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Dryad

Genetic architecture of heritable leaf microbes

Boyle, Julia1; Frederickson, Megan1; Stinchcombe, John1

Published May 14, 2024 on Dryad. https://doi.org/10.5061/dryad.rbnzs7hjz

Data files

Abstract

Background

Host-associated microbiomes are shaped by both their environment and host genetics, and often impact host performance. The scale of host genetic variation important to microbes is largely unknown, yet fundamental to the community assembly of host-associated microbiomes, and with implications for the eco-evolutionary dynamics of microbes and hosts. Using Ipomoea hederacea, Ivy-leaved morning glory, we generated matrilines differing in quantitative genetic variation and leaf shape, which is controlled by a single Mendelian locus. We then investigated the relative roles of Mendelian and quantitative genetic variation in structuring the leaf microbiome, and how these two sources of genetic variation contributed to microbe heritability.

Results

We found that despite large effects of the environment, both Mendelian and quantitative genetic host variation were important in contributing to microbe heritability, and that the cumulative small effect genomic differences due to matriline explained as much or more microbial variation than a single large effect locus. Furthermore, our results are the first to suggest that leaf shape itself contributes to variation in the abundances of some microbes in the leaf microbiome.

Conclusions

The genetic architecture of plant-associated microbiomes depends on both quantitative genetic variation and Mendelian traits, with similar contributions to microbe heritability. Our results demonstrate the roles of different scales of host genetic variation in the assembly of a natural microbiome. The genetic basis and heritability of a host’s microbial phenotype is important for host evolution and ecology because microbes can affect host fitness, and because it can influence reciprocal selection between hosts and microbiomes. Additionally, when host-associated microbiomes have heritability, then this suggests they have the capacity to evolve as other host traits might, with potentially adaptive functions.