RXLR Effector AVR2 Up-Regulates a Brassinosteroid-Responsive bHLH Transcription Factor to Suppress Immunity

Dionne Turnbull, Lina Yang, Shaista Naqvi, Susan Breen, Lydia Welsh, Jennifer Stephens, Jenny Morris, Petra C. Boevink, Pete E. Hedley, Jiasui Zhan, Paul R. J. Birch, Eleanor M. Gilroy (Lead / Corresponding author)

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Abstract

An emerging area in plant research focuses on antagonism between regulatory systems governing growth and immunity. Such crosstalk represents a point of vulnerability for pathogens to exploit. AVR2, an RXLR effector secreted by the potato blight pathogen Phytophthora infestans, interacts with potato BSL1, a putative phosphatase implicated in growth-promoting brassinosteroid (BR) hormone signalling. Transgenic potato (Solanum tuberosum) plants expressing the effector exhibit transcriptional and phenotypic hallmarks of over-active BR signalling, and show enhanced susceptibility to P. infestans. Microarray analysis was used to identify a set of BR-responsive marker genes in potato, all of which are constitutively expressed to BR-induced levels in AVR2 transgenic lines. One of these genes was a bHLH transcription factor, designated StCHL1, homologous to AtCIB1 and AtHBI1 which are known to facilitate antagonism between BR and immune responses. Transient expression of either AVR2 or CHL1 enhanced leaf colonisation by P. infestans and compromised immune cell death activated by perception of the elicitin INF1. Knockdown of CHL1 transcript using Virus-Induced Gene Silencing (VIGS) reduced colonisation of P. infestans on Nicotiana benthamiana. Moreover, the ability of AVR2 to suppress INF1-triggered cell death was attenuated in NbCHL1 silenced plants, indicating that NbCHL1 was important for this effector activity. Thus AVR2 exploits crosstalk between BR signalling and innate immunity in Solanum species, representing a novel, indirect mode of innate immune suppression by a filamentous pathogen effector.
Original languageEnglish
Pages (from-to)356-369
Number of pages14
JournalPlant Physiology
Volume174
Issue number1
Early online date1 May 2017
DOIs
Publication statusPublished - May 2017

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Brassinosteroids
Basic Helix-Loop-Helix Transcription Factors
brassinosteroids
Phytophthora infestans
Solanum tuberosum
Immunity
Up-Regulation
transcription factors
immunity
potatoes
cell death
pathogens
Cell Death
genetically modified organisms
Solanum
Aptitude
Nicotiana benthamiana
Gene Silencing
gene silencing
Microarray Analysis

Keywords

  • Journal article

Cite this

Turnbull, Dionne ; Yang, Lina ; Naqvi, Shaista ; Breen, Susan ; Welsh, Lydia ; Stephens, Jennifer ; Morris, Jenny ; Boevink, Petra C. ; Hedley, Pete E. ; Zhan, Jiasui ; Birch, Paul R. J. ; Gilroy, Eleanor M. / RXLR Effector AVR2 Up-Regulates a Brassinosteroid-Responsive bHLH Transcription Factor to Suppress Immunity. In: Plant Physiology. 2017 ; Vol. 174, No. 1. pp. 356-369.
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abstract = "An emerging area in plant research focuses on antagonism between regulatory systems governing growth and immunity. Such crosstalk represents a point of vulnerability for pathogens to exploit. AVR2, an RXLR effector secreted by the potato blight pathogen Phytophthora infestans, interacts with potato BSL1, a putative phosphatase implicated in growth-promoting brassinosteroid (BR) hormone signalling. Transgenic potato (Solanum tuberosum) plants expressing the effector exhibit transcriptional and phenotypic hallmarks of over-active BR signalling, and show enhanced susceptibility to P. infestans. Microarray analysis was used to identify a set of BR-responsive marker genes in potato, all of which are constitutively expressed to BR-induced levels in AVR2 transgenic lines. One of these genes was a bHLH transcription factor, designated StCHL1, homologous to AtCIB1 and AtHBI1 which are known to facilitate antagonism between BR and immune responses. Transient expression of either AVR2 or CHL1 enhanced leaf colonisation by P. infestans and compromised immune cell death activated by perception of the elicitin INF1. Knockdown of CHL1 transcript using Virus-Induced Gene Silencing (VIGS) reduced colonisation of P. infestans on Nicotiana benthamiana. Moreover, the ability of AVR2 to suppress INF1-triggered cell death was attenuated in NbCHL1 silenced plants, indicating that NbCHL1 was important for this effector activity. Thus AVR2 exploits crosstalk between BR signalling and innate immunity in Solanum species, representing a novel, indirect mode of innate immune suppression by a filamentous pathogen effector.",
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note = "This work was funded by the Scottish Government Rural and Environmental Science and Analytical Services Division (RESAS), the Genomia Fund, part of the European Regional Development Fund with financial support of KWS SAAT SE and the Biotechnology and Biological Research Sciences Council (BBSRC: projects BB/G015244/1, BB/K018183/1, BB/L026880/1). PhD student D.T was funded on BBSRC CASE Award Agreement 3379_CRT, PhD student L.Y. was supported by funding from the China Scholarship Council (CSC).",
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Turnbull, D, Yang, L, Naqvi, S, Breen, S, Welsh, L, Stephens, J, Morris, J, Boevink, PC, Hedley, PE, Zhan, J, Birch, PRJ & Gilroy, EM 2017, 'RXLR Effector AVR2 Up-Regulates a Brassinosteroid-Responsive bHLH Transcription Factor to Suppress Immunity', Plant Physiology, vol. 174, no. 1, pp. 356-369. https://doi.org/10.1104/pp.16.01804

