The Multivesicular Bodies (MVBs)-Localized AAA ATPase LRD6-6 Inhibits Immunity and Cell Death Likely through Regulating MVBs-Mediated Vesicular Trafficking in Rice

Xiaobo Zhu; Junjie Yin; Sihui Liang; Ruihong Liang; Xiaogang Zhou; Zhixiong Chen; Wen Zhao; Jing Wang; Weitao Li; Min He; Can Yuan; Koji Miyamoto; Bingtian Ma; Jichun Wang; Peng Qin; Weilan Chen; Yuping Wang; Wenming Wang; Xianjun Wu; Hisakazu Yamane; Lihuang Zhu; Shigui Li; Xuewei Chen

doi:10.1371/journal.pgen.1006311

The Multivesicular Bodies (MVBs)-Localized AAA ATPase LRD6-6 Inhibits Immunity and Cell Death Likely through Regulating MVBs-Mediated Vesicular Trafficking in Rice

PLoS Genet. 2016 Sep 12;12(9):e1006311. doi: 10.1371/journal.pgen.1006311. eCollection 2016 Sep.

Authors

Xiaobo Zhu¹, Junjie Yin¹, Sihui Liang¹, Ruihong Liang¹, Xiaogang Zhou¹, Zhixiong Chen¹, Wen Zhao^{1

2}, Jing Wang¹, Weitao Li¹, Min He¹, Can Yuan¹, Koji Miyamoto³, Bingtian Ma¹, Jichun Wang¹, Peng Qin¹, Weilan Chen¹, Yuping Wang¹, Wenming Wang¹, Xianjun Wu¹, Hisakazu Yamane³, Lihuang Zhu², Shigui Li¹, Xuewei Chen¹

Affiliations

¹ State Key Laboratory of Hybrid Rice, Key Laboratory of Major Crop Diseases & Collaborative Innovation Center for Hybrid Rice in Yangtze River Basin, Rice Research Institute, Sichuan Agricultural University at Wenjiang, Chengdu, Sichuan, China.
² State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China.
³ Department of Biosciences, Faculty of Science and Engineering, Teikyo University, Utsunomiya, Tochigi, Japan.

Abstract

Previous studies have shown that multivesicular bodies (MVBs)/endosomes-mediated vesicular trafficking may play key roles in plant immunity and cell death. However, the molecular regulation is poorly understood in rice. Here we report the identification and characterization of a MVBs-localized AAA ATPase LRD6-6 in rice. Disruption of LRD6-6 leads to enhanced immunity and cell death in rice. The ATPase activity and homo-dimerization of LRD6-6 is essential for its regulation on plant immunity and cell death. An ATPase inactive mutation (LRD6-6E315Q) leads to dominant-negative inhibition in plants. The LRD6-6 protein co-localizes with the MVBs marker protein RabF1/ARA6 and interacts with ESCRT-III components OsSNF7 and OsVPS2. Further analysis reveals that LRD6-6 is required for MVBs-mediated vesicular trafficking and inhibits the biosynthesis of antimicrobial compounds. Collectively, our study shows that the AAA ATPase LRD6-6 inhibits plant immunity and cell death most likely through modulating MVBs-mediated vesicular trafficking in rice.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adenosine Triphosphatases / biosynthesis*
Adenosine Triphosphatases / genetics
Arabidopsis / genetics
Arabidopsis / growth & development
Arabidopsis Proteins / genetics
Arabidopsis Proteins / metabolism
Cell Death / genetics
Disease Resistance / genetics
Disease Resistance / immunology
Endosomal Sorting Complexes Required for Transport / genetics
Endosomal Sorting Complexes Required for Transport / metabolism
Endosomes / genetics
Endosomes / metabolism
Gene Expression Regulation, Plant
Immunity, Cellular / genetics*
Multivesicular Bodies / genetics*
Multivesicular Bodies / immunology
Mutation
Oryza / genetics
Oryza / growth & development
Plant Diseases / genetics
Plant Diseases / immunology
Plant Leaves / genetics
Plant Leaves / immunology
Plant Proteins / genetics*
Plants, Genetically Modified / genetics*
Plants, Genetically Modified / immunology
Protein Transport / genetics
rab GTP-Binding Proteins / genetics

Substances

Arabidopsis Proteins
Endosomal Sorting Complexes Required for Transport
Plant Proteins
VPS2.1 protein, Arabidopsis
Adenosine Triphosphatases
Ara6 protein, Arabidopsis
rab GTP-Binding Proteins

Grants and funding

This work was supported by NSFC (Grant Numbers: 31171622 and 31571994), Transgenic Projects from the Chinese Ministry of Agriculture (TPCMA) (Grant Number: 2014ZX0800903B),) Program for New Century Excellent Talents in University from the Ministry of Education in China, “Hundred Talents Plan” Foundation, Youth foundation (Grant Number: 13QNJJ0076), and Youth Innovation Team Foundation (Grant Number: 14CXTD0039 from Sichuan, China) to XC; NSFC (Grant Number: 31401351) to JinW, (Grant Number: 31501627) to WL and (Grant Number: 31601290) to JY; Specialized Research Fund for doctoral program of higher education (Grant Number: 20135103120004) to JinW; Key Project of Sichuan Education Department (Grant Number: 15ZA0020 to WL; and TPCMA (Grant Number: 2016ZX08001002) to BM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.