Polygenic heritability of the Populus trichocarpa foliar microbiome

Background/Question/Methods

Plants play an active role in shaping the species composition of bacteria, fungi, and other microbes that live on and in their tissues. As a result, plant microbiome composition varies both among and within host species and can be viewed as a complex heritable trait. However, specific genetic mechanisms that determine how plants influence microbiome composition overall have remained elusive, particularly in the phyllosphere where microbiome composition may be essential for host defense against pathogens, herbivores, and other environmental stressors. One reason it may be difficult to link microbiome composition to specific host-associated genetic mechanisms is that microbiome assembly in the phyllosphere is influenced by many complex traits (e.g., leaf morphology, phenology, etc.), making microbiome composition itself a highly polygenic trait. In this study, we tested the hypothesis that the foliar microbiome heritability is primarily the results of due to polygenic effects, as opposed to the effects of individual alleles. We also tested the hypothesis that foliar microbiome heritability varies among fungi and bacteria, and that heritability varies throughout the growing season. We used amplicon sequencing to profile microbial communities in the leaves of 800 genotypes of the model deciduous tree species, Populus trichocarpa (black cotton wood), sampled over two years from a common garden. In the first year we profiled fungal and bacterial communities, and in the second year we profiled foliar fungi at two time points, early and late in the growing season. For each of the 4 resulting data sets, we estimated the multivariate heritability of the foliar microbiome, as well as the heritability of individual microbial taxa, and conducted genome-wide association (GWAS) analyses of foliar microbiome phenotypes.

Results/Conclusions

We found that the composition of the P. trichocarpa foliar microbiome was significantly heritable across all data sets, but that heritability was greater for fungi than bacteria and in leaves sampled later in the growing season. Despite significant heritability, GWAS analyses did not reveal significant associations, supporting the hypothesis that microbiome composition is a highly polygenic trait. Consistent with our finding that the community composition of foliar fungi was more heritable than the community composition of bacteria, we identified individual taxa with significant heritability in all 3 fungal data sets, but none in the bacterial data. Heritable taxa included known foliar pathogens, as well as non-pathogenic endophytes suggesting that functionally diverse fungal taxa contribute to the polygenic heritability of the P. trichocarpa foliar microbiome