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.