Whole-Genome Duplication and Host Genotype Affect Rhizosphere Microbial Communities

Abstract

The composition of microbial communities found in association with plants is influenced by host phenotype and genotype. However, the ways in which specific genetic architectures of host plants shape microbiomes are unknown. Genome duplication events are common in the evolutionary history of plants and influence many important plant traits, and thus, they may affect associated microbial communities. Using experimentally induced whole-genome duplication (WGD), we tested the effect of WGD on rhizosphere bacterial communities in Arabidopsis thaliana. We performed 16S rRNA amplicon sequencing to characterize differences between microbiomes associated with specific host genetic backgrounds (Columbia versus Landsberg) and ploidy levels (diploid versus tetraploid). We modeled relative abundances of bacterial taxa using a hierarchical Bayesian approach. We found that host genetic background and ploidy level affected rhizosphere community composition. We then tested to what extent microbiomes derived from a specific genetic background or ploidy level affected plant performance by inoculating sterile seedlings with microbial communities harvested from a prior generation. We found a negative effect of the tetraploid Columbia microbiome on growth of all four plant genetic backgrounds. These findings suggest an interplay between host genetic background and ploidy level and bacterial community assembly with potential ramifications for host fitness. Given the prevalence of ploidy-level variation in both wild and managed plant populations, the effects on microbiomes of this aspect of host genetic architecture could be a widespread driver of differences in plant microbiomes. IMPORTANCE Plants influence the composition of their associated microbial communities, yet the underlying host-associated genetic determinants are typically unknown. Genome duplication events are common in the evolutionary history of plants and affect many plant traits. Using Arabidopsis thaliana, we characterized how whole-genome duplication affected the composition of rhizosphere bacterial communities and how bacterial communities associated with two host plant genetic backgrounds and ploidy levels affected subsequent plant growth. We observed an interaction between ploidy level and genetic background that affected both bacterial community composition and function. This research reveals how genome duplication, a widespread genetic feature of both wild and crop plant species, influences bacterial assemblages and affects plant growth.

Keywords: Arabidopsis thaliana; multinomial modeling; plant-microbe interactions; whole-genome duplication.

FIG 1

Relative abundance of each rhizosphere associated bacterial phylum in plants with differing genetic backgrounds. Each colored bar represents an individual rhizosphere sample. Phyla are arranged alphabetically. ASVs with a relative abundance of less than 0.05 were removed for graphical clarity.

FIG 2

Genotype and ploidy influence rhizosphere bacterial relative abundances. (a) Bacterial families identified as more abundant in the diploid rhizosphere are shown above the gray line, and those more abundant in the tetraploid rhizosphere appear below the gray line. (b) Bacterial families identified as more abundant in the Landsberg rhizosphere are shown above the gray line, and those more abundant in the rhizosphere of Columbia plants appear below the gray line. Log₁₀ fold change were calculated from relative abundance estimates obtained through hierarchical Bayesian modeling of read counts (see the text). Points represent individual ASVs within families.

FIG 3

(a and b) Residuals of observed growth differences in above- and belowground biomass for plants grown in soils inoculated with microbiomes shaped by each genotype, with effects of experimental block removed (blocking factors were host genetic background and ploidy level). Bar height represents the mean of residuals; bar color corresponds to soil inoculum across all plant genotypes. Error bars represent standard errors of the means. Lowercase letters denote significant differences among groups as determined by Tukey’s honestly significant difference (HSD) test. All genotypes inoculated with Columbia tetraploid microbiome had significantly reduced above- and belowground biomass. (c) Bacterial families identified as more abundant in the Columbia tetraploid rhizosphere are shown above the gray line. Those more abundant in the rhizosphere of all other treatment groups (inocula) appear below the gray line. The data depicted in this figure are sequencing data describing the rhizospheres from plants in each treatment group and are the data referenced in Fig. 1 and 2. Log₁₀ fold changes were calculated from relative abundance estimates obtained through hierarchical Bayesian modeling of rhizosphere associated ASV read counts following processing described in Materials and Methods. Points represent individual ASVs within families.