Phyllosphere microbiome assembly in wild green foxtail: designing synthetic communities for domesticated millet protection

Designing effective synthetic microbial communities (SynComs) allows for reconstitution of specific microbiome-associated plant phenotypes, including enhanced growth and tolerance to (a)biotic stresses. In particular, understanding the interplay of mechanisms dynamically structuring the microbiota assembly and functioning of wild crop ancestors has been proposed as a novel strategy to ‘rewild’ crop microbiomes for enhanced growth and health. Here, we profiled the phyllosphere microbiota of wild green foxtail millet plants collected from seven geographically diverse natural ecosystems and showed that variations in soil parameters and climatic conditions as well as plant genetic distance significantly correlated with bacterial and fungal community compositions. Environmental selection was found to strongly govern the assembly of bacterial communities with narrow habitat niche breadth, while dispersal limitation was predominant in structuring the assembly of fungal communities displaying broader substrate utilization. Specific bacterial and yeast genera were identified as core phyllosphere taxa based on their abundance and prevalence across the seven sampling sites. Moreover, several bacterial ( Bacillus , Pantoea , Methylobacterium ) and yeast genera ( Vishniacozyma , Filobasidium , Sporobolomyces ) displayed significant correlations with the abundances of one or more foliar pathogenic fungi, in particular Alternaria . Subsequent isolation and identification of these bacterial and yeast genera allowed the design of SynComs that protected the domesticated foxtail millet from leaf infections by Alternaria alternata . These results show that fundamental knowledge of the phyllosphere microbiota of a wild crop ancestor across large geographic scales can be leveraged to design cross-kingdom SynComs with beneficial traits for the health of their domesticated crop counterparts.