Cold stress significantly affects plant growth and productivity. Chloroplasts are hotspots of reactive oxygen species (ROS) production and also the cites for the biosynthesis of defense hormone salicylic acid (SA) under environmental stress conditions. However, how plants integrate ROS and SA signals to adapt to stress is poorly understood. Here, we report the Arabidopsis Filamentous temperature-sensitive H5 (FtsH5/VAR1), a thylakoid ATP-dependent zinc metalloprotease, plays an important role in plant cold stress tolerance. The var1-1 mutant displays an albino and retarded growth phenotype under cold stress. We identified a strong correlation of activated SA biosynthesis and signaling with the cold-sensitive phenotype of var1. Reduction of SA accumulation, by overexpressing of salicylate hydroxylase gene (NahG) or knocking out of SA biosynthesis-related genes (ICS1, EDS1, or PAD4), suppressed the albino phenotype of var1. Furthermore, we show that EXECUTOR1 (EX1)-mediated singlet oxygen (1O2) signaling acts upstream of EDS1 to regulate the expression of SA-responsive genes in var1 under cold stress. Importantly, we uncover a moonlighting function of EX2, which the mutation strongly suppresses the cold-sensitive phenotype of var1, in repression the expression of photosynthesis-associated nuclear genes. Together, these results reveal a crucial role of VAR1 in plant cold tolerance and a tight link between 1O2 and SA signaling, corroborating an unheeded function of EX2 in regulating the expression of photosynthesis genes.