MiR408 balances plant growth and heat response in rice

MicroRNAs are small noncoding RNAs that regulate gene expression by targeting complementary mRNA molecules. Among them, microRNA408 (miR408) is an ancient microRNA influencing plant growth and aiding in abiotic stress adaptation. We proved that miR408 sliced uclacyanin7 (UCL7) directly by degradome sequencing. However, the mechanisms underlying the balance between growth and stress response of rice (Oryza sativa L.) controlled by miR408 remain unclear. We conducted a study comparing Nipponbare (wild-type, WT) plants with miR408–3p-overexpression (miR408–3p-OX) and UCL7-overexpression (UCL7-OX) plants under normal and heat stress conditions. Through RNA-sequencing, physiological measurements, and phenotype examination, we observed that miR408 overexpression resulted in increased dry weight and grain yield, higher levels of ATP and non-structural carbohydrates (NSC), improved photosynthesis, and reduced H2O2 content, antioxidant enzyme activity, and ATPase activity in seedling plants compared to UCL7-OX plants. Additionally, the application of H2O2 scavengers, such as ascorbic acid (ASA) and dimethylthiourea (DMTU), further enhanced dry weight and photosynthesis by reducing H2O2 levels. Under heat stress conditions, miR408 overexpression sharply increased H2O2 content, antioxidant enzyme activity, ATP levels, and ATPase activity compared to UCL7-OX plants, thereby enhancing heat tolerance in rice seedlings. These findings suggest that miR408 and its target gene UCL7 participate in regulating energy homeostasis to achieve a balance between growth and heat response. This regulation involves modulating H2O2 levels and optimizing the relationship between the target of rapamycin (TOR) and SNF1-related protein kinase 1 (SnRK1) in rice.