Harnessing the phyllosphere microbiota of wild foxtail millet for designing beneficial cross-kingdom synthetic communities.

Understanding the interplay between mechanisms in plant microbiome assembly and functioning of wild ancestors has led to the proposal of a novel strategy to enhance resilience to the (a)biotic stresses of domesticated crops. The challenge is determining how to harness the diverse microbiota of wild crop ancestors in their natural habitats in order to design effective synthetic microbial communities (SynComs) that reconstitute specific microbiome-associated plant phenotypes. In this study, we profiled the phyllosphere microbiota of wild green foxtail 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 and dispersal limitation differently governed the assembly of bacterial and fungal communities with distinct habitat niche breadth. Specific bacterial and yeast genera were identified as core phyllosphere taxa of wild green foxtail millet on the basis of their abundance and prevalence across the seven sampling sites. Moreover, several genera of bacteria (Bacillus, Pantoea, Methylobacterium) and yeast (Vishniacozyma, Filobasidium, Sporobolomyces) displayed significant correlations with the abundances of one or more foliar pathogenic fungi, in particular fungi of the genus Alternaria. Subsequent isolation and characterization of these bacterial and yeast genera allowed the design of cross-kingdom SynComs that protected domesticated foxtail millet from leaf infections by Alternaria alternata. These results provide fundamental insight into the mechanisms governing the phyllosphere microbiota assembly of a wild crop ancestor across large geographic scales and a practical framework to leverage this fundamental knowledge for the design of SynComs that mitigate the biotic stress of the domesticated crop.