Ozone (O₃) in the troposphere negatively impacts crop growth and development, causing significant decreases in crop yield worldwide. This airborne pollutant does not come directly from smokestacks or vehicles, but instead is formed when other pollutants, mainly nitrogen oxides and volatile organic compounds, react in the presence of sunlight. In an increasingly polluted atmosphere, understanding what plants are tolerant of O₃ is critical to improving crop productivity and resilience.

In a collaboration between the Feedstock Production and Sustainability themes at the Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), researchers have studied the effects of elevated O₃ on five C₃ crops (chickpea, rice, snap bean, soybean, wheat) and four C₄ crops (sorghum, maize, Miscanthus × giganteus, switchgrass). Their findings, published in Proceedings of the National Academy of Sciences (PNAS), indicate that C₄ crops are much more tolerant of high O₃ concentrations than C₃ crops.

“Understanding the tolerance of C₄ bioenergy crops to air pollutants will help us deploy them strategically across landscapes around the world,” said Lisa Ainsworth (GEGC), Research Leader of the U.S. Department of Agriculture Agricultural Research Service’s (USDA-ARS) Global Change and Photosynthesis Research Unit and Adjunct Professor of Plant Biology at the University of Illinois.

Both C₃ and C₄ crops are major sources of food, bioenergy, and ethanol production worldwide. The difference between C₃ and C₄ plants lies in the carbon-fixation pathway they use during photosynthesis: C₃ plants convert CO₂ and sunlight into a 3-carbon molecule, whereas the first photosynthesis product of C₄ plants is a 4-carbon molecule. Additionally, the C₄ photosynthesis pathway starts in mesophyll cells that comprise the surface of the leaf, and then moves into bundle sheath cells that are deeper in the plant. This spatial separation is not present in the C₃ photosynthesis pathway. Scientists have historically assumed that C₄ plants are less sensitive to O₃ pollution than C₃ plants, but that assumption had not been thoroughly researched until this study.

“Variation in size and growing season length means that it is difficult to do side-by-side comparisons of the response of C₃ and C₄ crops to ozone in the field” said Shuai Li, primary author on the paper and a postdoc in CABBI. “This limits accurate comparisons of the O₃ sensitivity of C₃ and C₄ crops.”

By synthesizing available literature and unpublished data from crops grown with increased O₃ pollution in open-air field experiments over the past 20 years, authors performed a comprehensive analysis of the impact of O₃ on crop physiology and production in five C₃ crops and four C₄ crops.

“We focused on field experiments and quantified crop responses to a specific increase in O₃ pollution. This new method quantitatively showed that C₃ crops are more sensitive to elevated ozone than C₄ crops,” Li said.

The reasoning behind such a conclusion could to do with the differences in leaf anatomical features, stomatal conductance, and/or metabolic rates between the C₃ and C₄ crops. In C₃ plants, reactive oxygen species from O₃ degradation can damage the mesophyll cells where photosynthesis occurs. In C₄ plants, however, the spatial separation of the C₄ photosynthesis pathway helps prevent O₃ from infiltrating the bundle sheath cells where sugars are made. In addition, C₄ crops generally have lower stomatal conductance than C₃ crops, potentially resulting in less O₃ uptake in C₄ crops. These factors likely account for C₄ plants’ superior tolerance of O₃.

“This study enhances our understanding of the mechanisms of crops response to elevated O₃ and highlights practical relevance for crop management and O₃ tolerance improvement.” Li said.

Ozone pollution is increasing in many parts of the world. This study quantitatively showed that O₃-induced reductions in plant function and productivity are more severe in C₃ crops than in C₄ crops, likely because O₃ interacts differently with the C₃ and C₄ photosynthesis pathways. Based on this finding, agricultural lands in polluted environments can be managed to have improved overall performance. C₄ crops, particularly bioenergy feedstocks, can maintain productivity in regions with high O₃.

Other co-authors on this paper include Christopher Moller of USDA-ARS; Christopher Montes, USDA-ARS Plant Physiologist; Erik Sacks, Professor of Crop Sciences at Illinois and CABBI’s Feedstock Production Deputy Theme Leader; DoKyoung Lee, Professor of Crop Sciences at Illinois and a CABBI Sustainability researcher; and CABBI Director Andrew Leakey (GEGC), Professor and Head of Plant Biology at the Illinois.