Phytophthora infestans RXLR effectors act in concert at diverse subcellular locations to enhance host colonization

Shumei Wang, Hazel McLellan, Tatyana Bukharova, Qin He, Fraser Murphy, Jiayang Shi, Shaohui Sun, Pauline van Weymers, Yajuan Ren, Gaetan Thilliez, Haixia Wang, Xinwei Chen, Stefan Engelhardt, Vivianne Vleeshouwers, Eleanor M Gilroy, Stephen C Whisson, Ingo Hein, Xiaodan Wang, Zhendong Tian, Paul R J Birch & 1 others Petra C Boevink

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Abstract

Oomycetes such as the potato blight pathogen Phytophthora infestans deliver RXLR effectors into plant cells to manipulate host processes and promote disease. Knowledge of where they localize inside host cells is important in understanding their function. Fifty-two P. infestans RXLR effectors (PiRXLRs) up-regulated during early stages of infection were expressed as fluorescent protein (FP) fusions inside cells of the model host Nicotiana benthamiana. FP-PiRXLR fusions were predominantly nucleo-cytoplasmic, nuclear, or plasma membrane-associated. Some also localized to the endoplasmic reticulum, mitochondria, peroxisomes, or microtubules, suggesting diverse sites of subcellular activity. Seven of the 25 PiRXLRs examined during infection accumulated at sites of haustorium penetration, probably due to co-localization with host target processes; Pi16663 (Avr1), for example, localized to Sec5-associated mobile bodies which showed perihaustorial accumulation. Forty-five FP-RXLR fusions enhanced pathogen leaf colonization when expressed in Nicotiana benthamiana, revealing that their presence was beneficial to infection. Co-expression of PiRXLRs that target and suppress different immune pathways resulted in an additive enhancement of colonization, indicating the potential to study effector combinations using transient expression assays. We provide a broad platform of high confidence P. infestans effector candidates from which to investigate the mechanisms, singly and in combination, by which this pathogen causes disease.

Original languageEnglish
Article numberery360
Pages (from-to)343-356
Number of pages14
JournalJournal of Experimental Botany
Volume70
Issue number1
Early online date16 Oct 2018
DOIs
Publication statusPublished - 1 Jan 2019

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Phytophthora infestans
Nicotiana benthamiana
Tobacco
pathogens
Infection
Cell Membrane
Oomycetes
infection
cell fusion
Proteins
Peroxisomes
Cell Fusion
Nuclear Envelope
nuclear membrane
Plant Cells
peroxisomes
Solanum tuberosum
blight
Microtubules
Endoplasmic Reticulum

Keywords

  • Avirulence
  • biotrophy
  • effector-triggered susceptibility
  • pathogenicity
  • Phytophthora
  • RXLR effector
  • virulence

Cite this

Wang, Shumei ; McLellan, Hazel ; Bukharova, Tatyana ; He, Qin ; Murphy, Fraser ; Shi, Jiayang ; Sun, Shaohui ; van Weymers, Pauline ; Ren, Yajuan ; Thilliez, Gaetan ; Wang, Haixia ; Chen, Xinwei ; Engelhardt, Stefan ; Vleeshouwers, Vivianne ; Gilroy, Eleanor M ; Whisson, Stephen C ; Hein, Ingo ; Wang, Xiaodan ; Tian, Zhendong ; Birch, Paul R J ; Boevink, Petra C. / Phytophthora infestans RXLR effectors act in concert at diverse subcellular locations to enhance host colonization. In: Journal of Experimental Botany. 2019 ; Vol. 70, No. 1. pp. 343-356.
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abstract = "Oomycetes such as the potato blight pathogen Phytophthora infestans deliver RXLR effectors into plant cells to manipulate host processes and promote disease. Knowledge of where they localize inside host cells is important in understanding their function. Fifty-two P. infestans RXLR effectors (PiRXLRs) up-regulated during early stages of infection were expressed as fluorescent protein (FP) fusions inside cells of the model host Nicotiana benthamiana. FP-PiRXLR fusions were predominantly nucleo-cytoplasmic, nuclear, or plasma membrane-associated. Some also localized to the endoplasmic reticulum, mitochondria, peroxisomes, or microtubules, suggesting diverse sites of subcellular activity. Seven of the 25 PiRXLRs examined during infection accumulated at sites of haustorium penetration, probably due to co-localization with host target processes; Pi16663 (Avr1), for example, localized to Sec5-associated mobile bodies which showed perihaustorial accumulation. Forty-five FP-RXLR fusions enhanced pathogen leaf colonization when expressed in Nicotiana benthamiana, revealing that their presence was beneficial to infection. Co-expression of PiRXLRs that target and suppress different immune pathways resulted in an additive enhancement of colonization, indicating the potential to study effector combinations using transient expression assays. We provide a broad platform of high confidence P. infestans effector candidates from which to investigate the mechanisms, singly and in combination, by which this pathogen causes disease.",
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author = "Shumei Wang and Hazel McLellan and Tatyana Bukharova and Qin He and Fraser Murphy and Jiayang Shi and Shaohui Sun and {van Weymers}, Pauline and Yajuan Ren and Gaetan Thilliez and Haixia Wang and Xinwei Chen and Stefan Engelhardt and Vivianne Vleeshouwers and Gilroy, {Eleanor M} and Whisson, {Stephen C} and Ingo Hein and Xiaodan Wang and Zhendong Tian and Birch, {Paul R J} and Boevink, {Petra C}",
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Wang, S, McLellan, H, Bukharova, T, He, Q, Murphy, F, Shi, J, Sun, S, van Weymers, P, Ren, Y, Thilliez, G, Wang, H, Chen, X, Engelhardt, S, Vleeshouwers, V, Gilroy, EM, Whisson, SC, Hein, I, Wang, X, Tian, Z, Birch, PRJ & Boevink, PC 2019, 'Phytophthora infestans RXLR effectors act in concert at diverse subcellular locations to enhance host colonization', Journal of Experimental Botany, vol. 70, no. 1, ery360, pp. 343-356. https://doi.org/10.1093/jxb/ery360

