Rice black‐streaked dwarf virus P10 acts as either a synergistic or antagonistic determinant during superinfection with related or unrelated virus
Abstract
Summary Rice black‐streaked dwarf virus (RBSDV), a member of the genus Fijivirus , is a devastating pathogen of crop plants. RBSDV S10 encodes a capsid protein (P10) that is an important component of the double‐layered particle. However, little information is available on the roles of RBSDV P10 in viral infection or in interactions with other viruses. Here, we demonstrate that the expression of P10 in plants alleviates the symptoms of both RBSDV and the closely related Southern rice black‐streaked dwarf virus (SRBSDV), and reduces the disease incidence, but renders the plants more susceptible to the unrelated Rice stripe virus (RSV). Further experiments suggest that P10‐mediated resistance to RBSDV and SRBSDV operates at the protein level, rather than the RNA level, and is not a result of post‐transcriptional gene silencing. Transcriptomic data reveal that the expression of P10 in plants significantly suppresses the expression of rice defence‐related genes, which may play important roles in resistance to RSV infection. After infection with RBSDV, plants are more resistant to subsequent challenge by SRBSDV, but more susceptible to RSV. Overall, these results indicate that P10 acts as an important effector in virus interactions.
- Authors:
-
- Institute of Plant Virology Ningbo University Ningbo 315211 China, College of Plant Protection Nanjing Agricultural University Nanjing 210095 China, The State Key Laboratory Breeding 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 Sciences Hangzhou 310021 China
- Institute of Plant Virology Ningbo University Ningbo 315211 China, College of Plant Protection Northwest Agriculture and Forestry University Yangling 712100 Shaanxi China
- The State Key Laboratory Breeding 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 Sciences Hangzhou 310021 China
- Institute of Plant Virology Ningbo University Ningbo 315211 China, College of Plant Protection Nanjing Agricultural University Nanjing 210095 China
- Institute of Plant Virology Ningbo University Ningbo 315211 China
- The James Hutton Institute, Cell and Molecular Sciences Group Invergowrie Dundee DD2 5DA UK
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1494778
- Alternate Identifier(s):
- OSTI ID: 1494779
- Resource Type:
- Published Article
- Journal Name:
- Molecular Plant Pathology
- Additional Journal Information:
- Journal Name: Molecular Plant Pathology Journal Volume: 20 Journal Issue: 5; Journal ID: ISSN 1464-6722
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Zhang, Hehong, Tan, Xiaoxiang, He, Yuqing, Xie, Kaili, Li, Lulu, Wang, Rong, Hong, Gaojie, Li, Junmin, Li, Jing, Taliansky, Michael, MacFarlane, Stuart, Yan, Fei, Chen, Jianping, and Sun, Zongtao. Rice black‐streaked dwarf virus P10 acts as either a synergistic or antagonistic determinant during superinfection with related or unrelated virus. United Kingdom: N. p., 2019.
Web. doi:10.1111/mpp.12782.
Zhang, Hehong, Tan, Xiaoxiang, He, Yuqing, Xie, Kaili, Li, Lulu, Wang, Rong, Hong, Gaojie, Li, Junmin, Li, Jing, Taliansky, Michael, MacFarlane, Stuart, Yan, Fei, Chen, Jianping, & Sun, Zongtao. Rice black‐streaked dwarf virus P10 acts as either a synergistic or antagonistic determinant during superinfection with related or unrelated virus. United Kingdom. https://doi.org/10.1111/mpp.12782
Zhang, Hehong, Tan, Xiaoxiang, He, Yuqing, Xie, Kaili, Li, Lulu, Wang, Rong, Hong, Gaojie, Li, Junmin, Li, Jing, Taliansky, Michael, MacFarlane, Stuart, Yan, Fei, Chen, Jianping, and Sun, Zongtao. Thu .
"Rice black‐streaked dwarf virus P10 acts as either a synergistic or antagonistic determinant during superinfection with related or unrelated virus". United Kingdom. https://doi.org/10.1111/mpp.12782.
