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Allele frequency spectrum at locus NORK. The plot represents allele frequencies of 32 diallelic polymorphisms (excluding three insertion-deletion events and one triallelic site). Classes of polymorphism (singleton, doubleton, etc.) are represented on the X axis. The frequency of each class is represented on the Y axis. Note that only the frequency of the rarer allele for each site is represented. The only nonsynonymous mutation found in our sample is indicated here by an asterisk.
Source publication
Understanding the selective constraints of partner specificity in mutually beneficial symbiosis is a significant, yet largely unexplored, prospect of evolutionary biology. These selective constraints can be explored through the study of nucleotide polymorphism at loci controlling specificity. The membrane-anchored receptor NORK (nodulation receptor...
Contexts in source publication
Context 1
... but one are diallelic in the sample (the last was triallelic). Given the unrooted genealogical tree, all diallelic sites data can be ex- plained by single mutational steps, i.e., there is no homoplasy, whereas three steps are necessary to ex- plain the triallelic site. The distribution of allele fre- quencies at the 32 diallelic sites is shown in Fig. 3. Only one of these is nonsynonymous. The two states of this amino acid polymorphism are alanine (hydrophobic) and glutamate (acidic). For the GS intron fragment, we obtained 27 sequences of 496 nucleotides, containing two diallelic point substitu- truncatula ssp. tricycla). The numbers on the edges of the tree give the number of ...
Context 2
... found only one nonsynonymous mutation in the sample, indicating that fairly strong purifying selection is operating on the NORK protein. Inter- estingly, this site segregates at an intermediate fre- quency (Fig. 3) and codes for amino acids from distinct classes: the ancestral one is the hydrophobic alanine, and the derived one is the acidic glutamate. At this position, an alanine is found in all other legume sequences used for the interspecific analysis. The codon-based analysis classifies this site as under purifying selection (estimated x = ...
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Citations
... We did not find any known CSSP or LysM-RLK genes among the loci detected by our GWASs. This was somewhat expected, as constrained natural variability of these essential symbiotic genes due to selective processes was often found in previous nucleotide polymorphism analyses (De Mita et al., 2006Grillo et al., 2016) and in previous GWASs performed on nodulation phenotypes (Stanton-Geddes et al., 2013). This also suggests that these genes are not major determinants of natural variability in root developmental responses to LCOs, although some LysM-RLK genetic variants likely account for rhizobial host specificity (Sulima et al., 2017(Sulima et al., , 2019. ...
Lipo-chitooligosaccharides (LCOs) were originally found as symbiotic signals called Nod Factors (Nod-LCOs) controlling nodulation of legumes by rhizobia. More recently LCOs were also found in symbiotic fungi and, more surprisingly, very widely in the kingdom fungi including in saprophytic and pathogenic fungi. The LCO-V(C18:1, Fuc/MeFuc), hereafter called Fung-LCOs, are the LCO structures most commonly found in fungi. This raises the question of how legume plants, such as Medicago truncatula, can discriminate between Nod-LCOs and these Fung-LCOs. To address this question, we performed a Genome Wide Association Study on 173 natural accessions of Medicago truncatula, using a root branching phenotype and a newly developed local score approach. Both Nod- and Fung-LCOs stimulated root branching in most accessions but the root responses to these two types of LCO molecules were not correlated. Also, heritability of root response was higher for Nod-LCOs than for Fung-LCOs. We identified 123 loci for Nod-LCO and 71 for Fung-LCO responses, but only one was common. This suggests that Nod- and Fung-LCOs both control root branching but use different molecular mechanisms. The tighter genetic constraint of the root response to Fung-LCOs possibly reflects the ancestral origin of the biological activity of these molecules.
... Lysin motif receptor-like kinases (LysM-RLKs) are one of the most diverse and abundant families of plant membrane receptors responsible for specific recognition of biotic and abiotic signals (Tax and Kemmerling, 2012;Zipfel and Oldroyd, 2017). The precise evolutionary history of LysM-RLKs is not known, however, it inevitably includes gene duplications, rearrangements and neofunctionalization, resulting in a broad spectrum of plant receptors specialized to recognize particular molecules (De Mita et al., 2006;Zhang et al., 2007Zhang et al., , 2009Fliegmann and Bono, 2015). While some of these receptors are tuned to recognize primitive signals from pathogens, such as chitin and chitosan of fungal cell walls, others provide specificity for highly decorated signaling molecules like Nod and Myc factors that initiate the plantbacteria or arbuscular mycorrhizal symbioses. ...
