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An oomycete effector protein induces shade avoidance in Arabidopsis and attenuates salicylate signaling by binding to host proteins of the RADICAL-INDUCED CELL DEATH1 family

View ORCID ProfileLennart Wirthmueller, View ORCID ProfileShuta Asai, View ORCID ProfileGhanasyam Rallapalli, Jan Sklenar, Georgina Fabro, View ORCID ProfileDae Sung Kim, Ruth Lintermann, Pinja Jaspers, View ORCID ProfileMichael Wrzaczek, View ORCID ProfileJaakko Kangasjärvi, View ORCID ProfileDaniel MacLean, View ORCID ProfileFrank L. H. Menke, View ORCID ProfileMark J. Banfield, View ORCID ProfileJonathan D. G. Jones
doi: https://doi.org/10.1101/137844
Lennart Wirthmueller
1The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom
2Dahlem Centre of Plant Sciences, Department of Plant Physiology and Biochemistry, Freie Universität Berlin, Königin-Luise-Straβe 12-16, 14195 Berlin, Germany
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  • ORCID record for Lennart Wirthmueller
  • For correspondence: lennart.wirthmueller@fu-berlin.de jonathan.jones@tsl.ac.uk
Shuta Asai
1The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom
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Ghanasyam Rallapalli
1The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom
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Jan Sklenar
1The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom
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Georgina Fabro
1The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom
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Dae Sung Kim
1The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom
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Ruth Lintermann
2Dahlem Centre of Plant Sciences, Department of Plant Physiology and Biochemistry, Freie Universität Berlin, Königin-Luise-Straβe 12-16, 14195 Berlin, Germany
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Pinja Jaspers
3Division of Plant Biology, Department of Biosciences, University of Helsinki, FIN-00014 Helsinki, Finland
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Michael Wrzaczek
3Division of Plant Biology, Department of Biosciences, University of Helsinki, FIN-00014 Helsinki, Finland
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  • ORCID record for Michael Wrzaczek
Jaakko Kangasjärvi
3Division of Plant Biology, Department of Biosciences, University of Helsinki, FIN-00014 Helsinki, Finland
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  • ORCID record for Jaakko Kangasjärvi
Daniel MacLean
1The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom
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  • ORCID record for Daniel MacLean
Frank L. H. Menke
1The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom
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Mark J. Banfield
4Department of Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom
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Jonathan D. G. Jones
1The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom
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  • ORCID record for Jonathan D. G. Jones
  • For correspondence: lennart.wirthmueller@fu-berlin.de jonathan.jones@tsl.ac.uk
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Abstract

The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. During infection, Hpa like other biotrophic pathogens, suppresses activation of plant innate immunity by translocating effector proteins into host cells. Some of these effectors localize to the host cell nucleus where they may manipulate transcriptional reprogramming of plant defense genes. Here we report that the nuclear-localized Hpa effector HaRxL106, when expressed in Arabidopsis, induces shade avoidance and attenuates the transcriptional response to the defense signaling molecule salicylic acid. HaRxL106 interacts with RADICAL-INDUCED CELL DEATH1 (RCD1) and loss of RCD1 function renders Arabidopsis resilient against HaRxL106-mediated suppression of immunity. To further characterize the molecular functions of RCD1 we solved a crystal structure of RCD1’s Poly-(ADP-ribose)-Polymerase (PARP) domain and, based on non-conservation of amino acids constituting the active site of canonical PARPs, conclude that RCD1 has no PARP activity. We report that RCD1-type proteins are phosphorylated and identified histone-modifying Mut9-like kinases (MLKs) as RCD1-interacting proteins. A mlk1,3,4 triple mutant exhibits stronger SA-induced defense marker gene expression compared to wild-type plants. Our data suggest that HaRxL106 suppresses Arabidopsis innate immunity by manipulating the function(s) of RCD1 in the host cell nucleus and point towards a role of RCD1 as a transcriptional co-regulator that integrates signals from light and pathogen sensors.

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Posted May 14, 2017.
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An oomycete effector protein induces shade avoidance in Arabidopsis and attenuates salicylate signaling by binding to host proteins of the RADICAL-INDUCED CELL DEATH1 family
Lennart Wirthmueller, Shuta Asai, Ghanasyam Rallapalli, Jan Sklenar, Georgina Fabro, Dae Sung Kim, Ruth Lintermann, Pinja Jaspers, Michael Wrzaczek, Jaakko Kangasjärvi, Daniel MacLean, Frank L. H. Menke, Mark J. Banfield, Jonathan D. G. Jones
bioRxiv 137844; doi: https://doi.org/10.1101/137844
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An oomycete effector protein induces shade avoidance in Arabidopsis and attenuates salicylate signaling by binding to host proteins of the RADICAL-INDUCED CELL DEATH1 family
Lennart Wirthmueller, Shuta Asai, Ghanasyam Rallapalli, Jan Sklenar, Georgina Fabro, Dae Sung Kim, Ruth Lintermann, Pinja Jaspers, Michael Wrzaczek, Jaakko Kangasjärvi, Daniel MacLean, Frank L. H. Menke, Mark J. Banfield, Jonathan D. G. Jones
bioRxiv 137844; doi: https://doi.org/10.1101/137844

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