Medicago truncatula is a model legume species used to investigate plant-microorganism interactions, notably root symbioses. Massive population genomic and transcriptomic data now available for this species open the way for a comprehensive investigation of genomic variations associated with adaptation of M. truncatula to its environment. Here we performed a fine-scale genome scan of selective sweep signatures in Medicago truncatula using more than 15 million SNPs identified on 283 accessions from two populations (Circum and Far West), and exploited annotation and published transcriptomic data to identify biological processes associated with molecular adaptation. We identified 58 swept genomic regions with a 15 kb average length and comprising 3.3 gene models on average. The unimodal sweep state probability distribution in these regions enabled us to focus on the best single candidate gene per region. We detected two unambiguous species-wide selective sweeps, one of which appears to underlie morphological adaptation. Population genomic analyses of the remaining 56 sweep signatures indicate that sweeps identified in the Far West population are less population-specific and probably more ancient than those identified in the Circum population. Functional annotation revealed a predominance of immunity-related adaptations in the Circum population. Transcriptomic data from accessions of the Far West population allowed inference of four clusters of co-regulated genes putatively involved in the adaptive control of symbiotic carbon flow and nodule senescence, as well as in other root adaptations upon infection with soil microorganisms. We demonstrate that molecular adaptations in Medicago truncatula were primarily triggered by selective pressures from root-associated micro-organisms.
The Rhizobiaceae family of Gram-negative bacteria often engage in symbiosis with plants of economic importance. Historically, genetic studies to identify the function of individual genes, and characterize the biology of these bacteria have relied on the use of classical transposon mutagenesis. To increase the rate of scientific discovery in the Rhizobiaceae there is a need to adapt high-throughput genetic screens like insertion sequencing for use in this family of bacteria. Here we describe a Rhizobiaceae compatible MmeI-adapted mariner transposon that can be used with insertion sequencing for high-throughput genetic screening.
Benjamin J Perry and Christopher K Yost (2014), BMC Microbiology, 14:298
The objective of this symposium is to create a scientific event that is at the forefront of fundamental research in diverse aspects of legume biology.
The meeting will be divided into 5 sessions: 1) Symbiosis; 2) Genomics; 3) Pathogenesis; 4) Physiology and stress responses; 5) Development
The symposium will bring together about 150 participants in a rather informal atmosphere, facilitating exchanges. We also aim at proposing a highly attractive program at a moderate inscription fee to give the opportunity to researchers - in particular those at the early stage of their career – to participate to an exciting top-level scientific event. Young researchers will have the opportunity to present their work with a poster.
Bacterial surface components, especially exopolysaccharides, in combination with bacterial Quorum Sensing signals are crucial for the formation of biofilms in most species studied so far. Biofilm formation allows soil bacteria to colonize their surrounding habitat and survive common environmental stresses such as desiccation and nutrient limitation. This mode of life is often essential for survival in bacteria of the genera Mesorhizobium,Sinorhizobium, Bradyrhizobium, and Rhizobium. The role of biofilm formation in symbiosis has been investigated in detail for Sinorhizobium meliloti and Bradyrhizobium japonicum. However, for S. fredii this process has not been studied. In this work we have demonstrated that biofilm formation is crucial for an optimal root colonization and symbiosis between S. fredii SMH12 and Glycine max cv Osumi. In this bacterium, nod-gene inducing flavonoids and the NodD1 protein are required for the transition of the biofilm structure from monolayer to microcolony. Quorum Sensing systems are also required for the full development of both types of biofilms. In fact, both the nodD1 mutant and the lactonase strain (the lactonase enzyme prevents AHL accumulation) are defective in soybean root colonization. The impairment of the lactonase strain in its colonization ability leads to a decrease in the symbiotic parameters. Interestingly, NodD1 together with flavonoids activates certain quorum sensing systems implicit in the development of the symbiotic biofilm. Thus, S. fredii SMH12 by means of a unique key molecule, the flavonoid, efficiently forms biofilm, colonizes the legume roots and activates the synthesis of Nod factors, required for successfully symbiosis.