RXLR Effector AVR2 Up-Regulates a Brassinosteroid-Responsive bHLH Transcription Factor to Suppress Immunity. / Turnbull, Dionne; Yang, Lina; Naqvi, Shaista; Breen, Susan; Welsh, Lydia; Stephens, Jennifer; Morris, Jenny; Boevink, Petra C.; Hedley, Pete E.; Zhan, Jiasui; Birch, Paul R. J.; Gilroy, Eleanor M. (Lead / Corresponding author).

In: Plant Physiology, Vol. 174, No. 1, 05.2017, p. 356-369.

Research output: Contribution to journalArticle

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T1 - RXLR Effector AVR2 Up-Regulates a Brassinosteroid-Responsive bHLH Transcription Factor to Suppress Immunity

AU - Turnbull, Dionne

AU - Yang, Lina

AU - Naqvi, Shaista

AU - Breen, Susan

AU - Welsh, Lydia

AU - Stephens, Jennifer

AU - Morris, Jenny

AU - Boevink, Petra C.

AU - Hedley, Pete E.

AU - Zhan, Jiasui

AU - Birch, Paul R. J.

AU - Gilroy, Eleanor M.

N1 - This work was funded by the Scottish Government Rural and Environmental Science and Analytical Services Division (RESAS), the Genomia Fund, part of the European Regional Development Fund with financial support of KWS SAAT SE and the Biotechnology and Biological Research Sciences Council (BBSRC: projects BB/G015244/1, BB/K018183/1, BB/L026880/1). PhD student D.T was funded on BBSRC CASE Award Agreement 3379_CRT, PhD student L.Y. was supported by funding from the China Scholarship Council (CSC).

PY - 2017/5

Y1 - 2017/5

N2 - An emerging area in plant research focuses on antagonism between regulatory systems governing growth and immunity. Such crosstalk represents a point of vulnerability for pathogens to exploit. AVR2, an RXLR effector secreted by the potato blight pathogen Phytophthora infestans, interacts with potato BSL1, a putative phosphatase implicated in growth-promoting brassinosteroid (BR) hormone signalling. Transgenic potato (Solanum tuberosum) plants expressing the effector exhibit transcriptional and phenotypic hallmarks of over-active BR signalling, and show enhanced susceptibility to P. infestans. Microarray analysis was used to identify a set of BR-responsive marker genes in potato, all of which are constitutively expressed to BR-induced levels in AVR2 transgenic lines. One of these genes was a bHLH transcription factor, designated StCHL1, homologous to AtCIB1 and AtHBI1 which are known to facilitate antagonism between BR and immune responses. Transient expression of either AVR2 or CHL1 enhanced leaf colonisation by P. infestans and compromised immune cell death activated by perception of the elicitin INF1. Knockdown of CHL1 transcript using Virus-Induced Gene Silencing (VIGS) reduced colonisation of P. infestans on Nicotiana benthamiana. Moreover, the ability of AVR2 to suppress INF1-triggered cell death was attenuated in NbCHL1 silenced plants, indicating that NbCHL1 was important for this effector activity. Thus AVR2 exploits crosstalk between BR signalling and innate immunity in Solanum species, representing a novel, indirect mode of innate immune suppression by a filamentous pathogen effector.

AB - An emerging area in plant research focuses on antagonism between regulatory systems governing growth and immunity. Such crosstalk represents a point of vulnerability for pathogens to exploit. AVR2, an RXLR effector secreted by the potato blight pathogen Phytophthora infestans, interacts with potato BSL1, a putative phosphatase implicated in growth-promoting brassinosteroid (BR) hormone signalling. Transgenic potato (Solanum tuberosum) plants expressing the effector exhibit transcriptional and phenotypic hallmarks of over-active BR signalling, and show enhanced susceptibility to P. infestans. Microarray analysis was used to identify a set of BR-responsive marker genes in potato, all of which are constitutively expressed to BR-induced levels in AVR2 transgenic lines. One of these genes was a bHLH transcription factor, designated StCHL1, homologous to AtCIB1 and AtHBI1 which are known to facilitate antagonism between BR and immune responses. Transient expression of either AVR2 or CHL1 enhanced leaf colonisation by P. infestans and compromised immune cell death activated by perception of the elicitin INF1. Knockdown of CHL1 transcript using Virus-Induced Gene Silencing (VIGS) reduced colonisation of P. infestans on Nicotiana benthamiana. Moreover, the ability of AVR2 to suppress INF1-triggered cell death was attenuated in NbCHL1 silenced plants, indicating that NbCHL1 was important for this effector activity. Thus AVR2 exploits crosstalk between BR signalling and innate immunity in Solanum species, representing a novel, indirect mode of innate immune suppression by a filamentous pathogen effector.

KW - Journal article

U2 - 10.1104/pp.16.01804

DO - 10.1104/pp.16.01804

M3 - Article

VL - 174

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EP - 369

JO - Plant Physiology

JF - Plant Physiology

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