Rice black‐streaked dwarf virus P10 acts as either a synergistic or antagonistic determinant during superinfection with related or unrelated virus

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

doi:10.1111/mpp.12782

Rice black‐streaked dwarf virus P10 acts as either a synergistic or antagonistic determinant during superinfection with related or unrelated virus

Journal Article · Thu Feb 14 00:00:00 EST 2019 · Molecular Plant Pathology

DOI:https://doi.org/10.1111/mpp.12782· OSTI ID:1494778

Zhang, Hehong ^[1]; Tan, Xiaoxiang ^[2]; ^[3]; Xie, Kaili ^[1]; Li, Lulu ^[3]; Wang, Rong ^[4]; Hong, Gaojie ^[3]; Li, Junmin ^[5]; Li, Jing ^[3]; Taliansky, Michael ^[6]; MacFarlane, Stuart ^[6]; ^[5]; Chen, Jianping ^[1]; ^[1]

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

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.

View Journal Article

Sponsoring Organization:: USDOE

OSTI ID:: 1494778

Alternate ID(s):: OSTI ID: 1494779

Journal Information:: Molecular Plant Pathology, Journal Name: Molecular Plant Pathology Journal Issue: 5 Vol. 20; ISSN 1464-6722

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (55)

Identification of virus-derived siRNAs and their targets in RBSDV-infected rice by deep sequencing Lan, Ying; Li, Yanwu; E., Zhiguo Journal of Basic Microbiology, Vol. 58, Issue 3 https://doi.org/10.1002/jobm.201700325	journal	December 2017
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
The secretory pathway and the actomyosin motility system are required for plasmodesmatal localization of the P7-1 of rice black-streaked dwarf virus Sun, Zongtao; Zhang, Shanglin; Xie, Li Archives of Virology, Vol. 158, Issue 5 https://doi.org/10.1007/s00705-012-1585-3	journal	December 2012
HC-Pro, a potyvirus RNA silencing suppressor, cancels cycling of Cucumber mosaic virus in Nicotiana benthamiana plants Fukuzawa, Noriho; Itchoda, Noriko; Ishihara, Takeaki Virus Genes, Vol. 40, Issue 3 https://doi.org/10.1007/s11262-010-0460-0	journal	February 2010
Rice black-streaked dwarf virus: Its properties, morphology and intracellular localization Shikata, Eishiro; Kitagawa, Yoshichika Virology, Vol. 77, Issue 2 https://doi.org/10.1016/0042-6822(77)90502-5	journal	April 1977
Replication of potato virus X RNA is altered in coinfections with potato virus Y bance, Vicki Bowman Virology, Vol. 182, Issue 2 https://doi.org/10.1016/0042-6822(91)90589-4	journal	June 1991
Transmission characteristics of Southern rice black-streaked dwarf virus by rice planthoppers Pu, Lingling; Xie, Guohua; Ji, Chunyan Crop Protection, Vol. 41 https://doi.org/10.1016/j.cropro.2012.04.026	journal	November 2012
Rice black-streaked dwarf virus minor core protein P8 is a nuclear dimeric protein and represses transcription in tobacco protoplasts Liu, Huijun; Wei, Chunhong; Zhong, Yongwang FEBS Letters, Vol. 581, Issue 13 https://doi.org/10.1016/j.febslet.2007.04.071	journal	May 2007
One-step multiplex reverse transcription-polymerase chain reaction for the simultaneous detection of three rice viruses Cho, Sang-Yun; Jeong, Rae-Dong; Yoon, Young-Nam Journal of Virological Methods, Vol. 193, Issue 2 https://doi.org/10.1016/j.jviromet.2013.07.008	journal	November 2013
A simplified method for simultaneous detection of Rice stripe virus and Rice black-streaked dwarf virus in insect vector Li, Shuo; Wang, Xi; Xu, Jianxiang Journal of Virological Methods, Vol. 211 https://doi.org/10.1016/j.jviromet.2014.10.006	journal	January 2015
Structure and components of the globular and filamentous viroplasms induced by Rice black-streaked dwarf virus Xie, Li; Lv, Ming-fang; Song, Xi-Jiao Micron, Vol. 98 https://doi.org/10.1016/j.micron.2017.03.002	journal	July 2017
Aggregation of TMV CP plays a role in CP functions and in coat-protein-mediated resistance Asurmendi, S.; Berg, R. H.; Smith, T. J. Virology, Vol. 366, Issue 1 https://doi.org/10.1016/j.virol.2007.03.014	journal	September 2007
Coat protein-mediated resistance to TMV infection of Nicotiana tabacum involves multiple modes of interference by coat protein Bendahmane, Mohammed; Chen, Iju; Asurmendi, Sebastian Virology, Vol. 366, Issue 1 https://doi.org/10.1016/j.virol.2007.03.052	journal	September 2007
Rice black-streaked dwarf virus P10 induces membranous structures at the ER and elicits the unfolded protein response in Nicotiana benthamiana Sun, Zongtao; Yang, Di; Xie, Li Virology, Vol. 447, Issue 1-2 https://doi.org/10.1016/j.virol.2013.09.001	journal	December 2013
