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

Abstract

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.