HASTY-dependent miRNA cell-to-cell movement is required for systemic pathogen resistance in Arabidopsis

Plant defenses against pathogens are tightly regulated through complex gene expression control mechanisms. The precise activation and repression of defense-related genes are crucial to balancing the trade-off between growth and immunity. Micro RNAs (miRNAs) play a well-established role in the local regulation of plant-microbe interactions. While some miRNAs are also essential for systemic defense responses, their mechanisms of action, biogenesis, and long-distance mobility remain largely unexplored. Here, we show that HASTY (HST), a key factor in miRNA biogenesis and intercellular movement, is required for systemic defense activation. The impaired mobility of miRNAs in hst mutants correlates with a lack of systemic responses. In infected tissues, HST may enhance the co-transcriptional processing of specific pri-miRNAs, which promotes the cell-to-cell movement of their mature miRNAs and contributes to the activation of systemic defenses. Furthermore, two miRNAs that exhibit increased mobility during systemic defense induction are required for a proper systemic response. Interestingly, restoring miRNA mobility in the hst mutant without affecting miRNA abundance, or complementing it with a version of HST expressed exclusively in companion cells, is sufficient to restore systemic defense induction, highlighting the role of miRNA cell-to-cell movement. These findings shed light on the role of HST in plant immunity, linking miRNA biogenesis and mobility to the fine-tuned regulation of systemic defenses.