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Genetic Evolution of Root Nodule Symbioses
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Genetic Evolution of Root Nodule Symbioses

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Plant Genetics and Genomics".

Deadline for manuscript submissions: closed (15 July 2020) | Viewed by 47814

Special Issue Editor

Prof. Dr. Katharina Pawlowski

E-Mail Website
Guest Editor
Department of Ecology, Environment and Plant Sciences, Stockholm University, Stockholm, Sweden
Interests: plant; evolution; root nodule symbioses; arbuscular mycorrhiza
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

The evolution of nitrogen-fixing root nodule symbioses comprises the evolution of the microsymbiont, the host, as well as their co-evolution. The development of competing microsymbiont signals controlling host specificity, lipochito-oligosaccharides and effector proteins offers a plethora of evolutionary diversity. Experimental evolution of a pathogenic bacterium into a compatible symbiont could be demonstrated.

In the last two years, phylogenomic results have changed our views of the evolution of root nodule symbioses. The scattered occurrence of root nodule symbioses was previously explained by the assumption that the ancestor of Fagales, Fabales, Rosales, and Cucurbitales had acquired a predisposition based on which a root nodule symbiosis could, and in several cases did, evolve, sometimes with rhizobia and sometimes with Frankia strains—in short, the scattered distribution was explained by independent gains, and it was unclear whether the common ancestor was symbiotic. Now the preponderance of evidence supports a model where the common ancestor was symbiotic—although not necessarily capable of forming nodules—but the symbiotic capacity was subsequently lost in most lineages. Thus, the hypothesis of independent gains has been replaced by the hypothesis of independent losses. However, there are still a lot of open questions which should be answered based on newly available genome sequences and genomic tools: What are the signaling molecules used by Frankia strains? What is the basis for symbiotic efficiency—the adaptation of a particular microsymbiont to a particular host is an ongoing evolutionary process, but what are the molecular players? What are the reasons for the loss of the symbiosis in the majority of lineages? The forthcoming Special Issue aims to present a platform for the discussion of these new developments in root nodule symbioses.

Prof. Dr. Katharina Pawlowski
Guest Editor

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Keywords

  • Evolution
  • Symbiosis
  • Biological nitrogen fixation
  • Root nodules
  • Intracellular
  • Rhizobia
  • Frankia
  • Legumes
  • Actinorhizal plants
  • Lipochito-oligosaccharides
  • NIN
  • Type III secretion systems

