Breeding for broad-spectrum disease resistance alters the maize leaf microbiome

Leaf-associated microbes can drastically affect disease severity, and host genotype can influence the diversity and composition of the leaf microbiome. However, these processes have not been studied and linked in the context of breeding for improved disease resistance. Here, we demonstrate that breeding for broad-spectrum disease resistance altered leaf microbiome composition in field-grown maize. Quantitative trait loci (QTL) conferring resistance to multiple fungal pathogens were introgressed into a disease-susceptible genetic background, and microbiome composition of the resulting near-isogenic lines was compared to that of the original susceptible parent line in five fields over two years. Introgression of disease-resistance alleles shifted the relative abundance of diverse fungal and bacterial taxa by up to 1000-fold in both 3-week-old and 7-week-old plants; however, these effects varied among fields and years. With few exceptions, host genotype effects were not any stronger in fields with high disease pressure than in uninfected fields, and microbiome succession over time was similar in heavily infected plants and uninfected plants. Overall, our results suggest that QTL for broad-spectrum disease resistance--or closely linked genes--have direct pleiotropic effects on the leaf microbiome in maize. Additional manipulative experiments will be needed to determine the consequences, if any, for plant health and disease resistance.