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Special Issue "Molecular Signals in Nodulation Control"

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Biochemistry".

Deadline for manuscript submissions: closed (27 March 2016).

Special Issue Editors

Prof. Dr. Peter M. Gresshoff
E-Mail Website
Guest Editor
Centre for Integrative Legume Research (CILR), The University of Queensland, Brisbane St Lucia, QLD 4072, Australia
Interests: genetics and genomics of systemic control of nodulation in legumes; molecular genetics and molecular physiology of sustainable biofuel production from the legume tree Pongamia
Dr. Brett Ferguson
E-Mail Website
Guest Editor
Centre for Integrative Legume Research (CILR), The University of Queensland, Brisbane St Lucia, QLD 4072, Australia
Interests: legumes, legume nodulation and nitrogen fixation; Plant molecular physiology, signalling and development; plant functional genomics (genetics, transcriptomics); plant-microbe interactions (symbioses)

Special Issue Information

Dear Colleagues,

Our world is facing major problems relating to food production. According to an August 30th 2015 program of LANDLINE (ABC Australia), we lose 120,000,000 hectares of agricultural land per year due to population growth, associated urbanization, and desertification. The expected population of >10 billion human inhabitants of this planet by 2050 (only 35 years away!) will require an increase of 46% in staple grain production and about 76% in animal protein output. These goals may be difficult to achieve with predicted climate changes, sociological changes towards higher consumption, political and military unrest.

For these reasons, it is essential that we now focus biological research at increased productivity with increased sustainability. One aspect of plant production is the absolute requirement for nitrogen. It is a key element, next to carbon, in most biological molecules (such as metabolites, protein and even nucleic acids). In the past it was possible to recycle waste to supply this nitrogen need. However large-scale agriculture now relies on supplementation of field sites with industrial fertilisers including those providing nitrogen (such as various nitrate, urea, and ammonium formulation). This practice is NOT sustainable and not economically advantageous, as the increased yield is burdened by (1) the costs of energy-demanding production by the Haber-Bosch process, (2) environmental negatives such as nitrous oxide (a strong Greenhouse gas) release and (3) surface and ground water nitrification, leading to eutrophication (see the Mississippi River Delta in the Gulf of Mexico).

Thus, alternatives are needed. One of these is the natural process of nitrogen fixation as seen agriculturally in many legume crops, such as soybean, chickpea, clovers, medics, peas, peanuts, and even trees, such as acacia, robinia, and the biodiesel feedstock tree pongamia.

This process occurs in root organs called nodules, which are induced by a range of soil bacteria, broadly called “rhizobia”. These organised structures then provide the “prison” for the invading bacterium, so that the correct physiological conditions such as ample plant energy supply and restricted, but stable oxygen concentration are achieved.

Extensive international research on multiple levels of nodulation and nitrogen fixation over the last century have improved agricultural yield and lowered inputs. One only needs to look at the development of soybean in Brazil. Low and inconsistent yields half a century ago are now replaced by a robust and competitive industry.

However, like any biological process, there are genetic and environmental factors that control the outcome. There are legume mutants that fail to nodulate all together; some nodulate but fail to fix. There are acidic or nitrate-rich soils that suppress nodulation and, thus, the symbiotic input.

Research over the last decade has yielded insight into these, using approaches ranging from agronomic field trials to molecular genetic and genomic technologies. This Special Issue is devoted to the recent advances in the field of “Molecular Signals in Nodulation Control”. It is hoped that such advances help to increase the efficiency of the legume symbiosis, with the hope of providing an additional tool to resolve the anticipated problems associated with future food production.

