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; Grillo, Michael A.; Marshall‐Colón, Amy; Heath, Katy D.

doi:10.1128/mbio.01823-22

Cited by 15 publications

(18 citation statements)

References 145 publications

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“…In some cases, symbiosis can generate novel organisms, as in the ancient symbiosis between archaea and bacteria that gave rise to eukaryotes, for example (Sagan, 1967; Margulis & Fester, 1991). More commonly, the symbiosis between prokaryotic microbes and eukaryotic hosts gives rise to novel, emergent traits (Batstone, 2021; Batstone et al ., 2022), such as pathogen and herbivore resistance in agricultural crops (Van Wees, Van der Ent & Pieterse, 2008), and improved digestion of lactose in human infants (Wall et al ., 2009). Symbiotic interactions can vary from facultative to obligate for one or more partners, and outcomes range from pathogenic to beneficial, often depending on the environment and the genotypic identities of those interacting (Heath & Tiffin, 2007; Batstone et al ., 2018).…”

Section: Case Studies: Mechanisms Underlying Novelty Across Biologica...mentioning

confidence: 99%

Origins and evolution of biological novelty

2023

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Understanding the origins and impacts of novel traits has been a perennial interest in many realms of ecology and evolutionary biology. Here, we build on previous evolutionary and philosophical treatments of this subject to encompass novelties across biological scales and eco‐evolutionary perspectives. By defining novelties as new features at one biological scale that have emergent effects at other biological scales, we incorporate many forms of novelty that have previously been treated in isolation (such as novelty from genetic mutations, new developmental pathways, new morphological features, and new species). Our perspective is based on the fundamental idea that the emergence of a novelty, at any biological scale, depends on its environmental and genetic context. Through this lens, we outline a broad array of generative mechanisms underlying novelty and highlight how genomic tools are transforming our understanding of the origins of novelty. Lastly, we present several case studies to illustrate how novelties across biological scales and systems can be understood based on common mechanisms of change and their environmental and genetic contexts. Specifically, we highlight how gene duplication contributes to the evolution of new complex structures in visual systems; how genetic exchange in symbiosis alters functions of both host and symbiont, resulting in a novel organism; and how hybridisation between species can generate new species with new niches.

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Section: Case Studies: Mechanisms Underlying Novelty Across Biologica...mentioning

confidence: 99%

Origins and evolution of biological novelty

2023

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“…For example, by conducting multiple GWAS that involved inoculating two plant genotypes with one of c . 200 microbial strains, measuring multiple proxies of partner quality – or the fitness effect a microbial genotype confers to its host – and whole‐genome sequencing each strain, the identities and functions of microbial loci significantly associated with partner quality on one plant line have been shown to be largely different from those on the other plant line (Batstone et al ., 2021b), and thus can be considered loci underlying intergenomic epistasis (see also Burghardt et al ., 2017, 2018).…”

Section: Determining the Genetic Basis Of Plant Traitsmentioning

confidence: 99%

“…Rather than extensions of the microbial genome, MGEs instead represent distinct genomes nested within microbes, similar to how microbes are distinct from their plant hosts. Loci within MGEs not only have the potential to influence microbial traits, including antibiotic resistance (Förster et al ., 2015), but also plant traits via their interaction with microbes, including plant growth (Batstone et al ., 2021b). Therefore, genetic variation within MGEs, in addition to plants and microbes, must be explicitly accounted for if we want to understand how plant traits evolve (Box 1).…”

Section: Mobile Genetic Elements As Units Of Selectionmentioning

confidence: 99%

“…plasmids vs the bacterial chromosome) might interact with one another nonadditively (Harrison & Brockhurst, 2012; Box 1, Eqn 3), although we know comparatively little about how nested genomes within a microbial cell interact to produce variation in plant traits. Yet, nonadditive interactions are not ubiquitous; some microbes or MGEs have a wide host breadth and produce consistent effects on host fitness regardless of host genotype (solid lines in the figure in Box 1; Pahua et al ., 2018; Batstone et al ., 2021b). Partitioning additive (e.g.…”

