The MicroRNA408-Plantacyanin Module Regulates ROS Homeostasis in the Guard Cells to Balance Plant Growth and Drought Resistance

Yanzhi Yang, Lei Li
Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Shandong, 261000, China; State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing 100871, China

MicroRNA408 (miR408) is one of the most conserved miRNAs in land plants. Despite the knowledge that miR408 enhances photosynthesis while compromises stress tolerance in multiple plants, the cellular mechanism underlying its function remains largely unknown. Here, we show that the blue copper protein plantacyanin (PCY) in Arabidopsis is the primary target for miR408 in vegetative tissues, preferentially expressed in the guard cells, and associated with the endomembrane surrounding individual chloroplasts. We found that the MIR408 promoter is suppressed by multiple ABA-responsive transcription factors, thus allowing PCY to accumulate under stress conditions. Genetic analysis revealed that PCY elevates reactive oxygen species (ROS) in the guard cells, promotes stomatal closure, reduces photosynthetic gas exchange, and enhances drought resistance. Moreover, the miR408-plantacyanin module is sufficient to rescue the growth and drought tolerance phenotypes caused by gain- and loss-of-function of MYB44, an established positive regulator of ABA responses, indicating that the miR408-PCY module relays ABA signaling for regulating ROS homeostasis and drought resistance. These results demonstrate that miR408 regulates stomatal movement to balance growth and drought resistance, providing a mechanistic understanding of why miR408 is selected during land plant evolution and new insights into the long-pursued quest of breeding drought-tolerant and high-yielding crops.