Maize leaf endosphere microbiome was affected by domestication and shows patterns consistent with microbial dysbiosis

Whether domestication, post-domestication spread, and breeding affected the maize leaf endosphere microbiota is poorly understood despite the well-known effects of those processes on the crop's genetics and responses to the environment. We examined the leaf endosphere microbial communities associated with three plant groups (Zea mays): teosintes, maize landraces, and maize elite inbreds. The teosintes group included Balsas (Z. mays parviglumis) and perennial (Zea diploperennis) teosinte, and each maize (Z. mays mays) group included genotypes from Mexico and USA. We used 16S-V4 region amplicon sequencing of the leaf endophytic microbiota to infer how the microbial communities of inbred maize may have been shaped by the crop's evolution, and whether they were affected by: (i) the transition from a perennial life history to an annual life history in the teosintes; (ii) domestication of maize from Balsas teosinte; (iii) northward spread of landrace maize from Mexico to the US; and (iii) breeding of landrace maizes to produce elite inbreds.

The leaf endophytic microbial community differed among the plant groups and genotypes, and was affected by domestication, as indicated by a decline in bacterial diversity and changes in microbial community structure between wild (teosinte) and domesticated (maize) Zea. While the microbial community structure was stringent and regulated in the teosintes, it was variable in the maize landraces and inbreds, as evidenced by greater distances to centroid based on Euclidean dissimilarity metric. This pattern was suggestive of microbial dysbiosis in the leaf endosphere associated with domestication and is consistent with predictions of the Anna Karenina principle. This finding marks the first evidence of dysbiosis associated with domestication. FAPROTAX predictions suggested that the teosintes may harbor microbial communities enriched in taxa associated with cellulolytic, chitinolytic, and nitrate respiration functions, while the maizes showed higher fermentation and nitrate reduction functions.

Our results showed that the leaf endosphere microbial community structures in maize are consistent with alterations associated with dysbiosis. Our findings enhanced our understanding of the effects of anthropogenic processes including crop domestication, spread, and breeding on the leaf endosphere of elite maize cultivars, and may guide the development of evolutionarily-and ecologically sustainable biofertilizers and biocontrol agents.