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Research

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21 pages, 3625 KiB  
Article
Comparative Genomics Provides Insights into the Taxonomy of Azoarcus and Reveals Separate Origins of Nif Genes in the Proposed Azoarcus and Aromatoleum Genera
by Roberto Tadeu Raittz, Camilla Reginatto De Pierri, Marta Maluk, Marcelo Bueno Batista, Manuel Carmona, Madan Junghare, Helisson Faoro, Leonardo M. Cruz, Federico Battistoni, Emanuel de Souza, Fábio de Oliveira Pedrosa, Wen-Ming Chen, Philip S. Poole, Ray A. Dixon and Euan K. James
Genes 2021, 12(1), 71; https://doi.org/10.3390/genes12010071 - 7 Jan 2021
Cited by 12 | Viewed by 5023
Abstract
Among other attributes, the Betaproteobacterial genus Azoarcus has biotechnological importance for plant growth-promotion and remediation of petroleum waste-polluted water and soils. It comprises at least two phylogenetically distinct groups. The “plant-associated” group includes strains that are isolated from the rhizosphere or root interior [...] Read more.
Among other attributes, the Betaproteobacterial genus Azoarcus has biotechnological importance for plant growth-promotion and remediation of petroleum waste-polluted water and soils. It comprises at least two phylogenetically distinct groups. The “plant-associated” group includes strains that are isolated from the rhizosphere or root interior of the C4 plant Kallar Grass, but also strains from soil and/or water; all are considered to be obligate aerobes and all are diazotrophic. The other group (now partly incorporated into the new genus Aromatoleum) comprises a diverse range of species and strains that live in water or soil that is contaminated with petroleum and/or aromatic compounds; all are facultative or obligate anaerobes. Some are diazotrophs. A comparative genome analysis of 32 genomes from 30 Azoarcus-Aromatoleum strains was performed in order to delineate generic boundaries more precisely than the single gene, 16S rRNA, that has been commonly used in bacterial taxonomy. The origin of diazotrophy in Azoarcus-Aromatoleum was also investigated by comparing full-length sequences of nif genes, and by physiological measurements of nitrogenase activity using the acetylene reduction assay. Based on average nucleotide identity (ANI) and whole genome analyses, three major groups could be discerned: (i) Azoarcus comprising Az. communis, Az. indigens and Az. olearius, and two unnamed species complexes, (ii) Aromatoleum Group 1 comprising Ar. anaerobium, Ar. aromaticum, Ar. bremense, and Ar. buckelii, and (iii) Aromatoleum Group 2 comprising Ar. diolicum, Ar. evansii, Ar. petrolei, Ar. toluclasticum, Ar. tolulyticum, Ar. toluolicum, and Ar. toluvorans. Single strain lineages such as Azoarcus sp. KH32C, Az. pumilus, and Az. taiwanensis were also revealed. Full length sequences of nif-cluster genes revealed two groups of diazotrophs in Azoarcus-Aromatoleum with nif being derived from Dechloromonas in Azoarcus sensu stricto (and two Thauera strains) and from Azospira in Aromatoleum Group 2. Diazotrophy was confirmed in several strains, and for the first time in Az. communis LMG5514, Azoarcus sp. TTM-91 and Ar. toluolicum TT. In terms of ecology, with the exception of a few plant-associated strains in Azoarcus (s.s.), across the group, most strains/species are found in soil and water (often contaminated with petroleum or related aromatic compounds), sewage sludge, and seawater. The possession of nar, nap, nir, nor, and nos genes by most Azoarcus-Aromatoleum strains suggests that they have the potential to derive energy through anaerobic nitrate respiration, so this ability cannot be usefully used as a phenotypic marker to distinguish genera. However, the possession of bzd genes indicating the ability to degrade benzoate anaerobically plus the type of diazotrophy (aerobic vs. anaerobic) could, after confirmation of their functionality, be considered as distinguishing phenotypes in any new generic delineations. The taxonomy of the Azoarcus-Aromatoleum group should be revisited; retaining the generic name Azoarcus for its entirety, or creating additional genera are both possible outcomes. Full article
(This article belongs to the Special Issue Genetic Evolution of Root Nodule Symbioses)
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29 pages, 3828 KiB  
Article
Genome-Wide Identification of the CrRLK1L Subfamily and Comparative Analysis of Its Role in the Legume-Rhizobia Symbiosis
