ATP binding cassette proteins ABCG37 and ABCG33 function as potassium-independent cesium uptake carriers in Arabidopsis roots

Abstract

Radiocesium accumulated in the soil by nuclear accidents is a major environmental concern. The transport process of cesium (Cs⁺) is tightly linked to the indispensable plant nutrient potassium (K⁺) as they both belong to the group I alkali metals with similar chemical properties. Most of the transporters that had been characterized to date as Cs⁺ transporters are directly or indirectly linked to K⁺. Using a combinatorial approach of physiology, genetics, cell biology, and root uptake assay, here we identified two ATP-binding cassette (ABC) proteins, ABCG37 and ABCG33, as facilitators of Cs⁺ influx. A gain-of-function mutant of ABCG37 (abcg37-1) showed increased sensitivity to Cs⁺-induced root growth inhibition, while the double knockout mutant of ABCG33 and ABCG37 (abcg33-1abcg37-2) showed resistance, whereas the single loss-of-function mutants of ABCG33 and ABCG37 did not show any alteration in Cs⁺ response. In planta short-term radioactive Cs⁺-uptake assay along with growth and uptake assays in a heterologous system confirmed ABCG33 and ABCG37 as Cs⁺-uptake carriers. Potassium response and content were unaffected in the double-mutant background and yeast cells lacking potassium-uptake carriers transformed with ABCG33 and ABCG37 failed to grow in the absence of K⁺, confirming that Cs⁺ uptake by ABCG33 and ABCG37 is independent of K⁺. Collectively, this work identified two ABC proteins as new Cs⁺-influx carriers that act redundantly and independent of the K⁺-uptake pathway.

Keywords: ABC proteins; Arabidopsis; cesium; root biology; transport; uptake.