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, 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By synthesizing available literature and unpublished data from crops grown with increased O3 pollution in open-air field experiments over the past 20 years, authors performed a comprehensive analysis of the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 the Carl R. Woese Institute for Genomic Biology (IGB) at Illinois and 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, Professor and Head of Plant Biology at the Illinois.

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