Microbiome manipulation could dramatically affect crop plant health and productivity, making it a promising tool for sustainable agriculture. However, the interaction between host genetic variation and microbial community composition complicates the integration of plant microbiomes into crop improvement programs. For example, breeding for multiple disease resistance (MDR) involves genes that affect invasion success of several diverse pathogenic microorganisms, often via poorly understood mechanisms. Currently, it is unknown whether these broad-spectrum MDR loci also affect colonization by non-pathogenic microbes.
To address this question, we used germplasm from a real maize breeding population to compare microbiome composition and diversity before and after introgression of MDR loci. In three fields near Raleigh, NC, we planted 14 inbred maize lines and quantified their foliar fungal and bacterial communities using deep rDNA amplicon sequencing. Nine of these genotypes were near-isogenic lines that were ~80-95% genetically identical to a highly disease-susceptible parent, but with introgressed genome regions from a highly MDR parent that conferred partial resistance to three diverse fungal pathogens. By comparing microbiome composition of these near-isogenic lines to that of their disease-susceptible parent line, we tested the effects of various MDR loci on the establishment of non-pathogenic microbes in maize leaves.
Maize plants growing in different fields only ~1 km apart assembled distinct foliar fungal communities, differing in composition and in overall diversity by up to 30%. In addition to this environmental effect, the inbred maize lines also differed in species richness and evenness by about 30%; however, this genotype effect was only observed in one field. Microbiome diversity of near-isogenic lines was generally intermediate to that of the parent lines. However, the different introgressed loci distinguishing these lines affected different subsets of the community. For instance, several Sporobolomyces operational taxonomic units (OTUs) were reliably depleted (relative to the disease-susceptible parental line) in 6 out of 9 near-isogenic lines; in contrast, strong depletion of Cladosporium and Cryptococcus OTUs was only observed in a single near-isogenic line. Dioszegia, Phoma, and Phomopsis OTUs were enriched in several lines. Overall, our results indicate that in maize, some genes conferring resistance to multiple pathogens (or closely linked genes) also affect colonization by non-pathogenic endophytes and/or epiphytes. The consequence for MDR breeding will depend on whether the affected microbiome members are beneficial or harmful to the plant. Bacterial microbiome dynamics and the effects of pathogen invasion on microbiome composition may also be discussed.