Prof. Dr. Peter M. Gresshoff
Dr. Brett Ferguson
Guest Editors

Manuscript Submission Information

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Keywords

  • molecular control
  • hormones
  • legume
  • ligand modifications
  • miRNA
  • nodulation
  • peptides
  • receptors
  • symbiotic genes

Published Papers (9 papers)

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Editorial

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Editorial
Molecular Signals in Nodulation Control
Int. J. Mol. Sci. 2017, 18(1), 125; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms18010125 - 10 Jan 2017
Cited by 4 | Viewed by 1915
Abstract
Our world is facing major problems relating to food production. According to an August 30, 2015 program of LANDLINE (Australian Broadcasting Corporation, Australia),we lose 120,000,000 hectares of agricultural land per year due to population growth, associated urbanisation, and desertification. Full article
(This article belongs to the Special Issue Molecular Signals in Nodulation Control)

Research

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Communication
Expression Analysis of PIN Genes in Root Tips and Nodules of Medicago truncatula
Int. J. Mol. Sci. 2016, 17(8), 1197; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms17081197 - 25 Jul 2016
Cited by 15 | Viewed by 2461
Abstract
Polar auxin transport is dependent on the family of PIN-formed proteins (PINs), which are membrane transporters of anionic indole-3-acetic acid (IAA). It is assumed that polar auxin transport may be essential in the development and meristematic activity maintenance of Medicago truncatula [...] Read more.
Polar auxin transport is dependent on the family of PIN-formed proteins (PINs), which are membrane transporters of anionic indole-3-acetic acid (IAA). It is assumed that polar auxin transport may be essential in the development and meristematic activity maintenance of Medicago truncatula (M. truncatula) root nodules. However, little is known about the involvement of specific PIN proteins in M. truncatula nodulation. Using real-time quantitative PCR, we analyzed the expression patterns of all previously identified MtPIN genes and compared them between root nodules and root tips of M. truncatula. Our results demonstrated significant differences in the expression level of all 11 genes (MtPIN1MtPIN11) between examined organs. Interestingly, MtPIN9 was the only PIN gene with higher expression level in root nodules compared to root tips. This result is the first indication of PIN9 transporter potential involvement in M. truncatula nodulation. Moreover, relatively high expression level in root nodules was attributed to MtPINs encoding orthologs of Arabidopsis thaliana PIN5 subclade. PIN proteins from this subclade have been found to localize in the endoplasmic reticulum, which may indicate that the development and meristematic activity maintenance of M. truncatula root nodules is associated with intracellular homeostasis of auxins level and their metabolism in the endoplasmic reticulum. Full article
(This article belongs to the Special Issue Molecular Signals in Nodulation Control)
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Article
Molecular Signals Controlling the Inhibition of Nodulation by Nitrate in Medicago truncatula
Int. J. Mol. Sci. 2016, 17(7), 1060; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms17071060 - 02 Jul 2016
Cited by 21 | Viewed by 3829
Abstract
The presence of nitrogen inhibits legume nodule formation, but the mechanism of this inhibition is poorly understood. We found that 2.5 mM nitrate and above significantly inhibited nodule initiation but not root hair curling in Medicago trunatula. We analyzed protein abundance in [...] Read more.
The presence of nitrogen inhibits legume nodule formation, but the mechanism of this inhibition is poorly understood. We found that 2.5 mM nitrate and above significantly inhibited nodule initiation but not root hair curling in Medicago trunatula. We analyzed protein abundance in M. truncatula roots after treatment with either 0 or 2.5 mM nitrate in the presence or absence of its symbiont Sinorhizobium meliloti after 1, 2 and 5 days following inoculation. Two-dimensional gel electrophoresis combined with mass spectrometry was used to identify 106 differentially accumulated proteins responding to nitrate addition, inoculation or time point. While flavonoid-related proteins were less abundant in the presence of nitrate, addition of Nod gene-inducing flavonoids to the Sinorhizobium culture did not rescue nodulation. Accumulation of auxin in response to rhizobia, which is also controlled by flavonoids, still occurred in the presence of nitrate, but did not localize to a nodule initiation site. Several of the changes included defense- and redox-related proteins, and visualization of reactive oxygen species indicated that their induction in root hairs following Sinorhizobium inoculation was inhibited by nitrate. In summary, the presence of nitrate appears to inhibit nodulation via multiple pathways, including changes to flavonoid metabolism, defense responses and redox changes. Full article
