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Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat.

ABSTRACT: Despite the large morphological and physiological changes that plants have undergone through domestication, little is known about their impact on their microbiome. Here we characterized rhizospheric bacterial and fungal communities as well as the abundance of N-cycling microbial guilds across thirty-nine accessions of tetraploid wheat, Triticum turgidum, from four domestication groups ranging from the wild subspecies to the semi dwarf elite cultivars. We identified several microbial phylotypes displaying significant variation in their relative abundance depending on the wheat domestication group with a stronger impact of domestication on fungi. The relative abundance of potential fungal plant pathogens belonging to the Sordariomycetes class decreased in domesticated compared to wild emmer while the opposite was found for members of the Glomeromycetes, which are obligate plant symbionts. The depletion of nitrifiers and of arbuscular mycorrhizal fungi in elite wheat cultivars compared to primitive domesticated forms suggests that the Green Revolution has decreased the coupling between plant and rhizosphere microbes that are potentially important for plant nutrient availability. Both plant diameter and fine root percentage exhibited the highest number of associations with microbial taxa, highlighting their putative role in shaping the rhizosphere microbiota during domestication. Aside from domestication, significant variation of bacterial and fungal community composition was found among accessions within each domestication group. In particular, the relative abundances of Ophiostomataceae and of Rhizobiales were strongly dependent on the host accession, with heritability estimates of?~?27% and?~?25%, indicating that there might be room for genetic improvement via introgression of ancestral plant rhizosphere-beneficial microbe associations.

SUBMITTER: Spor A

PROVIDER: S-EPMC7376052 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat.

Spor Aymé A Roucou Agathe A Mounier Arnaud A Bru David D Breuil Marie-Christine MC Fort Florian F Vile Denis D Roumet Pierre P Philippot Laurent L Violle Cyrille C

Scientific reports 20200722 1

Despite the large morphological and physiological changes that plants have undergone through domestication, little is known about their impact on their microbiome. Here we characterized rhizospheric bacterial and fungal communities as well as the abundance of N-cycling microbial guilds across thirty-nine accessions of tetraploid wheat, Triticum turgidum, from four domestication groups ranging from the wild subspecies to the semi dwarf elite cultivars. We identified several microbial phylotypes d ...[more]

PMID: 32699344

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Project description:BackgroundThe rhizosphere microbiome, which is shaped by host genotypes, root exudates, and plant domestication, is crucial for sustaining agricultural plant growth. Despite its importance, how plant domestication builds up specific rhizosphere microbiomes and metabolic functions, as well as the importance of these affected rhizobiomes and relevant root exudates in maintaining plant growth, is not well understood. Here, we firstly investigated the rhizosphere bacterial and fungal communities of domestication and wild accessions of tetraploid wheat using amplicon sequencing (16S and ITS) after 9 years of domestication process at the main production sites in China. We then explored the ecological roles of root exudation in shaping rhizosphere microbiome functions by integrating metagenomics and metabolic genomics approaches. Furthermore, we established evident linkages between root morphology traits and keystone taxa based on microbial culture and plant inoculation experiments.ResultsOur results suggested that plant rhizosphere microbiomes were co-shaped by both host genotypes and domestication status. The wheat genomes contributed more variation in the microbial diversity and composition of rhizosphere bacterial communities than fungal communities, whereas plant domestication status exerted much stronger influences on the fungal communities. In terms of microbial interkingdom association networks, domestication destabilized microbial network and depleted the abundance of keystone fungal taxa. Moreover, we found that domestication shifted the rhizosphere microbiome from slow growing and fungi dominated to fast growing and bacteria dominated, thereby resulting in a shift from fungi-dominated membership with enrichment of carbon fixation genes to bacteria-dominated membership with enrichment of carbon degradation genes. Metagenomics analyses further indicated that wild cultivars of wheat possess higher microbial function diversity than domesticated cultivars. Notably, we found that wild cultivar is able to harness rhizosphere microorganism carrying N transformation (i.e., nitrification, denitrification) and P mineralization pathway, whereas rhizobiomes carrying inorganic N fixation, organic N ammonification, and inorganic P solubilization genes are recruited by the releasing of root exudates from domesticated wheat. More importantly, our metabolite-wide association study indicated that the contrasting functional roles of root exudates and the harnessed keystone microbial taxa with different nutrient acquisition strategies jointly determined the aboveground plant phenotypes. Furthermore, we observed that although domesticated and wild wheats recruited distinct microbial taxa and relevant functions, domestication-induced recruitment of keystone taxa led to a consistent growth regulation of root regardless of wheat domestication status.ConclusionsOur results indicate that plant domestication profoundly influences rhizosphere microbiome assembly and metabolic functions and provide evidence that host plants are able to harness a differentiated ecological role of root-associated keystone microbiomes through the release of root exudates to sustain belowground multi-nutrient cycles and plant growth. These findings provide valuable insights into the mechanisms underlying plant-microbiome interactions and how to harness the rhizosphere microbiome for crop improvement in sustainable agriculture. Video Abstract.