by Jorge Solis-Miranda, Citlali Fonseca-García, Noreide Nava, Ronal Pacheco and Carmen Quinto
Genes 2020, 11(7), 793; https://doi.org/10.3390/genes11070793 - 14 Jul 2020
Cited by 16 | Viewed by 4223
Abstract
The plant receptor-like-kinase subfamily CrRLK1L has been widely studied, and CrRLK1Ls have been described as crucial regulators in many processes in Arabidopsis thaliana (L.), Heynh. Little is known, however, about the functions of these proteins in other plant species, including potential roles in [...] Read more.
The plant receptor-like-kinase subfamily CrRLK1L has been widely studied, and CrRLK1Ls have been described as crucial regulators in many processes in Arabidopsis thaliana (L.), Heynh. Little is known, however, about the functions of these proteins in other plant species, including potential roles in symbiotic nodulation. We performed a phylogenetic analysis of CrRLK1L subfamily receptors of 57 different plant species and identified 1050 CrRLK1L proteins, clustered into 11 clades. This analysis revealed that the CrRLK1L subfamily probably arose in plants during the transition from chlorophytes to embryophytes and has undergone several duplication events during its evolution. Among the CrRLK1Ls of legumes and A. thaliana, protein structure, gene structure, and expression patterns were highly conserved. Some legume CrRLK1L genes were active in nodules. A detailed analysis of eight nodule-expressed genes in Phaseolus vulgaris L. showed that these genes were differentially expressed in roots at different stages of the symbiotic process. These data suggest that CrRLK1Ls are both conserved and underwent diversification in a wide group of plants, and shed light on the roles of these genes in legume–rhizobia symbiosis. Full article
(This article belongs to the Special Issue Genetic Evolution of Root Nodule Symbioses)
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17 pages, 3112 KiB  
Article
A Minimal Genetic Passkey to Unlock Many Legume Doors to Root Nodulation by Rhizobia
by Jovelyn Unay and Xavier Perret
Genes 2020, 11(5), 521; https://doi.org/10.3390/genes11050521 - 7 May 2020
Cited by 3 | Viewed by 4085
Abstract
In legume crops, formation of developmentally mature nodules is a prerequisite for efficient nitrogen fixation by populations of rhizobial bacteroids established inside nodule cells. Development of root nodules, and concomitant microbial colonization of plant cells, are constrained by sets of recognition signals exchanged [...] Read more.
In legume crops, formation of developmentally mature nodules is a prerequisite for efficient nitrogen fixation by populations of rhizobial bacteroids established inside nodule cells. Development of root nodules, and concomitant microbial colonization of plant cells, are constrained by sets of recognition signals exchanged by infecting rhizobia and their legume hosts, with much of the specificity of symbiotic interactions being determined by the flavonoid cocktails released by legume roots and the strain-specific nodulation factors (NFs) secreted by rhizobia. Hence, much of Sinorhizobium fredii strain NGR234 symbiotic promiscuity was thought to stem from a family of >80 structurally diverse NFs and associated nodulation keys in the form of secreted effector proteins and rhamnose-rich surface polysaccharides. Here, we show instead that a mini-symbiotic plasmid (pMiniSym2) carrying only the nodABCIJ, nodS and nodD1 genes of NGR234 conferred promiscuous nodulation to ANU265, a derivative strain cured of the large symbiotic plasmid pNGR234a. The ANU265::pMiniSym2 transconjugant triggered nodulation responses on 12 of the 22 legumes we tested. On roots of Macroptilium atropurpureum, Leucaena leucocephala and Vigna unguiculata, ANU265::pMiniSym2 formed mature-like nodule and successfully infected nodule cells. While cowpea and siratro responded to nodule colonization with defense responses that eventually eliminated bacteria, L. leucocephala formed leghemoglobin-containing mature-like nodules inside which the pMiniSym2 transconjugant established persistent intracellular colonies. These data show seven nodulation genes of NGR234 suffice to trigger nodule formation on roots of many hosts and to establish chronic infections in Leucaena cells. Full article
(This article belongs to the Special Issue Genetic Evolution of Root Nodule Symbioses)
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14 pages, 10284 KiB  
