The E3 Ligase APIP10 Connects the Effector AvrPiz-t to the NLR Receptor Piz-t in Rice

Although nucleotide-binding domain, leucine-rich repeat (NLR) proteins are the major immune receptors in plants, the mechanism that controls their activation and immune signaling remains elusive. Here, we report that the avirulence effector AvrPiz-t from Magnaporthe oryzae targets the rice E3 ligase...

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Published inPLoS pathogens Vol. 12; no. 3; p. e1005529
Main Authors Park, Chan Ho, Shirsekar, Gautam, Bellizzi, Maria, Chen, Songbiao, Songkumarn, Pattavipha, Xie, Xin, Shi, Xuetao, Ning, Yuese, Zhou, Bo, Suttiviriya, Pavinee, Wang, Mo, Umemura, Kenji, Wang, Guo-Liang
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.03.2016
Public Library of Science (PLoS)
Subjects
Apoptosis
Biology and Life Sciences
Cell death
Gene expression
Genomes
Health aspects
Infections
Ligases
Magnaporthe
NOD-like receptors
Oryza - enzymology
Oryza - microbiology
Pathogens
Physiological aspects
Plant Diseases - microbiology
Proteins
Research and Analysis Methods
Resistance to control
Rice
Ubiquitin-Protein Ligases - metabolism
Ubiquitination - immunology
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Abstract Although nucleotide-binding domain, leucine-rich repeat (NLR) proteins are the major immune receptors in plants, the mechanism that controls their activation and immune signaling remains elusive. Here, we report that the avirulence effector AvrPiz-t from Magnaporthe oryzae targets the rice E3 ligase APIP10 for degradation, but that APIP10, in return, ubiquitinates AvrPiz-t and thereby causes its degradation. Silencing of APIP10 in the non-Piz-t background compromises the basal defense against M. oryzae. Conversely, silencing of APIP10 in the Piz-t background causes cell death, significant accumulation of Piz-t, and enhanced resistance to M. oryzae, suggesting that APIP10 is a negative regulator of Piz-t. We show that APIP10 promotes degradation of Piz-t via the 26S proteasome system. Furthermore, we demonstrate that AvrPiz-t stabilizes Piz-t during M. oryzae infection. Together, our results show that APIP10 is a novel E3 ligase that functionally connects the fungal effector AvrPiz-t to its NLR receptor Piz-t in rice.
AbstractList   Although nucleotide-binding domain, leucine-rich repeat (NLR) proteins are the major immune receptors in plants, the mechanism that controls their activation and immune signaling remains elusive. Here, we report that the avirulence effector AvrPiz-t from Magnaporthe oryzae targets the rice E3 ligase APIP10 for degradation, but that APIP10, in return, ubiquitinates AvrPiz-t and thereby causes its degradation. Silencing of APIP10 in the non-Piz-t background compromises the basal defense against M. oryzae. Conversely, silencing of APIP10 in the Piz-t background causes cell death, significant accumulation of Piz-t, and enhanced resistance to M. oryzae, suggesting that APIP10 is a negative regulator of Piz-t. We show that APIP10 promotes degradation of Piz-t via the 26S proteasome system. Furthermore, we demonstrate that AvrPiz-t stabilizes Piz-t during M. oryzae infection. Together, our results show that APIP10 is a novel E3 ligase that functionally connects the fungal effector AvrPiz-t to its NLR receptor Piz-t in rice.
Although nucleotide-binding domain, leucine-rich repeat (NLR) proteins are the major immune receptors in plants, the mechanism that controls their activation and immune signaling remains elusive. Here, we report that the avirulence effector AvrPiz-t from Magnaporthe oryzae targets the rice E3 ligase APIP10 for degradation, but that APIP10, in return, ubiquitinates AvrPiz-t and thereby causes its degradation. Silencing of APIP10 in the non-Piz-t background compromises the basal defense against M. oryzae. Conversely, silencing of APIP10 in the Piz-t background causes cell death, significant accumulation of Piz-t, and enhanced resistance to M. oryzae, suggesting that APIP10 is a negative regulator of Piz-t. We show that APIP10 promotes degradation of Piz-t via the 26S proteasome system. Furthermore, we demonstrate that AvrPiz-t stabilizes Piz-t during M. oryzae infection. Together, our results show that APIP10 is a novel E3 ligase that functionally connects the fungal effector AvrPiz-t to its NLR receptor Piz-t in rice.
Although nucleotide-binding domain, leucine-rich repeat (NLR) proteins are the major immune receptors in plants, the mechanism that controls their activation and immune signaling remains elusive. Here, we report that the avirulence effector AvrPiz-t from Magnaporthe oryzae targets the rice E3 ligase APIP10 for degradation, but that APIP10, in return, ubiquitinates AvrPiz-t and thereby causes its degradation. Silencing of APIP10 in the non- Piz-t background compromises the basal defense against M . oryzae . Conversely, silencing of APIP10 in the Piz-t background causes cell death, significant accumulation of Piz-t, and enhanced resistance to M . oryzae , suggesting that APIP10 is a negative regulator of Piz-t. We show that APIP10 promotes degradation of Piz-t via the 26S proteasome system. Furthermore, we demonstrate that AvrPiz-t stabilizes Piz-t during M . oryzae infection. Together, our results show that APIP10 is a novel E3 ligase that functionally connects the fungal effector AvrPiz-t to its NLR receptor Piz-t in rice. Rice is the staple food for half of the world’s population. Rice diseases are, however, the major threat for stable rice production worldwide. Elucidating the molecular basis is pivotal for the development of durable resistance to control rice diseases. We previously found that the RING finger E3 ligase APIP6 interacts with AvrPiz-t and plays a role in rice PAMP-triggered immunity (PTI). In this study, we characterized another RING finger E3 ligase in rice, named APIP10. Like APIP6, APIP10 and AvrPiz-t degrade each other, and APIP10 is a positive regulator of PTI. Interestingly, reduction of APIP10 expression level in the Piz-t resistant plants causes severe cell death and accumulation of the NLR receptor Piz-t, indicating APIP10 is a negative regulator of Piz-t. We also show that APIP10 can promote Piz-t degradation while AvrPiz-t can stabilize Piz-t. Our results demonstrate that APIP10 is a target of a fungal effector and a negative regulator of an NLR receptor in plants.
