A Spontaneous Complementary Mutation Restores the RNA Silencing Suppression Activity of HC-Pro and the Virulence of Sugarcane Mosaic Virus

Cross-protection is a promising measure to control plant viral diseases. Reverse genetics had been recently adopted to generate attenuated mutants that have potential in cross-protection. But studies on the variability of the progeny viruses of the attenuated mutants are scarce. Sugarcane mosaic vir...

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Main Authors: Xiao-Jie Xu, Huan-Gai Li, De-Jie Cheng, Ling-Zhi Liu, Chao Geng, Yan-Ping Tian, Xiang-Dong Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.01279/full
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spelling doaj-74366929c098420eb6a83688b16a79242020-11-25T03:56:13ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-08-011110.3389/fpls.2020.01279549767A Spontaneous Complementary Mutation Restores the RNA Silencing Suppression Activity of HC-Pro and the Virulence of Sugarcane Mosaic VirusXiao-Jie Xu0Huan-Gai Li1De-Jie Cheng2Ling-Zhi Liu3Chao Geng4Yan-Ping Tian5Xiang-Dong Li6Shandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural University, Tai’an, ChinaProtein Science Laboratory of Ministry of Education, School of Life Sciences, Tsinghua University, Beijing, ChinaShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural University, Tai’an, ChinaShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural University, Tai’an, ChinaShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural University, Tai’an, ChinaShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural University, Tai’an, ChinaShandong Province Key Laboratory for Agricultural Microbiology, Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural University, Tai’an, ChinaCross-protection is a promising measure to control plant viral diseases. Reverse genetics had been recently adopted to generate attenuated mutants that have potential in cross-protection. But studies on the variability of the progeny viruses of the attenuated mutants are scarce. Sugarcane mosaic virus (SCMV; genus Potyvirus, family Potyviridae) is the prevalent virus inducing maize dwarf mosaic disease in China. Here, we showed that the substitution of arginine with isoleucine in the FRNK motif at position 184 of helper component-proteinase (HC-Pro) abolished its RNA silencing suppression (RSS) activity, drastically reduced the virulence and accumulation level of SCMV, and impaired the synergism between SCMV and maize chlorotic mottle virus. The attenuated mutant could protect maize plants from a severe infection of SCMV. However, a spontaneous mutation of glycine at position 440 to arginine in HC-Pro rescued the virulence and synergism with maize chlorotic mottle virus of SCMV and the RSS activity of HC-Pro. Similar results were obtained with tobacco vein banding mosaic virus and watermelon mosaic virus. These results provide novel evidence for the complementary mutation of potyviruses in maintaining the HC-Pro RSS activity and potyviral virulence and remind us of evaluating the potential risk of attenuated mutants thoroughly before applying for the control of plant viral diseases via cross-protection.https://www.frontiersin.org/article/10.3389/fpls.2020.01279/fullhelper component-proteinasePotyvirusRNA silencing suppressionspontaneous mutationsugarcane mosaic virusvirulence
collection DOAJ
language English
format Article
sources DOAJ
author Xiao-Jie Xu
Huan-Gai Li
De-Jie Cheng
Ling-Zhi Liu
Chao Geng
Yan-Ping Tian
Xiang-Dong Li
spellingShingle Xiao-Jie Xu
Huan-Gai Li
De-Jie Cheng
Ling-Zhi Liu
Chao Geng
Yan-Ping Tian
Xiang-Dong Li
A Spontaneous Complementary Mutation Restores the RNA Silencing Suppression Activity of HC-Pro and the Virulence of Sugarcane Mosaic Virus
Frontiers in Plant Science
helper component-proteinase
Potyvirus
RNA silencing suppression
spontaneous mutation
sugarcane mosaic virus
virulence
author_facet Xiao-Jie Xu
Huan-Gai Li
De-Jie Cheng
Ling-Zhi Liu
Chao Geng
Yan-Ping Tian
Xiang-Dong Li
author_sort Xiao-Jie Xu
title A Spontaneous Complementary Mutation Restores the RNA Silencing Suppression Activity of HC-Pro and the Virulence of Sugarcane Mosaic Virus
title_short A Spontaneous Complementary Mutation Restores the RNA Silencing Suppression Activity of HC-Pro and the Virulence of Sugarcane Mosaic Virus
title_full A Spontaneous Complementary Mutation Restores the RNA Silencing Suppression Activity of HC-Pro and the Virulence of Sugarcane Mosaic Virus
title_fullStr A Spontaneous Complementary Mutation Restores the RNA Silencing Suppression Activity of HC-Pro and the Virulence of Sugarcane Mosaic Virus
title_full_unstemmed A Spontaneous Complementary Mutation Restores the RNA Silencing Suppression Activity of HC-Pro and the Virulence of Sugarcane Mosaic Virus
title_sort spontaneous complementary mutation restores the rna silencing suppression activity of hc-pro and the virulence of sugarcane mosaic virus
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2020-08-01
description Cross-protection is a promising measure to control plant viral diseases. Reverse genetics had been recently adopted to generate attenuated mutants that have potential in cross-protection. But studies on the variability of the progeny viruses of the attenuated mutants are scarce. Sugarcane mosaic virus (SCMV; genus Potyvirus, family Potyviridae) is the prevalent virus inducing maize dwarf mosaic disease in China. Here, we showed that the substitution of arginine with isoleucine in the FRNK motif at position 184 of helper component-proteinase (HC-Pro) abolished its RNA silencing suppression (RSS) activity, drastically reduced the virulence and accumulation level of SCMV, and impaired the synergism between SCMV and maize chlorotic mottle virus. The attenuated mutant could protect maize plants from a severe infection of SCMV. However, a spontaneous mutation of glycine at position 440 to arginine in HC-Pro rescued the virulence and synergism with maize chlorotic mottle virus of SCMV and the RSS activity of HC-Pro. Similar results were obtained with tobacco vein banding mosaic virus and watermelon mosaic virus. These results provide novel evidence for the complementary mutation of potyviruses in maintaining the HC-Pro RSS activity and potyviral virulence and remind us of evaluating the potential risk of attenuated mutants thoroughly before applying for the control of plant viral diseases via cross-protection.
topic helper component-proteinase
Potyvirus
RNA silencing suppression
spontaneous mutation
sugarcane mosaic virus
virulence
url https://www.frontiersin.org/article/10.3389/fpls.2020.01279/full
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