A single amino acid substitution in the Arabidopsis FIERY1/HOS2 protein confers cold signaling specificity and lithium tolerance

Low temperature induces the expression of many plant genes through undefined signaling pathways. To gain insight into cold signal transduction mechanisms, we isolated Arabidopsis mutants that exhibited altered regulation of low temperature-induced gene expression. One such mutant, hos2, was shown previously to have an enhanced induction of stress-responsive genes by cold, whereas the expression of these genes under osmotic stress or the phytohormone absciscic acid (ABA) treatments was not affected. Here we further define the targets of HOS2 by examining the regulation of upstream cold-specific CBF transcription factor genes. It was found that the transcript levels of CBF2 and CBF3 were significantly higher in hos2 mutant plants than in the wild type under cold treatments, suggesting that HOS2 may act upstream of CBFs. The HOS2 gene was cloned using a map-based strategy. Surprisingly, HOS2 is identical to the FIERY1 gene that we had described previously. FIERY1 is a general negative regulator that controls cold, osmotic stress, and ABA signal transduction and possesses inositol polyphosphate 1-phosphatase activity. The hos2 mutation rendered the HOS2/FIERY1 recombinant protein completely inactive in the cold but did not substantially affect its activity at warm temperatures. Interestingly, the hos2 mutant protein is extremely tolerant to Li⁺. This study provides a unique example of a single amino acid substitution in a critical regulator that can lead to conditional changes in protein functions and distinct plant phenotypes. The results reinforce the notion that phosphoinositols are important second messengers in cold signal transduction, and shed light on how the diversity of plant tolerance to cold and other abiotic stresses may evolve due to variations in a common molecular switch.