NSs, the Silencing Suppressor of Tomato Spotted Wilt Orthotospovirus, Interferes With JA-Regulated Host Terpenoids Expression to Attract Frankliniella occidentalis

Jiao Du; Xiao Yu Song; Xiao Bin Shi; Xin Tang; Jian Bin Chen; Zhan Hong Zhang; Gong Chen; Zhuo Zhang; Xu Guo Zhou; Yong Liu; De Yong Zhang

doi:10.3389/fmicb.2020.590451

NSs, the Silencing Suppressor of Tomato Spotted Wilt Orthotospovirus, Interferes With JA-Regulated Host Terpenoids Expression to Attract Frankliniella occidentalis

Jiao Du, Xiao Yu Song, Xiao Bin Shi, Xin Tang, Jian Bin Chen, Zhan Hong Zhang, Gong Chen, Zhuo Zhang, Xu Guo Zhou, Yong Liu, De Yong Zhang

Entomology

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

4 Scopus citations

Abstract

Tomato spotted wilt orthotospovirus (TSWV) causes serious crop losses worldwide and is transmitted by Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). NSs protein is the silencing suppressor of TSWV and plays an important role in virus infection, cycling, and transmission process. In this research, we investigated the influences of NSs protein on the interaction of TSWV, plants, and F. occidentalis with the transgenic Arabidopsis thaliana. Compared with the wild-type Col-0 plant, F. occidentalis showed an increased number and induced feeding behavior on transgenic Arabidopsis thaliana expressing exogenous NSs. Further analysis showed that NSs reduced the expression of terpenoids synthesis-related genes and the content of monoterpene volatiles in Arabidopsis. These monoterpene volatiles played a repellent role in respect to F. occidentalis. In addition, the expression level of plant immune-related genes and the content of the plant resistance hormone jasmonic acid (JA) in transgenic Arabidopsis were reduced. The silencing suppressor of TSWV NSs alters the emission of plant volatiles and reduces the JA-regulated plant defenses, resulting in enhanced attractiveness of plants to F. occidentalis and may increase the transmission probability of TSWV.

Original language	English
Article number	590451
Journal	Frontiers in Microbiology
Volume	11
DOIs	https://doi.org/10.3389/fmicb.2020.590451
State	Published - Dec 10 2020

Bibliographical note

Funding Information:
This work was supported by the National Natural Science Foundation of China (Grant Nos. 31872932, 31871935, 31571981, and 31672003), the National Key R&D Program of China (2018YFE0112600), the Agriculture Research System of China (CARS-23-D-02); and the National Agricultural Outstanding Talent Program [(2015)62].

Funding Information:
We thank Prof. You-zhi Li (Hunan Agricultural University) and Prof. Feng-ming Yan (Henan Agricultural University) for kindly providing the instrument and materials for the EPG experiment. Funding. This work was supported by the National Natural Science Foundation of China (Grant Nos. 31872932, 31871935, 31571981, and 31672003), the National Key R&D Program of China (2018YFE0112600), the Agriculture Research System of China (CARS-23-D-02); and the National Agricultural Outstanding Talent Program [(2015)62].

Publisher Copyright:
© Copyright © 2020 Du, Song, Shi, Tang, Chen, Zhang, Chen, Zhang, Zhou, Liu and Zhang.

Keywords

Frankliniella occidentalis
NSs
insect behavior
monoterpene
tomato spotted wilt orthotospovirus

ASJC Scopus subject areas

Microbiology
Microbiology (medical)

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10.3389/fmicb.2020.590451

Cite this

Du, J., Song, X. Y., Shi, X. B., Tang, X., Chen, J. B., Zhang, Z. H., Chen, G., Zhang, Z., Zhou, X. G., Liu, Y., & Zhang, D. Y. (2020). NSs, the Silencing Suppressor of Tomato Spotted Wilt Orthotospovirus, Interferes With JA-Regulated Host Terpenoids Expression to Attract Frankliniella occidentalis. Frontiers in Microbiology, 11, Article 590451. https://doi.org/10.3389/fmicb.2020.590451

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title = "NSs, the Silencing Suppressor of Tomato Spotted Wilt Orthotospovirus, Interferes With JA-Regulated Host Terpenoids Expression to Attract Frankliniella occidentalis",

abstract = "Tomato spotted wilt orthotospovirus (TSWV) causes serious crop losses worldwide and is transmitted by Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). NSs protein is the silencing suppressor of TSWV and plays an important role in virus infection, cycling, and transmission process. In this research, we investigated the influences of NSs protein on the interaction of TSWV, plants, and F. occidentalis with the transgenic Arabidopsis thaliana. Compared with the wild-type Col-0 plant, F. occidentalis showed an increased number and induced feeding behavior on transgenic Arabidopsis thaliana expressing exogenous NSs. Further analysis showed that NSs reduced the expression of terpenoids synthesis-related genes and the content of monoterpene volatiles in Arabidopsis. These monoterpene volatiles played a repellent role in respect to F. occidentalis. In addition, the expression level of plant immune-related genes and the content of the plant resistance hormone jasmonic acid (JA) in transgenic Arabidopsis were reduced. The silencing suppressor of TSWV NSs alters the emission of plant volatiles and reduces the JA-regulated plant defenses, resulting in enhanced attractiveness of plants to F. occidentalis and may increase the transmission probability of TSWV.",