Article
Identification of Bradyrhizobium elkanii USDA61 Type III Effectors Determining Symbiosis with Vigna mungo
by Hien P. Nguyen, Safirah T. N. Ratu, Michiko Yasuda, Neung Teaumroong and Shin Okazaki
Genes 2020, 11(5), 474; https://doi.org/10.3390/genes11050474 - 27 Apr 2020
Cited by 11 | Viewed by 4436
Abstract
Bradyrhizobium elkanii USDA61 possesses a functional type III secretion system (T3SS) that controls host-specific symbioses with legumes. Here, we demonstrated that B. elkanii T3SS is essential for the nodulation of several southern Asiatic Vigna mungo cultivars. Strikingly, inactivation of either Nod factor synthesis [...] Read more.
Bradyrhizobium elkanii USDA61 possesses a functional type III secretion system (T3SS) that controls host-specific symbioses with legumes. Here, we demonstrated that B. elkanii T3SS is essential for the nodulation of several southern Asiatic Vigna mungo cultivars. Strikingly, inactivation of either Nod factor synthesis or T3SS in B. elkanii abolished nodulation of the V. mungo plants. Among the effectors, NopL was identified as a key determinant for T3SS-dependent symbiosis. Mutations of other effector genes, such as innB, nopP2, and bel2-5, also impacted symbiotic effectiveness, depending on host genotypes. The nopL deletion mutant formed no nodules on V. mungo, but infection thread formation was still maintained, thereby suggesting its pivotal role in nodule organogenesis. Phylogenetic analyses revealed that NopL was exclusively conserved among Bradyrhizobium and Sinorhizobium (Ensifer) species and showed a different phylogenetic lineage from T3SS. These findings suggest that V. mungo evolved a unique symbiotic signaling cascade that requires both NFs and T3Es (NopL). Full article
(This article belongs to the Special Issue Genetic Evolution of Root Nodule Symbioses)
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12 pages, 1379 KiB  
Article
The Peptidoglycan Biosynthesis Gene murC in Frankia: Actinorhizal vs. Plant Type
by Fede Berckx, Daniel Wibberg, Jörn Kalinowski and Katharina Pawlowski
Genes 2020, 11(4), 432; https://doi.org/10.3390/genes11040432 - 16 Apr 2020
Cited by 5 | Viewed by 3556
Abstract
Nitrogen-fixing Actinobacteria of the genus Frankia can be subdivided into four phylogenetically distinct clades; members of clusters one to three engage in nitrogen-fixing root nodule symbioses with actinorhizal plants. Mur enzymes are responsible for the biosynthesis of the peptidoglycan layer of bacteria. The [...] Read more.
Nitrogen-fixing Actinobacteria of the genus Frankia can be subdivided into four phylogenetically distinct clades; members of clusters one to three engage in nitrogen-fixing root nodule symbioses with actinorhizal plants. Mur enzymes are responsible for the biosynthesis of the peptidoglycan layer of bacteria. The four Mur ligases, MurC, MurD, MurE, and MurF, catalyse the addition of a short polypeptide to UDP-N-acetylmuramic acid. Frankia strains of cluster-2 and cluster-3 contain two copies of murC, while the strains of cluster-1 and cluster-4 contain only one. Phylogenetically, the protein encoded by the murC gene shared only by cluster-2 and cluster-3, termed MurC1, groups with MurC proteins of other Actinobacteria. The protein encoded by the murC gene found in all Frankia strains, MurC2, shows a higher similarity to the MurC proteins of plants than of Actinobacteria. MurC2 could have been either acquired via horizontal gene transfer or via gene duplication and convergent evolution, while murC1 was subsequently lost in the cluster-1 and cluster-4 strains. In the nodules induced by the cluster-2 strains, the expression levels of murC2 were significantly higher than those of murC1. Thus, there is clear sequence divergence between both types of Frankia MurC, and Frankia murC1 is in the process of being replaced by murC2, indicating selection in favour of murC2. Nevertheless, protein modelling showed no major structural differences between the MurCs from any phylogenetic group examined. Full article
(This article belongs to the Special Issue Genetic Evolution of Root Nodule Symbioses)
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15 pages, 3936 KiB  
Article
Ohr and OhrR Are Critical for Organic Peroxide Resistance and Symbiosis in Azorhizobium caulinodans ORS571
by Yang Si, Dongsen Guo, Shuoxue Deng, Xiuming Lu, Juanjuan Zhu, Bei Rao, Yajun Cao, Gaofei Jiang, Daogeng Yu, Zengtao Zhong and Jun Zhu
