Inactivation of Duplicated Nod Factor Receptor 5 (NFR5) Genes in Recessive Loss-of-Function Non-Nodulation Mutants of Allotetraploid Soybean (Glycine max L. Merr.)

Indrasumunar, Arief; Kereszt, Attila; Searle, Iain; Miyagi, Mikiko; Li, Dongxue; Nguyen, Cuc D.T.; Men, A.; Carroll, Bernard J.; Gresshoff, Peter M.

doi:10.1093/pcp/pcp178

Cited by 119 publications

(80 citation statements)

References 38 publications

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“…In root cells of the legume hosts, perception is mediated by Nod factor receptors (NFRs) containing ectodomains with three lysin motif (LysM) modules and cytoplasmic serine/threonine kinase domains (4)(5)(6)(7)(8)(9). Mutant studies in the model legumes Lotus japonicus (Lotus) and Medicago truncatula (Medicago) as well as the crop legumes soybean (10,11) and pea (5,6) have shown that NFRs are required for nodulation. Mutant analysis in Lotus identified two NFRs, NFR1 and NFR5, and phenotypic analysis showed that both nfr1 and nfr5 mutants are equally impaired in nodule initiation (4,5).…”

mentioning

confidence: 99%

Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding

Broghammer

Krusell

Blaise

et al. 2012

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

316

228

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Lipochitin oligosaccharides called Nod factors function as primary rhizobial signal molecules triggering legumes to develop new plant organs: root nodules that host the bacteria as nitrogen-fixing bacteroids. Here, we show that the Lotus japonicus Nod factor receptor 5 (NFR5) and Nod factor receptor 1 (NFR1) bind Nod factor directly at high-affinity binding sites. Both receptor proteins were posttranslationally processed when expressed as fusion proteins and extracted from purified membrane fractions of Nicotiana benthamiana or Arabidopsis thaliana. The N-terminal signal peptides were cleaved, and NFR1 protein retained its in vitro kinase activity. Processing of NFR5 protein was characterized by determining the N-glycosylation patterns of the ectodomain. Two different glycan structures with identical composition, Man 3 XylFucGlcNAc 4 , were identified by mass spectrometry and located at amino acid positions N68 and N198. Receptor-ligand interaction was measured by using ligands that were labeled or immobilized by application of chemoselective chemistry at the anomeric center. High-affinity ligand binding was demonstrated with both solid-phase and free solution techniques. The K d values obtained for Nod factor binding were in the nanomolar range and comparable to the concentration range sufficient for biological activity. Structure-dependent ligand specificity was shown by using chitin oligosaccharides. Taken together, our results suggest that ligand recognition through direct ligand binding is a key step in the receptor-mediated activation mechanism leading to root nodule development in legumes.lysin motif proteins | plant-microbe interactions | symbiotic signalling | lysin motif receptor-like kinase | non-self recognition F ormation of nitrogen-fixing root nodules relies on an intriguing signal exchange between the legume host and the bacterial microsymbiont (1). In this two-way exchange, Nod factors synthesized by rhizobia function as central signal molecules, which induce early physiological responses, gene expression, and cell division in susceptible legumes (1-3). In root cells of the legume hosts, perception is mediated by Nod factor receptors (NFRs) containing ectodomains with three lysin motif (LysM) modules and cytoplasmic serine/threonine kinase domains (4-9). Mutant studies in the model legumes Lotus japonicus (Lotus) and Medicago truncatula (Medicago) as well as the crop legumes soybean (10, 11) and pea (5, 6) have shown that NFRs are required for nodulation. Mutant analysis in Lotus identified two NFRs, NFR1 and NFR5, and phenotypic analysis showed that both nfr1 and nfr5 mutants are equally impaired in nodule initiation (4, 5). In Medicago, only mutation of the Nfr5 ortholog, Nfp, results in a nonnodulating phenotype, whereas the Nfr1 homolog Lyk3 is required for progression of infection threads (7-9, 12).The earliest plant responses to Nod factor, such as membrane depolarization, cytoplasmic alkalinization, calcium fluxes, calcium spiking, and root hair deformation (3, 13), are either strongly at...

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mentioning

confidence: 99%

Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding

Broghammer

Krusell

Blaise

et al. 2012

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

316

228

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“…In contrast, the dominant alleles Rj2, Rj3, Rj4, and Rfg1 have unique features that restrict nodulation with specific strains. The dominant nature of these genes is in contrast to the loss-offunction recessive alleles (rj1) in NFRs (18,22,23). Rj2/Rfg1 restricts nodulation with B. japonicum USDA122 and S. fredii USDA257 (24,25).…”

mentioning

confidence: 99%

“…The formation of symbiotic root nodules in soybean plants is controlled by several loci, referred to as the rj or Rj loci (17). The recessive alleles rj1 and rj5 were identified to be putative NF receptors and are referred to as nfr1 and nfr5, respectively (17)(18)(19), and rj7 was identified to be nts1, which is involved in the systemic regulation of nodulation (20,21). In contrast, the dominant alleles Rj2, Rj3, Rj4, and Rfg1 have unique features that restrict nodulation with specific strains.…”

