Special Issue "Genetics and Genomics of the Rhizobium-Legume Symbiosis"

A special issue of Genes (ISSN 2073-4425).

Deadline for manuscript submissions: closed (31 October 2017)

Special Issue Editors

Guest Editor
Dr. Mitchell Andrews

Faculty of Agriculture and Life Sciences, Lincoln University, Lincoln 7647, New Zealand
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Phone: +64 3 423 0692
Interests: nitrogen assimilation in plants; positive plant microbial interactions; classification and taxonomy of rhizobia; specificity in legume-rhizobium symbiosis
Guest Editor
Dr. Marcelo Fragomeni Simon

Embrapa Genetic Resources and Biotechnology, Brasilia DF 70770-917 , Brazil
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Interests: legume systematics and evolution; conservation; legume-rhizobium symbiosis
Guest Editor
Dr. Euan K. James

The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
Website | E-Mail
Interests: nitrogen fixation by legumes and non-legumes; beneficial plant-microbial interactions; ultrastructure of nitrogen-fixing symbioses; quantification of N-fixation; genomic analyses of diazotrophs

Special Issue Information

Dear Colleagues,

Leguminosae (Fabaceae, the legume family) is comprised of ca. 19,300 species, within 750 genera, which occur as herbs, shrubs, vines, or trees, in mainly terrestrial habitats, and are components of most of the world’s vegetation types. Most legume species can fix atmospheric nitrogen (N2) via symbiotic bacteria ( ‘rhizobia’) in root nodules and this can give them an advantage under low soil nitrogen (N) conditions if other factors are favorable for growth. Additionally, N2 fixation by legumes can be a major input of N into natural and agricultural ecosystems.

Genetic data have greatly increased our understanding of the biology and evolution of legumes, rhizobia, and legume–rhizobium symbiosis. For example, in 2017, a new classification of the legumes was proposed with six sub-families, based on the plastid matK gene sequences from ca. 20% of all legume species across ca. 90% of all currently recognized genera. These sub-families are a re-circumscribed Caesalpinioideae, Cercidoideae, Detarioideae, Dialioideae, Duparquetioideae and Papilionoideae. Additionally, over the past twenty-five years, phylogenetic analyses of sequences of the 16S ribosomal RNA (rRNA) gene, a range of ‘housekeeping’ genes and symbiosis genes (in particular, ‘nif’ genes, which encode the subunits of nitrogenase, the rhizobial enzyme that fixes N2, and ‘nod’ genes, which encode Nod factors that induce various symbiotic responses on legume roots) have shown that species from a range of genera in the Alphaproteobacteria (most commonly Bradyrhizobium, Ensifer Mesorhizobium and Rhizobium) and two genera in the Betaproteobacteria (Burkholderia (Paraburkholderia) and Cupriavidus)) can form N2 fixing nodules on specific legumes. Full genome sequences are becoming increasingly used in descriptions of rhizobia and in studies on their biology.

The nodulation process for almost all legumes studied is initiated by the legume production of a mix of compounds, mainly flavonoids, which induce synthesis of NodD protein in rhizobia. Different legumes produce different types/mixes of compounds. The NodD protein activates the transcription of other genes involved in the nodulation process including those required to produce Nod factors, the signal molecules produced by the rhizobia and detected by the plant that induce nodule organogenesis. The nodABC genes encode for the proteins required to make the core Nod factor structure. Nod factors from different rhizobia have a similar structure of a chitin-like N-acetyl glucosamine oligosaccharide backbone with a fatty acyl chain at the non-reducing end, but differ in their length of N-acetyl glucosamine oligosaccharide backbone and length and saturation of the fatty acid chain. The Nod-factor core is modified by species specific proteins, which results in various substitutions, including acetylation, glycosylation, methylation, and sulphation. Perception of the Nod-factor signal in legumes is mediated by Nod factor receptors. Specific nod genes have been shown to be major determinants of legume host specificity although legume-rhizobium specificity can be due to factors throughout the development of the symbiosis. The nif and nod genes are often carried on plasmids or symbiotic islands and these genes can be transferred (lateral transfer) between different bacterial species within a genus and more rarely across genera. This is an important mechanism, allowing legumes to form symbioses with rhizobia adapted to particular soils. It also maintains specificity between legume species and rhizobia species with specific symbiosis genes.

We invite submission of original research or review articles in which genetic/genomic data have been used to gain greater understanding of the biology/evolution of legumes, rhizobia and/or the legume rhizobium symbiosis.

Dr. Mitchell Andrews
Dr. Euan K. James
Dr. Marcelo Fragomeni Simon
Guest Editors

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Genes is an international peer-reviewed open access monthly journal published by MDPI.

