MicroRNA superfamilies descended from miR390 and their roles in secondary small interfering RNA Biogenesis in Eudicots

Plant Cell. 2013 May;25(5):1555-72. doi: 10.1105/tpc.113.110957. Epub 2013 May 21.

Abstract

Trans-acting small interfering RNAs (tasiRNAs) are a major class of small RNAs performing essential biological functions in plants. The first reported tasiRNA pathway, that of miR173-TAS1/2, produces tasiRNAs regulating a set of pentatricopeptide repeat (PPR) genes and has been characterized only in Arabidopsis thaliana to date. Here, we demonstrate that the microRNA (miRNA)-trans-acting small interfering RNA gene (TAS)-pentatricopeptide repeat-containing gene (PPR)-small interfering RNA pathway is a highly dynamic and widespread feature of eudicots. Nine eudicot plants, representing six different plant families, have evolved similar tasiRNA pathways to initiate phased small interfering RNA (phasiRNA) production from PPR genes. The PPR phasiRNA production is triggered by different 22-nucleotide miRNAs, including miR7122, miR1509, and fve-PPRtri1/2, and through distinct mechanistic strategies exploiting miRNA direct targeting or indirect targeting through TAS-like genes (TASL), one-hit or two-hit, or even two layers of tasiRNA-TASL interactions. Intriguingly, although those miRNA triggers display high sequence divergence caused by the occurrence of frequent point mutations and splicing shifts, their corresponding MIRNA genes show pronounced identity to the Arabidopsis MIR173, implying a common origin of this group of miRNAs (super-miR7122). Further analyses reveal that super-miR7122 may have evolved from a newly defined miR4376 superfamily, which probably originated from the widely conserved miR390. The elucidation of this evolutionary path expands our understanding of the course of miRNA evolution, especially for relatively conserved miRNA families.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis Proteins / genetics
  • Base Sequence
  • Cotyledon / classification
  • Cotyledon / genetics
  • Evolution, Molecular
  • Fragaria / genetics
  • Genetic Variation
  • Glycine max / genetics
  • Magnoliopsida / classification
  • Magnoliopsida / genetics*
  • Malus / genetics
  • Medicago / genetics
  • MicroRNAs / genetics*
  • Molecular Sequence Data
  • Multigene Family*
  • Phylogeny
  • Prunus / genetics
  • RNA, Plant / genetics*
  • RNA, Small Interfering / genetics*
  • Sequence Homology, Nucleic Acid
  • Signal Transduction / genetics
  • Species Specificity
  • Vitis / genetics

Substances

  • Arabidopsis Proteins
  • MIRN173 microRNA, Arabidopsis
  • MicroRNAs
  • RNA, Plant
  • RNA, Small Interfering
  • pentatricopeptide repeat protein, Arabidopsis