DOI: 10.5061/dryad.5dv41ns6r
title: Data from: Genome-wide association studies across environmental and genetic contexts reveal complex genetic architecture of symbiotic extended phenotypes

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, 1)
 loci whose identities depend on the environment, 2) those that depend on
 the host genotype with which rhizobia interact, and 3) universal loci that
 are likely important in all or most environments. IMPORTANCE: Given the
 rapid rise of research on how microbiomes can be harnessed to improve host
 health, understanding the contribution of microbial genetic variation to
 host phenotypic variation is pressing, and will better enable us to
 predict the evolution of (and select more precisely for) symbiotic
 extended phenotypes that impact host health. We uncover extensive
 context-dependency in both the identity and functions of symbiont loci
 that control host growth, which makes predicting the genes and pathways
 important for determining symbiotic outcomes under different conditions
 more challenging. Despite this context-dependency, we also resolve a core
 set of universal loci 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.
description: Detailed methods are included in the PDF associated with this
 dataset. We performed four greenhouse experiments to estimate partner
 quality phenotypes in <em>Sinorhizobium meliloti</em>. In each
 experiment, plants from one of two host lines (either A17 or DZA) were
 grown in single inoculation with each of 191 <em>S.
 meliloti</em> strains, with three to four replicates per strain per
 experiment (six to eight total replicates for each plant line x strain
 combination, N = 2,825 plants total). We measured multiple proxies of
 partner quality, namely leaf chlorophyll A content, plant height, number
 of leaves, and above-ground dried shoot biomass.
 Simutaneously, we sequenced the entire genomes of all 191
 <em>S. meliloti</em> strains, called single nucleotide
 polymorphisms (SNPs, henceforth referred to as variants), and performed
 genome-wide association tests that accounted for rhizobium population
 structure and included only unlinked variants. We determined which loci
 were significantly associated with partner quality using a permutation
 method, and binned these loci into three categories based on the
 context-dependency of their phenotypic effects, and thus, their
 contribution to the layers of the G→P map for each of our symbiotic
 extended phenotypes, as described in the abstract.
description: All raw data and code to reproduce analyses is available on
 GitHub
 (https://github.com/rtbatstone/complex_genetics_of_symbiosis/tree/main/Complex_genetics). While we focus the main text on shoot biomass, we additionally have data on leaf chlorophyl A content, plant height, and leaf number, which is accessible via GitHub.