The Potato MAP3K StVIK Is Required for the Phytophthora infestans RXLR Effector Pi17316 to Promote Disease

Fraser Murphy, Qin He, Miles Armstrong, Licida M. Giuliani, Petra C. Boevink, Wei Zhang, Zhendong Tian, Paul R. J. Birch (Lead / Corresponding author), Eleanor M. Gilroy (Lead / Corresponding author)

Research output: Contribution to journalArticle

14 Citations (Scopus)
99 Downloads (Pure)

Abstract

Plant pathogens deliver effectors to manipulate processes in their hosts, creating an environment for disease. Yet little is known about the host proteins that are targeted by effectors from filamentous pathogens. We show that both stable transgenic expression in potato and transient expression in Nicotiana benthamiana of the RXLR effector Pi17316 enhance leaf colonization by the late blight pathogen Phytophthora infestans. Expression of Pi17316 also attenuates cell death triggered by the pathogen-associated molecular pattern INF1, indicating that the effector suppresses pattern-triggered immunity. However, this effector does not attenuate cell death triggered by CF4/AVR4, Rx/PVX-CP or R3a/AVR3a, showing that it specifically suppresses INF1-triggered cell death (ICD). Pi17316 interacts directly in yeast two-hybrid assays with the potato (Solanum tuberosum) orthologue of BRL2/VH1-interacting kinase (StVIK), encoding a predicted mitogen-activated protein kinase kinase kinase (MAP3K). Interaction in planta was confirmed by co-immunoprecipitation and demonstrated to occur at the plant plasma membrane. Virus-induced gene silencing (VIGS) of VIK in N. benthamiana attenuated P. infestans colonization, whereas transient overexpression of StVIK enhanced P. infestans colonization, indicating that this host protein acts as a susceptibility (S) factor. Moreover, VIK overexpression specifically attenuated ICD, indicating it is a negative regulator of immunity. The abilities of Pi17316 to enhance P. infestans colonization or suppress ICD were significantly compromised in NbVIK-silenced plants, demonstrating that Pi17316 effector activity is mediated by this MAP3K. Thus, StVIK is exploited by P. infestans as an S factor to promote late blight disease.
Original languageEnglish
Pages (from-to)398-410
Number of pages13
JournalPlant Physiology
Volume177
Issue number1
Early online date27 Mar 2018
DOIs
Publication statusPublished - May 2018

Fingerprint

Phytophthora infestans
mitogen-activated protein kinase kinase kinase
Solanum tuberosum
phosphotransferases (kinases)
Cell Death
Phosphotransferases
potatoes
cell death
Immunity
Nicotiana benthamiana
MAP Kinase Kinase Kinases
pathogens
Two-Hybrid System Techniques
immunity
Gene Silencing
Immunoprecipitation
Tobacco
two hybrid system techniques
Proteins
gene silencing

