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

Authors: Tisdale, Ripley; ZOBEL, RICHARD - North Carolina State University; Burkey, Kent

Submitted to: Science of the Total Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/28/2020
Publication Date: 12/24/2020
Citation: Tisdale, R.H., Zobel, R.W., Burkey, K.O. 2020. Tropospheric ozone rapidly decreases root growth by altering carbon metabolism and detoxification capability in growing soybean roots. Science of the Total Environment. https://doi.org/10.1016/j.scitotenv.2020.144292.
DOI: https://doi.org/10.1016/j.scitotenv.2020.144292

Interpretive Summary: Ozone pollution is a major environmental threat to the US economy and its food security. Reductions in crop yields attributed to ozone have been steadily increasing. One such major US staple crop under threat is soybean. To confront this environmental challenge and optimize crop yield, and thus maintain food sources for a growing US and 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 tissue rather than on the major tissues that directly absorb vital nutrients from the soil: roots. Roots interact with microorganisms living in the soil to aid crops in their survival against environmental threats and stresses. In this study, USDA-ARS scientists in Raleigh, North Carolina and their collaborators at North Carolina State University compared the root structure and protein profiles of ozone-tolerant and ozone-sensitive soybean breeds grown under elevated ozone conditions. Our results produced robust evidence that ozone rapidly decreases root biomass and diameter by altering carbon metabolism and detoxification capability of roots developing during elevated ozone. This finding provides insightful agronomic measures to assess root traits and develop stress-tolerant and high-yield soybean.

Technical Abstract: 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, not roots, to plant fitness and final yield. 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 treated with charcoal-filtered (CF) air or elevated O3 (80 ppbv 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 high abundance of enzymes associated with redox status and detoxification capability contributes to overall O3 tolerance in roots. With O3 decreasing carbon resources by damaging photosynthesis in leaves, O3 rapidly and robustly reduces root growth by altering carbon source-sink balance between above- and below-ground tissues.