HASTY, the Arabidopsis EXPORTIN5 ortholog, regulates cell‐to‐cell and vascular microRNA movement

Plant microRNAs (miRNAs) guide cytosolic post‐transcriptional gene silencing of sequence‐complementary transcripts within the producing cells, as well as in distant cells and tissues. Here, we used an artificial miRNA‐based system (amiRSUL) in Arabidopsis thaliana to explore the still elusive mechanisms of inter‐cellular miRNA movement via forward genetics. This screen identified many mutant alleles of HASTY (HST), the ortholog of mammalian EXPORTIN5 (XPO5) with a recently reported role in miRNA biogenesis in Arabidopsis. In both epidermis‐peeling and grafting assays, amiRSUL levels were reduced much more substantially in miRNA‐recipient tissues than in silencing‐emitting tissues. We ascribe this effect to HST controlling cell‐to‐cell and phloem‐mediated movement of the processed amiRSUL, in addition to regulating its biogenesis. While HST is not required for the movement of free GFP or siRNAs, its cell‐autonomous expression in amiRSUL‐emitting tissues suffices to restore amiRSUL movement independently of its nucleo‐cytosolic shuttling activity. By contrast, HST is dispensable for the movement and activity of amiRSUL within recipient tissues. Finally, HST enables movement of endogenous miRNAs that display mostly unaltered steady‐state levels in hst mutant tissues. We discuss a role for HST as a hitherto unrecognized regulator of miRNA movement in relation to its recently assigned nuclear function at the nexus of MIRNA transcription and miRNA processing.