We show here that MtN5 is a NF-responsive gene expressed at a very early phase of symbiosis in epidermal cells and root hairs. MtN5 expression is induced in vitro by rhizobial effector molecules and by auxin and cytokinin, phytohormones involved in nodule organogenesis. Furthermore, lipid signaling is implicated in the response of MtN5 to rhizobia, since the activity of phospholipase D is required for MtN5 induction in S. meliloti-inoculated roots. MtN5-silenced roots inoculated with rhizobia display an increased root hair curling and a reduced number of invaded primordia compared to that in wild type roots, but with no impairment to nodule primordia formation. This phenotype is associated with the stimulation of ENOD11 expression, an early marker of infection, and with the down-regulation of Flotillin 4 (FLOT4), a protein involved in rhizobial entry.
Drought stress is a major factor limiting nitrogen fixation (NF) in crop production. However, the regulatory mechanism involved and the origin of the inhibition, whether local or systemic, is still controversial and so far scarcely studied in temperate forage legumes. Medicago truncatula plants were symbiotically grown with a split-root system and exposed to gradual water deprivation. Physiological parameters, NF activity, and amino acid content were measured. The partial drought treatment inhibited NF in the nodules directly exposed to drought stress. Concomitantly, in the droughted below-ground organs, amino acids accumulated prior to any drop in evapotranspiration (ET). It is concluded that drought exerts a local inhibition of NF and drives an overall accumulation of amino acids in diverse plant organs which is independent of the decrease in ET. The general increase in the majority of single amino acids in the whole plant questions the commonly accepted concept of a single amino acid acting as an N-feedback signal.
Understanding the interactions of plants with beneficial and pathogenic microbes is a promising avenue to improve crop productivity and agriculture sustainability. Proteomic techniques provide a unique angle to describe these intricate interactions and test hypotheses. The various approaches for proteomic analysis generally include protein/peptide separation and identification, but can also provide quantification and the characterization of post-translational modifications. In this review, we discuss how these techniques have been applied to the study of plant-microbe interactions. We also present some areas where this field of study would benefit from the utilization of newly developed methods that overcome previous limitations. Finally, we reinforce the need for expanding, integrating, and curating protein databases, as well as the benefits of combining protein-level datasets with those from genetic analyses and other high-throughput large-scale approaches for a systems-level view of plant-microbe interactions.
Dhileepkumar Jayaraman, Kari L. Forshey, Paul A. Grimsrud and Jean-Michel Ané
Arbuscular mycorrhizal (AM) fungi are involved in one of the most widespread plant–fungus interactions. A number of studies on the population dynamics of AM fungi have used mitochondrial (mt) DNA sequences, and yet mt AM fungus genomes are poorly known. To date, four mt genomes of three species of AM fungi are available, among which are two from Rhizophagus irregularis. In order to study intra- and interstrain mt genome variability of R. irregularis, we sequenced and de novo assembled four additional mt genomes of this species. We used 454 pyrosequencing and Illumina technologies to directly sequence mt genomes from total genomic DNA. The mt genomes are unique within each strain. Interstrain divergences in genome size, as a result of highly polymorphic intergenic and intronic sequences, were observed. The polymorphism is brought about by three types of variability generating element (VGE): homing endonucleases, DNA polymerase domain-containing open reading frames and small inverted repeats. Based on VGE positioning, mt sequences and nuclear markers, two subclades of R. irregularis were characterized. The discovery of VGEs highlights the great intraspecific plasticity of the R. irregularis mt genome. VGEs allow the design of powerful mt markers for the typing and monitoring of R. irregularis strains in genetic and population studies.