@article{osti_1494778,
title = {Rice black‐streaked dwarf virus P10 acts as either a synergistic or antagonistic determinant during superinfection with related or unrelated virus},
author = {Zhang, Hehong and Tan, Xiaoxiang and He, Yuqing and Xie, Kaili and Li, Lulu and Wang, Rong and Hong, Gaojie and Li, Junmin and Li, Jing and Taliansky, Michael and MacFarlane, Stuart and Yan, Fei and Chen, Jianping and Sun, Zongtao},
abstractNote = {Summary Rice black‐streaked dwarf virus (RBSDV), a member of the genus Fijivirus , is a devastating pathogen of crop plants. RBSDV S10 encodes a capsid protein (P10) that is an important component of the double‐layered particle. However, little information is available on the roles of RBSDV P10 in viral infection or in interactions with other viruses. Here, we demonstrate that the expression of P10 in plants alleviates the symptoms of both RBSDV and the closely related Southern rice black‐streaked dwarf virus (SRBSDV), and reduces the disease incidence, but renders the plants more susceptible to the unrelated Rice stripe virus (RSV). Further experiments suggest that P10‐mediated resistance to RBSDV and SRBSDV operates at the protein level, rather than the RNA level, and is not a result of post‐transcriptional gene silencing. Transcriptomic data reveal that the expression of P10 in plants significantly suppresses the expression of rice defence‐related genes, which may play important roles in resistance to RSV infection. After infection with RBSDV, plants are more resistant to subsequent challenge by SRBSDV, but more susceptible to RSV. Overall, these results indicate that P10 acts as an important effector in virus interactions.},
doi = {10.1111/mpp.12782},
journal = {Molecular Plant Pathology},
number = 5,
volume = 20,
place = {United Kingdom},
year = {Thu Feb 14 00:00:00 EST 2019},
month = {Thu Feb 14 00:00:00 EST 2019}
}
https://doi.org/10.1111/mpp.12782
Web of Science
Works referenced in this record:
Facilitative and antagonistic interactions between plant viruses in mixed infections: Plant virus interactions in mixed infections
journal, July 2011
- Syller, Jerzy
- Molecular Plant Pathology, Vol. 13, Issue 2
Distribution and genetic diversity of Southern rice black-streaked dwarf virus in China
journal, January 2013
- Cheng, Zhaobang; Li, Shuo; Gao, Ruizhen
- Virology Journal, Vol. 10, Issue 1
Mapping of Viral Genomic Regions Important in Cross-Protection Between Strains of a Potyvirus
journal, July 2002
- Valkonen, Jari P. T.; Rajamäki, Minna-Liisa; Kekarainen, Tuija
- Molecular Plant-Microbe Interactions, Vol. 15, Issue 7
Replication of potato virus X RNA is altered in coinfections with potato virus Y
journal, June 1991
- bance, Vicki Bowman
- Virology, Vol. 182, Issue 2
Enhanced transgene expression in rice following selection controlled by weak promoters
journal, January 2013
- Zhou, Jie; Yang, Yong; Wang, Xuming
- BMC Biotechnology, Vol. 13, Issue 1
Jasmonic acid-mediated defense suppresses brassinosteroid-mediated susceptibility to Rice black streaked dwarf virus infection in rice
journal, December 2016
- He, Yuqing; Zhang, Hehong; Sun, Zongtao
- New Phytologist, Vol. 214, Issue 1
Southern rice black-streaked dwarf virus: a white-backed planthopper-transmitted fijivirus threatening rice production in Asia
journal, January 2013
- Zhou, Guohui; Xu, Donglin; Xu, Dagao
- Frontiers in Microbiology, Vol. 4
Rice black-streaked dwarf virus outer capsid protein P10 has self-interactions and forms oligomeric complexes in solution
journal, July 2007
- Liu, Huijun; Wei, Chunhong; Zhong, Yongwang