(This article belongs to the Special Issue Molecular Signals in Nodulation Control)
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Article
Regulation of Small RNAs and Corresponding Targets in Nod Factor-Induced Phaseolus vulgaris Root Hair Cells
Int. J. Mol. Sci. 2016, 17(6), 887; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms17060887 - 04 Jun 2016
Cited by 16 | Viewed by 4745
Abstract
A genome-wide analysis identified the set of small RNAs (sRNAs) from the agronomical important legume Phaseolus vulgaris (common bean), including novel P. vulgaris-specific microRNAs (miRNAs) potentially important for the regulation of the rhizobia-symbiotic process. Generally, novel miRNAs are difficult to identify and [...] Read more.
A genome-wide analysis identified the set of small RNAs (sRNAs) from the agronomical important legume Phaseolus vulgaris (common bean), including novel P. vulgaris-specific microRNAs (miRNAs) potentially important for the regulation of the rhizobia-symbiotic process. Generally, novel miRNAs are difficult to identify and study because they are very lowly expressed in a tissue- or cell-specific manner. In this work, we aimed to analyze sRNAs from common bean root hairs (RH), a single-cell model, induced with pure Rhizobium etli nodulation factors (NF), a unique type of signal molecule. The sequence analysis of samples from NF-induced and control libraries led to the identity of 132 mature miRNAs, including 63 novel miRNAs and 1984 phasiRNAs. From these, six miRNAs were significantly differentially expressed during NF induction, including one novel miRNA: miR-RH82. A parallel degradome analysis of the same samples revealed 29 targets potentially cleaved by novel miRNAs specifically in NF-induced RH samples; however, these novel miRNAs were not differentially accumulated in this tissue. This study reveals Phaseolus vulgaris-specific novel miRNA candidates and their corresponding targets that meet all criteria to be involved in the regulation of the early nodulation events, thus setting the basis for exploring miRNA-mediated improvement of the common bean–rhizobia symbiosis. Full article
(This article belongs to the Special Issue Molecular Signals in Nodulation Control)
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Article
Metabolomic Profiling of Bradyrhizobium diazoefficiens-Induced Root Nodules Reveals Both Host Plant-Specific and Developmental Signatures
Int. J. Mol. Sci. 2016, 17(6), 815; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms17060815 - 27 May 2016
Cited by 26 | Viewed by 3624
Abstract
Bradyrhizobium diazoefficiens is a nitrogen-fixing endosymbiont, which can grow inside root-nodule cells of the agriculturally important soybean and other host plants. Our previous studies described B. diazoefficiens host-specific global expression changes occurring during legume infection at the transcript and protein level. In order [...] Read more.
Bradyrhizobium diazoefficiens is a nitrogen-fixing endosymbiont, which can grow inside root-nodule cells of the agriculturally important soybean and other host plants. Our previous studies described B. diazoefficiens host-specific global expression changes occurring during legume infection at the transcript and protein level. In order to further characterize nodule metabolism, we here determine by flow injection–time-of-flight mass spectrometry analysis the metabolome of (i) nodules and roots from four different B. diazoefficiens host plants; (ii) soybean nodules harvested at different time points during nodule development; and (iii) soybean nodules infected by two strains mutated in key genes for nitrogen fixation, respectively. Ribose (soybean), tartaric acid (mungbean), hydroxybutanoyloxybutanoate (siratro) and catechol (cowpea) were among the metabolites found to be specifically elevated in one of the respective host plants. While the level of C4-dicarboxylic acids decreased during soybean nodule development, we observed an accumulation of trehalose-phosphate at 21 days post infection (dpi). Moreover, nodules from non-nitrogen-fixing bacteroids (nifA and nifH mutants) showed specific metabolic alterations; these were also supported by independent transcriptomics data. The alterations included signs of nitrogen limitation in both mutants, and an increased level of a phytoalexin in nodules induced by the nifA mutant, suggesting that the tissue of these nodules exhibits defense and stress reactions. Full article
