Symbiotic properties and first analyses of the genomic sequence of the fast growing model strain Sinorhizobium fredii HH103 nodulating soybean

Margaret, Isabel; Becker, Anke; Blom, Jochen; Bonilla, Ildefonso; Goesmann, Alexander; Göttfert, Michael; Lloret, Javier; Mittard-Runte, Virginie; Rückert, Christian; Ruíz-Sainz, José E.; Vinardell, José‐María; Weidner, Stefan

doi:10.1016/j.jbiotec.2011.03.016

Cited by 67 publications

(59 citation statements)

References 64 publications

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“…fredii HH103, referred to here as HH103, is a broad-host-range bacterium that nodulates many legumes including soybean, which is considered to be its natural host plant (13). HH103 secretes at least eight Nops through the T3SS in response to genistein: NopA (ϳ7 kDa), NopB (ϳ21 kDa), NopC (ϳ11 kDa), NopD (ϳ180 kDa), NopL (ϳ37 kDa), NopM (ϳ60 kDa), NopP (ϳ32 kDa), and NopX (ϳ60 kDa) (14).…”

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The Sinorhizobium (Ensifer) fredii HH103 Nodulation Outer Protein NopI Is a Determinant for Efficient Nodulation of Soybean and Cowpea Plants

Jiménez‐Guerrero

Pérez‐Montaño

Medina

et al. 2017

Appl Environ Microbiol

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The type III secretion system (T3SS) is a specialized secretion apparatus that is commonly used by many plant and animal pathogenic bacteria to deliver proteins, termed effectors, to the interior of the host cells. These effectors suppress host defenses and interfere with signal transduction pathways to promote infection. Some rhizobial strains possess a functional T3SS, which is involved in the suppression of host defense responses, host range determination, and symbiotic efficiency. The analysis of the genome of the broad-host-range rhizobial strain Sinorhizobium fredii HH103 identified eight genes that code for putative T3SS effectors. Three of these effectors, NopL, NopP, and NopI, are Rhizobium specific. In this work, we demonstrate that NopI, whose amino acid sequence shows a certain similarity with NopP, is secreted through the S. fredii HH103 T3SS in response to flavonoids. We also determined that NopL can be considered an effector since it is directly secreted to the interior of the host cell as demonstrated by adenylate cyclase assays. Finally, the symbiotic phenotype of single, double, and triple nopI, nopL, and nopP mutants in soybean and cowpea was assayed, showing that NopI plays an important role in determining the number of nodules formed in both legumes and that the absence of both NopL and NopP is highly detrimental for symbiosis.IMPORTANCE The paper is focused on three Rhizobium-specific T3SS effectors of Sinorhizobium fredii HH103, NopL, NopP, and NopI. We demonstrate that S. fredii HH103 is able to secrete through the T3SS in response to flavonoids the nodulation outer protein NopI. Additionally, we determined that NopL can be considered an effector since it is secreted to the interior of the host cell as demonstrated by adenylate cyclase assays. Finally, nodulation assays of soybean and cowpea indicated that NopI is important for the determination of the number of nodules formed and that the absence of both NopL and NopP negatively affected nodulation. KEYWORDS:Sinorhizobium fredii, cowpea, effector, nodulation, soybean, symbiosis, type III secretion S oil bacteria, collectively known as rhizobia, induce the formation of specialized structures, called nodules, on the roots or stems of host legumes. Within these nodules, rhizobia differentiate into bacteroids that are able to reduce atmospheric nitrogen to ammonia, which is assimilated by the plant. In exchange, rhizobia are provided with a carbon source and an appropriate environment to promote bacterial growth (1).

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The Sinorhizobium (Ensifer) fredii HH103 Nodulation Outer Protein NopI Is a Determinant for Efficient Nodulation of Soybean and Cowpea Plants

Jiménez‐Guerrero

Pérez‐Montaño

Medina

et al. 2017

Appl Environ Microbiol

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“…Sinorhizobium fredii HH103 is a fast-growing rhizobial strain with a generation time of about 3 to 4 h, which was isolated from Chinese soil from Hubei Province (3). The strain is able to form nodules on agronomically advanced soybean cultivars (3,7). Competition studies revealed that in an acid soil the slow-growing Bradyrhizobium japonicum strain 110 outcompetes HH103, whereas in alkaline soils most of the nodules are colonized by HH103 (2).…”

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“…Competition studies revealed that in an acid soil the slow-growing Bradyrhizobium japonicum strain 110 outcompetes HH103, whereas in alkaline soils most of the nodules are colonized by HH103 (2). Besides soybean, which forms determinate nodules, HH103 infects a number of other legumes, including Glycyrrhiza uralensis, which develops indeterminate nodules (1,7). Sinorhizobium fredii HH103 is closely related to Rhizobium sp.…”