- Virus Research, Vol. 127, Issue 1
Development and use of three monoclonal antibodies for the detection of rice black-streaked dwarf virus in field plants and planthopper vectors
journal, January 2013
- Wu, Jianxiang; Ni, Yuequn; Liu, Huan
- Virology Journal, Vol. 10, Issue 1
Rice black-streaked dwarf virus P6 self-interacts to form punctate, viroplasm-like structures in the cytoplasm and recruits viroplasm-associated protein P9-1
journal, January 2011
- Wang, Qian; Tao, Tao; Zhang, Yanjing
- Virology Journal, Vol. 8, Issue 1
Synergistic Interaction Between Tomato chlorosis virus and Tomato spotted wilt virus Results in Breakdown of Resistance in Tomato
journal, November 2006
- García-Cano, Elena; Resende, Renato O.; Fernández-Muñoz, Rafael
- Phytopathology, Vol. 96, Issue 11
A simplified method for simultaneous detection of Rice stripe virus and Rice black-streaked dwarf virus in insect vector
journal, January 2015
- Li, Shuo; Wang, Xi; Xu, Jianxiang
- Journal of Virological Methods, Vol. 211
Effects of dicer-like endoribonucleases 2 and 4 on infection of Arabidopsis thaliana by cucumber mosaic virus and a mutant virus lacking the 2b counter-defence protein gene
journal, May 2009
- Ziebell, H.; Carr, J. P.
- Journal of General Virology, Vol. 90, Issue 9
Transcomplementation and synergism in plants: implications for viral transgenes?
journal, November 2007
- Latham, Jonathan R.; Wilson, Allison K.
- Molecular Plant Pathology, Vol. 0, Issue 0
Developing an understanding of cross-protection by Citrus tristeza virus
journal, January 2013
- Folimonova, Svetlana Y.
- Frontiers in Microbiology, Vol. 4
One-step multiplex reverse transcription-polymerase chain reaction for the simultaneous detection of three rice viruses
journal, November 2013
- Cho, Sang-Yun; Jeong, Rae-Dong; Yoon, Young-Nam
- Journal of Virological Methods, Vol. 193, Issue 2
A self-perpetuating repressive state of a viral replication protein blocks superinfection by the same virus
journal, March 2017
- Zhang, Xiao-Feng; Sun, Rong; Guo, Qin
- PLOS Pathogens, Vol. 13, Issue 3
A cucumber mosaic virus mutant lacking the 2b counter-defence protein gene provides protection against wild-type strains
journal, October 2007
- Ziebell, H.; Payne, T.; Berry, J. O.
- Journal of General Virology, Vol. 88, Issue 10
STV11 encodes a sulphotransferase and confers durable resistance to rice stripe virus
journal, September 2014
- Wang, Qi; Liu, Yuqiang; He, Jun
- Nature Communications, Vol. 5, Issue 1
Structure and components of the globular and filamentous viroplasms induced by Rice black-streaked dwarf virus
journal, July 2017
- Xie, Li; Lv, Ming-fang; Song, Xi-Jiao
- Micron, Vol. 98
Genetic diversity and population structure of rice stripe virus in China
journal, March 2009
- Wei, T. -Y.; Yang, J. -G.; Liao, F. -L.
- Journal of General Virology, Vol. 90, Issue 4
Rice Reoviruses in Insect Vectors
journal, August 2016
- Wei, Taiyun; Li, Yi
- Annual Review of Phytopathology, Vol. 54, Issue 1
C2 from Beet curly top virus promotes a cell environment suitable for efficient replication of geminiviruses, providing a novel mechanism of viral synergism
journal, March 2012
- Caracuel, Zaira; Lozano-Durán, Rosa; Huguet, Stéphanie
- New Phytologist, Vol. 194, Issue 3
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001
- Livak, Kenneth J.; Schmittgen, Thomas D.
- Methods, Vol. 25, Issue 4
Crystallographic Analysis Reveals Octamerization of Viroplasm Matrix Protein P9-1 of Rice Black Streaked Dwarf Virus
journal, November 2011
- Akita, F.; Higashiura, A.; Shimizu, T.
