Auxin-Mediated Transcriptional System with a Minimal Set of Components Is Critical for Morphogenesis through the Life Cycle in Marchantia polymorpha

PLoS Genet. 2015 May 28;11(5):e1005084. doi: 10.1371/journal.pgen.1005084. eCollection 2015 May.

Abstract

The plant hormone auxin regulates many aspects of plant growth and development. Recent progress in Arabidopsis provided a scheme that auxin receptors, TIR1/AFBs, target transcriptional co-repressors, AUX/IAAs, for degradation, allowing ARFs to regulate transcription of auxin responsive genes. The mechanism of auxin-mediated transcriptional regulation is considered to have evolved around the time plants adapted to land. However, little is known about the role of auxin-mediated transcription in basal land plant lineages. We focused on the liverwort Marchantia polymorpha, which belongs to the earliest diverging lineage of land plants. M. polymorpha has only a single TIR1/AFB (MpTIR1), a single AUX/IAA (MpIAA), and three ARFs (MpARF1, MpARF2, and MpARF3) in the genome. Expression of a dominant allele of MpIAA with mutations in its putative degron sequence conferred an auxin resistant phenotype and repressed auxin-dependent expression of the auxin response reporter proGH3:GUS. We next established a system for DEX-inducible auxin-response repression by expressing the putatively stabilized MpIAA protein fused with the glucocorticoid receptor domain (MpIAA(mDII)-GR). Repression of auxin responses in (pro)MpIAA:MpIAA(mDII)-GR plants caused severe defects in various developmental processes, including gemmaling development, dorsiventrality, organogenesis, and tropic responses. Transient transactivation assays showed that the three MpARFs had different transcriptional activities, each corresponding to their phylogenetic classifications. Moreover, MpIAA and MpARF proteins interacted with each other with different affinities. This study provides evidence that pleiotropic auxin responses can be achieved by a minimal set of auxin signaling factors and suggests that the transcriptional regulation mediated by TIR1/AFB, AUX/IAA, and three types of ARFs might have been a key invention to establish body plans of land plants. We propose that M. polymorpha is a good model to investigate the principles and the evolution of auxin-mediated transcriptional regulation and its roles in land plant morphogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis Proteins / genetics
  • DNA-Binding Proteins / genetics
  • Evolution, Molecular*
  • F-Box Proteins / genetics
  • Gene Expression Regulation, Plant
  • Indoleacetic Acids / metabolism*
  • Life Cycle Stages
  • Marchantia / genetics*
  • Marchantia / growth & development
  • Molecular Sequence Data
  • Morphogenesis / genetics
  • Mutation
  • Nuclear Proteins / genetics
  • Phylogeny
  • Plants, Genetically Modified
  • Receptors, Cell Surface / genetics
  • Transcription, Genetic*

Substances

  • AUX1 protein, Arabidopsis
  • Arabidopsis Proteins
  • DNA-Binding Proteins
  • F-Box Proteins
  • IAA1 protein, Arabidopsis
  • Indoleacetic Acids
  • Nuclear Proteins
  • Receptors, Cell Surface
  • TIR1 protein, Arabidopsis

Associated data

  • GENBANK/AB981316
  • GENBANK/AB981317
  • GENBANK/AB981318
  • GENBANK/AB981319
  • GENBANK/AB981320
  • GENBANK/AB981321

Grants and funding

This work was supported by a Grant-in-Aid for Scientific Research on Innovative Areas (25113009 to TK; 25119711 to KI), a Grant-in-Aid for Scientific Research (B) (26281059 to TK), Joint Research Project (to TK), JSPS Fellows (24-7037 to HK) from the Japan Society for the Promotion of Science, and the Australian Research Council (FF0561326 and DP110100070 to JLB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.