Plant genetic effects on microbial hubs impact host fitness in repeated field trials

Benjamin Brachi, Daniele Filiault, Hannah Whitehurst, Paul Darme, Pierre Le Gars, Marine Le Mentec, Timothy C. Morton, Envel Kerdaffrec, Fernando Rabanal, Alison Anastasio, Mathew S. Box, Susan Duncan, Feng Huang, Riley Leff, Polina Novikova, Matthew Perisin, Takashi Tsuchimatsu, Roderick Woolley, Caroline Dean, Magnus NordborgSvante Holm, Joy Bergelson

Research output: Contribution to journalArticlepeer-review


Although complex interactions between hosts and microbial associates are increasingly well documented, we still know little about how and why hosts shape microbial communities in nature. In addition, host genetic effects on microbial communities vary widely depending on the environment, obscuring conclusions about which microbes are impacted and which plant functions are important. We characterized the leaf microbiota of 200 Arabidopsis thaliana genotypes in eight field experiments and detected consistent host effects on specific, broadly distributed microbial species (operational taxonomic unit [OTUs]). Host genetic effects disproportionately influenced central ecological hubs, with heritability of particular OTUs declining with their distance from the nearest hub within the microbial network. These host effects could reflect either OTUs preferentially associating with specific genotypes or differential microbial success within them. Host genetics associated with microbial hubs explained over 10% of the variation in lifetime seed production among host genotypes across sites and years. We successfully cultured one of these microbial hubs and demonstrated its growth-promoting effects on plants in sterile conditions. Finally, genome-wide association mapping identified many putatively causal genes with small effects on the relative abundance of microbial hubs across sites and years, and these genes were enriched for those involved in the synthesis of specialized metabolites, auxins, and the immune system. Using untargeted metabolomics, we corroborate the consistent association between variation in specialized metabolites and microbial hubs across field sites. Together, our results reveal that host genetic variation impacts the microbial communities in consistent ways across environments and that these effects contribute to fitness variation among host genotypes.

Original languageEnglish (US)
Article numbere2201285119
JournalProceedings of the National Academy of Sciences of the United States of America
Issue number30
StatePublished - Jul 26 2022


  • Arabidopsis thaliana
  • fitness
  • genome-wide association study
  • microbial hubs
  • microbiome

ASJC Scopus subject areas

  • General


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