L-histidine makes Ni²⁺ ‘visible’ for plant signalling systems: Shading the light on Ni²⁺-induced Ca²⁺ and redox signalling in plants

Nickel is both an important nutrient and an ecotoxicant for plants. Organic ligands, such as L-histidine (His), play a key role in Ni²⁺ detoxification. Here, we show that His (added together with 0.01–10 mM Ni²⁺) decreases Ni²⁺ toxicity to Arabidopsis thaliana roots not only as a result of a decrease in Ni²⁺ activity, but also via the induction of signalling phenomena important for adaptation such as the generation of reactive oxygen species (ROS) and cytosolic Ca²⁺ transients. With the use of EPR spectroscopy, we demonstrate that Ni-His complexes generate hydroxyl radicals that is not detected by the addition of Ni²⁺ or His separately. Similarly, Ni-His complexes, but not Ni²⁺, activate Ca²⁺ influx and K⁺ efflux currents in patch-clamped root protoplasts resulting in distinct cytosolic Ca²⁺ signals and a transient K⁺ release. His prevented programmed cell death symptoms (cytoplasm shrinkage, protease and endonuclease activation) induced by Ni²⁺ and inhibited Ni²⁺ accumulation at [Ni²⁺]>0.3 mM. Intriguingly, priming of roots with Ni-His stimulated plant resistance to Ni²⁺. Overall, these data show that His triggers ROS-Ca²⁺-mediated reactions making Ni²⁺ ‘visible’ for plant signalling machinery and facilitating adaptation to the excess Ni²⁺.