Elevated ozone reshapes wheat root-associated microbiomes through coordinated plant responses and rhizosphere environmental filtering

ABSTRACT Elevated tropospheric ozone (O 3 ) threatens crop productivity, but how O 3 -induced changes in plant responses influence root-associated microbiomes remains unclear. We investigated the responses of microbial communities inhabiting the rhizosphere and root endosphere to elevated O 3 using four cultivars grown under ambient and 1.5-fold ambient O 3 in a field-based free-air O 3 -concentration enrichment (FACE) system. Plant traits, root-released organic carbon (ROC), rhizosphere properties, extracellular enzyme activities, and bacterial and fungal communities were jointly analyzed. Elevated O 3 reduced yield and root biomass, with cultivar-dependent changes in ROC. Elevated O 3 consistently increased rhizosphere pH and altered microbial resource allocation, increasing ecoenzymatic vector length by 4.1% and decreasing vector angle by 4.6%. Bacterial communities showed a stronger response than fungal taxonomic communities, particularly in the rhizosphere. However, variation partitioning indicated that soil properties, especially pH, rather than O 3 treatment alone, provided the strongest independent explanation for bacterial community variation. Fungal communities showed limited taxonomic turnover but exhibited shifts in predicted trophic guilds, including increased pathotroph- and saprotroph-associated groups and decreased symbiotroph-containing guilds under elevated O 3 . These results demonstrate that elevated O 3 reshapes the wheat root-associated microbiome through coordinated changes in plant performance, rhizosphere environmental filtering, and microbial functional strategies, highlighting the importance of plant-mediated processes in regulating belowground responses to atmospheric change. IMPORTANCE Elevated tropospheric O 3 is an increasing threat to crop production, but its effects on belowground microbial processes remain poorly understood. This study demonstrates that O 3 -induced root-associated microbiome changes are closely linked with altered plant carbon allocation and rhizosphere environmental conditions rather than O 3 exposure also. By integrating plant traits, soil properties, extracellular enzyme allocation, and microbial community analyses, we reveal a compartment-specific plant-soil-microbiome response to elevated O 3 . These findings improve our understanding of how atmospheric pollution may reshape crop-associated microbial functions and soil ecological processes under future climate change.

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Journal
Applied and Environmental Microbiology
Published
2026-11-10
DOI
https://doi.org/10.1128/aem.01858-26
Primary Topic
Plant responses to elevated CO2
Type
article
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article

Elevated ozone reshapes wheat root-associated microbiomes through coordinated plant responses and rhizosphere environmental filtering

Evgenios Agathokleous, Qi Wang, Yanze Ma, Zhaozhong Feng et al.
Applied and Environmental Microbiology
Plant responses to elevated CO2
article

Elevated ozone reshapes wheat root-associated microbiomes through coordinated plant responses and rhizosphere environmental filtering

Evgenios Agathokleous, Qi Wang, Yanze Ma, Zhaozhong Feng, Yansen Xu, Diquan Fu, Cheng Cheng
article en

Abstract

ABSTRACT Elevated tropospheric ozone (O 3 ) threatens crop productivity, but how O 3 -induced changes in plant responses influence root-associated microbiomes remains unclear. We investigated the responses of microbial communities inhabiting the rhizosphere and root endosphere to elevated O 3 using four cultivars grown under ambient and 1.5-fold ambient O 3 in a field-based free-air O 3 -concentration enrichment (FACE) system. Plant traits, root-released organic carbon (ROC), rhizosphere properties, extracellular enzyme activities, and bacterial and fungal communities were jointly analyzed. Elevated O 3 reduced yield and root biomass, with cultivar-dependent changes in ROC. Elevated O 3 consistently increased rhizosphere pH and altered microbial resource allocation, increasing ecoenzymatic vector length by 4.1% and decreasing vector angle by 4.6%. Bacterial communities showed a stronger response than fungal taxonomic communities, particularly in the rhizosphere. However, variation partitioning indicated that soil properties, especially pH, rather than O 3 treatment alone, provided the strongest independent explanation for bacterial community variation. Fungal communities showed limited taxonomic turnover but exhibited shifts in predicted trophic guilds, including increased pathotroph- and saprotroph-associated groups and decreased symbiotroph-containing guilds under elevated O 3 . These results demonstrate that elevated O 3 reshapes the wheat root-associated microbiome through coordinated changes in plant performance, rhizosphere environmental filtering, and microbial functional strategies, highlighting the importance of plant-mediated processes in regulating belowground responses to atmospheric change. IMPORTANCE Elevated tropospheric O 3 is an increasing threat to crop production, but its effects on belowground microbial processes remain poorly understood. This study demonstrates that O 3 -induced root-associated microbiome changes are closely linked with altered plant carbon allocation and rhizosphere environmental conditions rather than O 3 exposure also. By integrating plant traits, soil properties, extracellular enzyme allocation, and microbial community analyses, we reveal a compartment-specific plant-soil-microbiome response to elevated O 3 . These findings improve our understanding of how atmospheric pollution may reshape crop-associated microbial functions and soil ecological processes under future climate change.

Applied and Environmental Microbiology
Nanjing University of Information Science and Technology (CN)
Plant responses to elevated CO2
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