Combining GWAS and population genomic analyses to characterize coevolution in a legume-rhizobia symbiosis

Brendan Epstein, Liana Burghardt, Katy D. Heath, Michael A. Grillo, Adam Kostanecki, Tuomas Hamala, Nevin D. Young, Peter Tiffin

Research output: Contribution to journalArticlepeer-review

Abstract

The mutualism between legumes and rhizobia is clearly the product of past coevolution. However, the nature of ongoing evolution between these partners is less clear. To characterize the nature of recent coevolution between legumes and rhizobia, we used population genomic analysis to characterize selection on functionally annotated symbiosis genes as well as on symbiosis gene candidates identified through a two-species association analysis. For the association analysis, we inoculated each of 202 accessions of the legume host Medicago truncatula with a community of 88 Sinorhizobia (Ensifer) meliloti strains. Multistrain inoculation, which better reflects the ecological reality of rhizobial selection in nature than single-strain inoculation, allows strains to compete for nodulation opportunities and host resources and for hosts to preferentially form nodules and provide resources to some strains. We found extensive host by symbiont, that is, genotype-by-genotype, effects on rhizobial fitness and some annotated rhizobial genes bear signatures of recent positive selection. However, neither genes responsible for this variation nor annotated host symbiosis genes are enriched for signatures of either positive or balancing selection. This result suggests that stabilizing selection dominates selection acting on symbiotic traits and that variation in these traits is under mutation-selection balance. Consistent with the lack of positive selection acting on host genes, we found that among-host variation in growth was similar whether plants were grown with rhizobia or N-fertilizer, suggesting that the symbiosis may not be a major driver of variation in plant growth in multistrain contexts.

Original languageEnglish (US)
JournalMolecular ecology
DOIs
StateAccepted/In press - 2022

Bibliographical note

Funding Information:
We thank Amanda Gorton, Molly Meath, Erica Houser, Reda AI Abou‐Shanab, and Ivan Sosa Marquez for help with the tedious task of harvesting nodules. We also thank Jeremy Yoder and three anonymous reviewers for comments that improved the manuscript and helped us to clarify our thinking of coevolution. The Minnesota Supercomputing Institute (MSI) at the University of Minnesota provided resources that contributed to this research. This work was supported by the National Science Foundation under grant IOS‐1856744 and Department of Energy JGI CSP‐503446. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author and do not necessarily reflect the views of the National Science Foundation.

Publisher Copyright:
© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Keywords

  • Medicago
  • bacteria
  • microbes
  • mutualism
  • population genomics

PubMed: MeSH publication types

  • Journal Article

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