CAX1 suppresses Cd‐induced generation of reactive oxygen species in Arabidopsis halleri

• Published in: Plant, cell and environment Vol. 41; no. 10; pp. 2435 - 2448
• Main Authors: Ahmadi, Hassan, Corso, Massimiliano, Weber, Michael, Verbruggen, Nathalie, Clemens, Stephan
• Format: Journal Article
• Language: English
• Published: United States Wiley Subscription Services, Inc 01.10.2018; Wiley
• Subjects: Accumulation; Antiporters - metabolism; Antiporters - physiology; Arabidopsis; Arabidopsis - drug effects; Arabidopsis - metabolism; Arabidopsis halleri; Arabidopsis Proteins - metabolism; Arabidopsis Proteins - physiology; Biochemistry, Molecular Biology; Biodiversity; Biological evolution; Cadmium; Cadmium - pharmacology; Calcium; Calcium - metabolism; Calcium ions; Cation Transport Proteins - metabolism; Cation Transport Proteins - physiology; Dependence; extremophiles; Feedback loops; Gene Expression Profiling; Genetic analysis; Genetic transformation; Genomics; Genotypes; Homeostasis; Life Sciences; metal hyperaccumulation; metal hypertolerance; Metals; Molecular Networks; oxidative stress; Phenotypes; Plant breeding; Plants (botany); Plants, Genetically Modified; Positive feedback; Quantitative trait loci; Reactive oxygen species; Reactive Oxygen Species - metabolism; Vegetal Biology; cadmium; Arabidopsis halleri; metal hyperaccumulation; metal hypertolerance; extremophiles; oxidative stress
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.13362

The molecular analysis of metal hyperaccumulation in species such as Arabidopsis halleri offers the chance to gain insights into metal homeostasis and into the evolution of adaptation to extreme habitats. A prerequisite of metal hyperaccumulation is metal hypertolerance. Genetic analysis of a backcross population derived from Arabidopsis lyrata × A. halleri crosses revealed three quantitative trait loci for Cd hypertolerance. A candidate gene for Cdtol2 is AhCAX1, encoding a vacuolar Ca2+/H+ antiporter. We developed a method for the transformation of vegetatively propagated A. halleri plants and generated AhCAX1‐silenced lines. Upon Cd2+ exposure, several‐fold higher accumulation of reactive oxygen species (ROS) was detectable in roots of AhCAX1‐silenced plants. In accordance with the dependence of Cdtol2 on external Ca2+ concentration, this phenotype was exclusively observed in low Ca2+ conditions. The effects of external Ca2+ on Cd accumulation cannot explain the phenotype as they were not influenced by the genotype. Our data strongly support the hypothesis that higher expression of CAX1 in A. halleri relative to other Arabidopsis species represents a Cd hypertolerance factor. We propose a function of AhCAX1 in preventing a positive feedback loop of Cd‐elicited ROS production triggering further Ca2+‐dependent ROS accumulation. Metal hyperaccumulating species such as Arabidopsis halleri serve as models to gain insights into metal homeostasis and into the evolution of adaptation to extreme habitats. A gene hypothesized to be underlying one of the mapped quantitative trait loci for cadmium hypertolerance encodes the vacuolar Ca2+/H+ exchanger AhCAX1. We show here that partial loss of AhCAX1 function indeed compromises the ability of cadmium‐exposed A. halleri roots to suppress the accumulation of reactive oxygen species.