ARSENATE INDUCED CHLOROSIS 1/TRANSLOCON AT THE OUTER ENVOLOPE MEMBRANE OF CHLOROPLASTS 132 Protects Chloroplasts from Arsenic Toxicity

Arsenic (As) is highly toxic to plants and detoxified primarily through complexation with phytochelatins (PCs) and other thiol compounds. To understand the mechanisms of As toxicity and detoxification beyond PCs, we isolated an arsenate-sensitive mutant of Arabidopsis (Arabidopsis thaliana), arsenate induced chlorosis1 (aic1), in the background of the PC synthase-defective mutant cadmium-sensitive1-3 (cad1-3). Under arsenate stress, aid cad1-3 showed larger decreases in chlorophyll content and the number and size of chloroplasts than cad1-3 and a severely distorted chloroplast structure. The aid single mutant also was more sensitive to arsenate than the wild type (Columbia-0). As concentrations in the roots, shoots, and chloroplasts were similar between aic1 cad1-3 and cad1-3. Using genome resequencing and complementation, TRANSLOCON AT THE OUTER ENVOLOPE MEMBRANE OF CHLOROPLAST132 (TOC132) was identified as the mutant gene, which encodes a translocon protein involved in the import of preproteins from the cytoplasm into the chloroplasts. Proteomic analysis showed that the proteome of aic1 cad1-3 chloroplasts was more affected by arsenate stress than that of cad1-3. A number of proteins related to chloroplast ribosomes, photosynthesis, compound synthesis, and thioredoxin systems were less abundant in aid cad1-3 than in cad1-3 under arsenate stress. Our results indicate that chloroplasts are a sensitive target of As toxicity and that AlC1/Toc132 plays an important role in protecting chloroplasts from As toxicity.