Sandwich-like docking configurations of the heterodimeric complex of NFR5 and K1 Vicia sativa receptor-like kinases together with the putative ligand, Nod factor (NF) of Rhizobium leguminosarum bv. viciae, were modeled and two of the most probable configurations were assessed through the analysis of the mutual polymorphisms and conservatism. We carried out this analysis based on the hypothesis that in a contact zone of two docked components (proteins or ligands) the population polymorphism or conservatism is mutual, i.e., the variation in one component has a reflected variation in the other component. The population material of 30 wild-growing V. sativa (leaf pieces) was collected from a large field (uncultivated for the past 25-years) and pooled; form this pool, 100 randomly selected cloned fragments of NFR5 gene and 100 of K1 gene were sequenced by the Sanger method. Congruence between population trees of NFR5 and K1 haplotypes allowed us to select two respective haplotypes, build their 3D structures, and perform protein–protein docking. In a separate simulation, the protein-ligand docking between NFR5 and NF was carried out. We merged the results of the two docking experiments and extracted NFR5–NF–K1 complexes, in which NF was located within the cavity between two receptors. Molecular dynamics simulations indicated two out of six complexes as stable. Regions of mutual polymorphism in the contact zone of one complex overlapped with known NF structural variations produced by R. leguminosarum bv. viciae. A total of 74% of the contact zone of another complex contained mutually polymorphic and conservative areas. Common traits of the obtained two stable structures allowed us to hypothesize the functional role of three-domain structure of plant LysM-RLKs in their heteromers.
... Although reciprocal inoculation experiments are powerful because they reflect whole-organism performance in native and foreign environments, genotype-by-environment interactions are sensitive to experimental conditions (Kawecki & Ebert, 2004) The Medicago genes involved in symbiotic interactions with rhizobia are well-characterized and highly conserved in legumes (Branca et al., 2011;De Mita, Santoni, Hochu, Ronfort, & Bataillon, 2006;Gorton et al., 2012;van Rhijn & Vanderleyden, 1995;Rostas, Kondorosi, Horvath, Simoncsits, & Kondorosi, 1986;Stanton-Geddes et al., 2013). Medicago lupulina is a close relative of M. truncatula (Bena, 2001;Yoder et al., 2013), and both plants fix nitrogen with both Ensifer species tested in our experiment (Béna et al., 2005). ...
Local adaptation is a common but not ubiquitous feature of species interactions, and understanding the circumstances under which it evolves illuminates the factors that influence adaptive population divergence. Antagonistic species interactions dominate the local adaptation literature relative to mutualistic ones, preventing an overall assessment of adaptation within interspecific interactions. Here, we tested whether the legume Medicago lupulina is adapted to the locally abundant species of mutualistic nitrogen-fixing rhizobial bacteria that vary in frequency across its eastern North American range. We reciprocally inoculated northern and southern M. lupulina genotypes with the northern (Ensifer medicae) or southern bacterium (E. meliloti) in a greenhouse experiment. Despite producing different numbers of root nodules (the structures in which the plants house the bacteria), neither northern nor southern plants produced more seeds, flowered earlier, or were more likely to flower when inoculated with their local rhizobia. We then used a pre-existing dataset to perform a genome scan for loci that showed elevated differentiation between field-collected plants that hosted different bacteria. None of the loci we identified belonged to the well-characterized suite of legume–rhizobia symbiosis genes, suggesting that the rhizobia do not drive genetic divergence between M. lupulina populations. Our results demonstrate that symbiont local adaptation has not evolved in this mutualism despite large-scale geographic variation in the identity of the interacting species.
... Studies made possible by this data have identifi ed new candidate genes for host-symbiont compatibility ( Stanton-Geddes et al., 2013 ) and found genes with previously identifi ed roles in symbiosis among regions of the genome with the strongest signals of species-wide positive selection ( Paape et al., 2013 ) and geographically specifi c, selective sweeps ( Bonhomme et al., 2015 ). Studies have also compared signs of selection in small sets of symbiosis-related genes and sets of putatively neutral control loci and found that the selective histories of some, but not all, symbiosis genes diff er from the controls ( De Mita et al., 2006 ). With whole-genome data, it is possible to perform a similar comparison at a larger scale. ...
