The THO Complex Non-Cell-Autonomously Represses Female Germline Specification through the TAS3-ARF3 Module

Curr Biol. 2017 Jun 5;27(11):1597-1609.e2. doi: 10.1016/j.cub.2017.05.021. Epub 2017 May 25.

Abstract

In most sexually reproducing plants, a single somatic, sub-epidermal cell in an ovule is selected to differentiate into a megaspore mother cell, which is committed to giving rise to the female germline. However, it remains unclear how intercellular signaling among somatic cells results in only one cell in the sub-epidermal layer differentiating into the megaspore mother cell. Here we uncovered a role of the THO complex in restricting the megaspore mother cell fate to a single cell. Mutations in TEX1, HPR1, and THO6, components of the THO/TREX complex, led to the formation of multiple megaspore mother cells, which were able to initiate gametogenesis. We demonstrated that TEX1 repressed the megaspore mother cell fate by promoting the biogenesis of TAS3-derived trans-acting small interfering RNA (ta-siRNA), which represses ARF3 expression. The TEX1 protein was present in epidermal cells, but not in the germline, and, through TAS3-derived ta-siRNA, restricted ARF3 expression to the medio domain of ovule primordia. Expansion of ARF3 expression into lateral epidermal cells in a TAS3 ta-siRNA-insensitive mutant led to the formation of supernumerary megaspore mother cells, suggesting that TEX1- and TAS3-mediated restriction of ARF3 expression limits excessive megaspore mother cell formation non-cell-autonomously. Our findings reveal the role of a small-RNA pathway in the regulation of female germline specification in Arabidopsis.

Keywords: ARF3; HPR1; RDR6; TEX1; THO; THOC6; female gametophyte; megaspore mother cell; siRNA; tasiR-ARF.

MeSH terms

  • Arabidopsis
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Gametogenesis, Plant / physiology*
  • Gene Expression Regulation, Plant / physiology*
  • Mutation
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Ovule / physiology*
  • RNA, Small Interfering / genetics*
  • RNA, Small Interfering / metabolism
  • RNA-Dependent RNA Polymerase / genetics
  • RNA-Dependent RNA Polymerase / metabolism
  • Signal Transduction / genetics*

Substances

  • Arabidopsis Proteins
  • DNA-Binding Proteins
  • ETT protein, Arabidopsis
  • Nuclear Proteins
  • RNA, Small Interfering
  • TEX1 protein, Arabidopsis
  • RDR6 protein, Arabidopsis
  • RNA-Dependent RNA Polymerase