eIF4A, a target of siRNA derived from rice stripe virus, negatively regulates antiviral autophagy by interacting with ATG5 in Nicotiana benthamiana.

Autophagy is induced by viral infection and has antiviral functions in plants, but the underlying mechanism is poorly understood. We previously identified a viral small interfering RNA (vsiRNA) derived from rice stripe virus (RSV) RNA4 that contributes to the leaf-twisting and stunting symptoms caus...

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Autores principales: Xiangxiang Zhang, Yueyan Yin, Yunhe Su, Zhaoxing Jia, Liangliang Jiang, Yuwen Lu, Hongying Zheng, Jiejun Peng, Shaofei Rao, Guanwei Wu, Jianping Chen, Fei Yan
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Publicado: Public Library of Science (PLoS) 2021
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spelling oai:doaj.org-article:20a1dffce653408ba291a5b8ddaa4bb02021-12-02T20:00:05ZeIF4A, a target of siRNA derived from rice stripe virus, negatively regulates antiviral autophagy by interacting with ATG5 in Nicotiana benthamiana.1553-73661553-737410.1371/journal.ppat.1009963https://doaj.org/article/20a1dffce653408ba291a5b8ddaa4bb02021-09-01T00:00:00Zhttps://doi.org/10.1371/journal.ppat.1009963https://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Autophagy is induced by viral infection and has antiviral functions in plants, but the underlying mechanism is poorly understood. We previously identified a viral small interfering RNA (vsiRNA) derived from rice stripe virus (RSV) RNA4 that contributes to the leaf-twisting and stunting symptoms caused by this virus by targeting the host eukaryotic translation initiation factor 4A (eIF4A) mRNA for silencing. In addition, autophagy plays antiviral roles by degrading RSV p3 protein, a suppressor of RNA silencing. Here, we demonstrate that eIF4A acts as a negative regulator of autophagy in Nicotiana benthamiana. Silencing of NbeIF4A activated autophagy and inhibited RSV infection by facilitating autophagic degradation of p3. Further analysis showed that NbeIF4A interacts with NbATG5 and interferes with its interaction with ATG12. Overexpression of NbeIF4A suppressed NbATG5-activated autophagy. Moreover, expression of vsiRNA-4A, which targets NbeIF4A mRNA for cleavage, induced autophagy by silencing NbeIF4A. Finally, we demonstrate that eIF4A from rice, the natural host of RSV, also interacts with OsATG5 and suppresses OsATG5-activated autophagy, pointing to the conserved function of eIF4A as a negative regulator of antiviral autophagy. Taken together, these results reveal that eIF4A negatively regulates antiviral autophagy by interacting with ATG5 and that its mRNA is recognized by a virus-derived siRNA, resulting in its silencing, which induces autophagy against viral infection.Xiangxiang ZhangYueyan YinYunhe SuZhaoxing JiaLiangliang JiangYuwen LuHongying ZhengJiejun PengShaofei RaoGuanwei WuJianping ChenFei YanPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 17, Iss 9, p e1009963 (2021)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
Xiangxiang Zhang
Yueyan Yin
Yunhe Su
Zhaoxing Jia
Liangliang Jiang
Yuwen Lu
Hongying Zheng
Jiejun Peng
Shaofei Rao
Guanwei Wu
Jianping Chen
Fei Yan
eIF4A, a target of siRNA derived from rice stripe virus, negatively regulates antiviral autophagy by interacting with ATG5 in Nicotiana benthamiana.
description Autophagy is induced by viral infection and has antiviral functions in plants, but the underlying mechanism is poorly understood. We previously identified a viral small interfering RNA (vsiRNA) derived from rice stripe virus (RSV) RNA4 that contributes to the leaf-twisting and stunting symptoms caused by this virus by targeting the host eukaryotic translation initiation factor 4A (eIF4A) mRNA for silencing. In addition, autophagy plays antiviral roles by degrading RSV p3 protein, a suppressor of RNA silencing. Here, we demonstrate that eIF4A acts as a negative regulator of autophagy in Nicotiana benthamiana. Silencing of NbeIF4A activated autophagy and inhibited RSV infection by facilitating autophagic degradation of p3. Further analysis showed that NbeIF4A interacts with NbATG5 and interferes with its interaction with ATG12. Overexpression of NbeIF4A suppressed NbATG5-activated autophagy. Moreover, expression of vsiRNA-4A, which targets NbeIF4A mRNA for cleavage, induced autophagy by silencing NbeIF4A. Finally, we demonstrate that eIF4A from rice, the natural host of RSV, also interacts with OsATG5 and suppresses OsATG5-activated autophagy, pointing to the conserved function of eIF4A as a negative regulator of antiviral autophagy. Taken together, these results reveal that eIF4A negatively regulates antiviral autophagy by interacting with ATG5 and that its mRNA is recognized by a virus-derived siRNA, resulting in its silencing, which induces autophagy against viral infection.
format article
author Xiangxiang Zhang
Yueyan Yin
Yunhe Su
Zhaoxing Jia
Liangliang Jiang
Yuwen Lu
Hongying Zheng
Jiejun Peng
Shaofei Rao
Guanwei Wu
Jianping Chen
Fei Yan
author_facet Xiangxiang Zhang
Yueyan Yin
Yunhe Su
Zhaoxing Jia
Liangliang Jiang
Yuwen Lu
Hongying Zheng
Jiejun Peng
Shaofei Rao
Guanwei Wu
Jianping Chen
Fei Yan
author_sort Xiangxiang Zhang
title eIF4A, a target of siRNA derived from rice stripe virus, negatively regulates antiviral autophagy by interacting with ATG5 in Nicotiana benthamiana.
title_short eIF4A, a target of siRNA derived from rice stripe virus, negatively regulates antiviral autophagy by interacting with ATG5 in Nicotiana benthamiana.
title_full eIF4A, a target of siRNA derived from rice stripe virus, negatively regulates antiviral autophagy by interacting with ATG5 in Nicotiana benthamiana.
title_fullStr eIF4A, a target of siRNA derived from rice stripe virus, negatively regulates antiviral autophagy by interacting with ATG5 in Nicotiana benthamiana.
title_full_unstemmed eIF4A, a target of siRNA derived from rice stripe virus, negatively regulates antiviral autophagy by interacting with ATG5 in Nicotiana benthamiana.
title_sort eif4a, a target of sirna derived from rice stripe virus, negatively regulates antiviral autophagy by interacting with atg5 in nicotiana benthamiana.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/20a1dffce653408ba291a5b8ddaa4bb0
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