A transcriptomic analysis of the effect of genistein on Sinorhizobium fredii HH103 reveals novel rhizobial genes putatively involved in symbiosis

Pérez‐Montaño, Francisco; Jiménez‐Guerrero, Irene; Acosta‐Jurado, Sebastián; Navarro‐Gómez, Pilar; Ollero, Francisco Javier; Ruíz-Sainz, José E.; Vinardell, José‐María

doi:10.1038/srep31592

Cited by 46 publications

(94 citation statements)

References 58 publications

(87 reference statements)

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“…As previously published, the expression of nopP, nopL, and nopI is regulated by flavonoids and by the transcriptional regulators NodD1 and TtsI (28,39). Secretion of several Nops to the extracellular medium through the T3SS has been previously reported in HH103, including NopL and NopP (14).…”

Section: Resultsmentioning

confidence: 62%

“…The HH103 nopI and nopL genes are preceded by tts boxes (Fig. 1), and their transcription upon flavonoid induction was blocked when the nodD1 and ttsI genes were inactivated (39), indicating that the expression of both genes was flavonoid, NodD1, and TtsI dependent. Besides, secretion of NopI to the extracellular medium upon flavonoid induction (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…The analyses of the S. fredii HH103 genome and transcriptome have shown that this strain possesses at least eight genes coding for putative effectors: gunA, nopC, nopD, nopI, nopL, nopM (nopM1 and nopM2), nopP, and nopT (39). Four of them, nopC, nopI, nopL, and nopP, have only been described in rhizobia and, therefore, can be considered Rhizobium specific (18,34).…”

Section: Discussionmentioning

confidence: 99%

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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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Section: Resultsmentioning

confidence: 62%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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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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“…As mentioned above, previous RNA‐seq analyses carried out with S. fredii HH103 led to the identification of 100 DEGs upon treatment with genistein (Pérez‐Montaño et al, ) that could be assigned to three different groups based on the presence or absence of functional nod (NB) or tts (TB) boxes in their promoter sequences. Seventy‐seven out of these 100 genes were also found as DEGs in the three strains in the presence of exudates when compared to the wild‐type strain grown in the absence of flavonoids, whereas 1, 3 and 4 DEGs were found only in the wild‐type and in the nolR and nodD2 mutants respectively.…”

Section: Resultsmentioning

confidence: 99%

“…In order to better understand the symbiotic behaviour of the S. fredii HH103 nolR and nodD2 derivatives with Lotus , we carried out a transcriptomic study by RNAseq of HH103 Rif R , SVQ515 ( nodD2 ) and SVQ548 ( nolR ) grown in the presence of L. japonicus Gifu root exudates (Supporting Information Datasets S1–S3 respectively) and compared to the results obtained for the wild‐type strain grown in the absence of exudates (Pérez‐Montaño et al, ). We have considered as differentially expressed genes (DEGs) those that, in the presence of exudates, showed a fold‐change in their expression lower than −4 (i.e.…”

Section: Resultsmentioning

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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GmTNRP1, associated with rhizobial type‐III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max)

Liu

et al. 2023

Food and Energy Security

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Soybean is a rich source of protein and oil for humans. It forms a symbiotic association with rhizobia to fix atmospheric nitrogen for its growth and development.Rhizobial type-III effectors act as important signaling molecules in symbiosis.However, they are poorly studied. In this study, mutation of TtsI in Sinorhizobium fredii HH103 reduced nodule numbers and dry weights in SN14 (cultivated soybean) and ZYD00006 (wild soybean). Moreover, it reduced nitrogenase activity in SN14 but not in ZYD00006. Based on the differences in nitrogenase activity between SN14 and ZYD00006 inoculated with HH103 and the TtsI mutant, two conditional quantitative trait loci associated with nitrogenase activity were identified in chromosome segment substitution lines derived from SN14 and ZYD00006.Using transcriptome analysis, single-nucleotide polymorphism (SNP) analysis, and qRT-PCR, Glyma.13G150000 (GmTNRP1) was identified as a candidate gene in soybean that was associated with nitrogenase activity, along with NopT (a type-III effector). In addition, GmTNRP1 (an LRR-RK family protein located on the cell membrane) was observed to be induced by NopT to negatively regulate nitrogenase activity. In transgenic hairy roots with GmTNRP1 silencing, no significant difference was observed in terms of nitrogenase activity between nodules inoculated with the NopT mutant and those inoculated with HH103 (wild type).However, the nitrogenase activity in the nodules decreased after overexpression of GmTNRP1. SNP located in the GmTNRP1 promoter affected its expression in response to NopT. Haplotype analysis revealed that SN14 belonged to Hap1 and ZYD00006 belonged to Hap2, which explained the different results in the two varieties. To the best of our knowledge, this is the first study to identify a soybean gene associated with a rhizobial type-III effector in the nodules. GmTNRP1 can negatively regulate nitrogenase activity in the nodules. This study enhanced the

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A transcriptomic analysis of the effect of genistein on Sinorhizobium fredii HH103 reveals novel rhizobial genes putatively involved in symbiosis

Cited by 46 publications

References 58 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

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

GmTNRP1, associated with rhizobial type‐III effector NopT, regulates nitrogenase activity in the nodules of soybean (Glycine max)

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