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

Authors: ZHANG, KAILE - University Of Florida; Zentella, Rodolfo; Burkey, Kent; LIAO, HUI-LING - University Of Florida; Tisdale, Ripley

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/13/2024
Publication Date: 3/6/2024
Citation: Zhang, K., Zentella Gomez, R., Burkey, K.O., Liao, H., Tisdale, R.H. 2024. Long-term tropospheric ozone pollution disrupts plant-microbe-soil interactions in the agroecosystem. Nature Communications. 30(3). Article e17215. https://doi.org/10.1111/gcb.17215.
DOI: https://doi.org/10.1111/gcb.17215

Interpretive Summary: Ozone pollution is a serious environmental threat to the US economy and its food security. Soybean, a major US staple crop, has an $18.7 billion export value, but ozone jeopardizes its production. Due to this mounting threat, US soybean now faces a steep 18% drop in annual yield. Beyond its direct effects on soybean, ozone severely impacts soil health by its overall effect on plant health. However, while ozone continues to critically damage agricultural ecosystems, it remains largely overlooked. This environmental challenge must be confronted by optimizing food sources for a growing US and global population and through strategic soil health maintenance. Together, breeders, plant researchers, and ecologists are currently developing soybean genetic varieties able to withstand environmental impacts and support robust agricultural ecosystems. The USDA-ARS PSRU scientists in Raleigh, North Carolina have identified two soybean variations with contrasting ozone sensitivity and investigated the cause-and-effect relationships between soybean ozone-resilient traits and soil microbial communities. This has been accomplished through a field-based ozone pollution simulation system under conventional field management practices. Employing soil microbial genomics and machine learning technologies, USDA-ARS scientists pinpointed which symbiotic soil microbes enhance soybean resilience to ozone and which soil microbes deteriorate soil quality under ozone pollution. This study demonstrated that long-term ozone pollution profoundly degraded plant performance and soil health, alerting experts to a potential agroecosystem crisis. These findings highlight the urgent need for adaptive strategies against ozone damage and future food and economic losses.

Technical Abstract: 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.