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Casein Kinase 1 Regulates Cytorhabdovirus Replication and Transcription by Phosphorylating a Phosphoprotein Serine-Rich Motif

Qiang Gao, Teng Yan, Zhen-Jia Zhang, Song-Yu Liu, Xiao-Dong Fang, Dong-Min Gao, Yi-Zhou Yang, Wen-Ya Xu, Ji-Hui Qiao, Qing Cao, Zhi-Hang Ding, Ying Wang, Jialin Yu, Xian-Bing Wang
Qiang Gao
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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  • ORCID record for Qiang Gao
Teng Yan
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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  • ORCID record for Teng Yan
Zhen-Jia Zhang
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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  • ORCID record for Zhen-Jia Zhang
Song-Yu Liu
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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  • ORCID record for Song-Yu Liu
Xiao-Dong Fang
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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  • ORCID record for Xiao-Dong Fang
Dong-Min Gao
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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  • ORCID record for Dong-Min Gao
Yi-Zhou Yang
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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  • ORCID record for Yi-Zhou Yang
Wen-Ya Xu
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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Ji-Hui Qiao
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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Qing Cao
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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  • ORCID record for Qing Cao
Zhi-Hang Ding
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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Ying Wang
bCollege of Plant Protection, China Agricultural University, Beijing 100193, China
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Jialin Yu
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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Xian-Bing Wang
aState Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China
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  • ORCID record for Xian-Bing Wang
  • For correspondence: wangxianbing@cau.edu.cn

Published September 2020. DOI: https://doi.org/10.1105/tpc.20.00369

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  • © 2020 American Society of Plant Biologists. All rights reserved.

Abstract

Casein kinase 1 (CK1) family members are conserved Ser/Thr protein kinases that regulate important developmental processes in all eukaryotic organisms. However, the functions of CK1 in plant immunity remain largely unknown. Barley yellow striate mosaic virus (BYSMV), a plant cytorhabdovirus, infects cereal crops and is obligately transmitted by the small brown planthopper (SBPH; Laodelphax striatellus). The BYSMV phosphoprotein (P) exists as two forms with different mobilities corresponding to 42 kD (P42) and 44 kD (P44) in SDS-PAGE gels. Mass spectrometric analyses revealed a highly phosphorylated serine-rich (SR) motif at the C-terminal intrinsically disordered region of the P protein. The Ala-substitution mutant (PS5A) in the SR motif stimulated virus replication, whereas the phosphorylation-mimic mutant (PS5D) facilitated virus transcription. Furthermore, PS5A and PS5D associated preferentially with nucleocapsid protein–RNA templates and the large polymerase protein to provide optimal replication and transcription complexes, respectively. Biochemistry assays demonstrated that plant and insect CK1 protein kinases could phosphorylate the SR motif and induce conformational changes from P42 to P44. Moreover, overexpression of CK1 or a dominant-negative mutant impaired the balance between P42 and P44, thereby compromising virus infections. Our results demonstrate that BYSMV recruits the conserved CK1 kinases to achieve its cross-kingdom infection in host plants and insect vectors.

  • Received May 11, 2020.
  • Revised June 24, 2020.
  • Accepted July 7, 2020.
  • Published July 8, 2020.
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Casein Kinase 1 Regulates Cytorhabdovirus Replication and Transcription by Phosphorylating a Phosphoprotein Serine-Rich Motif
Qiang Gao, Teng Yan, Zhen-Jia Zhang, Song-Yu Liu, Xiao-Dong Fang, Dong-Min Gao, Yi-Zhou Yang, Wen-Ya Xu, Ji-Hui Qiao, Qing Cao, Zhi-Hang Ding, Ying Wang, Jialin Yu, Xian-Bing Wang
The Plant Cell Sep 2020, 32 (9) 2878-2897; DOI: 10.1105/tpc.20.00369

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Casein Kinase 1 Regulates Cytorhabdovirus Replication and Transcription by Phosphorylating a Phosphoprotein Serine-Rich Motif
Qiang Gao, Teng Yan, Zhen-Jia Zhang, Song-Yu Liu, Xiao-Dong Fang, Dong-Min Gao, Yi-Zhou Yang, Wen-Ya Xu, Ji-Hui Qiao, Qing Cao, Zhi-Hang Ding, Ying Wang, Jialin Yu, Xian-Bing Wang
The Plant Cell Sep 2020, 32 (9) 2878-2897; DOI: 10.1105/tpc.20.00369
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The Plant Cell: 32 (9)
The Plant Cell
Vol. 32, Issue 9
Sep 2020
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