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Keywords

  • Classification and taxonomy of legumes
  • Classification and taxonomy of rhizobia
  • Legume biology; Rhizobia biology
  • Specificity of the legume-rhizobium symbiosis
  • Horizontal gene transfer
  • nod genes
  • Bacterial symbionts
  • Nitrogen fixation
  • Evolutionary history of the legume-rhizobium symbiosis

Published Papers (12 papers)

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Research

Jump to: Review

Open AccessArticle In BPS1 Downregulated Roots, the BYPASS1 Signal Disrupts the Induction of Cortical Cell Divisions in Bean-Rhizobium Symbiosis
Genes 2018, 9(1), 11; doi:10.3390/genes9010011
Received: 1 November 2017 / Revised: 23 December 2017 / Accepted: 27 December 2017 / Published: 3 January 2018
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Abstract
BYPASS1 (BPS1), which is a well-conserved gene in plants, is required for normal root and shoot development. In the absence of BPS1 gene function, Arabidopsis overproduces a mobile signalling compound (the BPS1 signal) in roots, and this transmissible signal arrests shoot
[...] Read more.
BYPASS1 (BPS1), which is a well-conserved gene in plants, is required for normal root and shoot development. In the absence of BPS1 gene function, Arabidopsis overproduces a mobile signalling compound (the BPS1 signal) in roots, and this transmissible signal arrests shoot growth and causes abnormal root development. In addition to the shoot and root meristem activities, the legumes also possess transient meristematic activity in root cortical cells during Rhizobium symbiosis. We explored the role of Phaseolus vulgaris BPS1 during nodule primordium development using an RNA-interference (RNAi) silencing approach. Our results show that upon Rhizobium infection, the PvBPS1-RNAi transgenic roots failed to induce cortical cell divisions without affecting the rhizobia-induced root hair curling and infection thread formation. The transcript accumulation of early nodulin genes, cell cyclins, and cyclin-dependent kinase genes was affected in RNAi lines. Interestingly, the PvBPS1-RNAi root nodule phenotype was partially rescued by exogenous application of fluridone, a carotenoid biosynthesis inhibitor, which was used because the carotenoids are precursors of BPS1 signalling molecules. Furthermore, we show that the PvBPS1 promoter was active in the nodule primordia. Together, our data show that PvBPS1 plays a vital role in the induction of meristematic activity in root cortical cells and in the establishment of nodule primordia during Phaseolus-Rhizobium symbiosis. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Open AccessArticle Differential Preference of Burkholderia and Mesorhizobium to pH and Soil Types in the Core Cape Subregion, South Africa
Genes 2018, 9(1), 2; doi:10.3390/genes9010002
Received: 31 October 2017 / Revised: 8 December 2017 / Accepted: 13 December 2017 / Published: 22 December 2017
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Abstract
Over 760 legume species occur in the ecologically-heterogeneous Core Cape Subregion (CCR) of South Africa. This study tested whether the main symbionts of CCR legumes (Burkholderia and Mesorhizobium) are phylogenetically structured by altitude, pH and soil types. Rhizobial strains were isolated
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Over 760 legume species occur in the ecologically-heterogeneous Core Cape Subregion (CCR) of South Africa. This study tested whether the main symbionts of CCR legumes (Burkholderia and Mesorhizobium) are phylogenetically structured by altitude, pH and soil types. Rhizobial strains were isolated from field nodules of diverse CCR legumes and sequenced for 16S ribosomic RNA (rRNA), recombinase A (recA) and N-acyltransferase (nodA). Phylogenetic analyses were performed using Bayesian and maximum likelihood techniques. Phylogenetic signals were determined using the D statistic for soil types and Pagel’s λ for altitude and pH. Phylogenetic relationships between symbionts of the narrowly-distributed Indigofera superba and those of some widespread CCR legumes were also determined. Results showed that Burkholderia is restricted to acidic soils, while Mesorhizobium occurs in both acidic and alkaline soils. Both genera showed significant phylogenetic clustering for pH and most soil types, but not for altitude. Therefore, pH and soil types influence the distribution of Burkholderia and Mesorhizobium in the CCR. All strains of Indigofera superba were identified as Burkholderia, and they were nested within various clades containing strains from outside its distribution range. It is, therefore, hypothesized that I. superba does not exhibit rhizobial specificity at the intragenic level. Implications for CCR legume distributions are discussed. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Open AccessArticle Genome-Wide Transcriptional Changes and Lipid Profile Modifications Induced by Medicago truncatula N5 Overexpression at an Early Stage of the Symbiotic Interaction with Sinorhizobium meliloti
Genes 2017, 8(12), 396; doi:10.3390/genes8120396
Received: 30 October 2017 / Revised: 6 December 2017 / Accepted: 11 December 2017 / Published: 19 December 2017
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Abstract
Plant lipid-transfer proteins (LTPs) are small basic secreted proteins, which are characterized by lipid-binding capacity and are putatively involved in lipid trafficking. LTPs play a role in several biological processes, including the root nodule symbiosis. In this regard, the Medicago truncatula nodulin 5
