Multiple Mutualist Effects generate synergistic selection and strengthen fitness alignment in a tripartite interaction between legumes, rhizobia, and mycorrhizal fungi

A goal of modern biology is to develop the genotype-phenotype (G-P) map, a predictive understanding of how genomic information generates the organismal trait variation that forms the basis of both natural and managed communities. As microbiome research advances, however, it has become clear that many of these traits are governed by genetic variation encoded not only by the host's own genome, but also by the genomes of myriad cryptic symbionts. Thus many ecologically-important traits are likely symbiotic extended phenotypes, and this recognition adds even more complexity to our conceptions of the G-P map. In model symbioses such as the legume-rhizobium mutualism, host growth and fitness often depend on genetic variation in symbiont partner quality, and our ability to manipulate host and symbiont genotype combinations, combined with increasingly precise sequencing and mapping approaches, provides an opportunity to characterize the genetic nature of these symbiotic extended phenotypes. Here we use naturally-occurring genetic variation in 191 strains of the nitrogen-fixing symbiont Ensifer meliloti in four mapping experiments to study the genomic architecture of symbiotic partner quality within and across environmental contexts and host genotypes. We demonstrate the quantitative genetic nature of symbiotic extended phenotypes, including extensive context-dependency in both the identity and functions of symbiont loci that control host growth. We additionally resolve a core set of universal loci from populations in the native range that are likely important in all or most environments, and thus, serve as excellent targets both for genetic engineering and future coevolutionary studies of symbiosis.

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“…Includes detailed methods, additional results, seven (7) (105). Briefly, strains were grown as described above.…”

Section: Supplemental Materialsmentioning

confidence: 99%

“…Detailed methods, additional results, and twelve (12) supplementary figures are available on Zenodo (68) (doi: https://doi.org/10.5281/zenodo.5550958). Seven (7) supplementary datasets are available on Dryad (68) (doi: https://doi.org/10.5061/dryad.5dv41ns6r).…”

Section: Supplemental Materialsmentioning

confidence: 99%

Genome-wide association studies across environmental and genetic contexts reveal complex genetic architecture of symbiotic extended phenotypes

Batstone

Lindgren

Allsup

et al. 2021

Preprint

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Tripartite interactions among free‐living, N‐fixing bacteria, arbuscular mycorrhizal fungi, and plants: Mutualistic benefits and community response to co‐inoculation

Kasanke,

Cheeke,

Moran

et al. 2024

Soil Science Soc of Amer J

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Interactions between arbuscular mycorrhizal (AM) fungi and free‐living nitrogen fixers (FLNF) occur in the rhizosphere where they can enhance plant nutrient acquisition, impact plant growth, and affect soil processes. Tripartite mutualism commonly occurs between nodule‐forming plants, symbiotic diazotrophs, and AM fungi, and can occur between non‐nodulating plants, FLNF, and AM fungi. However, information on the extent of, and controls on, tripartite mutualism in non‐nodulating plant systems is limited to a small number of crop plants and culturable microbial inoculum, mostly in greenhouse growing conditions. We conducted a systematic literature review to synthesize the current understanding of the responses of plants, AM fungi, and FLNF to co‐inoculation, as well as the conditions affecting tripartite mutualism and the magnitude and range of benefits conferred. Our review shows that plants generally benefit from co‐inoculation with AM fungi and FLNF taxa, but benefits are highly variable and context dependent, ranging from 94% reduction in plant shoot biomass to 255% increase in total plant biomass. Additionally, the presence of AM fungi can increase abundance of FLNF and the presence of FLNF can increase AM fungal root colonization, but these responses also vary widely. Major factors influencing variation in response to co‐inoculation by all organisms include plant phenology/age, soil type and nutrient availability, and partner pairing. There is potential for leveraging these tripartite mutualisms to improve plant productivity and soil microbial function, but successful application is more likely with a thorough understanding of the environmental and mechanistic controls on these relationships and testing of field‐scale implementation.

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Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally-occurring isolates of a model plant symbiont

Batstone

Burghardt

Heath

2021

Preprint

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Although mutualisms are defined as net beneficial interactions among species, whether fitness conflict or alignment drive the evolution of these interactions is unclear. Examining the relationships between host and symbiont fitness proxies at both the organismal and genomic levels can provide new insights. Here, we utilized data from several genome-wide association studies (GWAS) that involved 191 strains of the N-fixing rhizobium symbiont, Ensifer meliloti, collected from natural populations being paired in single or mixed inoculation with two genotypes of the host Medicago truncatula to determine how different proxies of microbial fitness were related to one another, and examine signatures of fitness conflict and alignment between host and symbiont at both the whole-organism and genomic levels. We found little evidence for fitness conflict; instead, loci tended to have concordant effects on both host and symbiont fitness and showed heightened nucleotide diversity and signatures of balancing selection compared to the rest of the genome. We additionally found that single versus competitive measures of rhizobium fitness are distinct, and that the latter should be used given that they better reflect the ecological conditions rhizobia experience in nature. Our results suggest that although conflict appears to be largely resolved in natural populations of rhizobia, mutualistic coevolution between legumes and rhizobia can nonetheless maintain genetic diversity, potentially explaining why variation in symbiotic traits persists in nature.

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Multiple Mutualist Effects generate synergistic selection and strengthen fitness alignment in a tripartite interaction between legumes, rhizobia, and mycorrhizal fungi

Cited by 3 publications

References 52 publications

Genome-wide association studies across environmental and genetic contexts reveal complex genetic architecture of symbiotic extended phenotypes

Genome-wide association studies across environmental and genetic contexts reveal complex genetic architecture of symbiotic extended phenotypes

Tripartite interactions among free‐living, N‐fixing bacteria, arbuscular mycorrhizal fungi, and plants: Mutualistic benefits and community response to co‐inoculation

Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally-occurring isolates of a model plant symbiont

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