Genes 2020, 11(3), 335; https://doi.org/10.3390/genes11030335 - 20 Mar 2020
Cited by 14 | Viewed by 3252
Abstract
Azorhizobium caulinodans is a symbiotic nitrogen-fixing bacterium that forms both root and stem nodules on Sesbania rostrata. During nodule formation, bacteria have to withstand organic peroxides that are produced by plant. Previous studies have elaborated on resistance to these oxygen radicals in [...] Read more.
Azorhizobium caulinodans is a symbiotic nitrogen-fixing bacterium that forms both root and stem nodules on Sesbania rostrata. During nodule formation, bacteria have to withstand organic peroxides that are produced by plant. Previous studies have elaborated on resistance to these oxygen radicals in several bacteria; however, to the best of our knowledge, none have investigated this process in A. caulinodans. In this study, we identified and characterised the organic hydroperoxide resistance gene ohr (AZC_2977) and its regulator ohrR (AZC_3555) in A. caulinodans ORS571. Hypersensitivity to organic hydroperoxide was observed in an ohr mutant. While using a lacZ-based reporter system, we revealed that OhrR repressed the expression of ohr. Moreover, electrophoretic mobility shift assays demonstrated that OhrR regulated ohr by direct binding to its promoter region. We showed that this binding was prevented by OhrR oxidation under aerobic conditions, which promoted OhrR dimerization and the activation of ohr. Furthermore, we showed that one of the two conserved cysteine residues in OhrR, Cys11, was critical for the sensitivity to organic hydroperoxides. Plant assays revealed that the inactivation of Ohr decreased the number of stem nodules and nitrogenase activity. Our data demonstrated that Ohr and OhrR are required for protecting A. caulinodans from organic hydroperoxide stress and play an important role in the interaction of the bacterium with plants. The results that were obtained in our study suggested that a thiol-based switch in A. caulinodans might sense host organic peroxide signals and enhance symbiosis. Full article
(This article belongs to the Special Issue Genetic Evolution of Root Nodule Symbioses)
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13 pages, 2314 KiB  
Article
Evolution of the Small Family of Alternative Splicing Modulators Nuclear Speckle RNA-Binding Proteins in Plants
by Leandro Lucero, Jeremie Bazin, Johan Rodriguez Melo, Fernando Ibañez, Martín D. Crespi and Federico Ariel
Genes 2020, 11(2), 207; https://doi.org/10.3390/genes11020207 - 18 Feb 2020
Cited by 11 | Viewed by 3456
Abstract
RNA-Binding Protein 1 (RBP1) was first identified as a protein partner of the long noncoding RNA (lncRNA) ENOD40 in Medicago truncatula, involved in symbiotic nodule development. RBP1 is localized in nuclear speckles and can be relocalized to the cytoplasm by the interaction [...] Read more.
RNA-Binding Protein 1 (RBP1) was first identified as a protein partner of the long noncoding RNA (lncRNA) ENOD40 in Medicago truncatula, involved in symbiotic nodule development. RBP1 is localized in nuclear speckles and can be relocalized to the cytoplasm by the interaction with ENOD40. The two closest homologs to RBP1 in Arabidopsis thaliana were called Nuclear Speckle RNA-binding proteins (NSRs) and characterized as alternative splicing modulators of specific mRNAs. They can recognize in vivo the lncRNA ALTERNATIVE SPLICING COMPETITOR (ASCO) among other lncRNAs, regulating lateral root formation. Here, we performed a phylogenetic analysis of NSR/RBP proteins tracking the roots of the family to the Embryophytes. Strikingly, eudicots faced a reductive trend of NSR/RBP proteins in comparison with other groups of flowering plants. In Medicago truncatula and Lotus japonicus, their expression profile during nodulation and in specific regions of the symbiotic nodule was compared to that of the lncRNA ENOD40, as well as to changes in alternative splicing. This hinted at distinct and specific roles of each member during nodulation, likely modulating the population of alternatively spliced transcripts. Our results establish the basis to guide future exploration of NSR/RBP function in alternative splicing regulation in different developmental contexts along the plant lineage. Full article
(This article belongs to the Special Issue Genetic Evolution of Root Nodule Symbioses)
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Review

