Plant stem cell maintenance involves direct transcriptional repression of differentiation program

Abstract In animal systems, master regulatory transcription factors (TFs) mediate stem cell maintenance through a direct transcriptional repression of differentiation promoting TFs. Whether similar mechanisms operate in plants is not known. In plants, shoot apical meristems serve as reservoirs of st...

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Main Authors: Ram Kishor Yadav, Mariano Perales, Jérémy Gruel, Carolyn Ohno, Marcus Heisler, Thomas Girke, Henrik Jönsson, G Venugopala Reddy
Format: Article
Language:English
Published: Springer Nature 2013-04-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.1038/msb.2013.8
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author Ram Kishor Yadav
Mariano Perales
Jérémy Gruel
Carolyn Ohno
Marcus Heisler
Thomas Girke
Henrik Jönsson
G Venugopala Reddy
author_facet Ram Kishor Yadav
Mariano Perales
Jérémy Gruel
Carolyn Ohno
Marcus Heisler
Thomas Girke
Henrik Jönsson
G Venugopala Reddy
author_sort Ram Kishor Yadav
collection DOAJ
description Abstract In animal systems, master regulatory transcription factors (TFs) mediate stem cell maintenance through a direct transcriptional repression of differentiation promoting TFs. Whether similar mechanisms operate in plants is not known. In plants, shoot apical meristems serve as reservoirs of stem cells that provide cells for all above ground organs. WUSCHEL, a homeodomain TF produced in cells of the niche, migrates into adjacent cells where it specifies stem cells. Through high‐resolution genomic analysis, we show that WUSCHEL represses a large number of genes that are expressed in differentiating cells including a group of differentiation promoting TFs involved in leaf development. We show that WUS directly binds to the regulatory regions of differentiation promoting TFs; KANADI1, KANADI2, ASYMMETRICLEAVES2 and YABBY3 to repress their expression. Predictions from a computational model, supported by live imaging, reveal that WUS‐mediated repression prevents premature differentiation of stem cell progenitors, being part of a minimal regulatory network for meristem maintenance. Our work shows that direct transcriptional repression of differentiation promoting TFs is an evolutionarily conserved logic for stem cell regulation.
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spelling doaj-art-43707dc6e24e466ca88d5cda388af39a2025-08-20T03:46:37ZengSpringer NatureMolecular Systems Biology1744-42922013-04-019111310.1038/msb.2013.8Plant stem cell maintenance involves direct transcriptional repression of differentiation programRam Kishor Yadav0Mariano Perales1Jérémy Gruel2Carolyn Ohno3Marcus Heisler4Thomas Girke5Henrik Jönsson6G Venugopala Reddy7Department of Botany and Plant Sciences, Center for Plant Cell Biology (CEPCEB), Institute of Integrative Genome Biology (IIGB), University of CaliforniaDepartment of Botany and Plant Sciences, Center for Plant Cell Biology (CEPCEB), Institute of Integrative Genome Biology (IIGB), University of CaliforniaComputational Biology and Biological Physics Group, Department of Astronomy and Theoretical Physics, Lund UniversityEuropean Molecular Biology LaboratoryEuropean Molecular Biology LaboratoryDepartment of Botany and Plant Sciences, Center for Plant Cell Biology (CEPCEB), Institute of Integrative Genome Biology (IIGB), University of CaliforniaComputational Biology and Biological Physics Group, Department of Astronomy and Theoretical Physics, Lund UniversityDepartment of Botany and Plant Sciences, Center for Plant Cell Biology (CEPCEB), Institute of Integrative Genome Biology (IIGB), University of CaliforniaAbstract In animal systems, master regulatory transcription factors (TFs) mediate stem cell maintenance through a direct transcriptional repression of differentiation promoting TFs. Whether similar mechanisms operate in plants is not known. In plants, shoot apical meristems serve as reservoirs of stem cells that provide cells for all above ground organs. WUSCHEL, a homeodomain TF produced in cells of the niche, migrates into adjacent cells where it specifies stem cells. Through high‐resolution genomic analysis, we show that WUSCHEL represses a large number of genes that are expressed in differentiating cells including a group of differentiation promoting TFs involved in leaf development. We show that WUS directly binds to the regulatory regions of differentiation promoting TFs; KANADI1, KANADI2, ASYMMETRICLEAVES2 and YABBY3 to repress their expression. Predictions from a computational model, supported by live imaging, reveal that WUS‐mediated repression prevents premature differentiation of stem cell progenitors, being part of a minimal regulatory network for meristem maintenance. Our work shows that direct transcriptional repression of differentiation promoting TFs is an evolutionarily conserved logic for stem cell regulation.https://doi.org/10.1038/msb.2013.8central zoneCLAVATA3shoot apical meristemstem cell nicheWUSCHEL
spellingShingle Ram Kishor Yadav
Mariano Perales
Jérémy Gruel
Carolyn Ohno
Marcus Heisler
Thomas Girke
Henrik Jönsson
G Venugopala Reddy
Plant stem cell maintenance involves direct transcriptional repression of differentiation program
Molecular Systems Biology
central zone
CLAVATA3
shoot apical meristem
stem cell niche
WUSCHEL
title Plant stem cell maintenance involves direct transcriptional repression of differentiation program
title_full Plant stem cell maintenance involves direct transcriptional repression of differentiation program
title_fullStr Plant stem cell maintenance involves direct transcriptional repression of differentiation program
title_full_unstemmed Plant stem cell maintenance involves direct transcriptional repression of differentiation program
title_short Plant stem cell maintenance involves direct transcriptional repression of differentiation program
title_sort plant stem cell maintenance involves direct transcriptional repression of differentiation program
topic central zone
CLAVATA3
shoot apical meristem
stem cell niche
WUSCHEL
url https://doi.org/10.1038/msb.2013.8
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