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Research ArticleLARGE-SCALE BIOLOGY ARTICLES
Open Access

Arabidopsis Defense against Botrytis cinerea: Chronology and Regulation Deciphered by High-Resolution Temporal Transcriptomic Analysis

Oliver Windram, Priyadharshini Madhou, Stuart McHattie, Claire Hill, Richard Hickman, Emma Cooke, Dafyd J. Jenkins, Christopher A. Penfold, Laura Baxter, Emily Breeze, Steven J. Kiddle, Johanna Rhodes, Susanna Atwell, Daniel J. Kliebenstein, Youn-sung Kim, Oliver Stegle, Karsten Borgwardt, Cunjin Zhang, Alex Tabrett, Roxane Legaie, Jonathan Moore, Bärbel Finkenstadt, David L. Wild, Andrew Mead, David Rand, Jim Beynon, Sascha Ott, Vicky Buchanan-Wollaston, Katherine J. Denby
Oliver Windram
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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Priyadharshini Madhou
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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Stuart McHattie
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Claire Hill
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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Richard Hickman
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Emma Cooke
cMolecular Organization and Assembly of Cells Doctoral Training Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Dafyd J. Jenkins
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Christopher A. Penfold
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Laura Baxter
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Emily Breeze
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Steven J. Kiddle
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Johanna Rhodes
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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Susanna Atwell
dDepartment of Plant Sciences, University of California, Davis, California 95616
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Daniel J. Kliebenstein
dDepartment of Plant Sciences, University of California, Davis, California 95616
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Youn-sung Kim
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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Oliver Stegle
eMax Planck Institute for Developmental Biology and Max Planck Institute for Intelligent Systems, 72076 Tuebingen, Germany
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Karsten Borgwardt
eMax Planck Institute for Developmental Biology and Max Planck Institute for Intelligent Systems, 72076 Tuebingen, Germany
fZentrum für Bioinformatik, Eberhard Karls Universität, 72076 Tuebingen, Germany
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Cunjin Zhang
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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Alex Tabrett
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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Roxane Legaie
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Jonathan Moore
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Bärbel Finkenstadt
gDepartment of Statistics, University of Warwick, Coventry CV4 7AL, United Kingdom
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David L. Wild
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Andrew Mead
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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David Rand
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Jim Beynon
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Sascha Ott
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Vicky Buchanan-Wollaston
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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Katherine J. Denby
aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
bWarwick Systems Biology Centre, University of Warwick, Coventry CV4 7AL, United Kingdom
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  • For correspondence: k.j.denby@warwick.ac.uk

Published September 2012. DOI: https://doi.org/10.1105/tpc.112.102046

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  • © 2012 American Society of Plant Biologists. All rights reserved.

Abstract

Transcriptional reprogramming forms a major part of a plant’s response to pathogen infection. Many individual components and pathways operating during plant defense have been identified, but our knowledge of how these different components interact is still rudimentary. We generated a high-resolution time series of gene expression profiles from a single Arabidopsis thaliana leaf during infection by the necrotrophic fungal pathogen Botrytis cinerea. Approximately one-third of the Arabidopsis genome is differentially expressed during the first 48 h after infection, with the majority of changes in gene expression occurring before significant lesion development. We used computational tools to obtain a detailed chronology of the defense response against B. cinerea, highlighting the times at which signaling and metabolic processes change, and identify transcription factor families operating at different times after infection. Motif enrichment and network inference predicted regulatory interactions, and testing of one such prediction identified a role for TGA3 in defense against necrotrophic pathogens. These data provide an unprecedented level of detail about transcriptional changes during a defense response and are suited to systems biology analyses to generate predictive models of the gene regulatory networks mediating the Arabidopsis response to B. cinerea.

  • Glossary

    MAMP
    microbe-associated molecular pattern
    DAMP
    damage-associated molecular pattern
    PG
    polygalacturonase
    OG
    oligogalacturonide
    MAP
    mitogen-activated protein
    ET
    ethylene
    SA
    salicylic acid
    JA
    jasmonic acid
    TF
    transcription factor
    ChIP
    chromatin immunoprecipitation
    HAI
    hours after inoculation
    GP2S
    Gaussian process two-sample test
    GO
    Gene Ontology
    TOFDE
    time of first differential expression
    ABA
    abscisic acid
    nsLTP
    nonspecific lipid transfer protein
    PMEI
    pectin methylesterase inhibitor
    GST
    glutathione S-transferase
    CSI
    causal structure identification
    Col-0
    Columbia-0
    PAL
    phenylalanine ammonium lyase
    GEO
    Gene Expression Omnibus
    FDR
    false discovery rate
    DEG
    differentially expressed gene
    • Received June 29, 2012.
    • Revised August 14, 2012.
    • Accepted September 7, 2012.
    • Published September 28, 2012.

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    Arabidopsis Defense against Botrytis cinerea: Chronology and Regulation Deciphered by High-Resolution Temporal Transcriptomic Analysis
    Oliver Windram, Priyadharshini Madhou, Stuart McHattie, Claire Hill, Richard Hickman, Emma Cooke, Dafyd J. Jenkins, Christopher A. Penfold, Laura Baxter, Emily Breeze, Steven J. Kiddle, Johanna Rhodes, Susanna Atwell, Daniel J. Kliebenstein, Youn-sung Kim, Oliver Stegle, Karsten Borgwardt, Cunjin Zhang, Alex Tabrett, Roxane Legaie, Jonathan Moore, Bärbel Finkenstadt, David L. Wild, Andrew Mead, David Rand, Jim Beynon, Sascha Ott, Vicky Buchanan-Wollaston, Katherine J. Denby
    The Plant Cell Sep 2012, 24 (9) 3530-3557; DOI: 10.1105/tpc.112.102046

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    Arabidopsis Defense against Botrytis cinerea: Chronology and Regulation Deciphered by High-Resolution Temporal Transcriptomic Analysis
    Oliver Windram, Priyadharshini Madhou, Stuart McHattie, Claire Hill, Richard Hickman, Emma Cooke, Dafyd J. Jenkins, Christopher A. Penfold, Laura Baxter, Emily Breeze, Steven J. Kiddle, Johanna Rhodes, Susanna Atwell, Daniel J. Kliebenstein, Youn-sung Kim, Oliver Stegle, Karsten Borgwardt, Cunjin Zhang, Alex Tabrett, Roxane Legaie, Jonathan Moore, Bärbel Finkenstadt, David L. Wild, Andrew Mead, David Rand, Jim Beynon, Sascha Ott, Vicky Buchanan-Wollaston, Katherine J. Denby
    The Plant Cell Sep 2012, 24 (9) 3530-3557; DOI: 10.1105/tpc.112.102046
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    The Plant Cell Online: 24 (9)
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    • Alternative Crassulacean Acid Metabolism Modes Provide Environment-Specific Water-Saving Benefits in a Leaf Metabolic Model
    • ARADEEPOPSIS, an Automated Workflow for Top-View Plant Phenomics using Semantic Segmentation of Leaf States
    • Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis
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