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confidence: 99%

Identification of Bradyrhizobium elkanii Genes Involved in Incompatibility with Soybean Plants Carrying the Rj4 Allele

Faruque

Miwa

Yasuda

et al. 2015

Appl Environ Microbiol

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c Symbioses between leguminous plants and soil bacteria known as rhizobia are of great importance to agricultural production and nitrogen cycling. While these mutualistic symbioses can involve a wide range of rhizobia, some legumes exhibit incompatibility with specific strains, resulting in ineffective nodulation. The formation of nodules in soybean plants (Glycine max) is controlled by several host genes, which are referred to as Rj genes. The soybean cultivar BARC2 carries the Rj4 gene, which restricts nodulation by specific strains, including Bradyrhizobium elkanii USDA61. Here we employed transposon mutagenesis to identify the genetic locus in USDA61 that determines incompatibility with soybean varieties carrying the Rj4 allele. Introduction of the Tn5 transposon into USDA61 resulted in the formation of nitrogen fixation nodules on the roots of soybean cultivar BARC2 (Rj4 Rj4). Sequencing analysis of the sequence flanking the Tn5 insertion revealed that six genes encoding a putative histidine kinase, transcriptional regulator, DNA-binding transcriptional activator, helix-turn-helix-type transcriptional regulator, phage shock protein, and cysteine protease were disrupted. The cysteine protease mutant had a high degree of similarity with the type 3 effector protein XopD of Xanthomonas campestris. Our findings shed light on the diverse and complicated mechanisms that underlie these highly host-specific interactions and indicate the involvement of a type 3 effector in Rj4 nodulation restriction, suggesting that Rj4 incompatibility is partly mediated by effector-triggered immunity. P lants of the legume family can effectively make their own fertilizers by forming symbioses with a diverse group of nitrogen-fixing soil bacteria known as rhizobia. This cross-kingdom collaboration is characterized by the formation of the root nodule, a specialized plant organ that provides an optimized environment in which the bacteria convert atmospheric nitrogen into ammonia. The symbiotic interactions between leguminous plants and Rhizobium bacteria show high species specificity, which is determined by the exchange of signal molecules. The best-known determinants of host specificity derived from rhizobia are the so-called Nod factors (NFs), which comprise a family of lipochitooligosaccharides with various strain-specific chemical decorations (1). Legume roots excrete flavonoid compounds that can interact specifically with the rhizobial transcriptional factor NodD. Activation of NodD induces the expression of nodulation genes in rhizobia, which are required for the synthesis of NFs (2, 3). NFs are received by host NF receptors (NFRs) and activate host signal transduction pathways that lead to root hair infection and nodule organogenesis (2, 3). A recent study showed that introduction of the putative NFRs NFR1 and NFR5 of Lotus japonicus into Medicago truncatula initiated nodulation of the transgenic roots by the L. japonicus symbiont Mesorhizobium loti (4, 5). Thus, NFs and their receptor proteins contribute significantly to the de...

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“…4 As shown by the nod49 and rj1 mutants, GmNFR1β alone in combination with GmNFR5α/β cannot efficiently recognize Nod factor in epidermal and root hair cells to induce root hair deformation, curling and infection thread formation. In contrast GmNFR1α was able to facilitate these steps as shown by functional nodulation in the GmNFR1β Q513* mutant not know whether the GmNFR1β mutation in PI437.654 is causally connected to its nematode resistance phenotype.…”

Section: Isolation Of Gmnfr1α and Gmnfr1β Genesmentioning

confidence: 97%

“…It requires the reception of a Rhizobiumderived 'Nodulation Factor' (NF, a lipooligosaccharide) by a presumptive receptor kinase complex (NFR1/LYK3 plus NFR5/ NFP), both part of the LysM receptor kinase family. [1][2][3][4][5] These Nod factor receptors were not thought to be involved in Myc factor perception, but Maillet et al 6 suggest that NFP, not LYK3 is partly involved in the Myc-signal-elicited root branching stimulation response. In Parasponia andersonii, the only non-legume species that acquired rhizobia symbiosis, a single NFP/ NFR5-like receptor fulfil a dual symbiotic function of both rhizobia and arbuscular mycorrhizae.…”

Section: General Concept Of Nod Factor Perception In Legumesmentioning

confidence: 99%

Evolutionary duplication of lipo-oligochitin-like receptor genes in soybean differentiates their function in cell division and cell invasion

Indrasumunar

Gresshoff

2011

Plant Signaling & Behavior

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Inactivation of Duplicated Nod Factor Receptor 5 (NFR5) Genes in Recessive Loss-of-Function Non-Nodulation Mutants of Allotetraploid Soybean (Glycine max L. Merr.)

Cited by 119 publications

References 38 publications

Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding

Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding

Identification of Bradyrhizobium elkanii Genes Involved in Incompatibility with Soybean Plants Carrying the Rj4 Allele

Evolutionary duplication of lipo-oligochitin-like receptor genes in soybean differentiates their function in cell division and cell invasion

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