Phytophthora infestans RXLR effectors target parallel steps in an immune signal transduction pathway

Yajuan Ren, Miles Armstrong, Yetong Qi, Hazel McLellan, Cheng Zhong, Bowen Du, Paul R. J. Birch, Zhendong Tian

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Abstract

The potato ( Solanum tuberosum) blight pathogen Phytophthora infestans delivers Arg-X-Leu-Arg (RXLR) effector proteins into host cells to subvert plant immune responses and promote colonization. We show that transient expression and stable transgenic expression of the RXLR effector Pi22926 in Nicotiana benthamiana promotes leaf colonization by P. infestans. Pi22926 suppresses cell death triggered by coexpression of the Cladosporium fulvum avirulence protein Avr4 and the tomato ( Solanum lycopersicum) resistance protein Cf4. Pi22926 interacts with a potato mitogen-activated protein kinase kinase kinase, StMAP3Kβ2, in the nucleoplasm. Virus-induced gene silencing (VIGS) of the ortholog NbMAP3Kβ2 in N. benthamiana enhances P. infestans colonization and attenuates Cf4/Avr4-induced cell death, indicating that this host protein is a positive regulator of immunity. Cell death induced by Cf4/Avr4 is dependent on NbMAP3Kε and NbMAP3Kβ2, indicating that these MAP3Ks function in the same signaling pathway. VIGS of NbMAP3Kβ2 does not compromise cell death triggered by overexpression of MAP3Kε. Similarly, VIGS of NbMAP3Kε does not attenuate cell death triggered by MAP3Kβ2, demonstrating that these MAP3K proteins function in parallel. In agreement, Pi22926 or another RXLR effector, PexRD2, only suppresses cell death triggered by expression of StMAP3Kβ2 or StMAP3Kε, respectively. Our data reveal that two P. infestans effectors, PexRD2 and Pi22926, promote P. infestans colonization by targeting MAP3K proteins that act in parallel in the same signal transduction pathway.

Original languageEnglish
Pages (from-to)2227-2239
Number of pages13
JournalPlant Physiology
Volume180
Issue number4
Early online date19 Jun 2019
DOIs
Publication statusPublished - Aug 2019

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Phytophthora infestans
mitogen-activated protein kinase kinase kinase
signal transduction
cell death
Signal Transduction
Cell Death
Gene Silencing
gene silencing
Solanum tuberosum
proteins
Nicotiana benthamiana
Lycopersicon esculentum
Viruses
Proteins
viruses
leucylarginine
Plant Immunity
potatoes
Passalora fulva
MAP Kinase Kinase Kinases

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Ren, Yajuan ; Armstrong, Miles ; Qi, Yetong ; McLellan, Hazel ; Zhong, Cheng ; Du, Bowen ; Birch, Paul R. J. ; Tian, Zhendong. / Phytophthora infestans RXLR effectors target parallel steps in an immune signal transduction pathway. In: Plant Physiology. 2019 ; Vol. 180, No. 4. pp. 2227-2239.
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title = "Phytophthora infestans RXLR effectors target parallel steps in an immune signal transduction pathway",
abstract = "The potato ( Solanum tuberosum) blight pathogen Phytophthora infestans delivers Arg-X-Leu-Arg (RXLR) effector proteins into host cells to subvert plant immune responses and promote colonization. We show that transient expression and stable transgenic expression of the RXLR effector Pi22926 in Nicotiana benthamiana promotes leaf colonization by P. infestans. Pi22926 suppresses cell death triggered by coexpression of the Cladosporium fulvum avirulence protein Avr4 and the tomato ( Solanum lycopersicum) resistance protein Cf4. Pi22926 interacts with a potato mitogen-activated protein kinase kinase kinase, StMAP3Kβ2, in the nucleoplasm. Virus-induced gene silencing (VIGS) of the ortholog NbMAP3Kβ2 in N. benthamiana enhances P. infestans colonization and attenuates Cf4/Avr4-induced cell death, indicating that this host protein is a positive regulator of immunity. Cell death induced by Cf4/Avr4 is dependent on NbMAP3Kε and NbMAP3Kβ2, indicating that these MAP3Ks function in the same signaling pathway. VIGS of NbMAP3Kβ2 does not compromise cell death triggered by overexpression of MAP3Kε. Similarly, VIGS of NbMAP3Kε does not attenuate cell death triggered by MAP3Kβ2, demonstrating that these MAP3K proteins function in parallel. In agreement, Pi22926 or another RXLR effector, PexRD2, only suppresses cell death triggered by expression of StMAP3Kβ2 or StMAP3Kε, respectively. Our data reveal that two P. infestans effectors, PexRD2 and Pi22926, promote P. infestans colonization by targeting MAP3K proteins that act in parallel in the same signal transduction pathway.",
author = "Yajuan Ren and Miles Armstrong and Yetong Qi and Hazel McLellan and Cheng Zhong and Bowen Du and Birch, {Paul R. J.} and Zhendong Tian",
note = "Funding: National Natural Science Foundation of China (NSFC) 31761143007, 31471550 Zhendong Tian; The Fundamental Research Funds for the Central Universities of China 2662017PY069 Zhendong Tian; Biotechnology and Biological Sciences Research Council (BBSRC) BB/G015244/1,BB/K018183/1,BB/L026880/1 Paul R. J. Birch; The Scottish Government Rural and Environment Sciences and Anlytical Services Division Paul R. J. Birch",
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Phytophthora infestans RXLR effectors target parallel steps in an immune signal transduction pathway. / Ren, Yajuan; Armstrong, Miles; Qi, Yetong; McLellan, Hazel; Zhong, Cheng; Du, Bowen; Birch, Paul R. J.; Tian, Zhendong.

