Metagenomic and biochemical analyses reveal the potential of silicon to alleviate arsenic toxicity in rice (Oryza sativa L.)

Abstract

Arsenic (As) pollution in agricultural systems poses a serious threat to crop productivity and food safety. Silicon (Si) has been reported to mitigate toxic effects of heavy metals in plants. However, the mechanisms behind Si-mediated alleviation of As toxicity in rice (Oryza sativa L.) remain poorly understood. Here, we performed metagenomic and biochemical analyses to investigate the potential of Si in alleviating As toxicity to rice plants. As exposure reduced plant growth, chlorophyll contents, antioxidant enzyme levels and soil enzymes activity, while increasing reactive oxygen species (ROS) activity and inducing alterations in the rhizosphere microbiome of rice seedlings. Silicon amendments enhanced rice growth (24%), chlorophyll a (25%), and chlorophyll b (26.7%), indicating enhanced photosynthetic capacity. Si amendments also led to the upregulation of antioxidant enzymes viz., superoxide dismutase (15.4%), and peroxidase (15.6%), resulting in reduced ROS activity and oxidative stress compared to the As-treated control. Furthermore, Si treatment reduced uptake and translocation of As in rice plants, as evidenced by the analysis of elemental contents. Microscopic examination of leaf and root ultrastructure showed that Si mitigated As-induced cellular damage and maintained normal morphology. Metagenomic analysis of the rice rhizosphere microbiome revealed that Si application modulated composition and diversity of microbial communities e.g., Proteobacteria, Actinobacteria, and Firmicutes. Additionally, Si amendments upregulated the relative expression levels of OsGSH, OsPCs, OsNIP1;1 and OsNIP3;3 genes, while the expression levels of the OsLis1 and OsLis2 genes were significantly downregulated compared with As-treated rice plants. Overall, these findings contribute to our understanding of Si-mediated plant resilience to As stress and offer potential strategies for sustainable agriculture in As-contaminated regions.