Organizer-Derived WOX5 Signal Maintains Root Columella Stem Cells through Chromatin-Mediated Repression of CDF4 Expression

Limin Pi; Ernst Aichinger; Eric van der Graaff; Cristina I Llavata-Peris; Dolf Weijers; Lars Hennig; Edwin Groot; Thomas Laux

doi:10.1016/j.devcel.2015.04.024

Organizer-Derived WOX5 Signal Maintains Root Columella Stem Cells through Chromatin-Mediated Repression of CDF4 Expression

Dev Cell. 2015 Jun 8;33(5):576-88. doi: 10.1016/j.devcel.2015.04.024. Epub 2015 May 28.

Authors

Limin Pi¹, Ernst Aichinger¹, Eric van der Graaff¹, Cristina I Llavata-Peris², Dolf Weijers², Lars Hennig³, Edwin Groot¹, Thomas Laux⁴

Affiliations

¹ BIOSS Centre for Biological Signalling Studies, Faculty of Biology, Albert-Ludwigs-University Freiburg, Schänzlestrasse 1, 79104 Freiburg, Germany.
² Laboratory of Biochemistry, Wageningen University, Dreijenlaan 3, 6703HA Wageningen, the Netherlands.
³ Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007 Uppsala, Sweden.
⁴ BIOSS Centre for Biological Signalling Studies, Faculty of Biology, Albert-Ludwigs-University Freiburg, Schänzlestrasse 1, 79104 Freiburg, Germany. Electronic address: laux@biologie.uni-freiburg.de.

PMID: 26028217
DOI: 10.1016/j.devcel.2015.04.024

Abstract

Stem cells in plants and animals are maintained pluripotent by signals from adjacent niche cells. In plants, WUSCHEL HOMEOBOX (WOX) transcription factors are central regulators of stem cell maintenance in different meristem types, yet their molecular mode of action has remained elusive. Here we show that in the Arabidopsis root meristem, the WOX5 protein moves from the root niche organizer, the quiescent center, into the columella stem cells, where it directly represses the transcription factor gene CDF4. This creates a gradient of CDF4 transcription, which promotes differentiation opposite to the WOX5 gradient, allowing stem cell daughter cells to exit the stem cell state. We further show that WOX5 represses CDF4 transcription by recruiting TPL/TPR co-repressors and the histone deacetylase HDA19, which consequently induces histone deacetylation at the CDF4 regulatory region. Our results show that chromatin-mediated repression of differentiation programs is a common strategy in plant and animal stem cell niches.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Acetylation
Arabidopsis / genetics
Arabidopsis / growth & development
Arabidopsis / metabolism*
Arabidopsis Proteins / genetics*
Arabidopsis Proteins / metabolism
Cell Differentiation*
Chromatin / genetics*
Chromatin Immunoprecipitation
Co-Repressor Proteins / genetics
Co-Repressor Proteins / metabolism
Electrophoretic Mobility Shift Assay
Gene Expression Regulation, Developmental
Gene Expression Regulation, Plant
Histone Deacetylases / genetics
Histone Deacetylases / metabolism
Histones / metabolism
Homeodomain Proteins / genetics
Homeodomain Proteins / metabolism*
In Situ Hybridization
Meristem / cytology*
Meristem / metabolism
Microarray Analysis
Microscopy, Confocal
Nuclear Pore Complex Proteins / genetics
Nuclear Pore Complex Proteins / metabolism
Plant Roots / cytology*
Plant Roots / metabolism
Promoter Regions, Genetic / genetics
Signal Transduction
Stem Cell Niche
Stem Cells / cytology*
Stem Cells / metabolism

Substances

Arabidopsis Proteins
Chromatin
Co-Repressor Proteins
Histones
Homeodomain Proteins
Nuclear Pore Complex Proteins
TPR protein, Arabidopsis
WUSCHEL protein, Arabidopsis
topless protein, Arabidopsis
HDA19 protein, Arabidopsis
Histone Deacetylases