Audience Academic
Author Park, Chan Ho
Wang, Guo-Liang
Umemura, Kenji
Songkumarn, Pattavipha
Ning, Yuese
Wang, Mo
Shi, Xuetao
Suttiviriya, Pavinee
Zhou, Bo
Bellizzi, Maria
Shirsekar, Gautam
Chen, Songbiao
Xie, Xin
AuthorAffiliation 2 State Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
4 Meiji Seika Kaisha Ltd, Health & Bioscience Laboratories, Tokyo, Japan
1 Department of Plant Pathology, Ohio State University, Columbus, Ohio, United States of America
University of California, Davis Genome Center, UNITED STATES
3 Biotechnology Research Institute, Fujian Academy of Agricultural Sciences, Fuzhou, Fujian, China
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– name: 1 Department of Plant Pathology, Ohio State University, Columbus, Ohio, United States of America
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– name: University of California, Davis Genome Center, UNITED STATES
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  surname: Wang
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  organization: State Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27031246$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2016 Public Library of Science
2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Park CH, Shirsekar G, Bellizzi M, Chen S, Songkumarn P, Xie X, et al. (2016) The E3 Ligase APIP10 Connects the Effector AvrPiz-t to the NLR Receptor Piz-t in Rice. PLoS Pathog 12(3): e1005529. doi:10.1371/journal.ppat.1005529
2016 Park et al 2016 Park et al
2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Park CH, Shirsekar G, Bellizzi M, Chen S, Songkumarn P, Xie X, et al. (2016) The E3 Ligase APIP10 Connects the Effector AvrPiz-t to the NLR Receptor Piz-t in Rice. PLoS Pathog 12(3): e1005529. doi:10.1371/journal.ppat.1005529
Copyright_xml – notice: COPYRIGHT 2016 Public Library of Science
– notice: 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Park CH, Shirsekar G, Bellizzi M, Chen S, Songkumarn P, Xie X, et al. (2016) The E3 Ligase APIP10 Connects the Effector AvrPiz-t to the NLR Receptor Piz-t in Rice. PLoS Pathog 12(3): e1005529. doi:10.1371/journal.ppat.1005529
– notice: 2016 Park et al 2016 Park et al
– notice: 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Park CH, Shirsekar G, Bellizzi M, Chen S, Songkumarn P, Xie X, et al. (2016) The E3 Ligase APIP10 Connects the Effector AvrPiz-t to the NLR Receptor Piz-t in Rice. PLoS Pathog 12(3): e1005529. doi:10.1371/journal.ppat.1005529
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DocumentTitleAlternate APIP10 Regulates the NLR Receptor Piz-t
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I have read the journal's policy and the authors of this manuscript have the following competing interests: Kenji Umemur is employed by Meiji Seika Kaisha Ltd, Japan.
Conceived and designed the experiments: CHP GS KU GLW. Performed the experiments: CHP GS MB SC XX XS YN BZ PSu PSo MW. Analyzed the data: CHP GSu GLW. Contributed reagents/materials/analysis tools: MB SC PSo. Wrote the paper: CHP GS GLW.
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4816579/
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SSID ssj0041316
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Snippet Although nucleotide-binding domain, leucine-rich repeat (NLR) proteins are the major immune receptors in plants, the mechanism that controls their activation...
  Although nucleotide-binding domain, leucine-rich repeat (NLR) proteins are the major immune receptors in plants, the mechanism that controls their activation...
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StartPage e1005529
SubjectTerms Apoptosis
Biology and Life Sciences
Cell death
Gene expression
Genomes
Health aspects
Infections
Ligases
Magnaporthe
NOD-like receptors
Oryza - enzymology
Oryza - microbiology
Pathogens
Physiological aspects
Plant Diseases - microbiology
Proteins
Research and Analysis Methods
Resistance to control
Rice
Ubiquitin-Protein Ligases - metabolism
Ubiquitination - immunology
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Title The E3 Ligase APIP10 Connects the Effector AvrPiz-t to the NLR Receptor Piz-t in Rice
URI https://www.ncbi.nlm.nih.gov/pubmed/27031246
https://www.proquest.com/docview/1777280460/abstract/
https://search.proquest.com/docview/1778709287
https://pubmed.ncbi.nlm.nih.gov/PMC4816579
https://doaj.org/article/2807deef61bb419bb8e915d70f0a97d1
http://dx.doi.org/10.1371/journal.ppat.1005529
Volume 12
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