In: Plant Physiology, Vol. 180, No. 4, 08.2019, p. 2227-2239.

Research output: Contribution to journalArticle

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T1 - Phytophthora infestans RXLR effectors target parallel steps in an immune signal transduction pathway

AU - Ren, Yajuan

AU - Armstrong, Miles

AU - Qi, Yetong

AU - McLellan, Hazel

AU - Zhong, Cheng

AU - Du, Bowen

AU - Birch, Paul R. J.

AU - Tian, Zhendong

N1 - Funding: National Natural Science Foundation of China (NSFC) 31761143007, 31471550 Zhendong Tian; The Fundamental Research Funds for the Central Universities of China 2662017PY069 Zhendong Tian; Biotechnology and Biological Sciences Research Council (BBSRC) BB/G015244/1,BB/K018183/1,BB/L026880/1 Paul R. J. Birch; The Scottish Government Rural and Environment Sciences and Anlytical Services Division Paul R. J. Birch

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N2 - The potato ( Solanum tuberosum) blight pathogen Phytophthora infestans delivers Arg-X-Leu-Arg (RXLR) effector proteins into host cells to subvert plant immune responses and promote colonization. We show that transient expression and stable transgenic expression of the RXLR effector Pi22926 in Nicotiana benthamiana promotes leaf colonization by P. infestans. Pi22926 suppresses cell death triggered by coexpression of the Cladosporium fulvum avirulence protein Avr4 and the tomato ( Solanum lycopersicum) resistance protein Cf4. Pi22926 interacts with a potato mitogen-activated protein kinase kinase kinase, StMAP3Kβ2, in the nucleoplasm. Virus-induced gene silencing (VIGS) of the ortholog NbMAP3Kβ2 in N. benthamiana enhances P. infestans colonization and attenuates Cf4/Avr4-induced cell death, indicating that this host protein is a positive regulator of immunity. Cell death induced by Cf4/Avr4 is dependent on NbMAP3Kε and NbMAP3Kβ2, indicating that these MAP3Ks function in the same signaling pathway. VIGS of NbMAP3Kβ2 does not compromise cell death triggered by overexpression of MAP3Kε. Similarly, VIGS of NbMAP3Kε does not attenuate cell death triggered by MAP3Kβ2, demonstrating that these MAP3K proteins function in parallel. In agreement, Pi22926 or another RXLR effector, PexRD2, only suppresses cell death triggered by expression of StMAP3Kβ2 or StMAP3Kε, respectively. Our data reveal that two P. infestans effectors, PexRD2 and Pi22926, promote P. infestans colonization by targeting MAP3K proteins that act in parallel in the same signal transduction pathway.

AB - The potato ( Solanum tuberosum) blight pathogen Phytophthora infestans delivers Arg-X-Leu-Arg (RXLR) effector proteins into host cells to subvert plant immune responses and promote colonization. We show that transient expression and stable transgenic expression of the RXLR effector Pi22926 in Nicotiana benthamiana promotes leaf colonization by P. infestans. Pi22926 suppresses cell death triggered by coexpression of the Cladosporium fulvum avirulence protein Avr4 and the tomato ( Solanum lycopersicum) resistance protein Cf4. Pi22926 interacts with a potato mitogen-activated protein kinase kinase kinase, StMAP3Kβ2, in the nucleoplasm. Virus-induced gene silencing (VIGS) of the ortholog NbMAP3Kβ2 in N. benthamiana enhances P. infestans colonization and attenuates Cf4/Avr4-induced cell death, indicating that this host protein is a positive regulator of immunity. Cell death induced by Cf4/Avr4 is dependent on NbMAP3Kε and NbMAP3Kβ2, indicating that these MAP3Ks function in the same signaling pathway. VIGS of NbMAP3Kβ2 does not compromise cell death triggered by overexpression of MAP3Kε. Similarly, VIGS of NbMAP3Kε does not attenuate cell death triggered by MAP3Kβ2, demonstrating that these MAP3K proteins function in parallel. In agreement, Pi22926 or another RXLR effector, PexRD2, only suppresses cell death triggered by expression of StMAP3Kβ2 or StMAP3Kε, respectively. Our data reveal that two P. infestans effectors, PexRD2 and Pi22926, promote P. infestans colonization by targeting MAP3K proteins that act in parallel in the same signal transduction pathway.

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DO - 10.1104/pp.18.00625

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