Project description:The seed-transmitted microorganisms and the microbiome of the soil in which the plant grows are major drivers of the rhizosphere microbiome, a crucial component of the plant holobiont. The seed-borne microbiome can be even coevolved with the host plant as a result of adaptation and vertical transmission over generations. The reduced genome diversity and crossing events during domestication might have influenced plant traits that are important for root colonization by seed-borne microbes and also rhizosphere recruitment of microbes from the bulk soil. However, the impact of the breeding on seed-transmitted microbiome composition and the plant ability of microbiome selection from the soil remain unknown. Here, we analyzed both endorhiza and rhizosphere microbiome of two couples of genetically related wild and cultivated wheat species (Aegilops tauschii/Triticum aestivum and T. dicoccoides/T. durum) grown in three locations, using 16S rRNA gene and ITS2 metabarcoding, to assess the relative contribution of seed-borne and soil-derived microbes to the assemblage of the rhizosphere microbiome. We found that more bacterial and fungal ASVs are transmitted from seed to the endosphere of all species compared with the rhizosphere, and these transmitted ASVs were species-specific regardless of location. Only in one location, more microbial seed transmission occurred also in the rhizosphere of A. tauschii compared with other species. Concerning soil-derived microbiome, the most distinct microbial genera occurred in the rhizosphere of A. tauschii compared with other species in all locations. The rhizosphere of genetically connected wheat species was enriched with similar taxa, differently between locations. Our results demonstrate that host plant criteria for soil bank's and seed-originated microbiome recruitment depend on both plants' genotype and availability of microorganisms in a particular environment. This study also provides indications of coevolution between the host plant and its associated microbiome resulting from the vertical transmission of seed-originated taxa.

Project description:BackgroundPlant-beneficial bacterial inoculants are of great interest in agriculture as they have the potential to promote plant growth and health. However, the inoculation of the rhizosphere microbiome often results in a suboptimal or transient colonization, which is due to a variety of factors that influence the fate of the inoculant. To better understand the fate of plant-beneficial inoculants in complex rhizosphere microbiomes, composed by hundreds of genotypes and multifactorial selection mechanisms, controlled studies with high-complexity soil microbiomes are needed.ResultsWe analysed early compositional changes in a taxa-rich natural soil bacterial community under both exponential nutrient-rich and stationary nutrient-limited growth conditions (i.e. growing and stable communities, respectively) following inoculation with the plant-beneficial bacterium Pseudomonas protegens in a bulk soil or a wheat rhizosphere environment. P. protegens successfully established under all conditions tested and was more abundant in the rhizosphere of the stable community. Nutrient availability was a major factor driving microbiome composition and structure as well as the underlying assembly processes. While access to nutrients resulted in communities assembled mainly by homogeneous selection, stochastic processes dominated under the nutrient-deprived conditions. We also observed an increased rhizosphere selection effect under nutrient-limited conditions, resulting in a higher number of amplicon sequence variants (ASVs) whose relative abundance was enriched. The inoculation with P. protegens produced discrete changes, some of which involved other Pseudomonas. Direct competition between Pseudomonas strains partially failed to replicate the observed differences in the microbiome and pointed to a more complex interaction network.ConclusionsThe results of this study show that nutrient availability is a major driving force of microbiome composition, structure and diversity in both the bulk soil and the wheat rhizosphere and determines the assembly processes that govern early microbiome development. The successful establishment of the inoculant was facilitated by the wheat rhizosphere and produced discrete changes among other members of the microbiome. Direct competition between Pseudomonas strains only partially explained the microbiome changes, indicating that indirect interactions or spatial distribution in the rhizosphere or soil interface may be crucial for the survival of certain bacteria. Video Abstract.

Dataset Information

Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat.

Publications

Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat.

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