[...] Read more.
Plant lipid-transfer proteins (LTPs) are small basic secreted proteins, which are characterized by lipid-binding capacity and are putatively involved in lipid trafficking. LTPs play a role in several biological processes, including the root nodule symbiosis. In this regard, the Medicago truncatula nodulin 5 (MtN5) LTP has been proved to positively regulate the nodulation capacity, controlling rhizobial infection and nodule primordia invasion. To better define the lipid transfer protein MtN5 function during the symbiosis, we produced MtN5-downregulated and -overexpressing plants, and we analysed the transcriptomic changes occurring in the roots at an early stage of Sinorhizobium meliloti infection. We also carried out the lipid profile analysis of wild type (WT) and MtN5-overexpressing roots after rhizobia infection. The downregulation of MtN5 increased the root hair curling, an early event of rhizobia infection, and concomitantly induced changes in the expression of defence-related genes. On the other hand, MtN5 overexpression favoured the invasion of the nodules by rhizobia and determined in the roots the modulation of genes that are involved in lipid transport and metabolism as well as an increased content of lipids, especially galactolipids that characterize the symbiosome membranes. Our findings suggest the potential participation of LTPs in the synthesis and rearrangement of membranes occurring during the formation of the infection threads and the symbiosome membrane. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Open AccessArticle Requirements for Efficient Thiosulfate Oxidation in Bradyrhizobium diazoefficiens
Genes 2017, 8(12), 390; doi:10.3390/genes8120390
Received: 8 November 2017 / Revised: 7 December 2017 / Accepted: 12 December 2017 / Published: 15 December 2017
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Abstract
One of the many disparate lifestyles of Bradyrhizobium diazoefficiens is chemolithotrophic growth with thiosulfate as an electron donor for respiration. The employed carbon source may be CO2 (autotrophy) or an organic compound such as succinate (mixotrophy). Here, we discovered three new facets
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One of the many disparate lifestyles of Bradyrhizobium diazoefficiens is chemolithotrophic growth with thiosulfate as an electron donor for respiration. The employed carbon source may be CO2 (autotrophy) or an organic compound such as succinate (mixotrophy). Here, we discovered three new facets of this capacity: (i) When thiosulfate and succinate were consumed concomitantly in conditions of mixotrophy, even a high molar excess of succinate did not exert efficient catabolite repression over the use of thiosulfate. (ii) Using appropriate cytochrome mutants, we found that electrons derived from thiosulfate during chemolithoautotrophic growth are preferentially channeled via cytochrome c550 to the aa3-type heme-copper cytochrome oxidase. (iii) Three genetic regulators were identified to act at least partially in the expression control of genes for chemolithoautotrophic thiosulfate oxidation: RegR and CbbR as activators, and SoxR as a repressor. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Open AccessArticle Transcriptome Analysis of Paraburkholderia phymatum under Nitrogen Starvation and during Symbiosis with Phaseolus Vulgaris
Genes 2017, 8(12), 389; doi:10.3390/genes8120389
Received: 31 October 2017 / Revised: 29 November 2017 / Accepted: 4 December 2017 / Published: 15 December 2017
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Abstract
Paraburkholderia phymatum belongs to the β-subclass of proteobacteria. It has recently been shown to be able to nodulate and fix nitrogen in symbiosis with several mimosoid and papilionoid legumes. In contrast to the symbiosis of legumes with α-proteobacteria, very little is known about
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Paraburkholderia phymatum belongs to the β-subclass of proteobacteria. It has recently been shown to be able to nodulate and fix nitrogen in symbiosis with several mimosoid and papilionoid legumes. In contrast to the symbiosis of legumes with α-proteobacteria, very little is known about the molecular determinants underlying the successful establishment of this mutualistic relationship with β-proteobacteria. In this study, we performed an RNA-sequencing (RNA-seq) analysis of free-living P. phymatum growing under nitrogen-replete and -limited conditions, the latter partially mimicking the situation in nitrogen-deprived soils. Among the genes upregulated under nitrogen limitation, we found genes involved in exopolysaccharides production and in motility, two traits relevant for plant root infection. Next, RNA-seq data of P. phymatum grown under free-living conditions and from symbiotic root nodules of Phaseolus vulgaris (common bean) were generated and compared. Among the genes highly upregulated during symbiosis, we identified—besides the nif gene cluster—an operon encoding a potential cytochrome o ubiquinol oxidase (Bphy_3646-49). Bean root nodules induced by a cyoB mutant strain showed reduced nitrogenase and nitrogen fixation abilities, suggesting an important role of the cytochrome for respiration inside the nodule. The analysis of mutant strains for the RNA polymerase transcription factor RpoN (σ54) and its activator NifA indicated that—similar to the situation in α-rhizobia—P. phymatum RpoN and NifA are key regulators during symbiosis with P. vulgaris. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Open AccessArticle Regulatory Elements Located in the Upstream Region of the Rhizobium leguminosarum rosR Global Regulator Are Essential for Its Transcription and mRNA Stability
