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

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

Deadline for manuscript submissions: 31 October 2017

Special Issue Editors

Guest Editor
Dr. Mitchell Andrews

Faculty of Agriculture and Life Sciences, Lincoln University, Lincoln 7647, New Zealand
Website | E-Mail
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

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All papers will be peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

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.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 1200 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

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

This special issue is now open for submission, see below for planned papers.

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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