The miRNA-ROS interactome: Orchestrating plant resilience to environmental fluxes

As sessile organisms, plants constantly face environmental stresses that disrupt reactive oxygen species (ROS) homeostasis. ROS function as critical signaling molecules orchestrating stress adaptation, while microRNAs (miRNAs) have emerged as master regulators of gene expression. Accumulating evidence reveals a bidirectional regulatory network between miRNAs and ROS. In this review, we first examine how miRNAs compartment-specific regulate ROS metabolism in the apoplast, mitochondria, and chloroplasts. We then delineate the multi-layered control of miRNA biogenesis by ROS, encompassing redox-sensitive transcription factors, epigenetic modifications, and post-translational modifications. By integrating these modules into plant responses to abiotic and biotic stresses, we highlight both evolutionarily conserved patterns and stress-specific adaptations essential for ROS homeostasis. The miRNA-ROS interactome emerges as an integrative regulatory framework characterized by evolutionary conservation, spatial compartmentalization, and integration with phytohormone, nutrient, and calcium signaling networks. After identifying critical knowledge gaps in spatiotemporal dynamics and inter-organellar coordination, we propose future research directions leveraging single-cell omics, redox imaging, and synthetic biology. This provides a translational pathway for engineering stress-resilient crops through precise manipulation of miRNA-ROS modules, advancing sustainable agriculture in the context of climate change.