Understanding the role of ethylene-mediated metabolic priming in plant stress resilience

Ethylene, a key phytohormone, regulates vital plant processes, including germination, fruit ripening, senescence, organ abscission, and stress tolerance, influencing agricultural productivity. Our research in the Binder Lab uncovered that ethylene pre-treatment of germinating seeds in the dark primes them for enhanced growth and stress tolerance in later developmental stages. Ethylene-treated plants develop longer roots, larger leaves, and greater shoot mass due to increased photosynthesis, carbon assimilation, and sugar metabolism. Metabolomic and transcriptomic analyses show the upregulation of genes related to photosynthesis, sugar metabolism, and cellular development. While plants typically balance resource allocation between growth and defense, ethylene-mediated metabolic priming likely generates surplus sugars derived from photosynthesis and carbon assimilation, promoting both faster growth and stress resilience. Stress induces reactive oxygen species (ROS) accumulation, leading to leaf damage, stunted growth, and even death. Ethylene-primed plants show lower ROS buildup and higher sugar content, which correlates to a higher percentage of survival after being exposed to extreme temperature changes, low oxygen, the presence of salt, copper, and flagellin peptide. In contrast, unprimed plants show higher ROS accumulation and lower sugar content, which leads to a drastically lower percentage of survival. CINV1 and CINV2, cytosolic invertases, are important for this priming effect; knocking them out eliminates the priming effect on both growth and stress tolerance. We also tested gene expression profiles of key sugar metabolism genes and core stress genes responsible for ROS detoxification and scavenging. Interestingly, core stress and sugar metabolism genes were found to be regulated differently depending on the specific stress encountered, with and without priming, indicating a nuanced response to environmental cues that is not just regulated by priming alone. The ability of seedlings to survive stress is crucial for plant survival. Our study illustrates that brief ethylene exposure to germinating seedlings leads to enhanced stress tolerance across various stresses through increased sugar accumulation and decreased levels of reactive oxygen species. Further, we demonstrate that proper breakdown of sucrose and normal carbohydrate metabolism are necessary for ethylene-priming responses.