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Seed-Derived Microbial Colonization of Wild Emmer and Domesticated Bread Wheat (Triticum dicoccoides and T. aestivum) Seedlings Shows Pronounced Differences in Overall Diversity and Composition - PubMed

  • ️Wed Jan 01 2020

Seed-Derived Microbial Colonization of Wild Emmer and Domesticated Bread Wheat (Triticum dicoccoides and T. aestivum) Seedlings Shows Pronounced Differences in Overall Diversity and Composition

Ezgi Özkurt et al. mBio. 2020.

Abstract

The composition of the plant microbiota may be altered by ecological and evolutionary changes in the host population. Seed-associated microbiota, expected to be largely vertically transferred, have the potential to coadapt with their host over generations. Strong directional selection and changes in the genetic composition of plants during domestication and cultivation may have impacted the assembly and transmission of seed-associated microbiota. Nonetheless, the effect of plant speciation and domestication on the composition of these microbes is poorly understood. Here, we have investigated the composition of bacteria and fungi associated with the wild emmer wheat (Triticum dicoccoides) and domesticated bread wheat (Triticum aestivum). We show that vertically transmitted bacteria, but not fungi, of domesticated bread wheat species T. aestivum are less diverse and more inconsistent among individual plants compared to those of the wild emmer wheat species T. dicoccoides. We propagated wheat seeds under sterile conditions to characterize the colonization of seedlings by seed-associated microbes. Hereby, we show markedly different community compositions and diversities of leaf and root colonizers of the domesticated bread wheat compared to the wild emmer wheat. By propagating the wild emmer wheat and domesticated bread wheat in two different soils, we furthermore reveal a small effect of plant genotype on microbiota assembly. Our results suggest that domestication and prolonged breeding have impacted the vertically transferred bacteria, but only to a lesser extent have affected the soil-derived microbiota of bread wheat.IMPORTANCE Genetic and physiological changes associated with plant domestication have been studied for many crop species. Still little is known about the impact of domestication on the plant-associated microbiota. In this study, we analyze the seed-associated and soil-derived bacterial and fungal microbiota of domesticated bread wheat and wild emmer wheat. We show a significant difference in the seed-associated, but not soil-derived, bacterial communities of the wheat species. Interestingly, we find less pronounced effects on the fungal communities. Overall, this study provides novel insight into the diversity of vertically transmitted microbiota of wheat and thereby contributes to our understanding of wheat as a "metaorganism." Insight into the wheat microbiota is of fundamental importance for the development of improved crops.

Keywords: agriculture; microbiota assembly; plant breeding; plant domestication; plant microbiota; seed microbiota; seed-associated microbiome; wheat domestication; wheat microbiota.

Copyright © 2020 Özkurt et al.

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Figures

FIG 1
FIG 1

Estimates of α diversity in the seed-associated microbiota of different wheat genotypes show similar microbial feature diversities in domesticated and wild wheat. Shown is the α diversity of (A) bacterial and (B) fungal features in the seeds of different wheat species, including T. boeoticum (wild_Tb), T. urartu (wild_Tu), T. dicoccoides (wild_Td), and T. aestivum from Turkey (landrace) and Germany (inbred). Each dot in the box plots shows the microbial feature diversity of a single seed. Pairwise comparisons of α diversity showed no significant difference between wheat genotypes.

FIG 2
FIG 2

Compositions of the seed-associated microbiota across different wheat genotypes. Shown are the mean relative abundances of the (A) 20 most abundant bacterial features and (B) 15 most abundant fungal features at the family level in seeds of the different wheat genotypes of T. boeoticum (wild_Tb), T. urartu (wild_Tu), T. dicoccoides (wild_Td), and T. aestivum from Turkey (landrace) and Germany (inbred). Color for each feature ranges from blue (minimum of 0) to red with higher relative abundance values. IS, incertae sedis taxa.

FIG 3
FIG 3

Significantly more diverse bacterial but not fungal communities are colonizing the wild wheat. Diversity of microbial features in different tissues of axenically grown wheat. Shown is the α diversity of (A) bacterial and (B) fungal taxa in seeds, leaves, and roots of the wild wheat T. dicoccoides (wild) and T. aestivum from Turkey (landrace) and Germany (inbred), respectively. Each dot in the box plots shows the microbial feature diversity of a single replicate. Global P values for each tissue based on Kruskal-Wallis test are shown in green, and P values of pairwise comparisons based on Conover’s test are in black. *, P < 0.05; **, P < 0.005; ns, nonsignificant.

FIG 4
FIG 4

Axenic seedlings of wheat are colonized by diverse bacterial and fungal taxa. Shown are the mean relative abundances of the 20 most abundant (A) bacterial and (B) fungal features at the family level in seeds, leaves, and roots of the German T. aestivum genotype (inbred), the Turkish T. aestivum genotype (landrace), and the wild wheat T. dicoccoides genotype (wild_Td), respectively. Colors for each taxon illustrate relative abundance and range from blue (minimum of 0) to red with higher relative abundance values. IS, incertae sedis taxa.

FIG 5
FIG 5

More similarity of bacterial community composition between replicates of the wild wheat seedlings compared to the domesticated wheat seedlings. Shown are Bray-Curtis distance metrics-based PCoA of (A) bacterial and (B) fungal communities of each seed, leaf, and root sample from the axenic experiment.

FIG 6
FIG 6

Soil type is a main determinant of microbial diversity in wheat seedlings. (A) Bray-Curtis distance-based PCoA of bacterial communities of plants grown in soil. (B) Summary statistics for the β diversity (PERMANOVA to estimate the explained variation by each factor and their interactions) and α diversity comparisons of the bacterial communities (two-way ANOVA as the global test and Tukey’s honest test as the post hoc test). Only significant P values are indicated. (C and D) Interaction plots showing α and β diversity comparisons of bacterial communities in (C) leaves and (D) roots of different wheat genotype grown in different soil types. Each dot in the α diversity comparisons shows the microbial feature diversity of a single replicate. In the box plots of β diversity comparisons, each dot shows a single pairwise comparison between two replicate plants. Tukey’s honest test after two-way ANOVA was performed for pairwise diversity comparisons. ms, marginally significant.

FIG 6
FIG 6

Soil type is a main determinant of microbial diversity in wheat seedlings. (A) Bray-Curtis distance-based PCoA of bacterial communities of plants grown in soil. (B) Summary statistics for the β diversity (PERMANOVA to estimate the explained variation by each factor and their interactions) and α diversity comparisons of the bacterial communities (two-way ANOVA as the global test and Tukey’s honest test as the post hoc test). Only significant P values are indicated. (C and D) Interaction plots showing α and β diversity comparisons of bacterial communities in (C) leaves and (D) roots of different wheat genotype grown in different soil types. Each dot in the α diversity comparisons shows the microbial feature diversity of a single replicate. In the box plots of β diversity comparisons, each dot shows a single pairwise comparison between two replicate plants. Tukey’s honest test after two-way ANOVA was performed for pairwise diversity comparisons. ms, marginally significant.

FIG 7
FIG 7

Halomonadaceae and Vibrionaceae are potential seed-derived microbes persisting in the leaves of soil-grown seedlings. (A) Mean relative abundances of Halomonadaceae and Vibrionaceae in the seeds and axenic seedlings (B) Mean relative abundances of Halomonadaceae and Vibrionaceae in the natural and agricultural soils and in the seedlings grown in these soils.

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