Long-term tropospheric ozone pollution disrupts plant-microbe-soil interactions in the agroecosystem.

Tropospheric ozone (O3 ) threatens agroecosystems, yet its long-term effects on intricate plant-microbe-soil interactions remain overlooked. This study employed two soybean genotypes of contrasting O3 -sensitivity grown in field plots exposed elevated O3 (eO3 ) and evaluated cause-effect relationships with their associated soil microbiomes and soil quality. Results revealed long-term eO3 effects on belowground soil microbiomes and soil health surpass damage visible on plants. Elevated O3 significantly disrupted belowground bacteria-fungi interactions, reduced fungal diversity, and altered fungal community assembly by impacting soybean physiological properties. Particularly, eO3 impacts on plant performance were significantly associated with arbuscular mycorrhizal fungi, undermining their contribution to plants, whereas eO3 increased fungal saprotroph proliferation, accelerating soil organic matter decomposition and soil carbon pool depletion. Free-living diazotrophs exhibited remarkable acclimation under eO3 , improving plant performance by enhancing nitrogen fixation. However, overarching detrimental consequences of eO3 negated this benefit. Overall, this study demonstrated long-term eO3 profoundly governed negative impacts on plant-soil-microbiota interactions, pointing to a potential crisis for agroecosystems. These findings highlight urgent needs to develop adaptive strategies to navigate future eO3 scenarios.

Microbial community dynamics responding to nutrient allocation associated with soybean cultivar 'Jake' ozone adaptation.

Tropospheric ozone (O3), a major air pollutant, leads to significant global yield loss in soybean [Glycine max (L.) Merr.]. Soybean cultivar 'Jake' shows O3 resilient traits in above-ground organs, but the root system remains sensitive to elevated O3 (eO3). Changing carbon (C) and nitrogen (N) resource composition during eO3 stress suggests that eO3 presumably alters belowground soil microbial communities and their driven nutrient transformation. Yet, the responses of belowground microbes to eO3 and their feedback on nutrient cycling in 'Jake' are unknown. In this study, we holistically investigated soil microbial communities associated with C and N dynamics and bacterial-fungal inter-kingdom networks in the rhizosphere and bulk soil at different developmental stages of 'Jake' grown under sub-ambient O3 [charcoal-filtered (CF) air, 12 h mean: 20 ppb] or eO3 (12 h mean: 87 ppb). The results demonstrated eO3 significantly decreased fungal diversity and complexity of microbial networks at different 'Jake' developmental stages, whereas bacterial diversity was more tolerant to eO3 in both bulk soil and rhizosphere. In the bulk soil, no O3-responsive microbial biomarkers were found to be associated with C and N content, implying eO3 may stimulate niche-based processes during 'Jake' growth. In contrast, this study identified O3-responsive microbial biomarkers that may contribute to the N acquisition (Chloroflexales) and C dynamics (Caldilineales, Thermomicrobiales, and Hypocreales) in the rhizosphere, which may support the O3 resilience of the 'Jake' cultivar. However, further investigation is required to confirm their specific contributions by determining changes in microbial gene expression. Overall, these findings conduce to an expanding knowledge base that O3 induces temporal and spatial changes in the effects of microbial and nutrient networks in the O3-tolerant agriculture ecosystems.

Impact of elevated ozone on yield and carbon-nitrogen content in soybean cultivar 'Jake'.

Tropospheric ozone (O3) is a pollutant that leads to significant global yield loss in soybean [Glycine max (L.) Merr.]. To ensure soybean productivity in areas of rising O3, it is important to identify tolerant genotypes. This work describes the response of the high-yielding soybean cultivar 'Jake' to elevated O3 concentrations. 'Jake' was treated with either low O3 [charcoal-filtered (CF) air, 12 h mean: 20 ppb] or with O3-enriched air (12 h mean: 87 ppb) over the course of the entire growing season. In contrast to the absence of O3-induced leaf injury under low O3, elevated O3 caused severe leaf injury and decreased stomatal conductance and photosynthesis. Although elevated O3 reduced total leaf area, leaf number, and plant height at different developmental stages, above-ground and root biomass remained unchanged. Analyzing carbon and nitrogen content, we found that elevated O3 altered allocation of both elements, which ultimately led to a 15 % yield loss by decreasing seed size but not seed number. We concluded that cultivar 'Jake' possesses developmental strength to tolerate chronic O3 conditions, attributes that make it suitable breeding material for the generation of new O3 tolerant lines.

Tropospheric ozone rapidly decreases root growth by altering carbon metabolism and detoxification capability in growing soybean roots.

High tropospheric ozone (O3) concentrations lead to significant global soybean (Glycine max) yield reductions. Research concerning O3 impacts on soybean has focused on the contributions of above-ground tissues. In this study, Mandarin (Ottawa) (O3-sensitive) and Fiskeby III (O3-tolerant) soybean genotypes provide contrasting materials to investigate O3 effects on root growth. We compared root morphological and proteomic changes when 16-day-old plants were treated with charcoal-filtered (CF) air or elevated O3 (80 ppb O3 for 7 h/day) in continuously stirred-tank reactors (CSTR) for 7 days. Our results showed that in Mandarin (Ottawa), decreased expression of enzymes involved in the tricarboxylic acid (TCA) cycle contributes to reduction of root biomass and diameter under elevated O3. In contrast, O3 tolerance in Fiskeby III roots was associated with O3-dependent induction of enzymes involved in glycolysis and O3-independent expression of enzymes involved in the ascorbate-glutathione cycle. We conclude that a decreased abundance of key redox enzymes in roots due to limited carbon availability rapidly alters root growth under O3 stress. However, maintaining a high abundance of enzymes associated with redox status and detoxification capability contributes to overall O3 tolerance in roots.