Cite this

Murphy, F., He, Q., Armstrong, M., Giuliani, L. M., Boevink, P. C., Zhang, W., ... Gilroy, E. M. (2018). The Potato MAP3K StVIK Is Required for the Phytophthora infestans RXLR Effector Pi17316 to Promote Disease. Plant Physiology, 177(1), 398-410. https://doi.org/10.1104/pp.18.00028
Murphy, Fraser ; He, Qin ; Armstrong, Miles ; Giuliani, Licida M. ; Boevink, Petra C. ; Zhang, Wei ; Tian, Zhendong ; Birch, Paul R. J. ; Gilroy, Eleanor M. / The Potato MAP3K StVIK Is Required for the Phytophthora infestans RXLR Effector Pi17316 to Promote Disease. In: Plant Physiology. 2018 ; Vol. 177, No. 1. pp. 398-410.
@article{5a5bdadc71c645e19da3113783053a27,
title = "The Potato MAP3K StVIK Is Required for the Phytophthora infestans RXLR Effector Pi17316 to Promote Disease",
abstract = "Plant pathogens deliver effectors to manipulate processes in their hosts, creating an environment for disease. Yet little is known about the host proteins that are targeted by effectors from filamentous pathogens. We show that both stable transgenic expression in potato and transient expression in Nicotiana benthamiana of the RXLR effector Pi17316 enhance leaf colonization by the late blight pathogen Phytophthora infestans. Expression of Pi17316 also attenuates cell death triggered by the pathogen-associated molecular pattern INF1, indicating that the effector suppresses pattern-triggered immunity. However, this effector does not attenuate cell death triggered by CF4/AVR4, Rx/PVX-CP or R3a/AVR3a, showing that it specifically suppresses INF1-triggered cell death (ICD). Pi17316 interacts directly in yeast two-hybrid assays with the potato (Solanum tuberosum) orthologue of BRL2/VH1-interacting kinase (StVIK), encoding a predicted mitogen-activated protein kinase kinase kinase (MAP3K). Interaction in planta was confirmed by co-immunoprecipitation and demonstrated to occur at the plant plasma membrane. Virus-induced gene silencing (VIGS) of VIK in N. benthamiana attenuated P. infestans colonization, whereas transient overexpression of StVIK enhanced P. infestans colonization, indicating that this host protein acts as a susceptibility (S) factor. Moreover, VIK overexpression specifically attenuated ICD, indicating it is a negative regulator of immunity. The abilities of Pi17316 to enhance P. infestans colonization or suppress ICD were significantly compromised in NbVIK-silenced plants, demonstrating that Pi17316 effector activity is mediated by this MAP3K. Thus, StVIK is exploited by P. infestans as an S factor to promote late blight disease.",
author = "Fraser Murphy and Qin He and Miles Armstrong and Giuliani, {Licida M.} and Boevink, {Petra C.} and Wei Zhang and Zhendong Tian and Birch, {Paul R. J.} and Gilroy, {Eleanor M.}",
note = "We thank Professor Mark Banfield (John Innes Centre), and members of the Dundee Effector Consortium (particularly Piers Hemsley and Sebastian Eves van den Akker) for helpful discussions during this work. We are grateful for financial support from the Biotechnology and Biological Sciences Research Council (BBSRC) (grants BB/G015244/1, BB/K018183/1, BB/L026880/1) for PRJB and QH, the BBSRC doctoral training programme EASTBIO for funding FM, Scottish Government Rural and Environment Science and Analytical Services Division (RESAS) for funding EG, PCB and PRJB, and The Fundamental Research Funds for the Central Universities, Grant no. 2662017PY069, for funding potato transformation work in ZT’s lab.",
year = "2018",
month = "5",
doi = "10.1104/pp.18.00028",
language = "English",
volume = "177",
pages = "398--410",
journal = "Plant Physiology",
issn = "0032-0889",
publisher = "American Society of Plant Biologists",
number = "1",

}

Murphy, F, He, Q, Armstrong, M, Giuliani, LM, Boevink, PC, Zhang, W, Tian, Z, Birch, PRJ & Gilroy, EM 2018, 'The Potato MAP3K StVIK Is Required for the Phytophthora infestans RXLR Effector Pi17316 to Promote Disease', Plant Physiology, vol. 177, no. 1, pp. 398-410. https://doi.org/10.1104/pp.18.00028

The Potato MAP3K StVIK Is Required for the Phytophthora infestans RXLR Effector Pi17316 to Promote Disease. / Murphy, Fraser; He, Qin; Armstrong, Miles; Giuliani, Licida M.; Boevink, Petra C.; Zhang, Wei; Tian, Zhendong; Birch, Paul R. J. (Lead / Corresponding author); Gilroy, Eleanor M. (Lead / Corresponding author).

In: Plant Physiology, Vol. 177, No. 1, 05.2018, p. 398-410.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The Potato MAP3K StVIK Is Required for the Phytophthora infestans RXLR Effector Pi17316 to Promote Disease

AU - Murphy, Fraser

AU - He, Qin

AU - Armstrong, Miles

AU - Giuliani, Licida M.

AU - Boevink, Petra C.

AU - Zhang, Wei

AU - Tian, Zhendong

AU - Birch, Paul R. J.

AU - Gilroy, Eleanor M.

