Significance of the Diversification of Wheat Species for the Assembly and Functioning of the Root-Associated Microbiome

Abstract

Wheat, one of the major crops in the world, has had a complex history that includes genomic hybridizations between Triticum and Aegilops species and several domestication events, which resulted in various wild and domesticated species (especially Triticum aestivum and Triticum durum), many of them still existing today. The large body of information available on wheat-microbe interactions, however, was mostly obtained without considering the importance of wheat evolutionary history and its consequences for wheat microbial ecology. This review addresses our current understanding of the microbiome of wheat root and rhizosphere in light of the information available on pre- and post-domestication wheat history, including differences between wild and domesticated wheats, ancient and modern types of cultivars as well as individual cultivars within a given wheat species. This analysis highlighted two major trends. First, most data deal with the taxonomic diversity rather than the microbial functioning of root-associated wheat microbiota, with so far a bias toward bacteria and mycorrhizal fungi that will progressively attenuate thanks to the inclusion of markers encompassing other micro-eukaryotes and archaea. Second, the comparison of wheat genotypes has mostly focused on the comparison of T. aestivum cultivars, sometimes with little consideration for their particular genetic and physiological traits. It is expected that the development of current sequencing technologies will enable to revisit the diversity of the wheat microbiome. This will provide a renewed opportunity to better understand the significance of wheat evolutionary history, and also to obtain the baseline information needed to develop microbiome-based breeding strategies for sustainable wheat farming.

Keywords: domestication; microbial interactions; rhizosphere; root microbiome; symbiosis; wheat.

FIGURE 1

Relationship between wheat roots and soil/microbial components. (A) Structure of the rhizosphere, rhizoplane, and endosphere (not to scale). The rhizosphere is the soil in the immediate vicinity of the root, where the root has a major direct impact on soil organization and microbial functioning. The rhizoplane is the interface between the root surface and the soil. The endosphere corresponds to root internal tissues. Adapted from York et al. (2016) and Ding et al. (2019). (B) Major root-level microbial contributions to biotic interactions and biogeochemical cycles linked to plant growth and health. Root colonization by microorganisms is mediated by plant signals and exudates, which attract or repel soil microorganisms. Biotic interactions in the rhizosphere include plant-microorganism interactions and microorganism/microorganism interactions, with beneficial (+), deleterious (-) or neutral effects ( = ). Major microbial transformations are indicated for C, N, and P biogeochemical cycles. Metal biotransformations are not reviewed. A particular microbial taxon may be involved in several different biotic interactions (left box) and biotransformations (right box). ISR, Induced Systemic Resistance; ACC, 1-AminoCyclopropane-1-Carboxylate. Dashed arrows are used for abiotic volatilization phenomena.

FIGURE 2

The origin of durum and bread wheat, and literature comparisons. Wild wheats are represented in purple, while domesticated wheats are in turquoise. (A) Wild and domesticated species involved in wheat evolution and leading to pasta (T. durum) and bread (T. aestivum) wheats are indicated (adapted from Mujeeb-Kazi, 2006), as well as examples of key scientific issues investigated with them (shown with small squares with the color code indicated below the panel). The ancestors of pasta and bread wheats underwent hybridization and polyploidization events involving genomes A, S, B, and D. A simplified version of wheat evolutionary history is depicted. The A and S genomes arose by divergence from a common ancestor (not shown) circa 7 million years Before Present (BP) (Pont et al., 2019). The B genome probably descends from the S genome and is therefore a close relative of Aegilops speltoides (SS) (Fricano et al., 2014). A first hybridization event is speculated to have taken place between A (T. urartu) and S (A. speltoides/A. mutica) genomes, 5–6 million years BP (Glémin et al., 2019), leading to the D genome upon homoploid hybrid speciation. A second hybridization event took place about 500,000 years BP between this B genome donor and T. urartu (A genome), leading to the wild tetraploid T. dicoccoides, and later to the domesticated emmer T. dicoccon. A third hybridization event (10,000 years BP) involved T. dicoccon and an ascendant of current A. tauschii (D genome), leading to the hexaploid wheat T. aestivum. It is unclear whether the latter hybridization and domestication events took place at the same time or not, and the wild form of the hexaploid hybrid remains unknown. A fourth cross, between T. aestivum and T. dicoccon, is probably at the origin of the hexaploid wheat Triticum spelta (Fricano et al., 2014). Wheat genomes are composed of 14 (AA, BB or DD), 28 (AABB), or 42 chromosomes (AABBDD). Dashed arrows are used for uncertain events. In the history of Triticeae, other domestication events also occurred but without leading to species extensively cultivated nowadays, as for example the wild einkorn Triticum monococcum subsp. beoticum (A genome, genomically close to but not interfertile with T. urartu; Fricano et al., 2014) was domesticated to become Triticum monococcum subsp. monococcum (not shown). (B) Key literature comparisons between individual wheat species are indicated using colored lines connecting the corresponding species included; the type of comparison is shown using letters a-l, and is specified in the legend, along with the corresponding reference(s). The figure points to an unbalance in the consideration of wheat species, as previous investigation have studied T. durum, T. aestivum, and T. dicoccoides extensively, T. urartu, T. dicoccon, and A. tauschii to a lesser extent, but the other species have been seldom considered. We identified eight studies comparing wheat genomic and phenotypic properties and seven others comparing the microbiota associated to different wheat species, which shows that plant properties and microbiota properties are described to the same extent. Multiple comparisons between T. durum, T. dicoccon, and T. dicoccoides were made (five studies), probably because this represents a good model for domestication studies, but only one considered the microbiota (h). Only 3 of 15 studies, with a focus on seminal roots (c) or arbuscular mycorrhizal fungi (g), covered all main events of wheat history.

FIGURE 3

Heatmap of major phyla affiliated with (A) bacteria, (B) archaea, and (C) fungi in rhizosphere soil (RS) and root/endosphere (RE) of wheats and non-wheat plants based on results from selected studies. Only phyla with relative abundance >0.5% in at least one study are shown. The color intensity in each cell denotes the transformed relative abundance [log₂((100x)+0.02)] of a phylum in each study for each plant type. For details on individual conditions, see Supplementary Table 1.