Dysbiosis in Maize Leaf Endosphere Microbiome is Associated with Domestication

Abstract

Background The effect of domestication and breeding on maize leaf endosphere microbiota is scarcely understood, a knowledge gap is vital to be filled given their roles in plant health. We examined the leaf endosphere microbial communities associated with three plant-groups; teosinte, landraces and elite inbred maize, with the latter including both Mexican and US lines. Particularly, we used 16S-V4 region amplicon sequencing of the leaf endosphere microbiomes to infer how the microbial community of elite 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 wild; (ii) transformation of annual life into landrace maize via domestication; (iii) the northward spread of landrace maize from Mexico to the US; and (iii) breeding of landrace maizes to produce elite inbreds. Additionally, we investigated biomarker taxa, and likely functional profiles using LEfSe analysis, network analysis, and FAPROTAX. Results The leaf endosphere microbial community differed among the plant-groups and genotypes, and was markedly 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 highly stringent and regulated in the teosintes, post-domestication maize landraces and elite inbreds showed high variability, suggesting microbial dysbiosis in the leaf endosphere associated with domestication, and consistent with predictions of the Anna Karenina principle. As such, this finding marks the first evidence of dysbiosis associated with plant domestication. Co-occurrence network analyses revealed the complexity of the network structure increased with domestication. Furthermore, FAPROTAX predictions suggested that the teosintes possessed higher cellulolytic, chitinolytic, and nitrate respiration functions, while the maize landraces and elite inbreds showed higher fermentation and nitrate reduction functions. Conclusions Our results showed the leaf endosphere microbial community structures are consistent with community alterations associated with dysbiosis. Altogether, our findings enhanced our understanding of the effects of anthropogenic processes such as 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.