Pérez-Montaño F, Jiménez-Guerrero I, Del Cerro P, Baena-Ropero I, López-Baena FJ, Ollero FJ, Bellogín R, Lloret J, Espuny R. (2014). PLoS One. 2014 Aug 28;9(8):e105901.
Mutualistic symbioses between eukaryotes and beneficial microorganisms of their microbiome play an essential role in nutrition, protection against disease, and development of the host. However, the impact of beneficial symbionts on the evolution of host genomes remains poorly characterized. Here we used the independent loss of the most widespread plant–microbe symbiosis, arbuscular mycorrhization (AM), as a model to address this question. Using a large phenotypic approach and phylogenetic analyses, we present evidence that loss of AM symbiosis correlates with the loss of many symbiotic genes in the Arabidopsis lineage (Brassicales). Then, by analyzing the genome and/or transcriptomes of nine other phylogenetically divergent non-host plants, we show that this correlation occurred in a convergent manner in four additional plant lineages, demonstrating the existence of an evolutionary pattern specific to symbiotic genes. Finally, we use a global comparative phylogenomic approach to track this evolutionary pattern among land plants. Based on this approach, we identify a set of 174 highly conserved genes and demonstrate enrichment in symbiosis-related genes. Our findings are consistent with the hypothesis that beneficial symbionts maintain purifying selection on host gene networks during the evolution of entire lineages.
Smut fungi are well-suited to investigate the ecology and evolution of plant pathogens, as they are strictly biotrophic, yet cultivable on media. Here we report the genome sequence of Melanopsichium pennsylvanicum, closely related to Ustilago maydis and other Poaceae-infecting smuts, but parasitic to a dicot plant. To explore the evolutionary patterns resulting from host adaptation after this huge host jump, the genome of Me. pennsylvanicum was sequenced and compared with the genomes of U. maydis, Sporisorium reilianum, and U. hordei. Although all four genomes had a similar completeness in CEGMA (Core Eukaryotic Genes Mapping Approach) analysis, gene absence was highest in Me. pennsylvanicum, and most pronounced in putative secreted proteins, which are often considered as effector candidates. In contrast, the amount of private genes was similar among the species, highlighting that gene loss rather than gene gain is the hallmark of adaptation after the host jump to the dicot host. Our analyses revealed a trend of putative effectors to be next to another putative effector, but the majority of these are not in clusters and thus the focus on pathogenicity clusters might not be appropriate for all smut genomes. Positive selection studies revealed that Me. pennsylvanicum has the highest number and proportion of genes under positive selection. In general, putative effectors showed a higher proportion of positively selected genes than noneffector candidates. The 248 putative secreted effectors found in all four smut genomes might constitute a core set needed for pathogenicity, whereas those 92 that are found in all grass-parasitic smuts but have no ortholog in Me. pennsylvanicum might constitute a set of effectors important for successful colonization of grass hosts.
Bacterial intercellular communication is crucial for developing population and community structures and for pathogenic and symbiotic interactions with eukaryotic hosts. Many Gram-negative bacteria use N-acyl-homoserine lactones (AHLs) in quorum sensing-related signaling. Although it is likely that specific transport mechanisms are required for long-chain AHLs to overcome the outer membrane, mechanisms promoting uptake have not been reported so far. Here we present evidence that homologs of the outer membrane long-chain fatty acid transporter FadL facilitate uptake of long-chain AHLs, which closes an important gap in our understanding of quorum sensing signaling. Our findings suggest that bacteria responding to long-chain AHLs have evolved specificity of FadL toward these signal molecules and have partly lost the ability to transport long-chain fatty acid by this protein.
