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rgs-CaM Detects and Counteracts Viral RNA Silencing Suppressors in Plant Immune Priming

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Title: rgs-CaM Detects and Counteracts Viral RNA Silencing Suppressors in Plant Immune Priming
Authors: Jeon, Eun Jin Browse this author
Tadamura, Kazuki Browse this author
Murakami, Taiki Browse this author
Inaba, Jun-ichi Browse this author
Kim, Bo Min Browse this author
Sato, Masako Browse this author
Atsumi, Go Browse this author
Kuchitsu, Kazuyuki Browse this author
Masuta, Chikara Browse this author →KAKEN DB
Nakahara, Kenji S. Browse this author →KAKEN DB
Keywords: systemic acquired resistance
calmodulin-like protein
RNA silencing suppressor
cucumber mosaic virus
priming
RNA interference
innate immunity
plant viruses
salicylic acid signaling
Issue Date: 1-Oct-2017
Publisher: American Society for Microbiology
Journal Title: Journal of Virology
Volume: 91
Issue: 19
Start Page: UNSP e00761-17
Publisher DOI: 10.1128/JVI.00761-17
PMID: 28724770
Abstract: Primary infection of a plant with a pathogen that causes high accumulation of salicylic acid in the plant typically via a hypersensitive response confers enhanced resistance against secondary infection with a broad spectrum of pathogens, including viruses. This phenomenon is called systemic acquired resistance (SAR), which is a plant priming for adaption to repeated biotic stress. However, the molecular mechanisms of SAR-mediated enhanced inhibition, especially of virus infection, remain unclear. Here, we show that SAR against cucumber mosaic virus (CMV) in tobacco plants (Nicotiana tabacum) involves a calmodulin-like protein, rgs-CaM. We previously reported the antiviral function of rgs-CaM, which binds to and directs degradation of viral RNA silencing suppressors (RSSs), including CMV 2b, via autophagy. We found that rgs-CaM-mediated immunity is ineffective against CMV infection in normally growing tobacco plants but is activated as a result of SAR induction via salicylic acid signaling. We then analyzed the effect of overexpression of rgs-CaM on salicylic acid signaling. Overexpressed and ectopically expressed rgs-CaM induced defense reactions, including cell death, generation of reactive oxygen species, and salicylic acid signaling. Further analysis using a combination of the salicylic acid analogue benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH) and the Ca2+ ionophore A23187 revealed that rgs-CaM functions as an immune receptor that induces salicylic acid signaling by simultaneously perceiving both viral RSS and Ca2+ influx as infection cues, implying its autoactivation. Thus, secondary infection of SAR-induced tobacco plants with CMV seems to be effectively inhibited through 2b recognition and degradation by rgs-CaM, leading to reinforcement of antiviral RNA silencing and other salicylic acid-mediated antiviral responses. IMPORTANCE Even without an acquired immune system like that in vertebrates, plants show enhanced whole-plant resistance against secondary infection with pathogens; this so-called systemic acquired resistance (SAR) has been known for more than half a century and continues to be extensively studied. SAR-induced plants strongly and rapidly express a number of antibiotics and pathogenesis-related proteins targeted against secondary infection, which can account for enhanced resistance against bacterial and fungal pathogens but are not thought to control viral infection. This study showed that enhanced resistance against cucumber mosaic virus is caused by a tobacco calmodulin-like protein, rgs-CaM, which detects and counteracts the major viral virulence factor (RNA silencing suppressor) after SAR induction. rgs-CaM-mediated SAR illustrates the growth versus defense trade-off in plants, as it targets the major virulence factor only under specific biotic stress conditions, thus avoiding the cost of constitutive activation while reducing the damage from virus infection.
Rights: Copyright © 2017 American Society for Microbiology.
Type: article (author version)
URI: http://hdl.handle.net/2115/68681
Appears in Collections:農学院・農学研究院 (Graduate School of Agriculture / Faculty of Agriculture) > 雑誌発表論文等 (Peer-reviewed Journal Articles, etc)

Submitter: 中原 健二

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