Domestication Impacts the Wheat-Associated Microbiota and the Rhizosphere Colonization by Seed- and Soil-Originated Microbiomes, Across Different Fields

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

Domestication affects the composition, diversity, and co-occurrence of the cereal seed microbiota

Introduction: The seed-associated microbiome has a strong influence on plant ecology, fitness, and productivity. Plant microbiota could be exploited for a more responsible crop management in sustainable agriculture. However, the relationships between seed microbiota and hosts related to the changes from ancestor species to breeded crops still remain poor understood. Objectives: Our aims were i) to understand the effect of cereal domestication on seed endophytes in terms of diversity, structure and co-occurrence, by comparing four cereal crops and the respective ancestor species; ii) to test the phylogenetic coherence between cereals and their seed microbiota (clue of co-evolution). Methods: We investigated the seed microbiota of four cereal crops (Triticum aestivum, Triticum monococcum, Triticum durum, and Hordeum vulgare), along with their respective ancestors (Aegilops tauschii, Triticum baeoticum, Triticum dicoccoides, and Hordeum spontaneum, respectively) using 16S rRNA gene metabarcoding, Randomly Amplified Polymorphic DNA (RAPD) profiling of host plants and co-evolution analysis. Results: The diversity of seed microbiota was generally higher in cultivated cereals than in wild ancestors, suggesting that domestication lead to a bacterial diversification. On the other hand, more microbe-microbe interactions were detected in wild species, indicating a better-structured, mature community. Typical human-associated taxa, such as Cutibacterium, dominated in cultivated cereals, suggesting an interkingdom transfers of microbes from human to plants during domestication. Co-evolution analysis revealed a significant phylogenetic congruence between seed endophytes and host plants, indicating clues of co-evolution between hosts and seed-associated microbes during domestication. Conclusion: This study demonstrates a diversification of the seed microbiome as a consequence of domestication, and provides clues of co-evolution between cereals and their seed microbiota. This knowledge is useful to develop effective strategies of microbiome exploitation for sustainable agriculture

Domestication caused taxonomical and functional shifts in the wheat rhizosphere microbiota, and weakened the natural bacterial biocontrol against fungal pathogens

Modern crops might have lost some of their functional traits, required for interacting with beneficial microbes, as a result of the genotypic/phenotypic modifications that occurred during domestication. Here, we studied the bacterial and fungal microbiota in the rhizosphere of two cultivated wheat species (Triticum aestivum and T. durum) and their respective ancestors (Aegilops tauschii and T. dicoccoides), in three experimental fields, by using metabarcoding of 16S rRNA genes and ITS2, coupled with co-occurrence network analysis. Moreover, the abundance of bacterial genes involved in N- and P-cycles was estimated by quantitative PCR, and urease, alkaline phosphatase and phosphomonoesterase activities were assessed by enzymatic tests. The relationships between microbiota and environmental metadata were tested by correlation analysis. The assemblage of core microbiota was affected by both site and plant species. No significant differences in the abundance of potential fungal pathogens between wild and cultivated wheat species were found; however, co-occurrence analysis showed more bacterial–fungal negative correlations in the wild species. Concerning functions, the nitrogen denitrification nirS gene was consistently more abundant in the rhizosphere of A. tauschii than T. aestivum. Urease activity was higher in the rhizosphere of each wild wheat species in at least two of the research locations. Several microbiota members, including potentially beneficial taxa such as Lysobacter and new taxa such as Blastocatellaceae, were found to be strongly correlated to rhizospheric soil metadata. Our results showed that a functional microbiome shift occurred as a result of wheat domestication. Notably, these changes also included the reduction of the natural biocontrol potential of rhizosphere-associated bacteria against pathogenic fungi, suggesting that domestication disrupted the equilibrium of plant-microbe relationships that had been established during million years of co-evolution