Quorum sensing (QS) using N-acyl homoserine lactones (AHLs) as signal molecules is a common strategy used by diverse Gram-negative bacteria. A widespread mechanism of AHL sensing involves binding of these molecules by cytosolic LuxR-type transcriptional regulators, which requires uptake of external AHLs. The outer membrane is supposed to be an efficient barrier for diffusion of long-chain AHLs. Here we report evidence that in Sinorhizobium meliloti, sensing of AHLs with acyl chains composed of 14 or more carbons is facilitated by the outer membrane protein FadLSm, a homolog of the Escherichia coli FadLEc long-chain fatty acid transporter. The effect of fadLSm on AHL sensing was more prominent for longer and more hydrophobic signal molecules. Using reporter gene fusions to QS target genes, we found that fadLSm increased AHL sensitivity and accelerated the course of QS. In contrast to FadLEc, FadLSm did not support uptake of oleic acid, but did contribute to growth on palmitoleic acid. FadLSm homologs from related symbiotic α-rhizobia and the plant pathogen Agrobacterium tumefaciens differed in their ability to facilitate long-chain AHL sensing or to support growth on oleic acid. FadLAt was found to be ineffective toward long-chain AHLs. We obtained evidence that the predicted extracellular loop 5 of FadLSm and further α-rhizobial FadL proteins contains determinants of specificity to long-chain AHLs. Replacement of a part of loop 5 by the corresponding region from α-rhizobial FadL proteins transferred sensitivity for long-chain AHLs to FadLA
Elizaveta Krol and Anke Becker (2014). . Proc Natl Acad Sci U S A. Jul 7. pii: 201404929. [Epub ahead of print]
For reasons that are unclear, no eukaryotic enzymes can break the triple bond of N2. The reduction of N2 to NH3 (nitrogen fixation) is limited to prokaryotes and is catalysed by nitrogenase. Since most of the nitrogen entering the biosphere (around 100 million metric tonnes of N2 per annum) does so through nitrogenase activity (lightning contributes about 10%), those plants that associate with nitrogen-fixing bacteria have a significant selective advantage under conditions of limiting nitrogen
J. Allan Downie (2014). Current Biology Volume 24, Issue 5, 3 March 2014, Pages R184–R19
Diverse and rapidly evolving pathogens cause plant diseases and epidemics that threaten crop yield and food security around the world. Research over the last 25 years has led to an increasingly clear conceptual understanding of the molecular components of the plant immune system. Combined with ever-cheaper DNA-sequencing technology and the rich diversity of germ plasm manipulated for over a century by plant breeders, we now have the means to begin development of durable (long-lasting) disease resistance beyond the limits imposed by conventional breeding and in a manner that will replace costly and unsustainable chemical controls.
Plant immune genes, or resistance genes, are involved in a co-evolutionary arms race with a diverse range of pathogens. In agronomically important grasses, such R genes have been extensively studied because of their role in pathogen resistance and in the breeding of resistant cultivars. In this study, we evaluate the importance of recombination, mutation and selection on the evolution of the R gene complex Rp1 of Sorghum, Triticum, Brachypodium,Oryza and Zea. Analyses show that recombination is widespread, and we detected 73 independent instances of sequence exchange, involving on average 1567 of 4692 nucleotides analysed (33.4%). We were able to date 24 interspecific recombination events and found that four occurred postspeciation, which suggests that genetic introgression took place between different grass species. Other interspecific events seemed to have been maintained over long evolutionary time, suggesting the presence of balancing selection. Significant positive selection (i.e. a relative excess of nonsynonymous substitutions (dN/dS>1)) was detected in 17–95 codons (0.42–2.02%). Recombination was significantly associated with areas with high levels of polymorphism but not with an elevated dN/dS ratio. Finally, phylogenetic analyses show that recombination results in a general overestimation of the divergence time (mean = 14.3%) and an alteration of the gene tree topology if the tree is not calibrated. Given that the statistical power to detect recombination is determined by the level of polymorphism of the amplicon as well as the number of sequences analysed, it is likely that many studies have underestimated the importance of recombination relative to the mutation rate.
Phytobiomes 2015: Designing a New Paradigm for Crop Improvement brings together renowned experts in diverse fields related to phytobiomes with sessions ranging from the lessons that can be learned from other microbiome efforts to designing a path forward for a phytobiomes systems approach. Plan now to attend these 2 ½ days encompassing plenary speakers, discussions, and posters presentations.
