Uptake of atrazine in a paddy crop activates an epigenetic mechanism for degrading the pesticide in plants and environment

There is a rising public concern on accumulation of harmful pesticides in environment and crops. Epigenetic alteration caused by environmental contaminants is one of the key factors in the etiology of environmentally-associated diseases. Growing evidence shows that harmful pesticide atrazine (ATZ) has a profound effect on DNA methylation in human genome, however, little is known about the epigenetic mechanism underlying ATZ accumulation and degradation in plants, particularly in edible plants growing in the ATZ-contaminated areas. This study investigated the atrazine elimination that was mediated by DNA methylation and histone modification in the food crop rice. Studies with two mutant Osmet1-1/2 defective in the genomic CG DNA methylation show significantly lower accumulation of atrazine than its wild-types. Profiling methylome and transcriptome of ATZ-exposed Osmet1 and wild-type identified many differentially methylated loci (≥2 fold change, p < 0.05), which were associated with activation of genes responsible for atrazine degradation in plants. Three demethylated loci OsGTF, OsHPL1 and OsGLH were expressed in eukaryotic yeast cells and found to eliminate a marked proportion of ATZ in growth environments by 48%, 43% and 32%, respectively, whereas the increased ATZ-degraded products were characterized using UPLC/Q-TOF-MS/MS. These results suggest that activation of the loci mediated by ATZ-induced hypomethylation could be responsible for the removal of ATZ in rice. Our work helps understand a new regulatory mechanism underlying the atrazine degradation in crops which may potentially reduce the environmental risks to human health through food chain.