An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota

Abstract

Root exudates influence the surrounding soil microbial community, and recent evidence demonstrates the involvement of ATP-binding cassette (ABC) transporters in root secretion of phytochemicals. In this study, we examined effects of seven Arabidopsis (Arabidopsis thaliana) ABC transporter mutants on the microbial community in native soils. After two generations, only the Arabidopsis abcg30 (Atpdr2) mutant had significantly altered both the fungal and bacterial communities compared with the wild type using automated ribosomal intergenic spacer analysis. Similarly, root exudate profiles differed between the mutants; however, the largest variance from the wild type (Columbia-0) was observed in abcg30, which showed increased phenolics and decreased sugars. In support of this biochemical observation, whole-genome expression analyses of abcg30 roots revealed that some genes involved in biosynthesis and transport of secondary metabolites were up-regulated, while some sugar transporters were down-regulated compared with genome expression in wild-type roots. Microbial taxa associated with Columbia-0 and abcg30 cultured soils determined by pyrosequencing revealed that exudates from abcg30 cultivated a microbial community with a relatively greater abundance of potentially beneficial bacteria (i.e. plant-growth-promoting rhizobacteria and nitrogen fixers) and were specifically enriched in bacteria involved in heavy metal remediation. In summary, we report how a single gene mutation from a functional plant mutant influences the surrounding community of soil organisms, showing that genes are not only important for intrinsic plant physiology but also for the interactions with the surrounding community of organisms as well.

Figure 1.

NMS analysis of fungal and bacterial community profiles of Arabidopsis wild type and ABC transporter mutant rhizospheric soil samples conducted using the relative Sorenson distance measure. All generation samples were analyzed simultaneously. A, Fungi; B, bacteria. G0, zero generation (before seeding); G1, first generation; G2, second generation; Ler, Landsberg erecta ecotype; T, negative control (soil without plant).

Figure 2.

A, PCA of Arabidopsis wild type (Col-0) and ABC transporter mutant root exudates using projected one-dimensional J-resolved spectrum. B, Percentage of matched two-dimensional J-resolved signals between wild type (Col-0) and Arabidopsis ABC transporter mutant root exudates. a, Col-0; b, abca7; c, dtx12; d, abcc2; e, abcg30; f, abcg34; g, abcg35; h, abcb1; i, abcb4; j, abcb27.

Figure 3.

Fungal (A) and bacterial (B) OTUs present in the 2nd generation of Atabcg30 and wild-type soils determined by rRNA pyrosequencing. Green, abcg30; blue, wild type (Col-0); pink, shared. C, Total estimated species richness (ACE and Chao) and Shannon diversity index (H). D, Significance of microbial libraries community profile comparison using ∫-libshuff. [See online article for color version of this figure.]

Figure 4.

Relative abundance of bacterial OTUs (1% dissimilarity) significantly up- (A) or down-regulated (B) in the abcg30 mutant soils compared to the wild type. Taxonomic assignments were made with the RDP II naïve Bayesian classifier (80% confidence threshold) using a single representative sequence for each OTU. Col-0, black bars; abcg30, gray bars.

Figure 5.

Relative abundance of fungal OTUs (1% dissimilarity) significantly down- (A) or up-regulated (B) in the abcg30 mutant soils compared to the wild type. Taxonomic assignments were made based on the nearest neighbor in GenBank (homology >80%) using a single representative sequence for each OTU. Col-0, black bars; abcg30, gray bars.