Genes 2017, 8(12), 388; doi:10.3390/genes8120388
Received: 18 October 2017 / Revised: 24 November 2017 / Accepted: 7 December 2017 / Published: 15 December 2017
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Abstract
Rhizobium leguminosarum bv. trifolii is a soil bacterium capable of establishing a symbiotic relationship with clover (Trifolium spp.). Previously, the rosR gene, encoding a global regulatory protein involved in motility, synthesis of cell-surface components, and other cellular processes was identified and characterized
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Rhizobium leguminosarum bv. trifolii is a soil bacterium capable of establishing a symbiotic relationship with clover (Trifolium spp.). Previously, the rosR gene, encoding a global regulatory protein involved in motility, synthesis of cell-surface components, and other cellular processes was identified and characterized in this bacterium. This gene possesses a long upstream region that contains several regulatory motifs, including inverted repeats (IRs) of different lengths. So far, the role of these motifs in the regulation of rosR transcription has not been elucidated in detail. In this study, we performed a functional analysis of these motifs using a set of transcriptional rosR-lacZ fusions that contain mutations in these regions. The levels of rosR transcription for different mutant variants were evaluated in R. leguminosarum using both quantitative real-time PCR and β-galactosidase activity assays. Moreover, the stability of wild type rosR transcripts and those with mutations in the regulatory motifs was determined using an RNA decay assay and plasmids with mutations in different IRs located in the 5′-untranslated region of the gene. The results show that transcription of rosR undergoes complex regulation, in which several regulatory elements located in the upstream region and some regulatory proteins are engaged. These include an upstream regulatory element, an extension of the -10 element containing three nucleotides TGn (TGn-extended -10 element), several IRs, and PraR repressor related to quorum sensing. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Open AccessArticle NAD1 Controls Defense-Like Responses in Medicago truncatula Symbiotic Nitrogen Fixing Nodules Following Rhizobial Colonization in a BacA-Independent Manner
Genes 2017, 8(12), 387; doi:10.3390/genes8120387
Received: 31 October 2017 / Revised: 4 December 2017 / Accepted: 11 December 2017 / Published: 14 December 2017
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Abstract
Legumes form endosymbiotic interaction with host compatible rhizobia, resulting in the development of nitrogen-fixing root nodules. Within symbiotic nodules, rhizobia are intracellularly accommodated in plant-derived membrane compartments, termed symbiosomes. In mature nodule, the massively colonized cells tolerate the existence of rhizobia without manifestation
[...] Read more.
Legumes form endosymbiotic interaction with host compatible rhizobia, resulting in the development of nitrogen-fixing root nodules. Within symbiotic nodules, rhizobia are intracellularly accommodated in plant-derived membrane compartments, termed symbiosomes. In mature nodule, the massively colonized cells tolerate the existence of rhizobia without manifestation of visible defense responses, indicating the suppression of plant immunity in the nodule in the favur of the symbiotic partner. Medicago truncatula DNF2 (defective in nitrogen fixation 2) and NAD1 (nodules with activated defense 1) genes are essential for the control of plant defense during the colonization of the nitrogen-fixing nodule and are required for bacteroid persistence. The previously identified nodule-specific NAD1 gene encodes a protein of unknown function. Herein, we present the analysis of novel NAD1 mutant alleles to better understand the function of NAD1 in the repression of immune responses in symbiotic nodules. By exploiting the advantage of plant double and rhizobial mutants defective in establishing nitrogen-fixing symbiotic interaction, we show that NAD1 functions following the release of rhizobia from the infection threads and colonization of nodule cells. The suppression of plant defense is self-dependent of the differentiation status of the rhizobia. The corresponding phenotype of nad1 and dnf2 mutants and the similarity in the induction of defense-associated genes in both mutants suggest that NAD1 and DNF2 operate close together in the same pathway controlling defense responses in symbiotic nodules. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Open AccessArticle Identification of Bradyrhizobium elkanii Genes Involved in Incompatibility with Vigna radiata
Genes 2017, 8(12), 374; doi:10.3390/genes8120374
Received: 28 October 2017 / Revised: 21 November 2017 / Accepted: 30 November 2017 / Published: 8 December 2017
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Abstract
The establishment of a root nodule symbiosis between a leguminous plant and a rhizobium requires complex molecular interactions between the two partners. Compatible interactions lead to the formation of nitrogen-fixing nodules, however, some legumes exhibit incompatibility with specific rhizobial strains and restrict nodulation
