Bacterial Molecular Signals in the Sinorhizobium fredii-Soybean Symbiosis

López‐Baena, Francisco Javier; Ruíz-Sainz, José E.; Rodrı́guez-Carvajal, Miguel A.; Vinardell, José‐María

doi:10.3390/ijms17050755

Cited by 88 publications

(147 citation statements)

References 149 publications

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“…However, the fact that an EPS − mutant of HH103 was not able to effectively nodulate L. japonicus Gifu (Acosta‐Jurado et al, ) suggests that a reduction in the production of this polysaccharide is not related to the symbiotic phenotype of the nolR mutant with this legume. T3SS‐delivered effectors are also known to play an important role in determining host compatibility in many rhizobia‐legume interactions (López‐Baena et al, ). In our study, several T3SS genes were slightly overexpressed in the nolR and nodD2 mutants when cultured in the presence of Lotus japonicus Gifu root exudates, so a possible participation of T3SS‐effectors in the ability of these mutants to effectively nodulate L. japonicus cannot be discarded and we plan to further investigate this possibility in the next future.…”

Section: Discussionmentioning

confidence: 99%

Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii

Acosta‐Jurado

Rodríguez-Navarro

Kawaharada

et al. 2019

Environmental Microbiology

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Summary Sinorhizobium fredii HH103 RifR, a broad‐host‐range rhizobial strain, forms ineffective nodules with Lotus japonicus but induces nitrogen‐fixing nodules in Lotus burttii roots that are infected by intercellular entry. Here we show that HH103 RifR nolR or nodD2 mutants gain the ability to induce infection thread formation and to form nitrogen‐fixing nodules in L. japonicus Gifu. Microscopy studies showed that the mode of infection of L. burttii roots by the nodD2 and nolR mutants switched from intercellular entry to infection threads (ITs). In the presence of the isoflavone genistein, both mutants overproduced Nod‐factors. Transcriptomic analyses showed that, in the presence of Lotus japonicus Gifu root exudates, genes related to Nod factors production were overexpressed in both mutants in comparison to HH103 RifR. Complementation of the nodD2 and nolR mutants provoked a decrease in Nod‐factor production, the incapacity to form nitrogen‐fixing nodules with L. japonicus Gifu and restored the intercellular way of infection in L. burttii. Thus, the capacity of S. fredii HH103 RifR nodD2 and nolR mutants to infect L. burttii and L. japonicus Gifu by ITs and fix nitrogen L. japonicus Gifu might be correlated with Nod‐factor overproduction, although other bacterial symbiotic signals could also be involved.

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Section: Discussionmentioning

confidence: 99%

Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii

Acosta‐Jurado

Rodríguez-Navarro

Kawaharada

et al. 2019

Environmental Microbiology

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“…The symbiotic interaction between rhizobia and legumes relies on a complex interchange of molecular signals, in such a way that only compatible rhizobial strains will success in infecting plant host roots and being hosted inside nodules (Oldroyd, 2013;López-Baena et al, 2016). Legume roots exudate phenolic compounds called flavonoids that interact with the bacterial proteins NodD (Peck et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Sinorhizobium fredii HH103 syrM inactivation affects the expression of a large number of genes, impairs nodulation with soybean and extends the host‐range to Lotus japonicus

Acosta‐Jurado

Alias‐Villegas

Navarro‐Gómez

et al. 2020

Environmental Microbiology

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Summary Sinorhizobium fredii HH103 RifR is a broad host‐range rhizobial strain able to nodulate with soybean and Lotus burttii, but it is ineffective with L. japonicus. Here, we study the role of the HH103 RifR SyrM protein in the regulation of gene expression and its relevance in symbiosis with those three legumes. RNAseq analyses show that HH103 SyrM is an important transcriptional regulator not only in the presence of inducer flavonoids but also in its absence. Lack of SyrM increases Nod factors production and decreases genistein‐mediated repression of exopolysaccharide production in HH103. In symbiosis, mutation of syrM partially impaired interaction with soybean but improves effectiveness with L. burttii and extends the host‐rage to L. japonicus Gifu. In addition, HH103 syrM mutants enter in both Lotus species by infection threads, whereas HH103 uses the more primitive intercellular infection to enter into L. burttii roots These symbiotic phenotypes were previously observed in two other HH103 mutants affected in symbiotic regulators, nodD2 and nolR, revealing that in S. fredii HH103 numerous transcriptional regulators finely modulate symbiotic gene expression.

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“…This is the case of nopT, which codes for a protein with cysteine protease activity (29)(30)(31), and nopI and gunA, two genes that have not been previously described in other S. fredii strains (32). GunA, however, has already been described as an endoglucanase in Bradyrhizobium japonicum, but its inactivation does not affect symbiosis with soybean, cowpea, and mung bean (33).…”

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confidence: 99%

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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Bacterial Molecular Signals in the Sinorhizobium fredii-Soybean Symbiosis

Cited by 88 publications

References 149 publications

Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii

Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii

Sinorhizobium fredii HH103 syrM inactivation affects the expression of a large number of genes, impairs nodulation with soybean and extends the host‐range to Lotus japonicus

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

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