Natural variation among Arabidopsis accessions reveals malic acid as a key mediator of Nickel (Ni) tolerance

Abstract

Plants have evolved various mechanisms for detoxification that are specific to the plant species as well as the metal ion chemical properties. Malic acid, which is commonly found in plants, participates in a number of physiological processes including metal chelation. Using natural variation among Arabidopsis accessions, we investigated the function of malic acid in Nickel (Ni) tolerance and detoxification. The Ni-induced production of reactive oxygen species was found to be modulated by intracellular malic acid, indicating its crucial role in Ni detoxification. Ni tolerance in Arabidopsis may actively involve malic acid and/or complexes of Ni and malic acid. Investigation of malic acid content in roots among tolerant ecotypes suggested that a complex of Ni and malic acid may be involved in translocation of Ni from roots to leaves. The exudation of malic acid from roots in response to Ni treatment in either susceptible or tolerant plant species was found to be partially dependent on AtALMT1 expression. A lower concentration of Ni (10µM) treatment induced AtALMT1 expression in the Ni-tolerant Arabidopsis ecotypes. We found that the ecotype Santa Clara (S.C.) not only tolerated Ni but also accumulated more Ni in leaves compared to other ecotypes. Thus, the ecotype S.C. can be used as a model system to delineate the biochemical and genetic basis of Ni tolerance, accumulation, and detoxification in plants. The evolution of Ni hyperaccumulators, which are found in serpentine soils, is an interesting corollary to the fact that S.C. is also native to serpentine soils.