Microbiome differentiation between micro-sympatric maize and teosinte reveals domestication-driven functional erosion of the microbiome across plant compartments

Abstract

IntroductionCrop domestication has fundamentally transformed plant phenotypes through artificial selection, yet the consequences of domestication for plant-associated microbial communities across the plant-soil continuum remain poorly understood. Gap StatementWhile recent studies suggest that domestication impacts microbiome structures, the magnitude, mechanisms, and functional implications of such impacts have not been systematically quantified using controlled experimental designs that eliminate environmental confounding factors. AimTo characterize and quantify the effects of crop domestication on microbial community structure and function by comparing maize (Zea mays subsp. mays) and its wild ancestor Balsas teosinte (Zea mays subsp. parviglumis) across multiple plant compartments in an unmanipulated field setting in Mexico, maizes domestication center. MethodologyWe applied a micro-sympatric design in a natural setting to compare microbial communities between maize and Balsas teosinte across five plant compartments: bulk soil, rhizosphere, mucilage, leaves, and seeds. Full-length 16S rRNA gene sequencing was used for taxonomic characterization, Functional Annotation of Prokaryotic Taxa (FAPROTAX) and PICRUSt 2.0 were used to predict functional profiles, and network analysis was used to assess functional connectivity. ResultsCompartment identity explained 72.2% of variation in community structure, with consistent host effects across all niches (9.0%). Teosinte maintained significantly higher microbial diversity than maize across all compartments, with pronounced differences in seeds (32.0 {+/-} 1.9 vs 9.3 {+/-} 1.8 species, P < 0.01) and rhizosphere (60.3 {+/-} 5.8 vs 33.8 {+/-} 10.4 species, P < 0.01). Eighty-nine percent of predicted metabolic functions showed significant changes associated with domestication, with teosinte exhibiting enhanced nitrogen fixation (0.89 {+/-} 0.07 vs 0.44 {+/-} 0.04 in maize mucilage), siderophore production, and pathogen suppression. Network analysis revealed functional fragmentation in maize, with reduced connections (80 to 49) and lower clustering coefficients (0.62 {+/-} 0.03 vs 0.25 {+/-} 0.02, P < 0.001). ConclusionBalsas teosinte domestication fundamentally eroded microbial diversity and functional capacity in maize leading to a "domestication gap" that encompasses taxonomic loss, functional simplification, and network fragmentation, and replaced mutualistic plant-microbe partnerships with simplified microbial assemblages that may compromise crop resilience vis-a-vis a changing climate. Impact statementUnderstanding how plants select their microbial partners is crucial for enhancing agricultural productivity yet distinguishing between environmental and host genetic effects on microbiome assemblage remains challenging. Our study provides compelling evidence for host-driven microbiome assembly by comparing ancestral Balsas teosinte with derived maize growing in a common farm field in Mexico, eliminating environmental variation and experimental manipulation as confounding factors. By characterizing bacterial communities across different plant compartments, from soil to seed, we showed that each hosts genotype shaped divergent microbiome compositions despite growing in common environmental conditions. This research represents a significant step forward in understanding plant-microbe co-evolution during crop domestication and has three key implications. First, it suggests that microbiome traits were likely selected in conjunction with plant (host) traits during domestication and post-domestication selection. Second, it identifies specific bacterial communities that could be targeted for improving crop productivity and resilience. And third, it provides a methodological framework for studying host-microbe interactions in other crop-wild ancestor pairs. Our findings are particularly relevant for developing microbiome-based agricultural technologies and conservation strategies for beneficial plant-microbe interactions for deployment in traditional and modern farming systems. Data summaryThe authors confirm all supporting data, code and protocols have been provided within the article or through supplementary data files.