Intrapopulation genomics in a model mutualist: Population structure and candidate symbiosis genes under selection in
            <i>Medicago truncatula</i>

Grillo, Michael A.; Mita, Stéphane De; Burke, Patricia V.; Solórzano-Lowell, Kathryn L.S.; Heath, Katy D.

doi:10.1111/evo.13095

Cited by 18 publications

(29 citation statements)

References 104 publications

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“…Consistent with previous experiments (Heath and Tiffin ; Grillo et al. ; Burghardt et al. ), strain fitness depended strongly on host genotype and was skewed so that less than one‐fifth of the strains increased in relative frequency inside nodules (relative fitness > 0; Fig.…”

Section: Resultssupporting

confidence: 89%

Legacy of prior host and soil selection on rhizobial fitness in planta

2019

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Measuring selection acting on microbial populations in natural or even seminatural environments is challenging because many microbial populations experience variable selection. The majority of rhizobial bacteria are found in the soil. However, they also live symbiotically inside nodules of legume hosts and each nodule can release thousands of daughter cells back into the soil. We tested how past selection (i.e., legacies) by two plant genotypes and by the soil alone affected selection and genetic diversity within a population of 101 strains of Ensifer meliloti. We also identified allelic variants most strongly associated with soil‐ and host‐dependent fitness. In addition to imposing direct selection on rhizobia populations, soil and host environments had lasting effects across host generations. Host presence and genotype during the legacy period explained 22% and 12% of the variance in the strain composition of nodule communities in the second cohort, respectively. Although strains with high host fitness in the legacy cohort tended to be enriched in the second cohort, the diversity of the strain community was greater when the second cohort was preceded by host rather than soil legacies. Our results indicate the potential importance of soil selection driving the evolution of these plant‐associated microbes.

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Section: Resultssupporting

confidence: 89%

Legacy of prior host and soil selection on rhizobial fitness in planta

2019

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“…This is somehow expected as constrained natural variability on these essential symbiotic genes due to selective processes was often found in previous nucleotide polymorphism analyses (De Mita et al, 2006;De Mita et al, 2007;Grillo et al, 2016) and in previous GWAS studies 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 rhizobia host-specificity (Sulima et al, 2017;Sulima et al, 2019).…”

Section: Endosymbiosis Associated Locisupporting

confidence: 64%

Distinct genetic bases for plant root responses to lipo-chitooligosaccharide signal molecules from distinct microbial origins

Bonhomme

Bensmihen

Olivier

et al. 2020

Preprint

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SummaryLipo-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 perceive and 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 there was very little correlation in the ability to respond to these types of LCO molecules. Moreover, 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.

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“…While these genotypes were not selected due to a priori phenotypic differentiation, our previous work indicates that they possess genetic variation for symbiosis related genes and phenotypes. These genotypes are differentiated at DMI1, a key symbiosis gene known to be under selection in nature [109,110].…”

Section: Methodsmentioning

confidence: 99%

Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula

Brown

Grillo

Podowski

et al. 2020

Preprint

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Background Understanding the genetic and environmental factors that structure plant microbiomes is necessary for leveraging these interactions to address critical needs in agriculture, conservation, and sustainability. Legumes, which form root nodule symbioses with nitrogen-fixing rhizobia, have served as model plants for understanding the genetics and evolution of beneficial plant-microbe interactions for decades, and thus have added value as models of plant-microbiome interactions. Here we use a common garden experiment with 16S rRNA gene amplicon and shotgun metagenomic sequencing to study the drivers of microbiome diversity and composition in three genotypes of the model legume Medicago truncatula grown in two native soil communities. Results Bacterial diversity decreased between external (rhizosphere) and internal plant compartments (root endosphere, nodule endosphere, and leaf endosphere). Community composition was shaped by strong compartment × soil origin and compartment × plant genotype interactions, driven by significant soil origin effects in the rhizosphere and significant plant genotype effects in the root endosphere. Nevertheless all compartments were dominated by Ensifer , the genus of rhizobia that forms root nodule symbiosis with M. truncatula , and additional shotgun metagenomic sequencing suggests that the nodulating Ensifer were not genetically distinguishable from those elsewhere in the plant. We also identify a handful of OTUs that are common in nodule tissues, which are likely colonized from the root endosphere. Conclusions Our results demonstrate strong host filtering effects, with rhizospheres driven by soil origin and internal plant compartments driven by host genetics, and identify several key nodule-inhabiting taxa that coexist with rhizobia in the native range. Our results set the stage for future functional genetic experiments aimed at expanding our pairwise understanding of legume-rhizobium symbiosis towards a more mechanistic understanding of plant microbiomes.

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Intrapopulation genomics in a model mutualist: Population structure and candidate symbiosis genes under selection in Medicago truncatula

Cited by 18 publications

References 104 publications

Legacy of prior host and soil selection on rhizobial fitness in planta

Legacy of prior host and soil selection on rhizobial fitness in planta

Distinct genetic bases for plant root responses to lipo-chitooligosaccharide signal molecules from distinct microbial origins

Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula

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