Dimethylarsinic acid induces rice straighthead disease by causing genotoxicity and abnormal floral development

Background and aims: Microbial arsenic (As) methylation in paddy soil produces dimethylarsinic acid (DMA) as the main product, which can cause rice (Oryza sativa L.) straighthead disease characterized by floret sterility. The mode of DMA toxicity remains unclear. Methods: Pot and hydroponic experiments were conducted to investigate the effect of DMA and Silicon (Si) additions on floral development, genotoxicity and transcriptomic changes in rice reproductive organs. Results: DMA preferentially accumulated in rice spikelets and induced floral abnormality. Male fertility was reduced with lower pollen viability due to abnormal degeneration of tapetum under DMA stress. DMA also caused embryo sac defects including degenerated embryo sacs, unusual double ovules, and ovule-free ovaries, which impeded fertilization and reduced seed-setting. Terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling (TUNEL) and Comet assays showed that DMA accumulation led to DNA damage in the tapetum cells and embryo sacs. Expression of genes related to tapetum development, cell wall formation, and starch synthesis in anthers were frequently affected by DMA. Transcription of genes involved in carbohydrate metabolism in husks and ovaries were altered by DMA stress. Genes related to the DNA damage response and repair were also responsive to DMA stress. Si alleviated DMA toxicity by suppressing DMA accumulation in reproductive tissues. Conclusions: DMA induces genotoxicity in rice reproductive tissue and causes male and female sterility. DMA alters expression of genes associated with tapetum development, carbohydrate metabolism and DNA damage response. The strong genotoxic effect of DMA can be alleviated by supply of Si to rice plants.