91.9 % sequence similarity to M. loti and, as a consequence, all 14 Biserrula mesorhizobia given in Table 1 clustered with M. ciceri when a phylogenetic tree was developed (not shown) using the available partial dna...

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“…Many of the components of the nodulation process can be triggered by chemical signals synthesized by the bacterium, termed Nod factors (NFs) (10)(11)(12). These bacterial signals are lipochitooligosaccharides synthesized through the action of bacterial nod genes; they feature an N-acetyl D-glucosamine backbone modified by residues that confer specificity of action on particular host plants (13,14). The host plant responds to bacterial NFs by diverse molecular and cellular events, including deformed growth of root hairs, reinitiation of mitoses in root cortical cells, and expression of several genes called early nodulins, or ENODs, in the epidermis, cortex, and pericycle of the root (for a recent review, see ref.…”

mentioning

confidence: 99%

Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula

Wais

Galera

Oldroyd

et al. 2000

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

256

239

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The symbiotic interaction between Medicago truncatula and Sinorhizobium meliloti results in the formation of nitrogen-fixing nodules on the roots of the host plant. The early stages of nodule formation are induced by bacteria via lipochitooligosaccharide signals known as Nod factors (NFs). These NFs are structurally specific for bacterium-host pairs and are sufficient to cause a range of early responses involved in the host developmental program. Early events in the signal transduction of NFs are not well defined. We have previously reported that Medicago sativa root hairs exposed to NF display sharp oscillations of cytoplasmic calcium ion concentration (calcium spiking). To assess the possible role of calcium spiking in the nodulation response, we analyzed M. truncatula mutants in five complementation groups. Each of the plant mutants is completely Nod؊ and is blocked at early stages of the symbiosis. We defined two genes, DMI1 and DMI2, required in common for early steps of infection and nodulation and for calcium spiking. Another mutant, altered in the DMI3 gene, has a similar mutant phenotype to dmi1 and dmi2 mutants but displays normal calcium spiking. The calcium behavior thus implies that the DMI3 gene acts either downstream of calcium spiking or downstream of a common branch point for the calcium response and the later nodulation responses. Two additional mutants, altered in the NSP and HCL genes, which show root hair branching in response to NF, are normal for calcium spiking. This system provides an opportunity to use genetics to study ligand-stimulated calcium spiking as a signal transduction event.

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Functions of Rhizobial Nodulation Genes

Cited by 75 publications

References 162 publications

Structure-Function Analysis of Nod Factor-Induced Root Hair Calcium Spiking in Rhizobium-Legume Symbiosis

Structure-Function Analysis of Nod Factor-Induced Root Hair Calcium Spiking in Rhizobium-Legume Symbiosis

Mesorhizobium ciceri biovar biserrulae, a novel biovar nodulating the pasture legume Biserrula pelecinus L.

Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula

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