Damien Formey, Marion Molès, Alexandra Haouy, Bruno Savelli, Olivier Bouchez, Guillaume Bécard, Christophe Roux
Volume 196, Issue 4, pages 1217–1227, December 2012
New Zealand became geographically isolated about 80 million years ago and this separation gave rise to a unique native flora including four genera of legume, Carmichaelia, Clianthus and Montigena in the Carmichaelinae clade, tribe Galegeae, and Sophora, tribe Sophoreae, sub-family Papilionoideae. Ten bacterial strains isolated from NZ Carmichaelinae growing in natural ecosystems grouped close to the Mesorhizobium huakuii type strain in relation to their 16S rRNA and nifH gene sequences. However, the ten strains separated into four groups on the basis of their recA and glnII sequences: all groups were clearly distinct from all Mesorhizobium type strains. The ten strains separated into two groups on the basis of their nodA sequences but grouped closely together in relation to nodC sequences; all nodA and nodC sequences were novel. Seven strains selected and the M. huakuii type strain (isolated from Astragalus sinicus) produced functional nodules on Carmichaelia spp., Clianthus puniceus and A. sinicus but did not nodulate two Sophora species. We conclude that rhizobia closely related to M. huakuii on the basis of 16S rRNA and nifH gene sequences, but with variable recA and glnII genes and novel nodA and nodC genes, are common symbionts of NZ Carmichaelinae.
Heng Wee Tan, Bevan S. Weir, Noel Carter, Peter B. Heenan, Hayley J. Ridgway, Euan K. James, Janet I. Sprent, J. Peter W. Young, Mitchell Andrews (2012). PLoS ONE 7(10): e47677.
In two papers to be published in Current Biology, researchers from JIC and The Sainsbury Laboratory on the Norwich Research Park, and Rothamsted Research and the University of York identify genes that help plants interact with microbes in the soil.
Professor Giles Oldroyd of the John Innes Centre explains how plant roots form beneficial interactions with soil microbes. Almost all plants associate with mycorrhizal fungi to help in the uptake of nutrients such as phosphate. Some plants, particularly legumes, also associate with bacteria that ‘fix’ atmospheric nitrogen into a form the plant can use as fertiliser.
These two interactions are mediated within the plant by a common signalling pathway. The researchers have identified a specific mycorrhizal transcription factor. They also show how the signalling pathway has been recruited by pathogenic microbes, presenting a challenge to the plant. Its ability to form beneficial interactions can leave it vulnerable to invasion by pathogens.
Wang, E., Schornack, S., Marsh, J.F., Gobbato, E., Schwessinger, B., Eastmond, P., Schultze, M., Kamoun, S., and Oldroyd, G.E.D. (2012). A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. http://dx.doi.org/10.1016/j.cub.2012.09.043
Gobbato, E., Marsh, J.F., Vernie´ , T., Wang, E., Maillet, F., Kim, J., Miller, J.B., Sun, J., Bano, S.A., Ratet, P., et al. (2012). A GRAS-type transcription factor with a specific function in mycorrhizal signalling. Curr. Biol. http://dx.doi.org/10.1016/j.cub
The H2 is an obligate by-product of N-fixation. Recycling of H2 through uptake hydrogenase (Hup) inside the root nodules of leguminous plants is often considered an advantage for plants.
Rhizobia are soil bacteria capable of fixing atmospheric nitrogen when living in symbiosis with legumes inside root nodules. Nodulation is the fascinating result of complex interactions between the bacteria and the host.
In this segment, Dr. Gail Wilson, Associate Professor of Natural Resource ecology and management, joins Oklahoma Gardening host Kim Toscano for a close look at fungal life beneath the soil surface.
Nitrous oxide (N2O) is a greenhouse gas that is also capable of destroying the ozone layer1. Agricultural soil is the largest source of N2O (ref. 2). Soybean is a globally important leguminous crop, and hosts symbiotic nitrogen-fixing soil bacteria (rhizobia) that can also produce N2O (ref. 3). In agricultural soil, N2O is emitted from fertilizer and soil nitrogen. In soybean ecosystems, N2O is also emitted from the degradation of the root nodules4. Organic nitrogen inside the nodules is mineralized to NH4+, followed by nitrification and denitrification that produce N2O. N2O is then emitted into the atmosphere or is further reduced to N2 by N2O reductase (N2OR), which is encoded by the nosZ gene. Pure culture and vermiculite pot experiments showed lower N2O emission by nosZ+ strains5 and nosZ++ strains (mutants with increased N2OR activity)6 of Bradyrhizobium japonicum than by nosZ− strains. A pot experiment using soil confirmed these results7. Although enhancing N2OR activity has been suggested as a N2O mitigation option8, 9, this has never been tested in the field. Here, we show that post-harvest N2O emission from soybean ecosystems due to degradation of nodules can be mitigated by inoculation of nosZ+ and non-genetically modified organism nosZ++ strains of B. japonicum at a field scale.