(This article belongs to the Special Issue Molecular Signals in Nodulation Control)
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Article
Impact of Faba Bean-Seed Rhizobial Inoculation on Microbial Activity in the Rhizosphere Soil during Growing Season
Int. J. Mol. Sci. 2016, 17(5), 784; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms17050784 - 20 May 2016
Cited by 16 | Viewed by 2531
Abstract
Inoculation of legume seeds with Rhizobium affects soil microbial community and processes, especially in the rhizosphere. This study aimed at assessing the effect of Rhizobium inoculation on microbial activity in the faba bean rhizosphere during the growing season in a field experiment on [...] Read more.
Inoculation of legume seeds with Rhizobium affects soil microbial community and processes, especially in the rhizosphere. This study aimed at assessing the effect of Rhizobium inoculation on microbial activity in the faba bean rhizosphere during the growing season in a field experiment on a Haplic Luvisol derived from loess. Faba bean (Vicia faba L.) seeds were non-inoculated (NI) or inoculated (I) with Rhizobium leguminosarum bv. viciae and sown. The rhizosphere soil was analyzed for the enzymatic activities of dehydrogenases, urease, protease and acid phosphomonoesterase, and functional diversity (catabolic potential) using the Average Well Color Development, Shannon-Weaver, and Richness indices following the community level physiological profiling from Biolog EcoPlate™. The analyses were done on three occasions corresponding to the growth stages of: 5–6 leaf, flowering, and pod formation. The enzymatic activities were higher in I than NI (p < 0.05) throughout the growing season. However, none of the functional diversity indices differed significantly under both treatments, regardless of the growth stage. This work showed that the functional diversity of the microbial communities was a less sensitive tool than enzyme activities in assessment of rhizobial inoculation effects on rhizosphere microbial activity. Full article
(This article belongs to the Special Issue Molecular Signals in Nodulation Control)
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Article
Bacterial Molecular Signals in the Sinorhizobium fredii-Soybean Symbiosis
Int. J. Mol. Sci. 2016, 17(5), 755; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms17050755 - 18 May 2016
Cited by 52 | Viewed by 3092
Abstract
Sinorhizobium (Ensifer) fredii (S. fredii) is a rhizobial species exhibiting a remarkably broad nodulation host-range. Thus, S. fredii is able to effectively nodulate dozens of different legumes, including plants forming determinate nodules, such as the important crops soybean and [...] Read more.
Sinorhizobium (Ensifer) fredii (S. fredii) is a rhizobial species exhibiting a remarkably broad nodulation host-range. Thus, S. fredii is able to effectively nodulate dozens of different legumes, including plants forming determinate nodules, such as the important crops soybean and cowpea, and plants forming indeterminate nodules, such as Glycyrrhiza uralensis and pigeon-pea. This capacity of adaptation to different symbioses makes the study of the molecular signals produced by S. fredii strains of increasing interest since it allows the analysis of their symbiotic role in different types of nodule. In this review, we analyze in depth different S. fredii molecules that act as signals in symbiosis, including nodulation factors, different surface polysaccharides (exopolysaccharides, lipopolysaccharides, cyclic glucans, and K-antigen capsular polysaccharides), and effectors delivered to the interior of the host cells through a symbiotic type 3 secretion system. Full article
(This article belongs to the Special Issue Molecular Signals in Nodulation Control)
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Review