[...] Read more.
The establishment of a root nodule symbiosis between a leguminous plant and a rhizobium requires complex molecular interactions between the two partners. Compatible interactions lead to the formation of nitrogen-fixing nodules, however, some legumes exhibit incompatibility with specific rhizobial strains and restrict nodulation by the strains. Bradyrhizobium elkanii USDA61 is incompatible with mung bean (Vigna radiata cv. KPS1) and soybean cultivars carrying the Rj4 allele. Here, we explored genetic loci in USDA61 that determine incompatibility with V. radiata KPS1. We identified five novel B. elkanii genes that contribute to this incompatibility. Four of these genes also control incompatibility with soybean cultivars carrying the Rj4 allele, suggesting that a common mechanism underlies nodulation restriction in both legumes. The fifth gene encodes a hypothetical protein that contains a tts box in its promoter region. The tts box is conserved in genes encoding the type III secretion system (T3SS), which is known for its delivery of virulence effectors by pathogenic bacteria. These findings revealed both common and unique genes that are involved in the incompatibility of B. elkanii with mung bean and soybean. Of particular interest is the novel T3SS-related gene, which causes incompatibility specifically with mung bean cv. KPS1. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Open AccessArticle Non-Additive Transcriptomic Responses to Inoculation with Rhizobia in a Young Allopolyploid Compared with Its Diploid Progenitors
Genes 2017, 8(12), 357; doi:10.3390/genes8120357
Received: 1 November 2017 / Revised: 24 November 2017 / Accepted: 27 November 2017 / Published: 30 November 2017
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Abstract
Root nodule symbioses (nodulation) and whole genome duplication (WGD, polyploidy) are both important phenomena in the legume family (Leguminosae). Recently, it has been proposed that polyploidy may have played a critical role in the origin or refinement of nodulation. However, while nodulation and
[...] Read more.
Root nodule symbioses (nodulation) and whole genome duplication (WGD, polyploidy) are both important phenomena in the legume family (Leguminosae). Recently, it has been proposed that polyploidy may have played a critical role in the origin or refinement of nodulation. However, while nodulation and polyploidy have been studied independently, there have been no direct studies of mechanisms affecting the interactions between these phenomena in symbiotic, nodule-forming species. Here, we examined the transcriptome-level responses to inoculation in the young allopolyploid Glycine dolichocarpa (T2) and its diploid progenitor species to identify underlying processes leading to the enhanced nodulation responses previously identified in T2. We assessed the differential expression of genes and, using weighted gene co-expression network analysis (WGCNA), identified modules associated with nodulation and compared their expression between species. These transcriptomic analyses revealed patterns of non-additive expression in T2, with evidence of transcriptional responses to inoculation that were distinct from one or both progenitors. These differential responses elucidate mechanisms underlying the nodulation-related differences observed between T2 and the diploid progenitors. Our results indicate that T2 has reduced stress-related transcription, coupled with enhanced transcription of modules and genes implicated in hormonal signaling, both of which are important for nodulation. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Open AccessArticle Gene Silencing of Argonaute5 Negatively Affects the Establishment of the Legume-Rhizobia Symbiosis
Genes 2017, 8(12), 352; doi:10.3390/genes8120352
Received: 17 October 2017 / Revised: 20 November 2017 / Accepted: 22 November 2017 / Published: 28 November 2017
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Abstract
The establishment of the symbiosis between legumes and nitrogen-fixing rhizobia is finely regulated at the transcriptional, posttranscriptional and posttranslational levels. Argonaute5 (AGO5), a protein involved in RNA silencing, can bind both viral RNAs and microRNAs to control plant-microbe interactions and plant physiology. For
[...] Read more.
The establishment of the symbiosis between legumes and nitrogen-fixing rhizobia is finely regulated at the transcriptional, posttranscriptional and posttranslational levels. Argonaute5 (AGO5), a protein involved in RNA silencing, can bind both viral RNAs and microRNAs to control plant-microbe interactions and plant physiology. For instance, AGO5 regulates the systemic resistance of Arabidopsis against Potato Virus X as well as the pigmentation of soybean (Glycine max) seeds. Here, we show that AGO5 is also playing a central role in legume nodulation based on its preferential expression in common bean (Phaseolus vulgaris) and soybean roots and nodules. We also report that the expression of AGO5 is induced after 1 h of inoculation with rhizobia. Down-regulation of AGO5 gene in P. vulgaris and G. max causes diminished root hair curling, reduces nodule formation and interferes with the induction of three critical symbiotic genes: Nuclear Factor Y-B (NF-YB), Nodule Inception (NIN) and Flotillin2 (FLOT2). Our findings provide evidence that the common bean and soybean AGO5 genes play an essential role in the establishment of the symbiosis with rhizobia. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Review