Until recently it had been well established that the initial step in legume-rhizobia symbioses was flavonoid and Nod factor (NF) signaling. However, NF-independent symbiosis is now known to occur between Bradyrhizobium and some species of Aeschynomene. Since its discovery, this unusual symbiotic system has attracted attention and efforts have been devoted to revealing the NF-independent symbiotic mechanism, though the molecular mechanisms of nodule initiation still remain to be elucidated. NF-independent symbiosis is also interesting from the perspective of the evolution of legume-rhizobia symbiosis. In this mini-review, we discuss the current literature on the NF-independent symbiotic system in terms of phylogeny of the partners, infection, bacteroid differentiation, nodule structure, photosynthesis, endophytic features, and model host plant. We also discuss NF-independent symbiosis, which is generally regarded to be more primitive than NF-dependent symbiosis, because the bacteria invade host plants via “crack entry”. We propose three possible scenarios concerning the evolution of NF-independent symbiosis, which do not exclude the possibility that the NF-independent system evolved from NF-dependent interactions. Finally, we examine an interesting question on Bradyrhizobium-Aeschynomene mutualism, which is how they do initiate symbiosis without NF? Phylogenetic and genomic analyses of symbiotic and non-symbiotic bradyrhizobia with A. indica may be crucial to address the question, because of the very narrow phylogeny of natural endosymbionts without nod genes compared to other legume-rhizobia symbioses.
Takashi Okubo, Shohei Fukushima and Kiwamu Minamisawa (2012). Plant Cell Physiol doi: 10.1093/pcp/pcs150 First published online: November 18, 2012
The Fungal Genetics Policy Committee invites you to attend the 27th Fungal Genetics Conference, sponsored by the Genetics Society of America. The meeting is held every two years at the Asilomar Conference Grounds, Pacific Grove, California (near Monterey, California). The conference will open on Tuesday evening, March 12 with an Opening Mixer from 7:30 pm – 10:30 pm and end on Sunday, March 17. Regine Kahmann will present the Perkins/Metzenberg Lecture on Saturday, March 16 at 6:30 pm, followed by the banquet and closing party.
Chairs of the Scientific Program: Katherine Borkovich, University of California, Riverside Francis Martin, INRA, Nancy, France
As sessile organisms that cannot evade adverse environmental conditions, plants have evolved various adaptive strategies to cope with environmental stresses. One of the most successful adaptations is the formation of symbiotic associations with beneficial microbes. In these mutualistic interactions the partners exchange essential nutrients and improve their resistance to biotic and abiotic stresses. In arbuscular mycorrhiza (AM) and in root nodule symbiosis (RNS), AM fungi and rhizobia, respectively, penetrate roots and accommodate within the cells of the plant host. In these endosymbiotic associations, both partners keep their plasma membranes intact and use them to control the bidirectional exchange of signaling molecules and nutrients. Intracellular accommodation requires the exchange of symbiotic signals and the reprogramming of both interacting partners. This involves fundamental changes at the level of gene expression and of the cytoskeleton, as well as of organelles such as plastids, endoplasmic reticulum (ER), and the central vacuole. Symbiotic cells are highly compartmentalized and have a complex membrane system specialized for the diverse functions in molecular communication and nutrient exchange. Here, we discuss the roles of the different cellular membrane systems and their symbiosis-related proteins in AM and RNS, and we review recent progress in the analysis of membrane proteins involved in endosymbiosis.
