Genetic architecture of heritable leaf microbes

Abstract 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. We found that despite large effects of the environment, both Mendelian and quantitative genetic host variation contribute 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 phyllosphere microbes. Importance We investigated how host genetic variation affected the assembly of Ipomoea hederacea ’s natural microbiome. We found that the genetic architecture of leaf-associated microbiomes involves both quantitative genetic variation and Mendelian traits, with similar contributions to microbe heritability. The existence of Mendelian and quantitative genetic variation for host-associated microbes means that plant evolution at the leaf shape locus or other quantitative genetic loci has the potential to shape microbial abundance, and community composition. ### Competing Interest Statement The authors have declared no competing interest. * F1 : Filial 1 F2 : Filial 2 F3 : Filial 3 RNA : Ribonucleic acid DNA : Deoxyribonucleic acid QIIME2 : Quantitative insights into microbial ecology 2 RILs : Recombinant inbred lines PCoA : Principal coordinate analysis MAGIC : Multi-parent advanced generation inter-cross.