期刊名称:Proceedings of the National Academy of Sciences
印刷版ISSN:0027-8424
电子版ISSN:1091-6490
出版年度:2022
卷号:119
期号:30
DOI:10.1073/pnas.2201285119
语种:English
出版社:The National Academy of Sciences of the United States of America
摘要:Significance
Recent demonstrations of a genetic basis for variation among hosts in the microbiome leave unresolved the question of how commonly host genetic effects influence individual microbes, and whether these effects impact host fitness. We used replicated field studies in the north and south of Sweden to map host genetic effects in microbial community networks using genome-wide association mapping. By focusing on consistent effects across sites, we found effects of genetic variation on important microbial hubs that contributed to plant fitness in a manner robust to the environment. Our results suggest that ongoing efforts to harness host genotype effects on the microbiome for agricultural purposes can be successful and highlight the value of explicitly considering abiotic variation in those efforts.
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.
关键词:enArabidopsis thalianagenome-wide association studymicrobiomefitnessmicrobial hubs