Section: Nonadditivity Among Nested Scalesmentioning

confidence: 99%

“…Association mapping approaches are particularly useful for uncovering the genetic basis of features common within plant-microbe interactions, including symbiotic pleiotropy, that is, when a locus in one individual not only affects traits of that individual but also traits of its symbiotic partner (Batstone et al, 2021a); genotype by environment (G × E) interactions, that is, the loci that affect a particular trait of interest depend on the environment; and intergenomic epistasis (as described earlier). For example, by conducting multiple GWAS that involved inoculating two plant genotypes with one of c. 200 microbial strains, measuring multiple proxies of partner qualityor the fitness effect a microbial genotype confers to its hostand whole-genome sequencing each strain, the identities and functions of microbial loci significantly associated with partner quality on one plant line have been shown to be largely different from those on the other plant line (Batstone et al, 2021b), and thus can be considered New Phytologist (2022) 234: 28-34 www.newphytologist.com Ó 2021 The Author New Phytologist Ó 2021 New Phytologist Foundation loci underlying intergenomic epistasis (see also Burghardt et al, 2017.…”

Section: Determining the Genetic Basis Of Plant Traitsmentioning

confidence: 99%

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Genomes within genomes: nested symbiosis and its implications for plant evolution

Batstone

2021

New Phytologist

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Summary Many important plant traits are products of nested symbiosis: mobile genetic elements (MGEs) are nested within microbes, which in turn, are nested within plants. Plant trait variation is therefore not only determined by the plant’s genome, but also by loci within microbes and MGEs. Yet it remains unclear how interactions and coevolution within nested symbiosis impacts the evolution of plant traits. Despite the complexities of nested symbiosis, including nonadditive interactions, understanding the evolution of plant traits is facilitated by combining quantitative genetic and functional genomic approaches that explicitly consider sources of nested genetic variation (from loci in MGEs to microbiomes). Additionally, understanding coevolution within nested symbiosis enables us to design or select for MGEs that promote plant health.

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Genotypic variation in resource exchange, use, and production traits in the legume–rhizobia mutualism

Calvert,

Hoque,

Wood

2024

Ecology and Evolution

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Mutualisms, reciprocally beneficial interactions between two or more species, are ubiquitous in nature. A common feature of mutualisms is extensive context‐dependent variation in fitness outcomes. This context‐dependency is hypothesized to stem from the environment's mediation of the relative costs and benefits associated with mutualisms. However, traits related to the exchange of goods and services in mutualisms have received little attention in comparison to net fitness outcomes. In this study, we quantified the contribution of host and symbiont genotypes to variation in resource exchange, use, and production traits measured in the host using the model mutualism between legumes and nitrogen‐fixing rhizobia. We predicted that plant genotype × rhizobia genotype (G × G) effects would be common to resource exchange traits because resource exchange is hypothesized to be governed by both interacting partners through bargaining. On the other hand, we predicted that plant genotype effects would dominate host resource use and production traits because these traits are only indirectly related to the exchange of resources. Consistent with our prediction for resource exchange traits, but not our prediction for resource use and production traits, we found that rhizobia genotype and G × G effects were the most common sources of variation in the traits that we measured. The results of this study complement the commonly observed phenomenon of G × G effects for fitness by showing that numerous mutualism traits also exhibit G × G variation. Furthermore, our results highlight the possibility that the exchange of resources as well as how partners use and produce traded resources can influence the evolution of mutualistic interactions. Our study lays the groundwork for future work to explore the relationship between resource exchange, use and production traits and fitness (i.e., selection) to test the competing hypotheses proposed to explain the maintenance of fitness variation in mutualisms.

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

Cited by 15 publications

References 145 publications

Origins and evolution of biological novelty

Origins and evolution of biological novelty

Genomes within genomes: nested symbiosis and its implications for plant evolution

Genotypic variation in resource exchange, use, and production traits in the legume–rhizobia mutualism

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