N1 - We thank Professor Mark Banfield (John Innes Centre), and members of the Dundee Effector Consortium (particularly Piers Hemsley and Sebastian Eves van den Akker) for helpful discussions during this work. We are grateful for financial support from the Biotechnology and Biological Sciences Research Council (BBSRC) (grants BB/G015244/1, BB/K018183/1, BB/L026880/1) for PRJB and QH, the BBSRC doctoral training programme EASTBIO for funding FM, Scottish Government Rural and Environment Science and Analytical Services Division (RESAS) for funding EG, PCB and PRJB, and The Fundamental Research Funds for the Central Universities, Grant no. 2662017PY069, for funding potato transformation work in ZT’s lab.

PY - 2018/5

Y1 - 2018/5

N2 - Plant pathogens deliver effectors to manipulate processes in their hosts, creating an environment for disease. Yet little is known about the host proteins that are targeted by effectors from filamentous pathogens. We show that both stable transgenic expression in potato and transient expression in Nicotiana benthamiana of the RXLR effector Pi17316 enhance leaf colonization by the late blight pathogen Phytophthora infestans. Expression of Pi17316 also attenuates cell death triggered by the pathogen-associated molecular pattern INF1, indicating that the effector suppresses pattern-triggered immunity. However, this effector does not attenuate cell death triggered by CF4/AVR4, Rx/PVX-CP or R3a/AVR3a, showing that it specifically suppresses INF1-triggered cell death (ICD). Pi17316 interacts directly in yeast two-hybrid assays with the potato (Solanum tuberosum) orthologue of BRL2/VH1-interacting kinase (StVIK), encoding a predicted mitogen-activated protein kinase kinase kinase (MAP3K). Interaction in planta was confirmed by co-immunoprecipitation and demonstrated to occur at the plant plasma membrane. Virus-induced gene silencing (VIGS) of VIK in N. benthamiana attenuated P. infestans colonization, whereas transient overexpression of StVIK enhanced P. infestans colonization, indicating that this host protein acts as a susceptibility (S) factor. Moreover, VIK overexpression specifically attenuated ICD, indicating it is a negative regulator of immunity. The abilities of Pi17316 to enhance P. infestans colonization or suppress ICD were significantly compromised in NbVIK-silenced plants, demonstrating that Pi17316 effector activity is mediated by this MAP3K. Thus, StVIK is exploited by P. infestans as an S factor to promote late blight disease.

AB - Plant pathogens deliver effectors to manipulate processes in their hosts, creating an environment for disease. Yet little is known about the host proteins that are targeted by effectors from filamentous pathogens. We show that both stable transgenic expression in potato and transient expression in Nicotiana benthamiana of the RXLR effector Pi17316 enhance leaf colonization by the late blight pathogen Phytophthora infestans. Expression of Pi17316 also attenuates cell death triggered by the pathogen-associated molecular pattern INF1, indicating that the effector suppresses pattern-triggered immunity. However, this effector does not attenuate cell death triggered by CF4/AVR4, Rx/PVX-CP or R3a/AVR3a, showing that it specifically suppresses INF1-triggered cell death (ICD). Pi17316 interacts directly in yeast two-hybrid assays with the potato (Solanum tuberosum) orthologue of BRL2/VH1-interacting kinase (StVIK), encoding a predicted mitogen-activated protein kinase kinase kinase (MAP3K). Interaction in planta was confirmed by co-immunoprecipitation and demonstrated to occur at the plant plasma membrane. Virus-induced gene silencing (VIGS) of VIK in N. benthamiana attenuated P. infestans colonization, whereas transient overexpression of StVIK enhanced P. infestans colonization, indicating that this host protein acts as a susceptibility (S) factor. Moreover, VIK overexpression specifically attenuated ICD, indicating it is a negative regulator of immunity. The abilities of Pi17316 to enhance P. infestans colonization or suppress ICD were significantly compromised in NbVIK-silenced plants, demonstrating that Pi17316 effector activity is mediated by this MAP3K. Thus, StVIK is exploited by P. infestans as an S factor to promote late blight disease.

U2 - 10.1104/pp.18.00028

DO - 10.1104/pp.18.00028

M3 - Article

C2 - 29588335

VL - 177

SP - 398

EP - 410

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 1

ER -