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Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes

A goal of modern biology is to develop the genotype-phenotype (G→P) map, a predictive understanding of how genomic information generates 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 trai...

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Autores principales: Batstone, Rebecca T., Lindgren, Hanna, Allsup, Cassandra M., Goralka, Laura A., Riley, Alex B., Grillo, Michael A., Marshall-Colon, Amy, Heath, Katy D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9765617/
https://www.ncbi.nlm.nih.gov/pubmed/36286519
http://dx.doi.org/10.1128/mbio.01823-22
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author Batstone, Rebecca T.
Lindgren, Hanna
Allsup, Cassandra M.
Goralka, Laura A.
Riley, Alex B.
Grillo, Michael A.
Marshall-Colon, Amy
Heath, Katy D.
author_facet Batstone, Rebecca T.
Lindgren, Hanna
Allsup, Cassandra M.
Goralka, Laura A.
Riley, Alex B.
Grillo, Michael A.
Marshall-Colon, Amy
Heath, Katy D.
author_sort Batstone, Rebecca T.
collection PubMed
description A goal of modern biology is to develop the genotype-phenotype (G→P) map, a predictive understanding of how genomic information generates 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 symbiotic extended phenotypes, being governed by genetic variation encoded not only by the host’s own genome, but also by the genomes of myriad cryptic symbionts. Building a reliable G→P map therefore requires accounting for the multitude of interacting genes and even genomes involved in symbiosis. Here, we use naturally occurring genetic variation in 191 strains of the model microbial symbiont Sinorhizobium meliloti paired with two genotypes of the host Medicago truncatula in four genome-wide association studies (GWAS) to determine the genomic architecture of a key symbiotic extended phenotype—partner quality, or the fitness benefit conferred to a host by a particular symbiont genotype, within and across environmental contexts and host genotypes. We define three novel categories of loci in rhizobium genomes that must be accounted for if we want to build a reliable G→P map of partner quality; namely, (i) loci whose identities depend on the environment, (ii) those that depend on the host genotype with which rhizobia interact, and (iii) universal loci that are likely important in all or most environments.
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spelling pubmed-97656172022-12-21 Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes Batstone, Rebecca T. Lindgren, Hanna Allsup, Cassandra M. Goralka, Laura A. Riley, Alex B. Grillo, Michael A. Marshall-Colon, Amy Heath, Katy D. mBio Research Article A goal of modern biology is to develop the genotype-phenotype (G→P) map, a predictive understanding of how genomic information generates 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 symbiotic extended phenotypes, being governed by genetic variation encoded not only by the host’s own genome, but also by the genomes of myriad cryptic symbionts. Building a reliable G→P map therefore requires accounting for the multitude of interacting genes and even genomes involved in symbiosis. Here, we use naturally occurring genetic variation in 191 strains of the model microbial symbiont Sinorhizobium meliloti paired with two genotypes of the host Medicago truncatula in four genome-wide association studies (GWAS) to determine the genomic architecture of a key symbiotic extended phenotype—partner quality, or the fitness benefit conferred to a host by a particular symbiont genotype, within and across environmental contexts and host genotypes. We define three novel categories of loci in rhizobium genomes that must be accounted for if we want to build a reliable G→P map of partner quality; namely, (i) loci whose identities depend on the environment, (ii) those that depend on the host genotype with which rhizobia interact, and (iii) universal loci that are likely important in all or most environments. American Society for Microbiology 2022-10-26 /pmc/articles/PMC9765617/ /pubmed/36286519 http://dx.doi.org/10.1128/mbio.01823-22 Text en Copyright © 2022 Batstone et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Batstone, Rebecca T.
Lindgren, Hanna
Allsup, Cassandra M.
Goralka, Laura A.
Riley, Alex B.
Grillo, Michael A.
Marshall-Colon, Amy
Heath, Katy D.
Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes
title Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes
title_full Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes
title_fullStr Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes
title_full_unstemmed Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes
title_short Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes
title_sort genome-wide association studies across environmental and genetic contexts reveal complex genetic architecture of symbiotic extended phenotypes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9765617/
https://www.ncbi.nlm.nih.gov/pubmed/36286519
http://dx.doi.org/10.1128/mbio.01823-22
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