We are honored to host the 19th International Congress on Nitrogen Fixation (19th ICNF). The meeting will be held at the beautiful Asilomar Conference Grounds in Pacific Grove, CA
AsilomarAsilomar State Beach and Conference Grounds is a breathtaking 107 acres of ecologically diverse beachfront land. It is conveniently located just eight (8) miles from The Monterey Peninsula Airport (MRY), 80 miles form San Jose Airport (SJC), and 110 miles south of the San Francisco Airport (SFO).
Ever since their discovery as key regulators of the jasmonate (JA) signaling pathway (Chini et al., 2007; Thines et al., 2007; Yan et al., 2007), repressor proteins of the JASMONATE ZIM-domain (JAZ) family have been rising stars in research on hormonal regulation of plant growth and defense. In plant cells, JAZ repressor proteins interact with an E3 ubiquitin ligase complex (SCFCOI1) that together function as a JA receptor. In resting cells, JAZs block the activity of transcriptional regulators of JA responses by physically binding to them. Upon perception of bioactive JAs, JAZ proteins are rapidly degraded via the ubiquitin/26S proteasome-dependent proteolytic pathway. This releases the JAZ-bound transcription factors, resulting in the activation of downstream JA responses (Fig. 1a). JAs play a dominant role in regulating defense responses against herbivorous insects and necrotrophic pathogens, and in adaptive responses to beneficial soilborne microbes (Wasternack & Hause, 2013; Pieterse et al., 2014). In addition, JAs have a signal function in a myriad other processes, including abiotic stress reactions and plant growth responses to environmental cues (Wasternack & Hause, 2013). The JA pathway functions in the context of a complex network of hormone-regulated signaling pathways that, depending on the environmental or developmental condition, can act antagonistically or synergistically on each other to finely balance resource allocation between growth and defense and minimize fitness tradeoffs (Pieterse et al., 2012; Vos et al., 2013). In the process of balancing plant growth and defense, gibberellins (GAs) have emerged as dominant antagonists of the JA signaling output (Hou et al., 2013).
Horizontal gene transfer (HGT) is an important mode of adaptation and diversification of prokaryotes and eukaryotes and a major event underlying the emergence of bacterial pathogens and mutualists. Yet it remains unclear how complex phenotypic traits such as the ability to fix nitrogen with legumes have successfully spread over large phylogenetic distances. Here we show, using experimental evolution coupled with whole genome sequencing, that co-transfer of imuABC error-prone DNA polymerase genes with key symbiotic genes accelerates the evolution of a soil bacterium into a legume symbiont. Following introduction of the symbiotic plasmid of Cupriavidus taiwanensis, the Mimosa symbiont, into pathogenic Ralstonia solanacearum we challenged transconjugants to become Mimosa symbionts through serial plant-bacteria co-cultures. We demonstrate that a mutagenesis imuABC cassette encoded on the C. taiwanensis symbiotic plasmid triggered a transient hypermutability stage in R. solanacearum transconjugants that occurred before the cells entered the plant. The generated burst in genetic diversity accelerated symbiotic adaptation of the recipient genome under plant selection pressure, presumably by improving the exploration of the fitness landscape. Finally, we show that plasmid imuABC cassettes are over-represented in rhizobial lineages harboring symbiotic plasmids. Our findings shed light on a mechanism that may have facilitated the dissemination of symbiotic competency among α- and β-proteobacteria in natura and provide evidence for the positive role of environment-induced mutagenesis in the acquisition of a complex lifestyle trait. We speculate that co-transfer of complex phenotypic traits with mutagenesis determinants might frequently enhance the ecological success of HGT.
Horizontal gene transfer has an extraordinary impact on microbe evolution and diversification, by allowing exploration of new niches such as higher organisms. This is the case for rhizobia, a group of phylogenetically diverse bacteria that form a nitrogen-fixing symbiotic relationship with most leguminous plants. While these arose through horizontal transfer of symbiotic plasmids, this in itself is usually unproductive, and full expression of the acquired traits needs subsequent remodeling of the genome to ensure the ecological success of the transfer. Here we uncover a mechanism that accelerates the evolution of a soil bacterium into a legume symbiont. We show that key symbiotic genes are co-transferred with genes encoding stress-responsive error-prone DNA polymerases that transiently elevate the mutation rate in the recipient genome. This burst in genetic diversity accelerates the symbiotic evolution process under selection pressure from the host plant. A more widespread involvement of plasmid mutagenesis cassettes in rhizobium evolution is supported by their overrepresentation in rhizobia-containing lineages. Our findings provide evidence for the role of environment-induced mutagenesis in the acquisition of a complex lifestyle trait and predict that co-transfer of complex phenotypic traits with mutagenesis determinants might help successful horizontal gene transfer.
