Orchard management alters citrus root and rhizosphere microbiomes with functional consequences for plant performance

Agricultural management practices act as ecological disturbances that can restructure soil and plant-associated microbial communities, but the functional consequences of these microbial shifts on crop performance remain poorly understood. Here, we examined how common orchard inputs, including wood mulch, glyphosate, and humic acid, affect citrus root and rhizosphere microbiomes, leaf nutrient trajectories, and tree performance over a 3-year field experiment. Mulch emerged as the dominant driver of fungal community composition and taxonomic turnover, enriching for saprophytic fungi. Conversely, bacterial communities responded primarily to interactions among applications, particularly mulch × glyphosate, which was associated with significant depletions of bacterial genera in roots and rhizospheres. These microbiome changes corresponded with reduced tree carbon assimilation, transpiration, and yield, and altered leaf nutrients dynamics. To verify whether the microbial shifts were contributing to these plant phenotypic changes, we conducted a greenhouse experiment using field-derived soil microbiota. Active microbiota from mulch-treated soils reduced citrus seedling establishment and root growth relative to microbiota from nonmulched soils, whereas heat-killed controls eliminated these negative effects, demonstrating a causal relationship between management-induced microbiota changes and decreases in plant performance. The effect of mulch-associated microbiota on root growth further depended on glyphosate history, paralleling field observations. Humic acid increased root growth regardless of microbiota activity and moderated decreases in shoot growth by mulch-associated microbiota. Together, these results show that management practices can restructure citrus microbiomes and generate community-level traits that influence plant performance, highlighting the importance of incorporating microbial ecology and microbiome information when devising crop management strategies.