Functionally redundant RXLR effectors from Phytophthora infestans act at different steps to suppress early flg22-triggered immunity.
Genome sequences of several economically important phytopathogenic oomycetes have revealed the presence of large families of so-called RXLR effectors. Functional screens have identified RXLR effector repertoires that either compromise or induce plant defense responses. However, limited information is available about the molecular mechanisms underlying the modes of action of these effectors in planta. The perception of highly conserved pathogen- or microbe-associated molecular patterns (PAMPs/MAMPs), such as flg22, triggers converging signaling pathways recruiting MAP kinase cascades and inducing transcriptional re-programming, yielding a generic anti-microbial response. We used a highly synchronizable, pathogen-free protoplast-based assay to identify a set of RXLR effectors from Phytophthora infestans (PiRXLRs), the causal agent of potato and tomato light blight that manipulate early stages of flg22-triggered signaling. Of thirty-three tested PiRXLR effector candidates, eight, called Suppressor of early Flg22-induced Immune response (SFI), significantly suppressed flg22-dependent activation of a reporter gene under control of a typical MAMP-inducible promoter (pFRK1-Luc) in tomato protoplasts. We extended our analysis to Arabidopsis thaliana, a non-host plant species of P. infestans. From the aforementioned eight SFI effectors, three appeared to share similar functions in both Arabidopsis and tomato by suppressing transcriptional activation of flg22-induced marker genes downstream of post-translational MAP kinase activation. A further three effectors interfere with MAMP signaling at, or upstream of, the MAP kinase cascade in tomato, but not in Arabidopsis. Transient expression of the SFI effectors in Nicotiana benthamiana enhances susceptibility to P. infestans and, for the most potent effector, SFI1, nuclear localization is required for both suppression of MAMP signaling and virulence function. The present study provides a framework to decipher the molecular mechanisms underlying the manipulation of host MAMP-triggered immunity (MTI) by P. infestans and to understand the basis of host versus non-host resistance in plants towards P. infestans.
Department of Biochemistry, Centre for Plant Molecular Biology, Eberhard Karls University, Tübingen, Germany.
Xiangzi
X
Zheng
Division of Plant Sciences, University of Dundee (at James Hutton Institute), Invergowrie, Dundee, United Kingdom.
Hazel
H
McLellan
Department of Biochemistry, Centre for Plant Molecular Biology, Eberhard Karls University, Tübingen, Germany.
Malou
M
Fraiture
Department of Biochemistry, Centre for Plant Molecular Biology, Eberhard Karls University, Tübingen, Germany.
Xiaoyu
X
Liu
Cell and Molecular Sciences, The James Hutton Institute, University of Dundee, Invergowrie, Dundee, United Kingdom.
Petra C
PC
Boevink
Cell and Molecular Sciences, The James Hutton Institute, University of Dundee, Invergowrie, Dundee, United Kingdom.
Eleanor M
EM
Gilroy
Department of Biochemistry, Centre for Plant Molecular Biology, Eberhard Karls University, Tübingen, Germany.
Ying
Y
Chen
Division of Plant Sciences, University of Dundee (at James Hutton Institute), Invergowrie, Dundee, United Kingdom.
Kabindra
K
Kandel
Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel Aviv, Israel.
Guido
G
Sessa
Division of Plant Sciences, University of Dundee (at James Hutton Institute), Invergowrie, Dundee, United Kingdom; Cell and Molecular Sciences, The James Hutton Institute, University of Dundee, Invergowrie, Dundee, United Kingdom.
Paul R J
PR
Birch
Department of Biochemistry, Centre for Plant Molecular Biology, Eberhard Karls University, Tübingen, Germany.
Frédéric
F
Brunner
D017360:Arabidopsis / Q000235:genetics / Q000276:immunology* / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000276:immunology*; D018551:Solanum lycopersicum / Q000276:immunology / Q000382:microbiology; D020935:MAP Kinase Signaling System / Q000502:physiology*; D020929:Mitogen-Activated Protein Kinase Kinases / Q000235:genetics / Q000276:immunology*; D010455:Peptides / Q000235:genetics / Q000276:immunology*; D055750:Phytophthora infestans / Q000235:genetics / Q000276:immunology*; D057865:Plant Immunity / Q000502:physiology*
D029681:Arabidopsis Proteins; D010455:Peptides; D020929:Mitogen-Activated Protein Kinase Kinases