Jump to: Research

Open AccessReview Transcriptomic Studies of the Effect of nod Gene-Inducing Molecules in Rhizobia: Different Weapons, One Purpose
Genes 2018, 9(1), 1; doi:10.3390/genes9010001
Received: 24 October 2017 / Revised: 7 December 2017 / Accepted: 15 December 2017 / Published: 21 December 2017
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Abstract
Simultaneous quantification of transcripts of the whole bacterial genome allows the analysis of the global transcriptional response under changing conditions. RNA-seq and microarrays are the most used techniques to measure these transcriptomic changes, and both complement each other in transcriptome profiling. In this
[...] Read more.
Simultaneous quantification of transcripts of the whole bacterial genome allows the analysis of the global transcriptional response under changing conditions. RNA-seq and microarrays are the most used techniques to measure these transcriptomic changes, and both complement each other in transcriptome profiling. In this review, we exhaustively compiled the symbiosis-related transcriptomic reports (microarrays and RNA sequencing) carried out hitherto in rhizobia. This review is specially focused on transcriptomic changes that takes place when five rhizobial species, Bradyrhizobium japonicum (=diazoefficiens) USDA 110, Rhizobium leguminosarum biovar viciae 3841, Rhizobium tropici CIAT 899, Sinorhizobium (=Ensifer) meliloti 1021 and S. fredii HH103, recognize inducing flavonoids, plant-exuded phenolic compounds that activate the biosynthesis and export of Nod factors (NF) in all analysed rhizobia. Interestingly, our global transcriptomic comparison also indicates that each rhizobial species possesses its own arsenal of molecular weapons accompanying the set of NF in order to establish a successful interaction with host legumes. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Open AccessReview Synthesis of Rhizobial Exopolysaccharides and Their Importance for Symbiosis with Legume Plants
Genes 2017, 8(12), 360; doi:10.3390/genes8120360
Received: 31 October 2017 / Revised: 26 November 2017 / Accepted: 29 November 2017 / Published: 1 December 2017
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Abstract
Rhizobia dwell and multiply in the soil and represent a unique group of bacteria able to enter into a symbiotic interaction with plants from the Fabaceae family and fix atmospheric nitrogen inside de novo created plant organs, called nodules. One of the key
[...] Read more.
Rhizobia dwell and multiply in the soil and represent a unique group of bacteria able to enter into a symbiotic interaction with plants from the Fabaceae family and fix atmospheric nitrogen inside de novo created plant organs, called nodules. One of the key determinants of the successful interaction between these bacteria and plants are exopolysaccharides, which represent species-specific homo- and heteropolymers of different carbohydrate units frequently decorated by non-carbohydrate substituents. Exopolysaccharides are typically built from repeat units assembled by the Wzx/Wzy-dependent pathway, where individual subunits are synthesized in conjunction with the lipid anchor undecaprenylphosphate (und-PP), due to the activity of glycosyltransferases. Complete oligosaccharide repeat units are transferred to the periplasmic space by the activity of the Wzx flippase, and, while still being anchored in the membrane, they are joined by the polymerase Wzy. Here we have focused on the genetic control over the process of exopolysaccharides (EPS) biosynthesis in rhizobia, with emphasis put on the recent advancements in understanding the mode of action of the key proteins operating in the pathway. A role played by exopolysaccharide in Rhizobium–legume symbiosis, including recent data confirming the signaling function of EPS, is also discussed. Full article
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)
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Planned Papers

The below list represents only planned manuscripts. Some of these manuscripts have not been received by the Editorial Office yet. Papers submitted to MDPI journals are subject to peer-review.

Working Title: Lateral Transfer of Rhizobial Symbiosis Genes across and within Bacterial Genera: Occurrence and Importance?
Putative Authors:
Mitchell Andrews1, Sofie De Meyer2,3, Euan K. James4, Tomasz Stępkowski5, Marcelo F. Simon6, J. Peter W. Young7
Affiliations: 1Faculty of Agriculture and Life Sciences, Lincoln University, PO Box 84, Lincoln 7647, New Zealand
2Centre for Rhizobium Studies, Murdoch University, Murdoch 6150, WA, Australia and 3Laboratory of Microbiology, Department of Biochemistry and Microbiology, Ghent University, Ghent, Belgium
4James Hutton Institute, Invergowrie, Dundee, United Kingdom
5Autonomous Department of Microbial Biology, Faculty of Agriculture and Biology, Warsaw University of Life Sciences (SGGW), 02-776 Warsaw, Poland
6Embrapa Genetic Resources and Biotechnology, Brasilia DF 70770-917, Brazil
7Department of Biology, University of York, York, United Kingdom
Abstract: Lateral transfer of rhizobial symbiosis genes is a mechanism whereby rhizobia and non-rhizobial bacteria adapted to local soil conditions can become specific rhizobial symbionts of legumes growing in these soils. Symbiosis genes involved in lateral transfer have independent phylogenies different from the core genome of their ‘host’. Here the literature on legume-rhizobium symbioses in field soils is reviewed and cases where phylogenetic incongruence implies that lateral gene transfer of rhizobial symbiosis genes has occurred are collated. The occurrence and importance of lateral transfer of rhizobial symbiosis genes across and within bacterial genera is assessed.
Keywords: Leguminosae; N2 fixation; nodulation; nod genes; specificity