Decades of research on the evolution of mutualism has generated a wealth of possible ways whereby mutually beneficial interactions between species persist in spite of the apparent advantages to individuals that accept the benefits of mutualism without reciprocating - but identifying how any particular empirical system is stabilized against cheating remains challenging. Different hypothesized models of mutualism stability predict different forms of coevolutionary selection, and emerging high-throughput sequencing methods allow examination of the selective histories of mutualism genes and, thereby, the form of selection acting on those genes. Here, I review the evolutionary theory of mutualism stability and identify how differing models make contrasting predictions for the population genomic diversity and geographic differentiation of mutualism-related genes. As an example of the possibilities offered by genomic data, I analyze genes with roles in the symbiosis of Medicago truncatula and nitrogen-fixing rhizobial bacteria, the first classic mutualism in which extensive genomic resources have been developed for both partners. Medicago truncatula symbiosis genes, as a group, differ from the rest of the genome, but they vary in the form of selection indicated by their diversity and differentiation - some show signs of selection expected from roles in sanctioning noncooperative symbionts, while others show evidence of balancing selection expected from coevolution with symbiont signaling factors. I then assess the current state of development for similar resources in other mutualistic interactions and look ahead to identify ways in which modern sequencing technology can best inform our understanding of mutualists and mutualism.
... Moreover, the diversity in host-symbiont specifi city among species within the Fabaceae ( Wang et al., 2012 ;Oldroyd, 2013 ) implicates coevolution with rhizobia in shaping the signaling mechanisms of extant legumes. Additionally, there is molecular population genetic evidence for natural selection targeting known signaling genes within the genus Medicago ( De Mita et al., 2006. For the most part, however, molecular population genetics/genomics approaches have not been robustly associated with phenotypic differences in nodule occupancy or with environmental shift s (e.g., N availability) that might serve as agents of selection (but see Stanton-Geddes et al., 2013 ); this is a promising avenue for continued future work. ...
Premise of the study:
Resource mutualisms such as the symbiosis between legumes and nitrogen-fixing rhizobia are context dependent and are sensitive to various aspects of the environment, including nitrogen (N) addition. Mutualist hosts such as legumes are also thought to use mechanisms such as partner choice to discriminate among potential symbionts that vary in partner quality (fitness benefits conferred to hosts) and thus impose selection on rhizobium populations. Together, context dependency and partner choice might help explain why the legume-rhizobium mutualism responds evolutionarily to N addition, since plant-mediated selection that shifts in response to N might be expected to favor different rhizobium strains in different N environments.
Methods:
We test for the influence of context dependency on partner choice in the model legume, Medicago truncatula, using a factorial experiments with three plant families across three N levels with a mixed inoculation of three rhizobia strains.
Key results:
Neither the relative frequencies of rhizobium strains occupying host nodules, nor the size of those nodules, differed in response to N level.
Conclusions:
Despite the lack of context dependence, plant genotypes respond very differently to mixed populations of rhizobia, suggesting that these traits are genetically variable and thus could evolve in response to longer-term increases in N.
... It has been shown that resistance systems rely on the advantage of rare allele forms and that this prevents the loss of alleles by genetic drift thus leading to the maintenance of sometimes very old alleles (De Mita et al., 2006). In a departure from neutral evolution on a population level, directional selection that entails a rapid accumulation of nonsynonymous substitutions leading eventually to selected synonymous mutations may produce a selective sweep that induces hitchhiking effects around the locus under selection (Barton, 2000). ...
PhD thesis submitted in 2008 and resulted in a doctorate graduation in 2009.
... Lectins have long been thought to play a role in protection and in symbiosis through recognition of sugar moieties characterizing the surfaces of specific organisms (Sharon and Lis 2004). The necessity to either recognize partners (in order to trigger defense, infection or mutualism) or to escape recognition (to avoid infection or defense mechanisms) is a selective force shaping the evolutionary history of genes in interacting species (De Mita et al. 2006). Coevolution, the process of reciprocal changes between interacting species during evolution, molds the organization of communities that exist over periods long enough to allow selection of species traits (Thompson 2001). ...
Lectins are a diverse group of carbohydrate binding proteins often involved in cellular interactions. A lectin gene, lec-2, was identified in the mycobiont of the lichen Peltigera membranacea. Sequencing of lec-2 open reading frames from 21 individual samples showed an unexpectedly high level of polymorphism in the deduced protein (LEC-2), which was sorted into nine haplotypes based on amino acid sequence. Calculations showed that the rates of nonsynonymous versus synonymous nucleotide substitutions deviated significantly from the null hypothesis of neutrality, indicating strong positive selection. Molecular modeling revealed that most amino acid replacements were around the putative carbohydrate-binding pocket, indicating changes in ligand binding. Lectins have been thought to be involved in the recognition of photobiont partners in lichen symbioses, and the hypothesis that positive selection of LEC-2 is driven by variation in the Nostoc photobiont partner was tested by comparing mycobiont LEC-2 haplotypes and photobiont genotypes, as represented by the rbcLX region. It was not possible to pair up the two types of marker sequences without conflicts, suggesting that positive selection of LEC-2 was not due to variation in photobiont partners.
