Defective Mitochondrial Function by Mutation in THICK ALEURONE 1 Encoding a Mitochondrion-Targeted Single-Stranded DNA Binding Protein Leads to Increased Aleurone Cell Layers and Improved Nutrition in Rice.

ABSTRACT Cereal endosperm comprises an outer aleurone and an inner starchy endosperm. Although these two tissues have the same developmental origin, they differ in morphology, cell fate, and storage product accumulation, with the mechanism largely unknown. Here, we report the identification of the thick aleurone 1 (ta1) mutant that showed increased number of aleurone cell layers, and increased contents of nutritional factors including proteins, lipids, vitamins, dietary fibers and micronutrients in rice. The TA1 gene, expressed in embryo, aleurone and subaleurone in caryopses, encodes a mitochondrion-targeted OsmtSSB1 with single-stranded DNA binding activity. Cytological analyses revealed that the increased aleurone cell layers in ta1 were originated from a developmental switch of subaleurone towards aleurone, instead of towards starchy endosperm in the wild type. OsmtSSB1 interacted with mitochondrial DNA recombinase RECA3 and DNA helicase TWINKLE, and down-regulations of RECA3 or TWINKLE also led to ta1-like phenotypes. We further showed that the mutation in OsmtSSB1 caused elevated illegitimate recombinations in the mitochondrial genome, altered mitochondrial morphology and compromised energy supply, suggesting that the OsmtSSB1-mediated mitochondrial function plays a critical role in subaleurone cell fate determination in rice.