Remigi P, Capela D, Clerissi C, Tasse L, Torchet R, et al. (2014) Transient Hypermutagenesis Accelerates the Evolution of Legume Endosymbionts following Horizontal Gene Transfer. PLoS Biol 12(9): e1001942
Salicylic acid is an important signalling molecule in plant-microbe defence and symbiosis. We analysed the transcriptional responses of the nitrogen fixing plant symbiont, Rhizobium leguminosarum bv viciae 3841 to salicylic acid. Two MFS-type multicomponent efflux systems were induced in response to salicylic acid, rmrAB and the hitherto undescribed system salRAB. Based on sequence similarity salA and salB encode a membrane fusion and inner membrane protein respectively. salAB are positively regulated by the LysR regulator SalR. Disruption of salA significantly increased the sensitivity of the mutant to salicylic acid, while disruption of rmrA did not. A salA/rmrA double mutation did not have increased sensitivity relative to the salA mutant. Pea plants nodulated by salA or rmrA strains did not have altered nodule number or nitrogen fixation rates, consistent with weak expression of salA in the rhizosphere and in nodule bacteria. However, BLAST analysis revealed seventeen putative efflux systems in Rlv3841 and several of these were highly differentially expressed during rhizosphere colonisation, host infection and bacteroid differentiation. This suggests they have an integral role in symbiosis with host plants.
Tett AJ, Karunakaran R, Poole PS (2014). PLoS One. 2014 Aug 18;9(8):e103647
Plant pathogens deploy an array of virulence factors to suppress host defense and promote pathogenicity. Numerous strains of Pseudomonas syringae produce the phytotoxin coronatine (COR). A major aspect of COR function is its ability to mimic a bioactive jasmonic acid (JA) conjugate and thus target the JA-receptor COR-insensitive 1 (COI1). Biological activities of COR include stimulation of JA-signaling and consequent suppression of SA-dependent defense through antagonistic crosstalk, antagonism of stomatal closure to allow bacterial entry into the interior of plant leaves, contribution to chlorotic symptoms in infected plants, and suppression of plant cell wall defense through perturbation of secondary metabolism. Here, we review the virulence function of COR, including updates on these established activities as well as more recent findings revealing COI1-independent activity of COR and shedding light on cooperative or redundant defense suppression between COR and type III effector proteins.
Biological invasions can be serious threats to local and even global biodiversity, but despite much study, little is known about the factors that enable particular introduced species to be successful invaders (1). On page 862 of this issue, Vilcinskas et al. (2) report an important advance in understanding these factors. They show that the almost worldwide invasive triumph of the harlequin ladybird Harmonia axyridis (3) depends on the presence of a coexisting pathogen within the invading insect and also the insect's immunity to the pathogen.
Strain CPAC 7 (=SEMIA 5080) was recently reclassified into the new species Bradyrhizobium diazoefficiens; due to its outstanding efficiency in fixing nitrogen, it has been used in commercial inoculants for application to crops of soybean [Glycine max (L.) Merr.] in Brazil and other South American countries. Although the efficiency of B. diazoefficiens inoculant strains is well recognized, few data on their protein expression are available.
We provided a two-dimensional proteomic reference map of CPAC 7 obtained under free-living conditions, with the successful identification of 115 spots, representing 95 different proteins. The results highlighted the expression of molecular determinants potentially related to symbiosis establishment (e.g. inositol monophosphatase, IMPase), fixation of atmospheric nitrogen (N2) (e.g. NifH) and defenses against stresses (e.g. chaperones). By using bioinformatic tools, it was possible to attribute probable functions to ten hypothetical proteins. For another ten proteins classified as "NO related COG" group, we analyzed by RT-qPCR the relative expression of their coding-genes in response to the nodulation-gene inducer genistein. Six of these genes were up-regulated, including blr0227, which may be related to polyhydroxybutyrate (PHB) biosynthesis and competitiveness for nodulation.