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15 pages, 478 KiB  
Review
Evolution of NIN and NIN-like Genes in Relation to Nodule Symbiosis
by Jieyu Liu and Ton Bisseling
Genes 2020, 11(7), 777; https://doi.org/10.3390/genes11070777 - 11 Jul 2020
Cited by 38 | Viewed by 6598
Abstract
Legumes and actinorhizal plants are capable of forming root nodules symbiosis with rhizobia and Frankia bacteria. All these nodulating species belong to the nitrogen fixation clade. Most likely, nodulation evolved once in the last common ancestor of this clade. NIN (NODULE INCEPTION) is [...] Read more.
Legumes and actinorhizal plants are capable of forming root nodules symbiosis with rhizobia and Frankia bacteria. All these nodulating species belong to the nitrogen fixation clade. Most likely, nodulation evolved once in the last common ancestor of this clade. NIN (NODULE INCEPTION) is a transcription factor that is essential for nodulation in all studied species. Therefore, it seems probable that it was recruited at the start when nodulation evolved. NIN is the founding member of the NIN-like protein (NLP) family. It arose by duplication, and this occurred before nodulation evolved. Therefore, several plant species outside the nitrogen fixation clade have NLP(s), which is orthologous to NIN. In this review, we discuss how NIN has diverged from the ancestral NLP, what minimal changes would have been essential for it to become a key transcription controlling nodulation, and which adaptations might have evolved later. Full article
(This article belongs to the Special Issue Genetic Evolution of Root Nodule Symbioses)
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16 pages, 1767 KiB  
Review
Symbiotic Outcome Modified by the Diversification from 7 to over 700 Nodule-Specific Cysteine-Rich Peptides
by Proyash Roy, Mingkee Achom, Helen Wilkinson, Beatriz Lagunas and Miriam L. Gifford
Genes 2020, 11(4), 348; https://doi.org/10.3390/genes11040348 - 25 Mar 2020
Cited by 25 | Viewed by 5899
Abstract
Legume-rhizobium symbiosis represents one of the most successfully co-evolved mutualisms. Within nodules, the bacterial cells undergo distinct metabolic and morphological changes and differentiate into nitrogen-fixing bacteroids. Legumes in the inverted repeat lacking clade (IRLC) employ an array of defensin-like small secreted peptides (SSPs), [...] Read more.
Legume-rhizobium symbiosis represents one of the most successfully co-evolved mutualisms. Within nodules, the bacterial cells undergo distinct metabolic and morphological changes and differentiate into nitrogen-fixing bacteroids. Legumes in the inverted repeat lacking clade (IRLC) employ an array of defensin-like small secreted peptides (SSPs), known as nodule-specific cysteine-rich (NCR) peptides, to regulate bacteroid differentiation and activity. While most NCRs exhibit bactericidal effects in vitro, studies confirm that inside nodules they target the bacterial cell cycle and other cellular pathways to control and extend rhizobial differentiation into an irreversible (or terminal) state where the host gains control over bacteroids. While NCRs are well established as positive regulators of effective symbiosis, more recent findings also suggest that NCRs affect partner compatibility. The extent of bacterial differentiation has been linked to species-specific size and complexity of the NCR gene family that varies even among closely related species, suggesting a more recent origin of NCRs followed by rapid expansion in certain species. NCRs have diversified functionally, as well as in their expression patterns and responsiveness, likely driving further functional specialisation. In this review, we evaluate the functions of NCR peptides and their role as a driving force underlying the outcome of rhizobial symbiosis, where the plant is able to determine the outcome of rhizobial interaction in a temporal and spatial manner. Full article
(This article belongs to the Special Issue Genetic Evolution of Root Nodule Symbioses)
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20 pages, 2116 KiB  
Review
Experimental Evolution of Legume Symbionts: What Have We Learnt?
by Ginaini Grazielli Doin de Moura, Philippe Remigi, Catherine Masson-Boivin and Delphine Capela
Genes 2020, 11(3), 339; https://doi.org/10.3390/genes11030339 - 23 Mar 2020
Cited by 16 | Viewed by 6191
Abstract
Rhizobia, the nitrogen-fixing symbionts of legumes, are polyphyletic bacteria distributed in many alpha- and beta-proteobacterial genera. They likely emerged and diversified through independent horizontal transfers of key symbiotic genes. To replay the evolution of a new rhizobium genus under laboratory conditions, the symbiotic [...] Read more.
Rhizobia, the nitrogen-fixing symbionts of legumes, are polyphyletic bacteria distributed in many alpha- and beta-proteobacterial genera. They likely emerged and diversified through independent horizontal transfers of key symbiotic genes. To replay the evolution of a new rhizobium genus under laboratory conditions, the symbiotic plasmid of Cupriavidus taiwanensis was introduced in the plant pathogen Ralstonia solanacearum, and the generated proto-rhizobium was submitted to repeated inoculations to the C. taiwanensis host, Mimosa pudica L. This experiment validated a two-step evolutionary scenario of key symbiotic gene acquisition followed by genome remodeling under plant selection. Nodulation and nodule cell infection were obtained and optimized mainly via the rewiring of regulatory circuits of the recipient bacterium. Symbiotic adaptation was shown to be accelerated by the activity of a mutagenesis cassette conserved in most rhizobia. Investigating mutated genes led us to identify new components of R. solanacearum virulence and C. taiwanensis symbiosis. Nitrogen fixation was not acquired in our short experiment. However, we showed that post-infection sanctions allowed the increase in frequency of nitrogen-fixing variants among a non-fixing population in the M. pudica–C. taiwanensis system and likely allowed the spread of this trait in natura. Experimental evolution thus provided new insights into rhizobium biology and evolution. Full article
(This article belongs to the Special Issue Genetic Evolution of Root Nodule Symbioses)
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