Elevated CO2 alters soybean physiology and defense responses, and has disparate effects on susceptibility to diverse microbial pathogens

Authors: BREDOW, MELISSA - Iowa State University; KHWANBUA, EKKACHAI - Iowa State University; CHICOWSKI, ALINE SARTOR - Iowa State University; QI, YUNHUI - Iowa State University; BREITZMAN, MATTHEW - Iowa State University; Holan, Katerina; LIU, PENG - Iowa State University; Graham, Michelle; WHITHAM, STEVEN - Iowa State University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/3/2024
Publication Date: 1/9/2025
Citation: Bredow, M., Khwanbua, E., Chicowski, A., Qi, Y., Breitzman, M., Holan, K.L., Liu, P., Graham, M.A., Whitham, S.A. 2025. Elevated CO2 alters soybean physiology and defense responses, and has disparate effects on susceptibility to diverse microbial pathogens. New Phytologist. https://doi.org/10.1111/nph.20364.
DOI: https://doi.org/10.1111/nph.20364

Interpretive Summary: Atmospheric carbon dioxide (CO2) levels are rising at an unprecedented rate and are expected to have tangible effects on crop productivity and health. Increases in atmospheric CO2 levels have been associated with higher photosynthesis rates in some plants however, accumulating evidence suggests that plant nutrient content and resistance to abiotic or biotic stresses may also be affected. In this study, we investigated the effects of elevated CO2 on plant physiology and immunity in soybean. Plants were grown at current or future predicted atmospheric CO2 concentrations and challenged with diverse foliar and soil-borne pathogens. Elevated CO2 enhanced resistance to P. syringae species. Whole genome expression analyses indicated global shifts in soybean gene expression when grown under elevated CO2, particularly in response to P. syringae treatment. Soybean susceptibility to bean pod mottle virus (BPMV) and soybean mosaic virus (SMV) was also affected, with plants grown at elevated CO2 displaying lower resistance to both viruses. Plants infected Fusarium virguliforme were more susceptible at elevated CO2, although the underlying molecular mechanisms are unknown. No difference was observed in Pythium sylvaticum infection between the two CO2 concentrations. This work provides a foundation for our understanding of how changes in atmospheric CO2 levels could impact molecular responses to pathogen challenge in soybean.

Technical Abstract: Atmospheric carbon dioxide (CO2) levels are rising at an unprecedented rate and are expected to have tangible effects on crop productivity and health. Increases in atmospheric CO2 levels have been associated with higher photosynthesis rates in some plants however, accumulating evidence suggests that plant nutrient content and resistance to abiotic or biotic stresses may also be affected. In this study, we investigated the effects of elevated CO2 on plant physiology and immunity using the oilseed crop soybean (Glycine max). Plants were grown at current (419 ppm) or future predicted (550 ppm) atmospheric CO2 concentrations and challenged with diverse foliar and soil-borne pathogens. Elevated CO2 enhanced Pseudomonas syringae -triggered upregulation of the salicylic acid-marker gene Pathogenesis-Related Protein 1 (PR1) as well as flg22-induced oxidative species production and MAPK activation, corresponding to higher resistance to P. syringae species. RNA sequencing (RNA-seq) analysis indicated global shifts in soybean gene expression when grown under elevated CO2, particularly in response to P. syringae treatment. Soybean susceptibility to bean pod mottle virus (BPMV) and soybean mosaic virus (SMV) was also affected, with plants grown at elevated CO2 displaying lower resistance to both viruses, as well as lower PR1 expression and expression of the RNA silencing gene Agronaute 1. No difference was observed in Pythium sylvaticum infection between the two CO2 concentrations, while plants infected Fusarium virguliforme were more susceptible at elevated CO2, although the underlying molecular mechanisms are unknown. This work provides a foundation for our understanding of how changes in atmospheric CO2 levels could impact molecular responses to pathogen challenge in soybean and points to agents of potential concern in future climatic conditions.