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Research ArticleLARGE-SCALE BIOLOGY ARTICLE
Open Access

Inference of the Arabidopsis Lateral Root Gene Regulatory Network Suggests a Bifurcation Mechanism That Defines Primordia Flanking and Central Zones

Julien Lavenus, Tatsuaki Goh, Soazig Guyomarc’h, Kristine Hill, Mikael Lucas, Ute Voß, Kim Kenobi, Michael H. Wilson, Etienne Farcot, Gretchen Hagen, Thomas J. Guilfoyle, Hidehiro Fukaki, Laurent Laplaze, Malcolm J. Bennett
Julien Lavenus
aInstitut de Recherche pour le Développement, UMR DIADE, 34394 Montpellier cedex 5, France
bCentre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom
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Tatsuaki Goh
bCentre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom
cDepartment of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan
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Soazig Guyomarc’h
dUniversité de Montpellier, UMR DIADE, 34394 Montpellier cedex 5, France
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Kristine Hill
bCentre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom
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Mikael Lucas
aInstitut de Recherche pour le Développement, UMR DIADE, 34394 Montpellier cedex 5, France
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Ute Voß
bCentre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom
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Kim Kenobi
bCentre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom
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Michael H. Wilson
bCentre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom
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Etienne Farcot
bCentre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom
eInria, Virtual Plants Team, 34095 Montpellier cedex 5, France
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Gretchen Hagen
fUniversity of Missouri, Columbia, Missouri 65211
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Thomas J. Guilfoyle
fUniversity of Missouri, Columbia, Missouri 65211
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Hidehiro Fukaki
cDepartment of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan
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Laurent Laplaze
aInstitut de Recherche pour le Développement, UMR DIADE, 34394 Montpellier cedex 5, France
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  • For correspondence: laurent.laplaze@ird.fr bennett@nottingham.ac.uk
Malcolm J. Bennett
bCentre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom
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  • For correspondence: laurent.laplaze@ird.fr bennett@nottingham.ac.uk

Published May 2015. DOI: https://doi.org/10.1105/tpc.114.132993

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  • © 2015 American Society of Plant Biologists. All rights reserved.

Abstract

A large number of genes involved in lateral root (LR) organogenesis have been identified over the last decade using forward and reverse genetic approaches in Arabidopsis thaliana. Nevertheless, how these genes interact to form a LR regulatory network largely remains to be elucidated. In this study, we developed a time-delay correlation algorithm (TDCor) to infer the gene regulatory network (GRN) controlling LR primordium initiation and patterning in Arabidopsis from a time-series transcriptomic data set. The predicted network topology links the very early-activated genes involved in LR initiation to later expressed cell identity markers through a multistep genetic cascade exhibiting both positive and negative feedback loops. The predictions were tested for the key transcriptional regulator AUXIN RESPONSE FACTOR7 node, and over 70% of its targets were validated experimentally. Intriguingly, the predicted GRN revealed a mutual inhibition between the ARF7 and ARF5 modules that would control an early bifurcation between two cell fates. Analyses of the expression pattern of ARF7 and ARF5 targets suggest that this patterning mechanism controls flanking and central zone specification in Arabidopsis LR primordia.

  • Glossary

    LR
    lateral root
    LRP
    lateral root primordium
    GRN
    gene regulatory network
    TDCor
    time-delay correlation
    RAM
    root apical meristem
    ODE
    ordinary differential equation
    Col-0
    Columbia-0
    hag
    hours after gravistimulation
    DEX
    dexamethasone
    NAA
    naphthalene acetic acid
    CHX
    cycloheximide
    ChIP-qPCR
    chromatin immunoprecipitation-quantitative PCR
    • Received October 14, 2014.
    • Revised March 2, 2015.
    • Accepted April 7, 2015.
    • Published May 5, 2015.

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    Inference of the Arabidopsis Lateral Root Gene Regulatory Network Suggests a Bifurcation Mechanism That Defines Primordia Flanking and Central Zones
    Julien Lavenus, Tatsuaki Goh, Soazig Guyomarc’h, Kristine Hill, Mikael Lucas, Ute Voß, Kim Kenobi, Michael H. Wilson, Etienne Farcot, Gretchen Hagen, Thomas J. Guilfoyle, Hidehiro Fukaki, Laurent Laplaze, Malcolm J. Bennett
    The Plant Cell May 2015, 27 (5) 1368-1388; DOI: 10.1105/tpc.114.132993

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    Inference of the Arabidopsis Lateral Root Gene Regulatory Network Suggests a Bifurcation Mechanism That Defines Primordia Flanking and Central Zones
    Julien Lavenus, Tatsuaki Goh, Soazig Guyomarc’h, Kristine Hill, Mikael Lucas, Ute Voß, Kim Kenobi, Michael H. Wilson, Etienne Farcot, Gretchen Hagen, Thomas J. Guilfoyle, Hidehiro Fukaki, Laurent Laplaze, Malcolm J. Bennett
    The Plant Cell May 2015, 27 (5) 1368-1388; DOI: 10.1105/tpc.114.132993
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    The Plant Cell: 27 (5)
    The Plant Cell
    Vol. 27, Issue 5
    May 2015
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