Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha

New Phytol. 2018 Jun;218(4):1612-1630. doi: 10.1111/nph.15090. Epub 2018 Mar 25.


A plethora of developmental and physiological processes in land plants is influenced by auxin, to a large extent via alterations in gene expression by AUXIN RESPONSE FACTORs (ARFs). The canonical auxin transcriptional response system is a land plant innovation, however, charophycean algae possess orthologues of at least some classes of ARF and AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) genes, suggesting that elements of the canonical land plant system existed in an ancestral alga. We reconstructed the phylogenetic relationships between streptophyte ARF and AUX/IAA genes and functionally characterized the solitary class C ARF, MpARF3, in Marchantia polymorpha. Phylogenetic analyses indicate that multiple ARF classes, including class C ARFs, existed in an ancestral alga. Loss- and gain-of-function MpARF3 alleles result in pleiotropic effects in the gametophyte, with MpARF3 inhibiting differentiation and developmental transitions in multiple stages of the life cycle. Although loss-of-function Mparf3 and Mpmir160 alleles respond to exogenous auxin treatments, strong miR-resistant MpARF3 alleles are auxin-insensitive, suggesting that class C ARFs act in a context-dependent fashion. We conclude that two modules independently evolved to regulate a pre-existing ARF transcriptional network. Whereas the auxin-TIR1-AUX/IAA pathway evolved to repress class A/B ARF activity, miR160 evolved to repress class C ARFs in a dynamic fashion.

Keywords: Marchantia; AUXIN RESPONSE FACTOR (ARF); auxin; auxin signalling; class C ARF; land plant evolution; mir160.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Cell Differentiation* / drug effects
  • Evolution, Molecular*
  • Feedback, Physiological / drug effects
  • Gene Expression Regulation, Plant / drug effects
  • Genes, Plant
  • Indoleacetic Acids / pharmacology
  • Marchantia / cytology
  • Marchantia / genetics*
  • Marchantia / growth & development*
  • Marchantia / ultrastructure
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Multigene Family
  • Mutation / genetics
  • Phenotype
  • Phylogeny
  • Plant Development* / drug effects
  • Plant Proteins / chemistry
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Protein Domains
  • Signal Transduction / drug effects
  • Spores / drug effects
  • Spores / physiology
  • Transcription, Genetic / drug effects
  • Up-Regulation / drug effects
  • Up-Regulation / genetics


  • Indoleacetic Acids
  • MicroRNAs
  • Plant Proteins