Positive Gene Regulation by a Natural Protective miRNA Enables Arbuscular Mycorrhizal Symbiosis

Arbuscular mycorrhizal (AM) symbiosis associates most plants with fungi of the phylum Glomeromycota. The fungus penetrates into roots and forms within cortical cell branched structures called arbuscules for nutrient exchange. We discovered that miR171b has a mismatched cleavage site and is unable to downregulate the miR171 family target gene, LOM1 (LOST MERISTEMS 1). This mismatched cleavage site is conserved among plants that establish AM symbiosis, but not in non-mycotrophic plants. Unlike other members of the miR171 family, miR171b stimulates AM symbiosis and is expressed specifically in root cells that contain arbuscules. MiR171b protects LOM1 from negative regulation by other miR171 family members. These findings uncover a unique mechanism of positive post-transcriptional regulation of gene expression by miRNAs and demonstrate its relevance for the establishment of AM symbiosis. [Display omitted] •miR171b is specific to mycotrophic species and has a target gene cleavage site mismatch•miR171b accumulation activated target gene LOM1 expression and enhanced mycorrhization•miR171b is preferentially expressed in arbuscule-containing cells•miR171b expression protects LOM1 from silencing by other miR171 family members Arbuscular mycorrhizal symbiosis, a plant-fungal mutualistic relationship, is regulated by the miR171 family. Couzigou et al. discover that miR171b has evolved a target site mismatch such that instead of silencing, miR171b protects its target gene LOM1 from cleavage by other miR171 family members and thereby enables AM symbiosis.