CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication

Carbon catabolite repression 4 (CCR4) is a conserved mRNA deadenylase regulating posttranscriptional gene expression. However, regulation of CCR4 in virus infections is less understood. Here, we characterized a pro-viral role of CCR4 in replication of a plant cytorhabdovirus, Barley yellow striate m...

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Main Authors: Zhen-Jia Zhang, Qiang Gao, Xiao-Dong Fang, Zhi-Hang Ding, Dong-Min Gao, Wen-Ya Xu, Qing Cao, Ji-Hui Qiao, Yi-Zhou Yang, Chenggui Han, Ying Wang, Xuefeng Yuan, Dawei Li, Xian-Bing Wang
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/53753
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spelling doaj-0027be40e7844874a1c92c0a75f2d8a62021-05-05T20:56:36ZengeLife Sciences Publications LtdeLife2050-084X2020-03-01910.7554/eLife.53753CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replicationZhen-Jia Zhang0https://orcid.org/0000-0003-0473-2738Qiang Gao1Xiao-Dong Fang2Zhi-Hang Ding3Dong-Min Gao4Wen-Ya Xu5Qing Cao6Ji-Hui Qiao7Yi-Zhou Yang8Chenggui Han9Ying Wang10Xuefeng Yuan11Dawei Li12Xian-Bing Wang13https://orcid.org/0000-0003-3082-2462State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaCollege of Plant Protection, China Agricultural University, Beijing, ChinaCollege of Plant Protection, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology, College of Plant Protection, Shandong Agricultural University, Shandong Province Key Laboratory of Agricultural Microbiology, Tai'an, ChinaState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, ChinaCarbon catabolite repression 4 (CCR4) is a conserved mRNA deadenylase regulating posttranscriptional gene expression. However, regulation of CCR4 in virus infections is less understood. Here, we characterized a pro-viral role of CCR4 in replication of a plant cytorhabdovirus, Barley yellow striate mosaic virus (BYSMV). The barley (Hordeum vulgare) CCR4 protein (HvCCR4) was identified to interact with the BYSMV phosphoprotein (P). The BYSMV P protein recruited HvCCR4 from processing bodies (PBs) into viroplasm-like bodies. Overexpression of HvCCR4 promoted BYSMV replication in plants. Conversely, knockdown of the small brown planthopper CCR4 inhibited viral accumulation in the insect vector. Biochemistry experiments revealed that HvCCR4 was recruited into N–RNA complexes by the BYSMV P protein and triggered turnover of N-bound cellular mRNAs, thereby releasing RNA-free N protein to bind viral genomic RNA for optimal viral replication. Our results demonstrate that the co-opted CCR4-mediated RNA decay facilitates cytorhabdovirus replication in plants and insects.https://elifesciences.org/articles/53753plant cytorhabdovirusphosphoproteinCCR4RNA decayvirus-plant interactionbarley
collection DOAJ
language English
format Article
sources DOAJ
author Zhen-Jia Zhang
Qiang Gao
Xiao-Dong Fang
Zhi-Hang Ding
Dong-Min Gao
Wen-Ya Xu
Qing Cao
Ji-Hui Qiao
Yi-Zhou Yang
Chenggui Han
Ying Wang
Xuefeng Yuan
Dawei Li
Xian-Bing Wang
spellingShingle Zhen-Jia Zhang
Qiang Gao
Xiao-Dong Fang
Zhi-Hang Ding
Dong-Min Gao
Wen-Ya Xu
Qing Cao
Ji-Hui Qiao
Yi-Zhou Yang
Chenggui Han
Ying Wang
Xuefeng Yuan
Dawei Li
Xian-Bing Wang
CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication
eLife
plant cytorhabdovirus
phosphoprotein
CCR4
RNA decay
virus-plant interaction
barley
author_facet Zhen-Jia Zhang
Qiang Gao
Xiao-Dong Fang
Zhi-Hang Ding
Dong-Min Gao
Wen-Ya Xu
Qing Cao
Ji-Hui Qiao
Yi-Zhou Yang
Chenggui Han
Ying Wang
Xuefeng Yuan
Dawei Li
Xian-Bing Wang
author_sort Zhen-Jia Zhang
title CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication
title_short CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication
title_full CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication
title_fullStr CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication
title_full_unstemmed CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication
title_sort ccr4, a rna decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-03-01
description Carbon catabolite repression 4 (CCR4) is a conserved mRNA deadenylase regulating posttranscriptional gene expression. However, regulation of CCR4 in virus infections is less understood. Here, we characterized a pro-viral role of CCR4 in replication of a plant cytorhabdovirus, Barley yellow striate mosaic virus (BYSMV). The barley (Hordeum vulgare) CCR4 protein (HvCCR4) was identified to interact with the BYSMV phosphoprotein (P). The BYSMV P protein recruited HvCCR4 from processing bodies (PBs) into viroplasm-like bodies. Overexpression of HvCCR4 promoted BYSMV replication in plants. Conversely, knockdown of the small brown planthopper CCR4 inhibited viral accumulation in the insect vector. Biochemistry experiments revealed that HvCCR4 was recruited into N–RNA complexes by the BYSMV P protein and triggered turnover of N-bound cellular mRNAs, thereby releasing RNA-free N protein to bind viral genomic RNA for optimal viral replication. Our results demonstrate that the co-opted CCR4-mediated RNA decay facilitates cytorhabdovirus replication in plants and insects.
topic plant cytorhabdovirus
phosphoprotein
CCR4
RNA decay
virus-plant interaction
barley
url https://elifesciences.org/articles/53753
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