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Review
Specificity in Legume-Rhizobia Symbioses
Int. J. Mol. Sci. 2017, 18(4), 705; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms18040705 - 26 Mar 2017
Cited by 106 | Viewed by 5386
Abstract
Most species in the Leguminosae (legume family) can fix atmospheric nitrogen (N2) via symbiotic bacteria (rhizobia) in root nodules. Here, the literature on legume-rhizobia symbioses in field soils was reviewed and genotypically characterised rhizobia related to the taxonomy of the legumes [...] Read more.
Most species in the Leguminosae (legume family) can fix atmospheric nitrogen (N2) via symbiotic bacteria (rhizobia) in root nodules. Here, the literature on legume-rhizobia symbioses in field soils was reviewed and genotypically characterised rhizobia related to the taxonomy of the legumes from which they were isolated. The Leguminosae was divided into three sub-families, the Caesalpinioideae, Mimosoideae and Papilionoideae. Bradyrhizobium spp. were the exclusive rhizobial symbionts of species in the Caesalpinioideae, but data are limited. Generally, a range of rhizobia genera nodulated legume species across the two Mimosoideae tribes Ingeae and Mimoseae, but Mimosa spp. show specificity towards Burkholderia in central and southern Brazil, Rhizobium/Ensifer in central Mexico and Cupriavidus in southern Uruguay. These specific symbioses are likely to be at least in part related to the relative occurrence of the potential symbionts in soils of the different regions. Generally, Papilionoideae species were promiscuous in relation to rhizobial symbionts, but specificity for rhizobial genus appears to hold at the tribe level for the Fabeae (Rhizobium), the genus level for Cytisus (Bradyrhizobium), Lupinus (Bradyrhizobium) and the New Zealand native Sophora spp. (Mesorhizobium) and species level for Cicer arietinum (Mesorhizobium), Listia bainesii (Methylobacterium) and Listia angolensis (Microvirga). Specificity for rhizobial species/symbiovar appears to hold for Galega officinalis (Neorhizobium galegeae sv. officinalis), Galega orientalis (Neorhizobium galegeae sv. orientalis), Hedysarum coronarium (Rhizobium sullae), Medicago laciniata (Ensifer meliloti sv. medicaginis), Medicago rigiduloides (Ensifer meliloti sv. rigiduloides) and Trifolium ambiguum (Rhizobium leguminosarum sv. trifolii). Lateral gene transfer of specific symbiosis genes within rhizobial genera is an important mechanism allowing legumes to form symbioses with rhizobia adapted to particular soils. Strain-specific legume rhizobia symbioses can develop in particular habitats. Full article
(This article belongs to the Special Issue Molecular Signals in Nodulation Control)
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Review
Legume NADPH Oxidases Have Crucial Roles at Different Stages of Nodulation
Int. J. Mol. Sci. 2016, 17(5), 680; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms17050680 - 18 May 2016
Cited by 33 | Viewed by 2768
Abstract
Plant NADPH oxidases, formerly known as respiratory burst oxidase homologues (RBOHs), are plasma membrane enzymes dedicated to reactive oxygen species (ROS) production. These oxidases are implicated in a wide variety of processes, ranging from tissue and organ growth and development to signaling pathways [...] Read more.
Plant NADPH oxidases, formerly known as respiratory burst oxidase homologues (RBOHs), are plasma membrane enzymes dedicated to reactive oxygen species (ROS) production. These oxidases are implicated in a wide variety of processes, ranging from tissue and organ growth and development to signaling pathways in response to abiotic and biotic stimuli. Research on the roles of RBOHs in the plant’s response to biotic stresses has mainly focused on plant-pathogen interactions; nonetheless, recent findings have shown that these oxidases are also involved in the legume-rhizobia symbiosis. The legume-rhizobia symbiosis leads to the formation of the root nodule, where rhizobia reduce atmospheric nitrogen to ammonia. A complex signaling and developmental pathway in the legume root hair and root facilitate rhizobial entrance and nodule organogenesis, respectively. Interestingly, several reports demonstrate that RBOH-mediated ROS production displays versatile roles at different stages of nodulation. The evidence collected to date indicates that ROS act as signaling molecules that regulate rhizobial invasion and also function in nodule senescence. This review summarizes discoveries that support the key and versatile roles of various RBOH members in the legume-rhizobia symbiosis. Full article
(This article belongs to the Special Issue Molecular Signals in Nodulation Control)
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