- Journal of Virology, Vol. 86, Issue 2
Non-structural protein P6 encoded by rice black-streaked dwarf virus is recruited to viral inclusion bodies by binding to the viroplasm matrix protein P9-1
journal, May 2013
- Sun, L.; Xie, L.; Andika, I. B.
- Journal of General Virology, Vol. 94, Issue Pt_8
Initial infection of roots and leaves reveals different resistance phenotypes associated with coat protein gene-mediated resistance to Potato mop-top virus
journal, May 2002
- Germundsson, Anna; Barker, Hugh; Valkonen, Jari P. T.
- Journal of General Virology, Vol. 83, Issue 5
Rice black streaked dwarf virus P7-2 forms a SCF complex through binding to Oryza sativa SKP1-like proteins, and interacts with GID2 involved in the gibberellin pathway
journal, May 2017
- Tao, Tao; Zhou, Cui-Ji; Wang, Qian
- PLOS ONE, Vol. 12, Issue 5
The secretory pathway and the actomyosin motility system are required for plasmodesmatal localization of the P7-1 of rice black-streaked dwarf virus
journal, December 2012
- Sun, Zongtao; Zhang, Shanglin; Xie, Li
- Archives of Virology, Vol. 158, Issue 5
CONTROL OF PAPAYA RINGSPOT VIRUS IN PAPAYA: A Case Study
journal, September 1998
- Gonsalves, Dennis
- Annual Review of Phytopathology, Vol. 36, Issue 1
Infection with Strains of Citrus Tristeza Virus Does Not Exclude Superinfection by Other Strains of the Virus
journal, November 2009
- Folimonova, S. Y.; Robertson, C. J.; Shilts, T.
- Journal of Virology, Vol. 84, Issue 3
Coat Protein-Mediated Resistance Against Virus Infection
journal, September 1990
- Beachy, R. N.; Loesch-Fries, S.; Tumer, N. E.
- Annual Review of Phytopathology, Vol. 28, Issue 1
P3N-PIPO of Clover yellow vein virus exacerbates symptoms in pea infected with White clover mosaic virus and is implicated in viral synergism
journal, January 2014
- Hisa, Yusuke; Suzuki, Haruka; Atsumi, Go
- Virology, Vol. 449
Rice black-streaked dwarf virus P10 induces membranous structures at the ER and elicits the unfolded protein response in Nicotiana benthamiana
journal, December 2013
- Sun, Zongtao; Yang, Di; Xie, Li
- Virology, Vol. 447, Issue 1-2
Gene Silencing without DNA: RNA-Mediated Cross-Protection between Viruses
journal, July 1999
- Ratcliff, Frank G.; MacFarlane, Stuart A.; Baulcombe, David C.
- The Plant Cell, Vol. 11, Issue 7
Synergism Between Southern rice black-streaked dwarf virus and Rice ragged stunt virus Enhances Their Insect Vector Acquisition
journal, July 2014
- Li, Shu; Wang, Han; Zhou, Guohui
- Phytopathology, Vol. 104, Issue 7
The Impact of “Coat Protein-Mediated Virus Resistance” in Applied Plant Pathology and Basic Research
journal, June 2017
- Lindbo, John A.; Falk, Bryce W.
- Phytopathology, Vol. 107, Issue 6
Transmission characteristics of Southern rice black-streaked dwarf virus by rice planthoppers
journal, November 2012
- Pu, Lingling; Xie, Guohua; Ji, Chunyan
- Crop Protection, Vol. 41
Genome-Wide Characterization of Rice Black Streaked Dwarf Virus-Responsive MicroRNAs in Rice Leaves and Roots by Small RNA and Degradome Sequencing
journal, December 2014
- Sun, Zongtao; He, Yuqing; Li, Junmin
- Plant and Cell Physiology, Vol. 56, Issue 4
Synergistic Interaction of Sweet potato chlorotic stunt virus ( Crinivirus ) with Carla-, Cucumo-, Ipomo-, and Potyviruses Infecting Sweet Potato
journal, June 2007
- Untiveros, Milton; Fuentes, Segundo; Salazar, Luis F.
