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

EMBO J. 2021 Aug 2;40(15):e107455. doi: 10.15252/embj.2020107455. Epub 2021 Jun 21.

Abstract

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.

Keywords: Arabidopsis; ARGONAUTE; HASTY; miRNA; movement.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / cytology
  • Arabidopsis / genetics*
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Biological Transport / genetics
  • Gene Expression Regulation, Plant
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Karyopherins / genetics
  • Karyopherins / metabolism*
  • MicroRNAs / metabolism*
  • Mutation
  • Phloem / cytology
  • Phloem / genetics
  • Plant Cells
  • Plant Roots / cytology
  • Plant Roots / genetics
  • Plants, Genetically Modified
  • RNA Interference
  • RNA, Plant
  • Xylem / cytology
  • Xylem / genetics

Substances

  • Arabidopsis Proteins
  • HASTY protein, Arabidopsis
  • Karyopherins
  • MicroRNAs
  • RNA, Plant
  • Green Fluorescent Proteins