Calcium sensor kinase activates potassium uptake systems in gland cells of Venus flytraps

The Darwin plant Dionaea muscipula is able to grow on mineral-poor soil, because it gains essential nutrients from captured animal prey. Given that no nutrients remain in the trap when it opens after the consumption of an animal meal, we here asked the question of how Dionaea sequesters prey-derived potassium. We show that prey capture triggers expression of a K⁺ uptake system in the Venus flytrap. In search of K⁺ transporters endowed with adequate properties for this role, we screened a Dionaea expressed sequence tag (EST) database and identified DmKT1 and DmHAK5 as candidates. On insect and touch hormone stimulation, the number of transcripts of these transporters increased in flytraps. After cRNA injection of K⁺-transporter genes into Xenopus oocytes, however, both putative K⁺ transporters remained silent. Assuming that calcium sensor kinases are regulating Arabidopsis K⁺ transporter 1 (AKT1), we coexpressed the putative K⁺ transporters with a large set of kinases and identified the CBL9-CIPK23 pair as the major activating complex for both transporters in Dionaea K⁺ uptake. DmKT1 was found to be a K⁺-selective channel of voltage-dependent high capacity and low affinity, whereas DmHAK5 was identified as the first, to our knowledge, proton-driven, high-affinity potassium transporter with weak selectivity. When the Venus flytrap is processing its prey, the gland cell membrane potential is maintained around −120 mV, and the apoplast is acidified to pH 3. These conditions in the green stomach formed by the closed flytrap allow DmKT1 and DmHAK5 to acquire prey-derived K⁺, reducing its concentration from millimolar levels down to trace levels.