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Research ArticleResearch Article
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The Magnaporthe oryzae Effector AvrPiz-t Targets the RING E3 Ubiquitin Ligase APIP6 to Suppress Pathogen-Associated Molecular Pattern–Triggered Immunity in Rice

Chan-Ho Park, Songbiao Chen, Gautam Shirsekar, Bo Zhou, Chang Hyun Khang, Pattavipha Songkumarn, Ahmed J. Afzal, Yuese Ning, Ruyi Wang, Maria Bellizzi, Barbara Valent, Guo-Liang Wang
Chan-Ho Park
aDepartment of Plant Pathology, Ohio State University, Columbus, OH 43210
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Songbiao Chen
aDepartment of Plant Pathology, Ohio State University, Columbus, OH 43210
bState Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
cBiotechnology Research Institute, Fujian Academy of Agricultural Sciences, Fuzhou, Fujian 350003, China
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Gautam Shirsekar
aDepartment of Plant Pathology, Ohio State University, Columbus, OH 43210
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Bo Zhou
dState Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, 310021 China
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Chang Hyun Khang
eDepartment of Plant Pathology, Kansas State University, Manhattan, KS, 66506
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Pattavipha Songkumarn
aDepartment of Plant Pathology, Ohio State University, Columbus, OH 43210
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Ahmed J. Afzal
fDepartment of Horticulture and Crop Science, Ohio State University, Columbus, OH 43210
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Yuese Ning
bState Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Ruyi Wang
bState Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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Maria Bellizzi
aDepartment of Plant Pathology, Ohio State University, Columbus, OH 43210
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Barbara Valent
eDepartment of Plant Pathology, Kansas State University, Manhattan, KS, 66506
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Guo-Liang Wang
aDepartment of Plant Pathology, Ohio State University, Columbus, OH 43210
bState Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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  • For correspondence: wang.620@osu.edu

Published November 2012. DOI: https://doi.org/10.1105/tpc.112.105429

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  • © 2012 American Society of Plant Biologists. All rights reserved.

Abstract

Although the functions of a few effector proteins produced by bacterial and oomycete plant pathogens have been elucidated in recent years, information for the vast majority of pathogen effectors is still lacking, particularly for those of plant-pathogenic fungi. Here, we show that the avirulence effector AvrPiz-t from the rice blast fungus Magnaporthe oryzae preferentially accumulates in the specialized structure called the biotrophic interfacial complex and is then translocated into rice (Oryza sativa) cells. Ectopic expression of AvrPiz-t in transgenic rice suppresses the flg22- and chitin-induced generation of reactive oxygen species (ROS) and enhances susceptibility to M. oryzae, indicating that AvrPiz-t functions to suppress pathogen-associated molecular pattern (PAMP)-triggered immunity in rice. Interaction assays show that AvrPiz-t suppresses the ubiquitin ligase activity of the rice RING E3 ubiquitin ligase APIP6 and that, in return, APIP6 ubiquitinates AvrPiz-t in vitro. Interestingly, agroinfection assays reveal that AvrPiz-t and AvrPiz-t Interacting Protein 6 (APIP6) are both degraded when coexpressed in Nicotiana benthamiana. Silencing of APIP6 in transgenic rice leads to a significant reduction of flg22-induced ROS generation, suppression of defense-related gene expression, and enhanced susceptibility of rice plants to M. oryzae. Taken together, our results reveal a mechanism in which a fungal effector targets the host ubiquitin proteasome system for the suppression of PAMP-triggered immunity in plants.

  • Glossary

    PAMP
    pathogen-associated molecular pattern
    PRR
    pattern recognition receptor
    PTI
    PAMP-triggered immunity
    ROS
    reactive oxygen species
    ETI
    effector-triggered immunity
    HR
    hypersensitive response
    UPS
    ubiquitin proteasome system (
    NBS-LRR
    nucleotide binding site–Leu-rich repeat
    BIC
    biotrophic interface complex
    GFP
    green fluorescent protein
    NPB
    Nipponbare
    qPCR
    quantitative PCR
    qRT-PCR
    quantitative RT-PCR
    GST
    glutathione S-transferase
    DAI
    days after agroinfection
    Co-IP
    coimmunoprecipitation
    BiFC
    bimolecular fluorescence complementation
    RFP
    red fluorescent protein
    RNAi
    RNA interference
    TRD
    Toride
    CT
    cycle threshold
    • Received September 19, 2012.
    • Revised October 24, 2012.
    • Accepted November 8, 2012.
    • Published November 30, 2012.

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    The Magnaporthe oryzae Effector AvrPiz-t Targets the RING E3 Ubiquitin Ligase APIP6 to Suppress Pathogen-Associated Molecular Pattern–Triggered Immunity in Rice
    Chan-Ho Park, Songbiao Chen, Gautam Shirsekar, Bo Zhou, Chang Hyun Khang, Pattavipha Songkumarn, Ahmed J. Afzal, Yuese Ning, Ruyi Wang, Maria Bellizzi, Barbara Valent, Guo-Liang Wang
    The Plant Cell Nov 2012, 24 (11) 4748-4762; DOI: 10.1105/tpc.112.105429

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    The Magnaporthe oryzae Effector AvrPiz-t Targets the RING E3 Ubiquitin Ligase APIP6 to Suppress Pathogen-Associated Molecular Pattern–Triggered Immunity in Rice
    Chan-Ho Park, Songbiao Chen, Gautam Shirsekar, Bo Zhou, Chang Hyun Khang, Pattavipha Songkumarn, Ahmed J. Afzal, Yuese Ning, Ruyi Wang, Maria Bellizzi, Barbara Valent, Guo-Liang Wang
    The Plant Cell Nov 2012, 24 (11) 4748-4762; DOI: 10.1105/tpc.112.105429
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