Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors

Kenji S. Nakahara; Chikara Masuta; Syouta Yamada; Hanako Shimura; Yukiko Kashihara; Tomoko S. Wada; Ayano Meguro; Kazunori Goto; Kazuki Tadamura; Kae Sueda; Toru Sekiguchi; Jun Shao; Noriko Itchoda; Takeshi Matsumura; Manabu Igarashi; Kimihito Ito; Richard W. Carthew; Ichiro Uyeda

doi:10.1073/pnas.1201628109

Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors

Kenji S. Nakahara^*, Chikara Masuta, Syouta Yamada, Hanako Shimura, Yukiko Kashihara, Tomoko S. Wada, Ayano Meguro, Kazunori Goto, Kazuki Tadamura, Kae Sueda, Toru Sekiguchi, Jun Shao, Noriko Itchoda, Takeshi Matsumura, Manabu Igarashi, Kimihito Ito, Richard W. Carthew, Ichiro Uyeda

^*Corresponding author for this work

Molecular Biosciences

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182 Scopus citations

Abstract

RNA silencing (RNAi) induced by virus-derived double-stranded RNA (dsRNA), which is in a sense regarded as a pathogen-associated molecular pattern (PAMP) of viruses, is a general plant defense mechanism. To counteract this defense, plant viruses express RNA silencing suppressors (RSSs), many of which bind to dsRNA and attenuate RNAi. We showed that the tobacco calmodulin-like protein, rgs-CaM, counterattacked viral RSSs by binding to their dsRNA-binding domains and sequestering them from inhibiting RNAi. Autophagy-like protein degradation seemed to operate to degrade RSSs with the sacrifice of rgs-CaM. These RSSs could thus be regarded as secondary viral PAMPs. This study uncovered a unique defense system in which an rgs-CaM-mediated countermeasure against viral RSSs enhanced host antiviral RNAi in tobacco.

Original language	English (US)
Pages (from-to)	10113-10118
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	109
Issue number	25
DOIs	https://doi.org/10.1073/pnas.1201628109
State	Published - Jun 19 2012

Keywords

Arms race
Innate immunity
Ubiquitin-26S proteasome

ASJC Scopus subject areas

General

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10.1073/pnas.1201628109

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Nakahara, K. S., Masuta, C., Yamada, S., Shimura, H., Kashihara, Y., Wada, T. S., Meguro, A., Goto, K., Tadamura, K., Sueda, K., Sekiguchi, T., Shao, J., Itchoda, N., Matsumura, T., Igarashi, M., Ito, K., Carthew, R. W., & Uyeda, I. (2012). Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors. Proceedings of the National Academy of Sciences of the United States of America, 109(25), 10113-10118. https://doi.org/10.1073/pnas.1201628109

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title = "Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors",

abstract = "RNA silencing (RNAi) induced by virus-derived double-stranded RNA (dsRNA), which is in a sense regarded as a pathogen-associated molecular pattern (PAMP) of viruses, is a general plant defense mechanism. To counteract this defense, plant viruses express RNA silencing suppressors (RSSs), many of which bind to dsRNA and attenuate RNAi. We showed that the tobacco calmodulin-like protein, rgs-CaM, counterattacked viral RSSs by binding to their dsRNA-binding domains and sequestering them from inhibiting RNAi. Autophagy-like protein degradation seemed to operate to degrade RSSs with the sacrifice of rgs-CaM. These RSSs could thus be regarded as secondary viral PAMPs. This study uncovered a unique defense system in which an rgs-CaM-mediated countermeasure against viral RSSs enhanced host antiviral RNAi in tobacco.",

keywords = "Arms race, Innate immunity, Ubiquitin-26S proteasome",

author = "Nakahara, {Kenji S.} and Chikara Masuta and Syouta Yamada and Hanako Shimura and Yukiko Kashihara and Wada, {Tomoko S.} and Ayano Meguro and Kazunori Goto and Kazuki Tadamura and Kae Sueda and Toru Sekiguchi and Jun Shao and Noriko Itchoda and Takeshi Matsumura and Manabu Igarashi and Kimihito Ito and Carthew, {Richard W.} and Ichiro Uyeda",

year = "2012",

month = jun,

day = "19",

doi = "10.1073/pnas.1201628109",

language = "English (US)",

volume = "109",

pages = "10113--10118",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

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Nakahara, KS, Masuta, C, Yamada, S, Shimura, H, Kashihara, Y, Wada, TS, Meguro, A, Goto, K, Tadamura, K, Sueda, K, Sekiguchi, T, Shao, J, Itchoda, N, Matsumura, T, Igarashi, M, Ito, K, Carthew, RW & Uyeda, I 2012, 'Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors', Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 25, pp. 10113-10118. https://doi.org/10.1073/pnas.1201628109

Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors. / Nakahara, Kenji S.; Masuta, Chikara; Yamada, Syouta et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, No. 25, 19.06.2012, p. 10113-10118.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors

AU - Nakahara, Kenji S.

AU - Masuta, Chikara

AU - Yamada, Syouta

AU - Shimura, Hanako

AU - Kashihara, Yukiko

AU - Wada, Tomoko S.

AU - Meguro, Ayano

AU - Goto, Kazunori

AU - Tadamura, Kazuki

AU - Sueda, Kae

AU - Sekiguchi, Toru

AU - Shao, Jun

AU - Itchoda, Noriko

AU - Matsumura, Takeshi

AU - Igarashi, Manabu

AU - Ito, Kimihito

AU - Carthew, Richard W.

AU - Uyeda, Ichiro

PY - 2012/6/19

Y1 - 2012/6/19

N2 - RNA silencing (RNAi) induced by virus-derived double-stranded RNA (dsRNA), which is in a sense regarded as a pathogen-associated molecular pattern (PAMP) of viruses, is a general plant defense mechanism. To counteract this defense, plant viruses express RNA silencing suppressors (RSSs), many of which bind to dsRNA and attenuate RNAi. We showed that the tobacco calmodulin-like protein, rgs-CaM, counterattacked viral RSSs by binding to their dsRNA-binding domains and sequestering them from inhibiting RNAi. Autophagy-like protein degradation seemed to operate to degrade RSSs with the sacrifice of rgs-CaM. These RSSs could thus be regarded as secondary viral PAMPs. This study uncovered a unique defense system in which an rgs-CaM-mediated countermeasure against viral RSSs enhanced host antiviral RNAi in tobacco.

AB - RNA silencing (RNAi) induced by virus-derived double-stranded RNA (dsRNA), which is in a sense regarded as a pathogen-associated molecular pattern (PAMP) of viruses, is a general plant defense mechanism. To counteract this defense, plant viruses express RNA silencing suppressors (RSSs), many of which bind to dsRNA and attenuate RNAi. We showed that the tobacco calmodulin-like protein, rgs-CaM, counterattacked viral RSSs by binding to their dsRNA-binding domains and sequestering them from inhibiting RNAi. Autophagy-like protein degradation seemed to operate to degrade RSSs with the sacrifice of rgs-CaM. These RSSs could thus be regarded as secondary viral PAMPs. This study uncovered a unique defense system in which an rgs-CaM-mediated countermeasure against viral RSSs enhanced host antiviral RNAi in tobacco.

KW - Arms race

KW - Innate immunity

KW - Ubiquitin-26S proteasome

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U2 - 10.1073/pnas.1201628109

DO - 10.1073/pnas.1201628109

M3 - Article

C2 - 22665793

AN - SCOPUS:84862528937

SN - 0027-8424

VL - 109

SP - 10113

EP - 10118

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 25

ER -

Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors

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Keywords

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