Agricultural Selection of Wheat Has Been Shaped by Plant-Microbe Interactions

Abstract

The influence of wheat (modern wheat, both bread and pasta, their wild ancestors and synthetic hybrids) on the microbiota of their roots and surrounding soil is characterized. We isolated lines of bread wheat by hybridizing diploid (Aegilops tauschii) with tetraploid Triticum durum and crossed it with a modern cultivar of Triticum aestivum. The newly created, synthetic hybrid wheat, which recapitulate the breeding history of wheat through artificial selection, is found to support a microbiome enriched in beneficial Glomeromycetes fungi, but also in, potentially detrimental, Nematoda. We hypothesize that during wheat domestication this plant-microbe interaction diminished, suggesting an evolutionary tradeoff; sacrificing advantageous nutrient acquisition through fungal interactions to minimize interaction with pathogenic fungi. Increased plant selection for Glomeromycetes and Nematoda is correlated with the D genome derived from A. tauschii. Despite differences in their soil microbiota communities, overall wheat plants consistently show a low ratio of eukaryotes to prokaryotes. We propose that this is a mechanism for protection against soil-borne fungal disease and appears to be deeply rooted in the wheat genome. We suggest that the influence of plants on the composition of their associated microbiota is an integral factor, hitherto overlooked, but intrinsic to selection during wheat domestication.

Keywords: Triticaeae; crop domestication; microbiota; polyploidy; rhizosphere; wheat.

FIGURE 1

Genetic relationship of wheat species used in this study. Dotted lines indicate hybridization and crossing performed for this study.

FIGURE 2

Venn diagrams of the prokaryotic microbiota from different wheat species in (A) rhizosphere and (B) root-associated niches showing the number and relative abundance of prokaryotic OTUs. Only OTUs that were found in both lines representing a species were analyzed. For the small overlapping regions, the OTU numbers are indicated with arrows. Core microbiota profile of the rhizosphere and root-associated community is presented.

FIGURE 3

PCoA plots of (A) total prokaryotic community, (B) prokaryotic rhizosphere community, (C) root-associated community, (D) eukaryotic rhizosphere community, (E) fungal rhizosphere community, and (F) Oomycetes rhizosphere community. Data points represent averaged (mean) location of all individual samples belonging to a given group, while error bars represent standard error.

FIGURE 4

Phylogenetic annotation of rhizosphere and root-associated OTUs found for each wheat species. Bars represent averaged relative abundance of each phyla for each wheat species. bulk soil n = 8, rhizosphere n = 24, 23, 18, 20, 24, root n = 23, 16, 15, 18, 23 biological replicates for each condition.

FIGURE 5

PCA plots of (A) prokaryotic root community and (B) eukaryotic rhizosphere community at the phylum level. Microbiota taxa are used as factors separating plants microbiota structure. The longer the line representing microbial taxa is, the strong effect it has for the sample differentiation. Samples located according to the lines’ directions are influenced by a particular taxon. α – alpha-, β – beta-, γ – gamma-, δ – Deltaproteobacteria.

FIGURE 6

(A) The relative abundance of Nematoda (left) and Glomeromycetes (right) in the microbial eukaryotic community. ANOVA F and P values are provided, and the letters present the result of pair-wise t-test with Bonferroni correction. (B) A. tauschii derived D genome increases the influence of these taxa, while the artificially selected D does not have such an effect, for panels (A,B) error bars represent standard error. Arrows indicate the hybridization and crosses conducted in this study. Different letters reflect significant difference between datasets in pair-wise t-test.