Glucose-G protein signaling plays a crucial role in tomato resilience to high temperature and elevated CO2.

Global climate change is accompanied by carbon dioxide (CO2) enrichment and high-temperature stress; however, how plants adapt to the combined environments and the underlying mechanisms remain largely unclear. Here, we show that elevated CO2 alleviated plant sensitivity to high-temperature stress, with significantly increased apoplastic glucose (Glc) levels in tomato (Solanum lycopersicum) leaves. Exogenous Glc treatment enhanced tomato resilience to high-temperature stress under ambient CO2 conditions. Cell-based biolayer interferometry, subcellular localization, and Split-Luc assays revealed that Glc bound to tomato regulator of G protein signaling 1 (RGS1) and induced RGS1 endocytosis and thereby RGS1-G protein α subunit (GPA1) dissociation in a concentration-dependent manner. Using rgs1 and gpa1 mutants, we found that RGS1 negatively regulated thermotolerance and was required for elevated CO2-Glc-induced thermotolerance. GPA1 positively regulated the elevated CO2-Glc-induced thermotolerance. Transcriptome and chlorophyll fluorescence parameter analysis further revealed that GPA1 integrated photosynthesis- and photoprotection-related mechanisms to regulate thermotolerance. These results demonstrate that Glc-RGS1-GPA1 signaling plays a crucial role in the elevated CO2-induced thermotolerance in tomato. This information enhances our understanding of the Glc-G protein signaling function in stress resilience in response to global climate change and will be helpful for genetic engineering approaches to improve plant resilience.