Phytophthora infestans RXLR effectors act in concert at diverse subcellular locations to enhance host colonization. / Wang, Shumei; McLellan, Hazel; Bukharova, Tatyana; He, Qin; Murphy, Fraser; Shi, Jiayang; Sun, Shaohui; van Weymers, Pauline; Ren, Yajuan; Thilliez, Gaetan; Wang, Haixia; Chen, Xinwei; Engelhardt, Stefan; Vleeshouwers, Vivianne; Gilroy, Eleanor M; Whisson, Stephen C; Hein, Ingo; Wang, Xiaodan; Tian, Zhendong; Birch, Paul R J; Boevink, Petra C (Lead / Corresponding author).

In: Journal of Experimental Botany, Vol. 70, No. 1, ery360, 01.01.2019, p. 343-356.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Phytophthora infestans RXLR effectors act in concert at diverse subcellular locations to enhance host colonization

AU - Wang, Shumei

AU - McLellan, Hazel

AU - Bukharova, Tatyana

AU - He, Qin

AU - Murphy, Fraser

AU - Shi, Jiayang

AU - Sun, Shaohui

AU - van Weymers, Pauline

AU - Ren, Yajuan

AU - Thilliez, Gaetan

AU - Wang, Haixia

AU - Chen, Xinwei

AU - Engelhardt, Stefan

AU - Vleeshouwers, Vivianne

AU - Gilroy, Eleanor M

AU - Whisson, Stephen C

AU - Hein, Ingo

AU - Wang, Xiaodan

AU - Tian, Zhendong

AU - Birch, Paul R J

AU - Boevink, Petra C

N1 - 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, BB/N009967/1), Scottish Government Rural and Environment Science and Analytical Services Division (RESAS), National Natural Science Foundation of China (31601600), China Postdoctoral Science Funding (2017M610214), The Fundamental Research Funds for the Central Universities (2662017PY069), Postdoctoral Funding of Heilongjiang Province (LBHZ16182), The Fundamental Research Funds for the Central Universities of China (Program No. 2662017PY069). S.W. and H.W were supported by funding from the China Scholarship Council (CSC)

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Oomycetes such as the potato blight pathogen Phytophthora infestans deliver RXLR effectors into plant cells to manipulate host processes and promote disease. Knowledge of where they localize inside host cells is important in understanding their function. Fifty-two P. infestans RXLR effectors (PiRXLRs) up-regulated during early stages of infection were expressed as fluorescent protein (FP) fusions inside cells of the model host Nicotiana benthamiana. FP-PiRXLR fusions were predominantly nucleo-cytoplasmic, nuclear, or plasma membrane-associated. Some also localized to the endoplasmic reticulum, mitochondria, peroxisomes, or microtubules, suggesting diverse sites of subcellular activity. Seven of the 25 PiRXLRs examined during infection accumulated at sites of haustorium penetration, probably due to co-localization with host target processes; Pi16663 (Avr1), for example, localized to Sec5-associated mobile bodies which showed perihaustorial accumulation. Forty-five FP-RXLR fusions enhanced pathogen leaf colonization when expressed in Nicotiana benthamiana, revealing that their presence was beneficial to infection. Co-expression of PiRXLRs that target and suppress different immune pathways resulted in an additive enhancement of colonization, indicating the potential to study effector combinations using transient expression assays. We provide a broad platform of high confidence P. infestans effector candidates from which to investigate the mechanisms, singly and in combination, by which this pathogen causes disease.

AB - Oomycetes such as the potato blight pathogen Phytophthora infestans deliver RXLR effectors into plant cells to manipulate host processes and promote disease. Knowledge of where they localize inside host cells is important in understanding their function. Fifty-two P. infestans RXLR effectors (PiRXLRs) up-regulated during early stages of infection were expressed as fluorescent protein (FP) fusions inside cells of the model host Nicotiana benthamiana. FP-PiRXLR fusions were predominantly nucleo-cytoplasmic, nuclear, or plasma membrane-associated. Some also localized to the endoplasmic reticulum, mitochondria, peroxisomes, or microtubules, suggesting diverse sites of subcellular activity. Seven of the 25 PiRXLRs examined during infection accumulated at sites of haustorium penetration, probably due to co-localization with host target processes; Pi16663 (Avr1), for example, localized to Sec5-associated mobile bodies which showed perihaustorial accumulation. Forty-five FP-RXLR fusions enhanced pathogen leaf colonization when expressed in Nicotiana benthamiana, revealing that their presence was beneficial to infection. Co-expression of PiRXLRs that target and suppress different immune pathways resulted in an additive enhancement of colonization, indicating the potential to study effector combinations using transient expression assays. We provide a broad platform of high confidence P. infestans effector candidates from which to investigate the mechanisms, singly and in combination, by which this pathogen causes disease.

KW - Avirulence

KW - biotrophy

KW - effector-triggered susceptibility

KW - pathogenicity

KW - Phytophthora

KW - RXLR effector

KW - virulence

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