The proteomic map contributed to the identification of several proteins of B. diaozoefficiens under free-living conditions and our approach--combining bioinformatics and gene-expression assays--resulted in new information about unknown genes that might play important roles in the establishment of the symbiosis with soybean.
This new species includes strain USDA110, an agriculturally superb soybean inoculant strain. The study seems to suggest new pathways of efficient symbiotic nitrogen fixation heretofor uncharacterized. I like it, I like it very much.
The symbiotic α-rhizobia Sinorhizobium meliloti, Bradyrhizobium japonicum, Rhizobium etli and the related plant pathogen Agrobacterium tumefaciens are important model organisms for studying plant-microbe interactions. These metabolically versatile soil bacteria are characterized by complex lifestyles and large genomes. Here we summarize the recent knowledge on their small non-coding RNAs (sRNAs) including conservation, function, and interaction of the sRNAs with the RNA chaperone Hfq. In each of these organisms, an inventory of hundreds of cis- and trans-encoded sRNAs with regulatory potential was uncovered by high-throughput approaches and used for the construction of 39 sRNA family models. Genome-wide analyses of hfq mutants and co-immunoprecipitation with tagged Hfq revealed a major impact of the RNA chaperone on the physiology of plant-associated α-proteobacteria including symbiosis and virulence. Highly conserved members of the SmelC411 family are the AbcR sRNAs, which predominantly regulate ABC transport systems. AbcR1 of A. tumefaciens controls the uptake of the plant-generated signaling molecule GABA and is a central regulator of nutrient uptake systems. It has similar functions in S. meliloti and the human pathogen Brucella abortus. As RNA degradation is an important process in RNA-based gene regulation, a short overview on ribonucleases in plant-associated α-proteobacteria concludes this review.
Anke Becker*, Aaron Overlöper, Jan-Philip Schlüter, Jan Reinkensmeier, Marta Robledo, Robert Giegerich, Franz Narberhaus, Elena Evguenieva-Hackenberg, Franz Narberhaus (2014). RNA Biol. Jul 8;11(5). [Epub ahead of print]
Nuclear calcium oscillations are a hallmark of symbiotically stimulated plant root cells. Activation of the central nuclear decoder, calcium- and calmodulin-dependent kinase (CCaMK), triggers the entire symbiotic program including root nodule organogenesis, but the mechanism of signal transduction by CCaMK was unknown. We show that CYCLOPS, a direct phosphorylation substrate of CCaMK, is a DNA-binding transcriptional activator. Two phosphorylated serine residues within the N-terminal negative regulatory domain of CYCLOPS are necessary for its activity. CYCLOPS binds DNA in a sequence-specific and phosphorylation-dependent manner and transactivates the NODULE INCEPTION (NIN) gene. A phosphomimetic version of CYCLOPS was sufficient to trigger root nodule organogenesis in the absence of rhizobia and CCaMK. CYCLOPS thus induces a transcriptional activation cascade, in which NIN and a heterotrimeric NF-Y complex act in hierarchical succession to initiate symbiotic root nodule development
Most of the characterized pathogen effectors are proteins, but Weiberg et al. (1) demonstrate that we can add RNA to the list of effectors with trans-kingdom activity. The new research involves Botrytis cinerea—a necrotrophic fungal pathogen that infects many plant species, including tomato and strawberry, on which it causes gray mold. Most notably, it is the noble rot that is so important for the production of exquisite dessert wines.
The new findings involve a class of small RNAs (sRNAs) that includes microRNAs and small interfering RNAs. These sRNAs are typically 20 to 24 nucleotides in length and they guide Argonaute (AGO) nucleases by Watson-Crick base pairing to coding or noncoding RNAs in either the nucleus or cytoplasm so that the targeted RNAs accumulate at a lower level than they would in the absence of the sRNA (3).
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