NS3 Protein from Rice stripe virus affects the expression of endogenous genes in Nicotiana benthamiana

Abstract Background Rice stripe virus (RSV) belongs to the genus Tenuivirus. It is transmitted by small brown planthoppers in a persistent and circulative-propagative manner and causes rice stripe disease (RSD). The NS3 protein of RSV, encoded by the viral strand of RNA3, is a viral suppressor of RN...

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Main Authors: Gentu Wu, Guixian Zheng, Qiao Hu, Mingge Ma, Mingjun Li, Xianchao Sun, Fei Yan, Ling Qing
Format: Article
Language:English
Published: BMC 2018-06-01
Series:Virology Journal
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12985-018-1014-7
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author Gentu Wu
Guixian Zheng
Qiao Hu
Mingge Ma
Mingjun Li
Xianchao Sun
Fei Yan
Ling Qing
author_facet Gentu Wu
Guixian Zheng
Qiao Hu
Mingge Ma
Mingjun Li
Xianchao Sun
Fei Yan
Ling Qing
author_sort Gentu Wu
collection DOAJ
description Abstract Background Rice stripe virus (RSV) belongs to the genus Tenuivirus. It is transmitted by small brown planthoppers in a persistent and circulative-propagative manner and causes rice stripe disease (RSD). The NS3 protein of RSV, encoded by the viral strand of RNA3, is a viral suppressor of RNA silencing (VSR). NS3 plays a significant role in viral infection, and NS3-transgenic plants manifest resistance to the virus. Methods The stability and availability of NS3 produced by transgenic Nicotiana benthamiana was investigated by northern blot analysis. The accumulation of virus was detected by western blot analysis. Transcriptome sequencing was used to identify differentially expressed genes (DEGs) in NS3-transgenic N. benthamiana. Results When the host plants were inoculated with RSV, symptoms and viral accumulation in NS3-transgenic N. benthamiana were reduced compared with the wild type. Transcriptome analysis identified 2533 differentially expressed genes (DEGs) in the NS3-transgenic N. benthamiana, including 597 upregulated genes and 1936 downregulated genes. These DEGs were classified into three Gene Ontology (GO) categories and were associated with 43 GO terms. KEGG pathway analysis revealed that these DEGs were involved in pathways associated with ribosomes (ko03010), photosynthesis (ko00195), photosynthesis-antenna proteins (ko00196), and carbon metabolism (ko01200). More than 70 DEGs were in these four pathways. Twelve DEGs were selected for RT-qPCR verification and subsequent analysis. The results showed that NS3 induced host resistance by affecting host gene expression. Conclusion NS3, which plays dual roles in the process of infection, may act as a VSR during RSV infection, and enable viral resistance in transgenic host plants. NS3 from RSV affects the expression of genes associated with ribosomes, photosynthesis, and carbon metabolism in N. benthamiana. This study enhances our understanding of the interactions between VSRs and host plants.
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spelling doaj.art-286cac905b6947e1ad19bf2877052d522022-12-22T00:48:54ZengBMCVirology Journal1743-422X2018-06-0115111010.1186/s12985-018-1014-7NS3 Protein from Rice stripe virus affects the expression of endogenous genes in Nicotiana benthamianaGentu Wu0Guixian Zheng1Qiao Hu2Mingge Ma3Mingjun Li4Xianchao Sun5Fei Yan6Ling Qing7Chongqing Key Laboratory of Plant Disease Biology, College of Plant Protection, Southwest UniversityChongqing Key Laboratory of Plant Disease Biology, College of Plant Protection, Southwest UniversityChongqing Key Laboratory of Plant Disease Biology, College of Plant Protection, Southwest UniversityChongqing Key Laboratory of Plant Disease Biology, College of Plant Protection, Southwest UniversityChongqing Key Laboratory of Plant Disease Biology, College of Plant Protection, Southwest UniversityChongqing Key Laboratory of Plant Disease Biology, College of Plant Protection, Southwest UniversityThe State Key Laboratory Breading Base for Sustainable Control of Pest and Disease, Key Laboratory of Biotechnology in Plant Protection of MOA of China and Zhejiang Province, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural SciencesChongqing Key Laboratory of Plant Disease Biology, College of Plant Protection, Southwest UniversityAbstract Background Rice stripe virus (RSV) belongs to the genus Tenuivirus. It is transmitted by small brown planthoppers in a persistent and circulative-propagative manner and causes rice stripe disease (RSD). The NS3 protein of RSV, encoded by the viral strand of RNA3, is a viral suppressor of RNA silencing (VSR). NS3 plays a significant role in viral infection, and NS3-transgenic plants manifest resistance to the virus. Methods The stability and availability of NS3 produced by transgenic Nicotiana benthamiana was investigated by northern blot analysis. The accumulation of virus was detected by western blot analysis. Transcriptome sequencing was used to identify differentially expressed genes (DEGs) in NS3-transgenic N. benthamiana. Results When the host plants were inoculated with RSV, symptoms and viral accumulation in NS3-transgenic N. benthamiana were reduced compared with the wild type. Transcriptome analysis identified 2533 differentially expressed genes (DEGs) in the NS3-transgenic N. benthamiana, including 597 upregulated genes and 1936 downregulated genes. These DEGs were classified into three Gene Ontology (GO) categories and were associated with 43 GO terms. KEGG pathway analysis revealed that these DEGs were involved in pathways associated with ribosomes (ko03010), photosynthesis (ko00195), photosynthesis-antenna proteins (ko00196), and carbon metabolism (ko01200). More than 70 DEGs were in these four pathways. Twelve DEGs were selected for RT-qPCR verification and subsequent analysis. The results showed that NS3 induced host resistance by affecting host gene expression. Conclusion NS3, which plays dual roles in the process of infection, may act as a VSR during RSV infection, and enable viral resistance in transgenic host plants. NS3 from RSV affects the expression of genes associated with ribosomes, photosynthesis, and carbon metabolism in N. benthamiana. This study enhances our understanding of the interactions between VSRs and host plants.http://link.springer.com/article/10.1186/s12985-018-1014-7Rice stripe virusNS3Suppressor of RNA silencingNicotiana benthamianaTranscriptomes
spellingShingle Gentu Wu
Guixian Zheng
Qiao Hu
Mingge Ma
Mingjun Li
Xianchao Sun
Fei Yan
Ling Qing
NS3 Protein from Rice stripe virus affects the expression of endogenous genes in Nicotiana benthamiana
Virology Journal
Rice stripe virus
NS3
Suppressor of RNA silencing
Nicotiana benthamiana
Transcriptomes
title NS3 Protein from Rice stripe virus affects the expression of endogenous genes in Nicotiana benthamiana
title_full NS3 Protein from Rice stripe virus affects the expression of endogenous genes in Nicotiana benthamiana
title_fullStr NS3 Protein from Rice stripe virus affects the expression of endogenous genes in Nicotiana benthamiana
title_full_unstemmed NS3 Protein from Rice stripe virus affects the expression of endogenous genes in Nicotiana benthamiana
title_short NS3 Protein from Rice stripe virus affects the expression of endogenous genes in Nicotiana benthamiana
title_sort ns3 protein from rice stripe virus affects the expression of endogenous genes in nicotiana benthamiana
topic Rice stripe virus
NS3
Suppressor of RNA silencing
Nicotiana benthamiana
Transcriptomes
url http://link.springer.com/article/10.1186/s12985-018-1014-7
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