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

doi:10.1105/tpc.112.102046

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 LegaieJonathan Moore, Bärbel Finkenstadt, David L. Wild, Andrew Mead, David Rand, Jim Beynon, Sascha Ott, Vicky Buchanan-Wollaston, Katherine J. Denby

Research output: Contribution to journal › Article › peer-review

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.

Original language	English
Pages (from-to)	3530-3557
Number of pages	28
Journal	The Plant Cell
Volume	24
Issue number	9
DOIs	https://doi.org/10.1105/tpc.112.102046
Publication status	Published - Sept 2012

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Windram, O., Madhou, P., Mchattie, S., Hill, C., Hickman, R., Cooke, E., Jenkins, D. J., Penfold, C. A., Baxter, L., Breeze, E., Kiddle, S. J., Rhodes, J., Atwell, S., Kliebenstein, D. J., Kim, Y. S., Stegle, O., Borgwardt, K., Zhang, C., Tabrett, A., ... Denby, K. J. (2012). Arabidopsis defense against Botrytis cinerea: Chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. The Plant Cell, 24(9), 3530-3557. https://doi.org/10.1105/tpc.112.102046

@article{36e2fa84cf834262998346988e9c2c9a,

title = "Arabidopsis defense against Botrytis cinerea: Chronology and regulation deciphered by high-resolution temporal transcriptomic analysis",

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.",

author = "Oliver Windram and Priyadharshini Madhou and Stuart Mchattie and Claire Hill and Richard Hickman and Emma Cooke and Jenkins, {Dafyd J.} and Penfold, {Christopher A.} and Laura Baxter and Emily Breeze and Kiddle, {Steven J.} and Johanna Rhodes and Susanna Atwell and Kliebenstein, {Daniel J.} and Kim, {Youn sung} and Oliver Stegle and Karsten Borgwardt and Cunjin Zhang and Alex Tabrett and Roxane Legaie and Jonathan Moore and B{\"a}rbel Finkenstadt and Wild, {David L.} and Andrew Mead and David Rand and Jim Beynon and Sascha Ott and Vicky Buchanan-Wollaston and Denby, {Katherine J.}",

year = "2012",

month = sep,

doi = "10.1105/tpc.112.102046",

language = "English",

volume = "24",

pages = "3530--3557",

journal = "The Plant Cell",

issn = "1040-4651",

publisher = "American Society of Plant Biologists",

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Windram, O, Madhou, P, Mchattie, S, Hill, C, Hickman, R, Cooke, E, Jenkins, DJ, Penfold, CA, Baxter, L, Breeze, E, Kiddle, SJ, Rhodes, J, Atwell, S, Kliebenstein, DJ, Kim, YS, Stegle, O, Borgwardt, K, Zhang, C, Tabrett, A, Legaie, R, Moore, J, Finkenstadt, B, Wild, DL, Mead, A, Rand, D, Beynon, J, Ott, S, Buchanan-Wollaston, V & Denby, KJ 2012, 'Arabidopsis defense against Botrytis cinerea: Chronology and regulation deciphered by high-resolution temporal transcriptomic analysis', The Plant Cell, vol. 24, no. 9, pp. 3530-3557. https://doi.org/10.1105/tpc.112.102046

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T1 - Arabidopsis defense against Botrytis cinerea

T2 - Chronology and regulation deciphered by high-resolution temporal transcriptomic analysis

AU - Windram, Oliver

AU - Madhou, Priyadharshini

AU - Mchattie, Stuart

AU - Hill, Claire

AU - Hickman, Richard

AU - Cooke, Emma

AU - Jenkins, Dafyd J.

AU - Penfold, Christopher A.

AU - Baxter, Laura

AU - Breeze, Emily

AU - Kiddle, Steven J.

AU - Rhodes, Johanna

AU - Atwell, Susanna

AU - Kliebenstein, Daniel J.

AU - Kim, Youn sung

AU - Stegle, Oliver

AU - Borgwardt, Karsten

AU - Zhang, Cunjin

AU - Tabrett, Alex

AU - Legaie, Roxane

AU - Moore, Jonathan

AU - Finkenstadt, Bärbel

AU - Wild, David L.

AU - Mead, Andrew

AU - Rand, David

AU - Beynon, Jim

AU - Ott, Sascha

AU - Buchanan-Wollaston, Vicky

AU - Denby, Katherine J.

PY - 2012/9

Y1 - 2012/9

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84868288164&partnerID=8YFLogxK

U2 - 10.1105/tpc.112.102046

DO - 10.1105/tpc.112.102046

M3 - Article

C2 - 23023172

AN - SCOPUS:84868288164

SN - 1040-4651

VL - 24

SP - 3530

EP - 3557

JO - The Plant Cell

JF - The Plant Cell

IS - 9

ER -

Arabidopsis defense against Botrytis cinerea: Chronology and regulation deciphered by high-resolution temporal transcriptomic analysis

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