Working Title: Genome Sequences of Ten New Zealand Sophora Mesorhizobium strains from Different Field Sites but with Similar Symbiosis Genes
Putative Authors: Mitchell Andrews1, Nguyen Tuan Dung1, James D. Morton1, Sofie De Meyer2,3, Euan K. James4, Peter B. Heenan5, J. Peter W. Young6
Affiliations:
1Faculty of Agriculture and Life Sciences, Lincoln University, PO Box 84, Lincoln 7647, New Zealand
2Centre for Rhizobium Studies, Murdoch University, Murdoch 6150, WA, Australia and 3Laboratory of Microbiology, Department of Biochemistry and Microbiology, Ghent University, Ghent, Belgium 
4James Hutton Institute, Invergowrie, Dundee, United Kingdom
5Landcare Research, Allan Herbarium, Christchurch, New Zealand
6Department of Biology, University of York, York, United Kingdom
Abstract: Previously, ninety-two mesorhizobial isolates from New Zealand endemic Sophora species growing in natural conditions were characterised. Sequences for the housekeeping genes (concatenated recA, gln11 and rpoB) of the isolates were novel and diverse while sequences for their symbiosis genes (nifH, nodA and nodC) were novel but showed high similarity across the isolates. Generally, isolates from the same field site showed similar 16S rRNA and housekeeping gene sequences. This apparent link between housekeeping gene sequences and field site is compatible with the proposal that lateral transfer of symbiosis genes to Mesorhizobium strains adapted to local soil conditions has occurred. Here, full genome sequences of ten different Mesorhizobium strains, including seven formally described species, representative of isolates sampled at different field sites were compared and differences between strains considered in relation to differences in conditions in their field sites.
Keywords: Lateral gene transfer; Leguminosae; N2 fixation; nodulation; nod genes

Working Title: Evolution of symbiotic preference between rhizobia and major legume lineages
Putative Authors: Marcelo F. Simon1, Mitchell Andrews2, Euan K. James3, Janet Sprent4
Affiliations:
1Embrapa Genetic Resources and Biotechnology, Brasilia DF 70770-917, Brazil
2Faculty of Agriculture and Life Sciences, Lincoln University, PO Box 84, Lincoln 7647, New Zealand
3James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK
4Division of Plant Sciences, University of Dundee at JHI, Invergowrie, Dundee, DD2 5DA, UK
Abstract: Association between legumes and nitrogen fixing bacteria is a prime example of symbiotic relationship between plant and bacteria. Recent increase in the studies on legume-rhizobia symbiosis have revealed a diverse range of genera within both Alphaproteobacterial and Betaproteobacterial classes able to nodulate legumes. Accumulating data from nodulation studies have often revealed specific relationships in which major legume lineages or genera are nodulated by a single group of rhizobia. Conversely, less specific legume-rhizobia relationships have also been reported, mainly for pantropical legume genera. Here we build on recent advances on legume phylogeny and legume-rhizobia symbioses to reconstruct the evolutionary history of the legume-rhizobia association. We used an ancestral character state reconstruction analysis to infer symbiotic associations onto a densely sampled genus-level legume phylogeny. This approach enabled us to investigate evolutionary changes of different groups of rhizobia on major legume lineages, and to answer some outstanding research questions: What are the major evolutionary trends regarding symbiotic preference in different legume lineages? Are rhizobia groups clustered along the legume phylogeny? How often symbiotic preference has switched during legume evolution?
Keywords: Leguminosae; evolution; N2 fixation; phylogenetics; rhizobium; symbiosis

Working Title: Genetic variation and relationships among Sophora (Fabaceae) species from New Zealand assessed by microsatellite markers
Putative Authors: Peter B. Heenan, CM Mitchell, Gary J. Houliston
Affiliations: Landcare Research, Lincoln, New Zealand
Corresponding author: Peter B. Heenan: kowhai1961@gmail.com
Abstract: We analysed 10 microsatellite markers for 649 individuals representing the geographic range of eight closely related endemic New Zealand species of Sophora. Structure analysis distinguished S. chathamicaS. fulvidaS. longicarinata and S. prostrata, with the remaining samples forming an unresolved group. A second structure analysis separated the unresolved group into two subgroups, and when these were analysed one subgroup resolved S. tetraptera and S. godleyi and the other subgroup did not clearly distinguish S. microphylla and S. molloyi. Our data suggest that considerable admixture occurs and this is most likely the result of hybridization and introgression. S. fulvida shows admixture with the sympatric S. chathamica but this is not reciprocal, and S. godleyi and S. molloyi exhibit admixture with the sympatric and widespread S.  microphylla.  S. tetraptera has two genotypes evenly distributed thoughout its range, with no obvious admixture with other species or geographic pattern. S. microphylla has a unique genotype in southern South Island where it is the only species present, and this may have survived the Last Glacial Maximum.

