Alternative splicing of pre-mRNAs can regulate the expression and function of proteins. As such it is a major tool of eukaryotes to adapt their proteome - and thus the whole organism - to external and internal changes of circumstances. In mammals body temperature cycles result in oscillating alternative splicing driven by rhythmic phosphorylation of SR-proteins. Recently, it has been shown that this is facilitated by temperature dependent activity of Cdc2-like kinases (CLKs). Temperature sensitivity is conserved across evolution and the active temperature range of the kinases is adapted to the body temperature or growth temperature of the corresponding organism. While it has been shown that the temperature dependence of CLK activity is mediated by conformational changes in the activation segment, the mechanisms by which the active temperature range of the kinases is adapted to the organisms body temperature remained elusive. Here we show multiple structural features fine-tuning the active temperature range of CLK homologues. We characterized a CLK homologue, CmLIK, and its substrate phosphorylation from the ancient thermophilic red alga C. merolae and could show that kinase activity at high temperatures is mediated by activation segment stabilization via a salt bridge in the P+1 loop. In contrast to other CLK homologues auto phosphorylation of CmLIK shows markedly different patterns than substrate phosphorylation. Furthermore, we identified an H-bond network from a residue in the P+1 loop of a CLK homologue from A. thaliana, AtAFC3, that stabilizes the activation segment and also mediates kinase activity at higher temperatures. We could show that AFCs play a role in heat responsive hypocotyl elongation in A. thaliana upstream of PIF4, the major regulator of thermomorphogenesis. Our results demonstrate stabilization of the P+1 loop of the activation segment as a common mechanism mediating CLK homologue activity at high temperatures. With the characterization of CmLIK we found a model system to study an ancient CLK homologue with activity at high temperatures. Our findings lay the foundation for exploration of genetic engineering of crop plant AFCs to facilitate kinase activity at higher temperatures and adapting their thermomorphogenesis accordingly. This could lead to a partial solution of the problems crop plant growth faces due to global warming.