The symbiotic association between plants and arbuscular mycorrhizal fungi is almost ubiquitous within the plant kingdom [1], and the early stages of the association are controlled by plant-derived strigolactone acting as a signal to the fungus in the rhizosphere [2–4] and lipochito-oligosaccharides acting as fungal signals to the plant [5]. Hyphopodia form at the root surface, allowing the initial invasion, and this is analogous to appressoria, infection structures of pathogenic fungi and oomycetes. Here, we characterize RAM2, a gene of Medicago truncatula required for colonization of the root by mycorrhizal fungi, which is necessary for appropriate hyphopodia and arbuscule formation. RAM2 encodes a glycerol-3-phosphate acyl transferase (GPAT) and is involved in the production of cutin monomers. Plants defective in RAM2 are unable to be colonized by arbuscular mycorrhizal fungi but also show defects in colonization by an oomycete pathogen, with the absence of appressoria formation. RAM2 defines a direct signaling function, because exogenous addition of the C16 aliphatic fatty acids associated with cutin are sufficient to promote hyphopodia/ appressoria formation. Thus, cutin monomers act as plant signals that promote colonization by arbuscular mycorrhizal fungi, and this signaling function has been recruited by pathogenic oomycetes to facilitate their own invasion.
New Zealand became geographically isolated about 80 million years ago and this separation gave rise to a unique native flora including four genera of legume, Carmichaelia, Clianthus and Montigena in the Carmichaelinae clade, tribe Galegeae, and...
Medicago truncatula is one of the most studied model plants. Nevertheless, the genome of this legume remains incompletely determined. We used RNA-Seq to characterize the transcriptome during the early organogenesis of the nodule and during its functioning. We detected 37,333 expressed transcription units (TUs), 1,670 had never been described before and were functionally annotated. We identified 7,595 new transcribed regions, mostly corresponding to 5’ and 3’ UTR extensions and new exons associated with 5,264 previously annotated genes. We also inferred 23,165 putative transcript isoforms from 6,587 genes and measured the abundance of transcripts for each isoform, which suggests an important role for alternative splicing in the generation of proteome diversity in M. truncatula. Finally, we carried out a differential expression analysis, which provided a comprehensive view of transcriptional reprogramming during nodulation. In particular, depletion of nitric oxide in roots inoculated with Sinorhizobium meliloti greatly increased our understanding of the role of this reactive species in the optimal establishment of the symbiotic interaction, in revealing differential patterns of expression for 2,030 genes and, in pointing to the inhibition of the expression of defense genes.
www.ibioseminars.org Legume plants form specialized root nodules to host "rhizobia", nitrogen-fixing bacterial symbionts. Plants which can host symbiotic nitrogen fixing rhizobia are able to grow without exogenous nitrogen fertilizer.
Rhizobial surface polysaccharides are required for nodule formation on the roots of at least some legumes but the mechanism(s) by which they act are yet to be determined. As a first step to investigate the function of exopolysaccharide (EPS) in the formation of determinate nodules, we isolated Mesorhizobium loti mutants affected in various steps of EPS biosynthesis and characterised their symbiotic phenotypes on two Lotus species. The wild-type M. loti strain R7A produced both high-molecular-weight EPS and lower-molecular-weight (LMW) polysaccharide fractions whilst most mutant strains produced only LMW fractions. Mutants affected in predicted early biosynthetic steps (e.g. exoB) formed nitrogen-fixing nodules on L. corniculatus and L. japonicus cv. Gifu, whereas mutants affected in mid/late biosynthetic steps (e.g. exoU) induced uninfected nodule primordia, and occasionally a few infected nodules following a lengthy delay. These mutants were disrupted at the stage of infection thread (IT) development. Symbiotically-defective EPS and Nod factor mutants functionally complemented each other in co-inoculation experiments. The majority of full-length ITs observed harbored only the EPS mutant strain and did not show bacterial release, whereas the nitrogen-fixing nodules contained both mutants. Examination of the symbiotic proficiency of the exoU mutant on various L. japonicus ecotypes revealed both host and environmental factors were linked to the requirement for EPS. These results reveal a complex function for M. loti EPS in determinate nodule formation and suggest that EPS plays a signalling role at both the stages of IT initiation and bacterial release.
Kelly S, Muszyński A, Kawaharada Y, Hubber AM, Sullivan J, Sandal N, Carlson R, Stougaard J, Ronson C. (2012). Mol Plant Microbe Interact. Nov 7. [Epub ahead of print]
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