Diversity and heritability of the maize rhizosphere microbiome under field conditions

Abstract

The rhizosphere is a critical interface supporting the exchange of resources between plants and their associated soil environment. Rhizosphere microbial diversity is influenced by the physical and chemical properties of the rhizosphere, some of which are determined by the genetics of the host plant. However, within a plant species, the impact of genetic variation on the composition of the microbiota is poorly understood. Here, we characterized the rhizosphere bacterial diversity of 27 modern maize inbreds possessing exceptional genetic diversity grown under field conditions. Randomized and replicated plots of the inbreds were planted in five field environments in three states, each with unique soils and management conditions. Using pyrosequencing of bacterial 16S rRNA genes, we observed substantial variation in bacterial richness, diversity, and relative abundances of taxa between bulk soil and the maize rhizosphere, as well as between fields. The rhizospheres from maize inbreds exhibited both a small but significant proportion of heritable variation in total bacterial diversity across fields, and substantially more heritable variation between replicates of the inbreds within each field. The results of this study should facilitate expanded studies to identify robust heritable plant-microbe interactions at the level of individual polymorphisms by genome wide association, so that plant-microbiome interactions can ultimately be incorporated into plant breeding.

Fig. 1.

Primer set influences the diversity profiles of the rhizosphere and bulk soil microbiota. (A) Relative abundances of the phyla and domains recovered using four different primer pairs (27F-338R, 515F-806R, 804F-1392R, 926F-1392R) applied to rhizosphere soils recovered from three maize genotypes (B73, Mol17, Ill14h) and four bulk soil samples. (B) Hierarchical clustering of the weighted UniFrac distance metric for the same sample set. To highlight patterns of clustering, branches are colored by sample origin (maize genotypes and bulk soil: light blue, B73; yellow, Mo17; pink, Ill14h; and green, Bulk Soil). Primer pairs are indicated on the branch labels (the forward primer is indicated) and are highlighted by the colored boxes (27F: orange; 515F: blue; 804F: green; 926F: brown).

Fig. 2.

Factors influencing rhizosphere and soil microbiome β-diversity. Variation in unweighted UniFrac dispersion by: (A) field environment (significance P < 5.00E-03); (B) bulk soil and the maize rhizosphere (P < 5.00E-03); (C) bulk soil and maize rhizosphere within all field environments (P < 5.00E-02); and (D) maize inbreds (P < 5.00E-02). Note that the percent variation explained by the PCs of this CAP analysis is indicated on the axes and refers to the fraction of the total variance (indicated in main text) explained by field (A), sample type (B), sample type by field (C), and maize inbred (D).

Fig. 3.

Fields can be differentiated based on their physiochemical properties. Principal component analysis of the correlation matrix detailing soil relatedness among locations (Table S3). Soil samples are colored by field of origin. The percent variation explained by each PC is indicated on the axes.