Impact of tropospheric ozone on root proteomes of two soybean genotypes with contrasting sensitivity to ozone

Authors: Zentella, Rodolfo; Burkey, Kent; Tisdale, Ripley

Submitted to: Environmental and Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/17/2023
Publication Date: 2/18/2023
Citation: Zentella Gomez, R., Burkey, K.O., Tisdale, R.H. 2023. Impact of tropospheric ozone on root proteomes of two soybean genotypes with contrasting sensitivity to ozone. Environmental and Experimental Botany. 208:105269. https://doi.org/10.1016/j.envexpbot.2023.105269.
DOI: https://doi.org/10.1016/j.envexpbot.2023.105269

Interpretive Summary: Ozone pollution is a serious environmental threat to the US economy and its food security. Reductions in crop yields attributed to ozone have been steadily increasing. Soybean, a major US staple crop, shows export value at $18.7 billion. However, soybean production has come under growing ozone threat and now faces a steep reduction in annual yield of more than 12%. To confront this environmental challenge and optimize crop yield, and thus maintain food sources for a growing global population, breeders and plant researchers are working to develop crops able to withstand environmental stresses. These efforts, however, have generally focused on above-ground tissues rather than on roots, the key tissues absorbing vital nutrients and interacting with soil environments and microorganism communities. In this study, USDA-ARS scientists and breeders in Raleigh, North Carolina have identified two soybean genotypes that show similar characteristics and yield under normal conditions, but only express contrasting phenotypes under elevated ozone conditions. The scientist took advantage of these soybean materials to answer the fundamental questions of how elevated ozone alters root performance through regulating proteomic profiles. The results demonstrate that elevated ozone rapidly decreases root growth and nodulation, which profoundly impairs nutrient acquisition and ultimately decreases seed productivity. By comparing root proteomic profiles from the contrasting genotypes, this research produced robust evidence that ozone alters metabolic pathways, including carbon metabolism, amino acid biosynthesis, and detoxification capability, which can impair root development and functions. This finding provides insightful agronomic measures to assess root traits and develop stress-tolerant, high-yield soybean.

Technical Abstract: Tropospheric ozone (O3), a critically harmful greenhouse gas, has steadily increased in over the last several decades, leading to significant soybean (Glycine max) yield loses worldwide. However, significant efforts have focused on the effect of elevated O3 on above-ground tissues rather than on roots, which support plant fitness and directly interact with soil ecosystems. To better assess the impact of elevated O3 on roots, this study investigated morphological and proteomic profiles of two soybean genotypes from the same genetic background but which possess contrasting O3 resilience¬¬: Fiskeby III (O3-tolerant) and Fiskeby 840-7-3 (O3-senstive). Plants were treated either with sub-ambient O3 (Charcoal-filtered air, 12 mean: 25 ppb) or elevated O3 (12 mean: 85 ppb) in a field-based air exhaustion system and harvested in flowering and pod-filling stages. Our results demonstrated that the effect of elevated O3 on decreasing root biomass was initiated in the flowering stage, while above-ground biomass was not altered. Also, O3-associated biomass reduction was more pronounced in both above-ground tissues and roots in the pod-filling stage. Season-long elevated O3 stress ultimately caused a 29% seed yield reduction in Fiskeby III, and 50% loss in Fiskeby 840-7-3. Root proteome analysis showed that the effect of O3 in roots was complex, including changes in protein expression corresponding to antioxidant pathways, nitrogen metabolism, TCA cycle, secondary metabolites and stress response pathways. Some of these changes may be in response to elevated O3 as an attempt by plants to mitigate the effects of a challenging environment, and others are likely genetic differences that confer an advantage to the O3 tolerant genotype. This finding provides further knowledge on O3-tolerent proteins, which could be applied to develop stress-resilient and high-yield soybean.