Special Issue "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: 15 July 2020.

Special Issue Editor

Prof. Dr. Katharina Pawlowski
Website
Guest Editor
Department of Ecology, Environment and Plant Sciences, Stockholm University, Stockholm, Sweden
Interests: plant; evolution; root nodule symbioses; arbuscular mycorrhiza

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 Thus, the hypothesis of independent gains has been replaced by the hypothesis of independent losses.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

Manuscript Submission Information

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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

Published Papers (7 papers)

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Research

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Open AccessArticle
A Minimal Genetic Passkey to Unlock Many Legume Doors to Root Nodulation by Rhizobia
Genes 2020, 11(5), 521; https://doi.org/10.3390/genes11050521 - 07 May 2020
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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Open AccessArticle
Identification of Bradyrhizobium elkanii USDA61 Type III Effectors Determining Symbiosis with Vigna mungo
Genes 2020, 11(5), 474; https://doi.org/10.3390/genes11050474 - 27 Apr 2020
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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Open AccessArticle
The Peptidoglycan Biosynthesis Gene murC in Frankia: Actinorhizal vs. Plant Type
Genes 2020, 11(4), 432; https://doi.org/10.3390/genes11040432 - 16 Apr 2020
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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Open AccessArticle
Ohr and OhrR Are Critical for Organic Peroxide Resistance and Symbiosis in Azorhizobium caulinodans ORS571
Genes 2020, 11(3), 335; https://doi.org/10.3390/genes11030335 - 20 Mar 2020
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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Open AccessArticle
Evolution of the Small Family of Alternative Splicing Modulators Nuclear Speckle RNA-Binding Proteins in Plants
Genes 2020, 11(2), 207; https://doi.org/10.3390/genes11020207 - 18 Feb 2020
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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Open AccessReview
Symbiotic Outcome Modified by the Diversification from 7 to over 700 Nodule-Specific Cysteine-Rich Peptides
Genes 2020, 11(4), 348; https://doi.org/10.3390/genes11040348 - 25 Mar 2020
Cited by 1
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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Open AccessReview
Experimental Evolution of Legume Symbionts: What Have We Learnt?
Genes 2020, 11(3), 339; https://doi.org/10.3390/genes11030339 - 23 Mar 2020
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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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.

Title: Autoregulation of Nodulation (AON) in legumes mirrors related plant development processes
Authors: Peter M. Gresshoff and Brett J. Ferguson
 
Title: Global diversity of Rhizobium leguminosarum symbionts of lentil
Authors: Riely, B.K. … and Cook, D.R.
 
Title: Genomic diversity and inoculant potential of a systematic collection of Ethiopia’s chickpea Mesorhizobia
Authors: Damtew, Z. … Cook, D.R. and Aseffa, F.
 
Title: Global diversity patterns in integrative conjugative elements of chickpea’s Mesorhizobia symbionts
Authors: Perilla-Henao, L., Greenlon, A. … Cook. D.R.
 
Title: Comparative genomics gives insights into the taxonomy of the Azoarcus-Aromatoleum group and reveals separate origins of nif in “plant-associated” aerobic Azoarcus and non-plant-associated anaerobic Aromatoleum
Authors: Marcel Lafos, Marta Maluk, Marcelo Batista, Madan Junghare, Manuel Carmona, Helisson Faoro, Leonardo M. Cruz, Federico Battistoni, Emanuel de Souza, Fabio Pedrosa, Wen-Ming Chen, Philip S. Poole, Ray A. Dixon, Euan K. James
 
Title: Harnessing transcriptome profiles during time course of actinorhizal nodulation to explore the role of LysM-RLKs gene family.
Authors: P. Francois, D. Gully, C. Longin, S. Cruveiller, D. Vallenet, M. Ouikene, J. Gueno, A. Sgahier, D. Bogusz, S. Svistoonoff, H. Gherbi, V. Hocher
 
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