DYSCALCULIA, a Venus flytrap mutant without the ability to count action potentials

Abstract

The Venus flytrap Dionaea muscipula estimates prey nutrient content by counting trigger hair contacts initiating action potentials (APs) and calcium waves traveling all over the trap.^1,2,3 A first AP is associated with a subcritical rise in cytosolic calcium concentration, but when the second AP arrives in time, calcium levels pass the threshold required for fast trap closure. Consequently, memory function and decision-making are timed via a calcium clock.^3,4 For higher numbers of APs elicited by the struggling prey, the Ca²⁺ clock connects to the networks governed by the touch hormone jasmonic acid (JA), which initiates slow, hermetic trap sealing and mining of the animal food stock.⁵ Two distinct phases of trap closure can be distinguished within Dionaea's hunting cycle: (1) very fast trap snapping requiring two APs and crossing of a critical cytosolic Ca²⁺ level and (2) JA-dependent slow trap sealing and prey processing induced by more than five APs. The Dionaea mutant DYSC is still able to fire touch-induced APs but does not snap close its traps and fails to enter the hunting cycle after prolonged mechanostimulation. Transcriptomic analyses revealed that upon trigger hair touch/AP stimulation, activation of calcium signaling is largely suppressed in DYSC traps. The observation that external JA application restored hunting cycle progression together with the DYSC phenotype and its transcriptional landscape indicates that DYSC cannot properly read, count, and decode touch/AP-induced calcium signals that are key in prey capture and processing.

Keywords: Dionaea cultivars; Dionaea muscipula; Venus flytrap; action potential; calcium signaling; carnivorous plants; counting in plants; plant mechanosensation; trap closure.