... Species-wide sampling in M. truncatula has uncovered patterns of polymorphism at both NFP and DMI3 that are consistent with historical purifying selection (De Mita et al. 2007). De Mita et al. (2006, 2007) have hypothesized that such purifying selection might have maintained high specificity of recognition and removed mutations deleterious to the establishment of symbiosis . Our results suggest that contemporary genetic variation at Nod factor signaling genes may potentially influence plant fitness in M. truncatula. ...
Mutualisms are known to be genetically variable, where the genotypes differ in the fitness benefits they gain from the interaction. To date, little is known about the loci that underlie such genetic variation in fitness or whether the loci influencing fitness are partner specific, and depend on the genotype of the interaction partner. In the legume-rhizobium mutualism, one set of potential candidate genes that may influence the fitness benefits of the symbiosis are the plant genes involved in the initiation of the signaling pathway between the two partners. Here we performed quantitative trait loci (QTL) mapping in Medicago truncatula in two different rhizobium strain treatments to locate regions of the genome influencing plant traits, assess whether such regions are dependent on the genotype of the rhizobial mutualist (QTL × rhizobium strain), and evaluate the contribution of sequence variation at known symbiosis signaling genes. Two of the symbiotic signaling genes, NFP and DMI3, colocalized with two QTL affecting average fruit weight and leaf number, suggesting that natural variation in nodulation genes may potentially influence plant fitness. In both rhizobium strain treatments, there were QTL that influenced multiple traits, indicative of either tight linkage between loci or pleiotropy, including one QTL with opposing effects on growth and reproduction. There was no evidence for QTL × rhizobium strain or genotype × genotype interactions, suggesting either that such interactions are due to small-effect loci or that more genotype-genotype combinations need to be tested in future mapping studies.
... Most sequences were obtained from genomic DNA, except for Lax2, which was sequenced from cDNA due to its large size. DNA extraction and genomic DNA amplifications and sequencing were performed as described in [41]. Total RNA was extracted from fresh leaves with a TRI REAGENT (T9424, Sigma W ) buffer. ...
Background
Gene duplications are a molecular mechanism potentially mediating generation of functional novelty. However, the probabilities of maintenance and functional divergence of duplicated genes are shaped by selective pressures acting on gene copies immediately after the duplication event. The ratio of non-synonymous to synonymous substitution rates in protein-coding sequences provides a means to investigate selective pressures based on genic sequences. Three molecular signatures can reveal early stages of functional divergence between gene copies: change in the level of purifying selection between paralogous genes, occurrence of positive selection, and transient relaxed purifying selection following gene duplication. We studied three pairs of genes that are known to be involved in an interaction with symbiotic bacteria and were recently duplicated in the history of the Medicago genus (Fabaceae). We sequenced two pairs of polygalacturonase genes (Pg11-Pg3 and Pg11a-Pg11c) and one pair of auxine transporter-like genes (Lax2-Lax4) in 17 species belonging to the Medicago genus, and sought for molecular signatures of differentiation between copies.
Results
Selective histories revealed by these three signatures of molecular differentiation were found to be markedly different between each pair of paralogs. We found sites under positive selection in the Pg11 paralogs while Pg3 has mainly evolved under purifying selection. The most recent paralogs examined Pg11a and Pg11c, are both undergoing positive selection and might be acquiring new functions. Lax2 and Lax4 paralogs are both under strong purifying selection, but still underwent a temporary relaxation of purifying selection immediately after duplication.
Conclusions
This study illustrates the variety of selective pressures undergone by duplicated genes and the effect of age of the duplication. We found that relaxation of selective constraints immediately after duplication might promote adaptive divergence.
... As we gain more and more evidence of selection for novel alleles (i.e. positive selection) at not only plant (De Mita et al. 2006 but also animal (Schwarz et al. 2008) loci encoding for surface receptors, we may discover that highly polymorphic host-symbiont recognition genes are not restricted to the former associations and that, even more importantly, are not necessarily a pathogenicity signature (Sachs et al. 2011). ...
For a microbial association to persist throughout generations, host progeny must either be capable of earning a microbial fortune from the environment (horizontal transmission) or inherit it from its parents (vertical transmission). The former modality relies on highly sophisticated molecular mechanisms of partners’ recognition. The latter modality, instead, presupposes the microbial partners to be as deeply integrated into the host life cycle and to associate with its earliest developmental stages. Besides the common trends that just started to emerge, I discuss the under-explored aspects of bacterial transmission such as its cell biology, and how extracellular microbial symbionts – in turn – ensure their daughter cells the symbiotic lifestyle.
