Temperature Sensitivity in a Potassium Channel from Land Plants

Abstract

The perception of temperature is a crucial sensory mechanism of living organisms and affects cellular and metabolic processes as well as behavior. In animals, changes in environmental temperature are detected by sensory neurons that express temperature sensitive ion channels. Among these, the family of transient receptor potential (TRP) channels plays a major role. In land plants no homologues for TRP channels are found and temperature sensitive ion channels have yet to be uncovered. KAT1 is a hyperpolarization activated potassium channel from Arabidopsis thaliana that regulates stomatal opening. This channel has voltage sensing domain (VSD) and pore domain (PD) similar to depolarization activated potassium channels. KAT1 was expressed in Xenopus laevis oocytes and the cut open voltage clamp technique was used to record the hyperpolarization induced currents. Rapid changes in temperature where achieved as described in the abstract “Probing Ion Channel Thermodynamics With Temperature Jumps In Oocytes”. Dramatic changes in the kinetics of activation and deactivation where observed. Applying a temperature jump before a hyperpolarizing voltage greatly speeds up channel activation with a significant reduction in the delay of the current onset. Changing the bath temperature greatly affects the kinetics of the channel but does not affect the relative conductance versus voltage relation indicating that the voltage dependent transitions are not involved in temperature sensitivity. The activation rate can be well described by two exponentials, each one with a Q10 of about 4. These results indicate that temperature activates KAT1 channels most likely by increasing the open probability trough changes in the coupling between the VSD and PD. The proposed mechanism is different from the allosteric regulation proposed for the TRP family channels. These results provide clues into the evolution of temperature sensitivity in plants. (Support: NIH GM030376)