keywords = "Frankliniella occidentalis, NSs, insect behavior, monoterpene, tomato spotted wilt orthotospovirus",

author = "Jiao Du and Song, {Xiao Yu} and Shi, {Xiao Bin} and Xin Tang and Chen, {Jian Bin} and Zhang, {Zhan Hong} and Gong Chen and Zhuo Zhang and Zhou, {Xu Guo} and Yong Liu and Zhang, {De Yong}",

note = "Funding Information: This work was supported by the National Natural Science Foundation of China (Grant Nos. 31872932, 31871935, 31571981, and 31672003), the National Key R&D Program of China (2018YFE0112600), the Agriculture Research System of China (CARS-23-D-02); and the National Agricultural Outstanding Talent Program [(2015)62]. Funding Information: We thank Prof. You-zhi Li (Hunan Agricultural University) and Prof. Feng-ming Yan (Henan Agricultural University) for kindly providing the instrument and materials for the EPG experiment. Funding. This work was supported by the National Natural Science Foundation of China (Grant Nos. 31872932, 31871935, 31571981, and 31672003), the National Key R&D Program of China (2018YFE0112600), the Agriculture Research System of China (CARS-23-D-02); and the National Agricultural Outstanding Talent Program [(2015)62]. Publisher Copyright: {\textcopyright} Copyright {\textcopyright} 2020 Du, Song, Shi, Tang, Chen, Zhang, Chen, Zhang, Zhou, Liu and Zhang.",

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AU - Du, Jiao

AU - Song, Xiao Yu

AU - Shi, Xiao Bin

AU - Tang, Xin

AU - Chen, Jian Bin

AU - Zhang, Zhan Hong

AU - Chen, Gong

AU - Zhang, Zhuo

AU - Zhou, Xu Guo

AU - Liu, Yong

AU - Zhang, De Yong

N1 - Funding Information: This work was supported by the National Natural Science Foundation of China (Grant Nos. 31872932, 31871935, 31571981, and 31672003), the National Key R&D Program of China (2018YFE0112600), the Agriculture Research System of China (CARS-23-D-02); and the National Agricultural Outstanding Talent Program [(2015)62]. Funding Information: We thank Prof. You-zhi Li (Hunan Agricultural University) and Prof. Feng-ming Yan (Henan Agricultural University) for kindly providing the instrument and materials for the EPG experiment. Funding. This work was supported by the National Natural Science Foundation of China (Grant Nos. 31872932, 31871935, 31571981, and 31672003), the National Key R&D Program of China (2018YFE0112600), the Agriculture Research System of China (CARS-23-D-02); and the National Agricultural Outstanding Talent Program [(2015)62]. Publisher Copyright: © Copyright © 2020 Du, Song, Shi, Tang, Chen, Zhang, Chen, Zhang, Zhou, Liu and Zhang.

PY - 2020/12/10

Y1 - 2020/12/10

N2 - Tomato spotted wilt orthotospovirus (TSWV) causes serious crop losses worldwide and is transmitted by Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). NSs protein is the silencing suppressor of TSWV and plays an important role in virus infection, cycling, and transmission process. In this research, we investigated the influences of NSs protein on the interaction of TSWV, plants, and F. occidentalis with the transgenic Arabidopsis thaliana. Compared with the wild-type Col-0 plant, F. occidentalis showed an increased number and induced feeding behavior on transgenic Arabidopsis thaliana expressing exogenous NSs. Further analysis showed that NSs reduced the expression of terpenoids synthesis-related genes and the content of monoterpene volatiles in Arabidopsis. These monoterpene volatiles played a repellent role in respect to F. occidentalis. In addition, the expression level of plant immune-related genes and the content of the plant resistance hormone jasmonic acid (JA) in transgenic Arabidopsis were reduced. The silencing suppressor of TSWV NSs alters the emission of plant volatiles and reduces the JA-regulated plant defenses, resulting in enhanced attractiveness of plants to F. occidentalis and may increase the transmission probability of TSWV.

AB - Tomato spotted wilt orthotospovirus (TSWV) causes serious crop losses worldwide and is transmitted by Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). NSs protein is the silencing suppressor of TSWV and plays an important role in virus infection, cycling, and transmission process. In this research, we investigated the influences of NSs protein on the interaction of TSWV, plants, and F. occidentalis with the transgenic Arabidopsis thaliana. Compared with the wild-type Col-0 plant, F. occidentalis showed an increased number and induced feeding behavior on transgenic Arabidopsis thaliana expressing exogenous NSs. Further analysis showed that NSs reduced the expression of terpenoids synthesis-related genes and the content of monoterpene volatiles in Arabidopsis. These monoterpene volatiles played a repellent role in respect to F. occidentalis. In addition, the expression level of plant immune-related genes and the content of the plant resistance hormone jasmonic acid (JA) in transgenic Arabidopsis were reduced. The silencing suppressor of TSWV NSs alters the emission of plant volatiles and reduces the JA-regulated plant defenses, resulting in enhanced attractiveness of plants to F. occidentalis and may increase the transmission probability of TSWV.

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KW - insect behavior

KW - monoterpene

KW - tomato spotted wilt orthotospovirus

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NSs, the Silencing Suppressor of Tomato Spotted Wilt Orthotospovirus, Interferes With JA-Regulated Host Terpenoids Expression to Attract Frankliniella occidentalis

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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