Alternative pathway to photorespiration protects growth and productivity at elevated temperatures in a model crop

Authors: CAVANAGH, AMANDA - University Of Illinois; SOUTH, PAUL - University Of Illinois; Bernacchi, Carl; ORT, DONALD - University Of Illinois

Submitted to: Plant Biotechnology Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/12/2021
Publication Date: 4/1/2022
Citation: Cavanagh, A.P., South, P.F., Bernacchi, C.J., Ort, D.R. 2022. Alternative pathway to photorespiration protects growth and productivity at elevated temperatures in a model crop. Plant Biotechnology Journal. 20(4):711-721. https://doi.org/10.1111/pbi.13750.
DOI: https://doi.org/10.1111/pbi.13750

Interpretive Summary: Crops are very sensitive to the extreme temperatures that are certainly going to become more common with the current global change trajectory. Efforts to stop global warming are lagging, which requires significant effort to adapt crops to extreme conditions to secure future global food supplies. This research uses a genetically modified model crop species, tobacco, that has altered photosynthesis pathways that are predicted to improve resilience in high temperature. The modification bypasses a natural pathway dealing with toxins that form in leaves at high temperatures. The new pathway uses less energy to remove the toxins and is predicted to confer resilience to higher temperatures. These plants were grown in an agricultural field using standard agronomic practices but with infrared heating arrays causing the plants to grow in hotter conditions. The control plants had decreases in growth and yield in hot growth environments, but the plants with the altered pathway had higher photosynthesis and higher biomass than the control plants. These results suggest that improving photosynthesis can potentially benefit crop resilience to global warming and lead to improved food security.

Technical Abstract: Adapting crops to warmer growing season temperatures is a major challenge in mitigating the impacts of climate change on crop production. Warming temperatures drive greater evaporative demand and can directly interfere with both reproductive and vegetative physiological processes. Most of the world’s crop species have C3 photosynthetic metabolism for which increasing temperature means higher rates of photorespiration, wherein the enzyme responsible for fixing CO2 fixes O2 instead followed by an energetically costly recycling pathway that spans several cell compartments. In C3 crops like wheat, rice and soybean, photorespiration translates into large yield losses that are predicted to increase as global temperature warms. Engineering less energy-intensive alternative photorespiratory pathways into crop chloroplasts drives increases in C3 biomass production under agricultural field conditions, but the efficacy of these pathways in mitigating the impact of warmer growing temperatures has not been tested. We grew tobacco plants expressing an alternative photorespiratory pathway under current and elevated temperatures (+5°C) in agricultural field conditions. Engineered plants exhibited higher photosynthetic quantum efficiency under heated conditions than the control plants, and produced 26% (between 16-37%) more total biomass than WT plants under heated conditions, compared to 11% (between 5-17%) under ambient conditions. That is, engineered plants sustained 15% (between 11 – 21%) less yield loss under heated conditions compared to non-engineered plants. These results support the theoretical predictions of temperature impacts on photorespiratory losses and provide insight toward the optimization strategies required to help sustain or improve C3 crop yields in a warming climate.