- Plant Disease, Vol. 91, Issue 6
HC-Pro, a potyvirus RNA silencing suppressor, cancels cycling of Cucumber mosaic virus in Nicotiana benthamiana plants
journal, February 2010
- Fukuzawa, Noriho; Itchoda, Noriko; Ishihara, Takeaki
- Virus Genes, Vol. 40, Issue 3
Characterization of RNA–Mediated Resistance to Tomato Spotted Wilt Virus in Transgenic Tobacco Plants
journal, October 1992
- Haan, Peter de; Gielen, Jan J. L.; Prins, Marcel
- Nature Biotechnology, Vol. 10, Issue 10
Detection and assignment of proteins encoded by rice black streaked dwarf fijivirus S7, S8, S9 and S10.
journal, June 1998
- Lee, B. C.; Isogai, M.; Uyeda, I.
- Journal of General Virology, Vol. 79, Issue 6
Identification of virus-derived siRNAs and their targets in RBSDV-infected rice by deep sequencing
journal, December 2017
- Lan, Ying; Li, Yanwu; E., Zhiguo
- Journal of Basic Microbiology, Vol. 58, Issue 3
The Coat Protein and NIa Protease of Two Potyviridae Family Members Independently Confer Superinfection Exclusion
journal, September 2016
- Tatineni, Satyanarayana; French, Roy
- Journal of Virology, Vol. 90, Issue 23
Coat protein-mediated resistance to TMV infection of Nicotiana tabacum involves multiple modes of interference by coat protein
journal, September 2007
- Bendahmane, Mohammed; Chen, Iju; Asurmendi, Sebastian
- Virology, Vol. 366, Issue 1
Antagonism or synergism between papaya ringspot virus and papaya mosaic virus in Carica papaya is determined by their order of infection
journal, February 2016
- Chávez-Calvillo, Gabriela; Contreras-Paredes, Carlos A.; Mora-Macias, Javier
- Virology, Vol. 489
Aggregation of TMV CP plays a role in CP functions and in coat-protein-mediated resistance
journal, September 2007
- Asurmendi, S.; Berg, R. H.; Smith, T. J.
- Virology, Vol. 366, Issue 1
Antagonistic within-host interactions between plant viruses: molecular basis and impact on viral and host fitness: Antagonistic interactions between plant viruses
journal, December 2015
- Syller, Jerzy; Grupa, Anna
- Molecular Plant Pathology, Vol. 17, Issue 5
Interference Between D and M Types of Plum pox virus in Japanese Plum Assessed by Specific Monoclonal Antibodies and Quantitative Real-Time Reverse Transcription-Polymerase Chain Reaction
journal, March 2006
- Capote, Nieves; Gorris, M. Teresa; Martínez, M. Carmen
- Phytopathology, Vol. 96, Issue 3
Host-dependent differences during synergistic infection by Potyviruses with potato virus X
journal, January 2004
- Gonzalez-Jara, P.; Tenllado, F.; Martinez-Garcia, B.
- Molecular Plant Pathology, Vol. 5, Issue 1
Characterization of Rice Black-Streaked Dwarf Virus- and Rice Stripe Virus-Derived siRNAs in Singly and Doubly Infected Insect Vector Laodelphax striatellus
journal, June 2013
- Li, Junmin; Andika, Ida Bagus; Shen, Jiangfeng
- PLoS ONE, Vol. 8, Issue 6
Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene
journal, May 1986
- Abel, P.; Nelson, R.; De, B.
- Science, Vol. 232, Issue 4751
Rice black-streaked dwarf virus minor core protein P8 is a nuclear dimeric protein and represses transcription in tobacco protoplasts
journal, May 2007
- Liu, Huijun; Wei, Chunhong; Zhong, Yongwang
- FEBS Letters, Vol. 581, Issue 13
Rice black-streaked dwarf virus: Its properties, morphology and intracellular localization
journal, April 1977
- Shikata, Eishiro; Kitagawa, Yoshichika
- Virology, Vol. 77, Issue 2