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Genome Sequence of the Soybean Symbiont Sinorhizobium fredii HH103

et al. 2012

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“…fredii mutants of ptsP or ptsO induce ineffective nodules on soybean. S. fredii strains can establish symbiosis with diverse legumes, including the important crops soybean (G. max, with determinate nodules) and pigeonpea (C. cajan, with indeterminate nodules) (34)(35)(36)(37). CCBAU 45436 represents a dominant sublineage of S. fredii that nodulates soybeans in alkaline-saline soils (17,38,39).…”

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Genetic Analysis Reveals the Essential Role of Nitrogen Phosphotransferase System Components in Sinorhizobium fredii CCBAU 45436 Symbioses with Soybean and Pigeonpea Plants

Wang

Feng

et al. 2016

Appl Environ Microbiol

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The nitrogen phosphotransferase system (PTS Ntr ) consists of EI Ntr , NPr, and EIIA Ntr . The active phosphate moiety derived from phosphoenolpyruvate is transferred through EI Ntr and NPr to EIIA Ntr . Sinorhizobium fredii can establish a nitrogen-fixing symbiosis with the legume crops soybean (as determinate nodules) and pigeonpea (as indeterminate nodules). In this study, S. fredii strains with mutations in ptsP and ptsO (encoding EI Ntr and NPr, respectively) formed ineffective nodules on soybeans, while a strain with a ptsN mutation (encoding EIIA Ntr ) was not defective in symbiosis with soybeans. Notable reductions in the numbers of bacteroids within each symbiosome and of poly-␤-hydroxybutyrate granules in bacteroids were observed in nodules infected by the ptsP or ptsO mutant strains but not in those infected with the ptsN mutant strain. However, these defects of the ptsP and ptsO mutant strains were recovered in ptsP ptsN and ptsO ptsN double-mutant strains, implying a negative role of unphosphorylated EIIA Ntr in symbiosis. Moreover, the symbiotic defect of the ptsP mutant was also recovered by expressing EI Ntr with or without the GAF domain, indicating that the putative glutamine-sensing domain GAF is dispensable in symbiotic interactions. The critical role of PTS Ntr in symbiosis was also observed when related PTS Ntr mutant strains of S. fredii were inoculated on pigeonpea plants. Furthermore, nodule occupancy and carbon utilization tests suggested that multiple outputs could be derived from components of PTS Ntr in addition to the negative role of unphosphorylated EIIA Ntr . In bacteria, the phosphotransferase system (PTS) is important for transport and signal transduction in cellular metabolism (1). Two general types of PTSs have been identified (Fig. 1): the sugar PTS, dedicated to carbohydrate transport, and the nitrogen PTS (PTS Ntr ), which exerts regulatory functions (2). In the canonical model of both PTSs, described in Gram-negative bacteria, the active phosphate moiety derived from phosphoenolpyruvate (PEP) is transferred through two general phosphotransferase proteins: enzyme I (EI, or EI Ntr ) and histidine protein (HPr or NPr) (2, 3). In the sugar PTS, HPr can then phosphorylate sugar-specific EIIA, which will pass the phosphate to the corresponding EIICB transport protein, allowing uptake of the sugar (3). With PTS Ntr , NPr can phosphorylate EIIA Ntr , which is a homolog of EIIA but is not active in sugar transport, as the required EIIB-and EIIC-like domains are lacking (2). Accumulating evidence has suggested that EIIA Ntr seems to exclusively serve regulatory functions. In Escherichia coli, for example, unphosphorylated EIIA Ntr directly binds the TrkA subunit of the low-affinity potassium transporter, thereby inhibiting uptake of potassium at high concentrations, while it stimulates autophosphorylation of KdpD through protein-protein interactions when the potassium level is low, enhancing the transcription of kdpFABC, which encode the high-affinity potassium transporter (4, 5). ...

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Symbiotic properties and first analyses of the genomic sequence of the fast growing model strain Sinorhizobium fredii HH103 nodulating soybean

Cited by 67 publications

References 64 publications

The Sinorhizobium (Ensifer) fredii HH103 Nodulation Outer Protein NopI Is a Determinant for Efficient Nodulation of Soybean and Cowpea Plants

The Sinorhizobium (Ensifer) fredii HH103 Nodulation Outer Protein NopI Is a Determinant for Efficient Nodulation of Soybean and Cowpea Plants

Genome Sequence of the Soybean Symbiont Sinorhizobium fredii HH103

Genetic Analysis Reveals the Essential Role of Nitrogen Phosphotransferase System Components in Sinorhizobium fredii CCBAU 45436 Symbioses with Soybean and Pigeonpea Plants

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