Working Title: Gene silencing of Argonaute5 negatively affects the establishment of the legume-rhizobia symbiosis
Putative Authors: María del Rocio Reyero-Saavedra1, Jenny Qiao2, María del Socorro Sánchez-Correa1, Marc Libault2 and Oswaldo Valdés-López1
Affiliations: 1 Laboratorio de Genómica Funcional de Leguminosas. Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México. Tlalnepantla, Estado de México, 54090, México
2 Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019, USA
Corresponding Authors: Oswaldo Valdés-López, Marc Libault
Abstract
: The establishment of the symbiosis between legumes and nitrogen-fixing rhizobia is finely regulated at the transcriptional, posttranscriptional and posttranslational levels. Argonaute5 (AGO5), protein involved in RNA silencing, is able to bind both viral RNAs and microRNAs to control plant-microbe interactions and plant physiology. For instance, AGO5 regulates the systemic resistance of Arabidopsis against Potato Virus as well as in the pigmentation of soybean (Glycine max) seeds. Here, we show that AGO5 is also playing a central role in legume nodulation based on its preferential expression in roots and nodules of soybean and common bean (Phaseolus vulgaris). We also report that the expression of AGO5 is induced after 1 hour of inoculation with rhizobia. Down-regulation of AGO5 gene in G. max and P. vulgaris prevents the nodule formation and the induction of the three critical symbiotic genes: Nuclear Factor Y-B (NF-YB), Nodule Inception (NIN) and Flotin2 (FLOT2). Our findings provide evidence that the soybean and common bean AGO5 gene plays an essential role in the establishment of the legume-rhizobia symbiosis.

Working Title: Synthesis of rhizobial exopolysaccharides and their importance for symbiosis with legume plants
Putative Authors: Małgorzata Marczak, Anna Skorupska et al.
Affiliations: Department of Genetics and Microbiology, Maria Curie-Skłodowska University, Akademicka 19, 20-033 Lublin, Poland
Abstract: Rizobia dwell and multiply in the soil and represent a unique group of bacteria able to enter into a symbiotic interaction with plants from Fabaceae family and fix atmospheric nitrogen inside de novo created plant organs, called nodules. One of the key determinants of the successful interaction between bacteria and plants are exopolysaccharides (EPSs). EPSs perform also different functions in the saprophytic lifestyle in the soil. Exopolysaccharides represent species-specific homo- and heteropolymers of different carbohydrate units frequently decorated by non-carbohydrate substituents. Exopolysaccharides biosynthesis is a multi-step process controlled by several genes and regulatory mechanisms, in response to different exogenous stimuli. Heteropolysacccharides are typically built from repeat units assembled by the Wzx/Wzy-dependent pathway, where individual subunits are synthesized in conjunction with the so-called lipid anchor, undecaprenylphosphate (und-PP), due to the activity of glycosyltransferases. Complete oligosaccharides are transferred to the periplasmic space by the activity of the Wzx flipase and while still being anchored in the membrane, they are joined by the polymerase Wzy. Genetic and structural studies indicate the existence of protein complexes wherein the various biosynthetic proteins form both homo- and heterooligomers. Here we focus on the genetic control over the process of EPS biosynthesis in rhizobia, with emphasis put on the recent advancements in understanding the mode of action of the key proteins operating in the Wzx/Wzy-dependent biosynthesis pathway. A role exopolysaccharide plays in rhizobium–legume symbiosis, including recent data confirming the signaling role EPS, will also be discussed.

Working Title: Signaling and transcriptional reprogramming of plant cells during nitrogen-fixing symbiosis
Putative Authors: Joaquín Clúa, Carla Roda, María Eugenia Zanetti, Flavio Blanco
Affiliations: Instituto de Biotecnología y Biología Molecular, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Centro Científico y Tecnológico-La Plata, Consejo Nacional de Investigaciones Científicas y Técnicas, 1900-La Plata, Argentina.
Abstract: The root nodule symbiosis between legumes and rhizobia is an exquisite biological interaction responsible for fixing a significant amount of nitrogen in terrestrial ecosystems. The success of this interaction depends on the recognition of the right partner by the plant within the richest microbial ecosystems on Earth, the soil. Recent metagenomic studies of soil biome have revealed its complexity, which includes microorganisms that affect plant fitness and growth in a beneficial, harmful, or neutral manner. In this scenario, understanding the molecular mechanisms by which legumes recognize and discriminate rhizobia from pathogens, but also between distinct rhizobia species and strains that differ in their symbiotic performance, is a big challenge. Intense research over the past 15 years allowed the identification of nodulation factors (NFs), exopolysaccharides, lipopolysaccharides and effector proteins produced by rhizobia as key molecular determinants of host specificity during nitrogen-fixing symbiosis. In this review, we will discuss the signaling molecules and transduction pathways underlying plant-rhizobia recognition, the interplay between the plant genetic responses and how high throughput sequencing technologies are enabling global approaches to study these biological interactions.

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