P3N-PIPO of Clover yellow vein virus exacerbates symptoms in pea infected with White clover mosaic virus and is implicated in viral synergism Hisa, Yusuke; Suzuki, Haruka; Atsumi, Go Virology, Vol. 449 https://doi.org/10.1016/j.virol.2013.11.016	journal	January 2014
Antagonism or synergism between papaya ringspot virus and papaya mosaic virus in Carica papaya is determined by their order of infection Chávez-Calvillo, Gabriela; Contreras-Paredes, Carlos A.; Mora-Macias, Javier Virology, Vol. 489 https://doi.org/10.1016/j.virol.2015.11.026	journal	February 2016
Rice black-streaked dwarf virus outer capsid protein P10 has self-interactions and forms oligomeric complexes in solution Liu, Huijun; Wei, Chunhong; Zhong, Yongwang Virus Research, Vol. 127, Issue 1 https://doi.org/10.1016/j.virusres.2007.03.017	journal	July 2007
Characterization of RNA–Mediated Resistance to Tomato Spotted Wilt Virus in Transgenic Tobacco Plants Haan, Peter de; Gielen, Jan J. L.; Prins, Marcel Nature Biotechnology, Vol. 10, Issue 10 https://doi.org/10.1038/nbt1092-1133	journal	October 1992
STV11 encodes a sulphotransferase and confers durable resistance to rice stripe virus Wang, Qi; Liu, Yuqiang; He, Jun Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5768	journal	September 2014
Genome-Wide Characterization of Rice Black Streaked Dwarf Virus-Responsive MicroRNAs in Rice Leaves and Roots by Small RNA and Degradome Sequencing Sun, Zongtao; He, Yuqing; Li, Junmin Plant and Cell Physiology, Vol. 56, Issue 4 https://doi.org/10.1093/pcp/pcu213	journal	December 2014
Mapping of Viral Genomic Regions Important in Cross-Protection Between Strains of a Potyvirus Valkonen, Jari P. T.; Rajamäki, Minna-Liisa; Kekarainen, Tuija Molecular Plant-Microbe Interactions, Vol. 15, Issue 7 https://doi.org/10.1094/MPMI.2002.15.7.683	journal	July 2002
Synergistic Interaction of Sweet potato chlorotic stunt virus ( Crinivirus ) with Carla-, Cucumo-, Ipomo-, and Potyviruses Infecting Sweet Potato Untiveros, Milton; Fuentes, Segundo; Salazar, Luis F. Plant Disease, Vol. 91, Issue 6 https://doi.org/10.1094/PDIS-91-6-0669	journal	June 2007
Synergism Between Southern rice black-streaked dwarf virus and Rice ragged stunt virus Enhances Their Insect Vector Acquisition Li, Shu; Wang, Han; Zhou, Guohui Phytopathology, Vol. 104, Issue 7 https://doi.org/10.1094/PHYTO-11-13-0319-R	journal	July 2014
The Impact of “Coat Protein-Mediated Virus Resistance” in Applied Plant Pathology and Basic Research Lindbo, John A.; Falk, Bryce W. Phytopathology, Vol. 107, Issue 6 https://doi.org/10.1094/PHYTO-12-16-0442-RVW	journal	June 2017
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 Capote, Nieves; Gorris, M. Teresa; Martínez, M. Carmen Phytopathology, Vol. 96, Issue 3 https://doi.org/10.1094/PHYTO-96-0320	journal	March 2006
Synergistic Interaction Between Tomato chlorosis virus and Tomato spotted wilt virus Results in Breakdown of Resistance in Tomato García-Cano, Elena; Resende, Renato O.; Fernández-Muñoz, Rafael Phytopathology, Vol. 96, Issue 11 https://doi.org/10.1094/PHYTO-96-1263	journal	November 2006
Detection and assignment of proteins encoded by rice black streaked dwarf fijivirus S7, S8, S9 and S10. Lee, B. C.; Isogai, M.; Uyeda, I. Journal of General Virology, Vol. 79, Issue 6 https://doi.org/10.1099/0022-1317-79-6-1487	journal	June 1998
Initial infection of roots and leaves reveals different resistance phenotypes associated with coat protein gene-mediated resistance to Potato mop-top virus Germundsson, Anna; Barker, Hugh; Valkonen, Jari P. T. Journal of General Virology, Vol. 83, Issue 5 https://doi.org/10.1099/0022-1317-83-5-1201	journal	May 2002
Genetic diversity and population structure of rice stripe virus in China Wei, T. -Y.; Yang, J. -G.; Liao, F. -L. Journal of General Virology, Vol. 90, Issue 4 https://doi.org/10.1099/vir.0.006858-0	journal	March 2009
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 Ziebell, H.; Carr, J. P. Journal of General Virology, Vol. 90, Issue 9 https://doi.org/10.1099/vir.0.012070-0	journal	May 2009
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 Sun, L.; Xie, L.; Andika, I. B. Journal of General Virology, Vol. 94, Issue Pt_8 https://doi.org/10.1099/vir.0.051698-0	journal	May 2013
A cucumber mosaic virus mutant lacking the 2b counter-defence protein gene provides protection against wild-type strains Ziebell, H.; Payne, T.; Berry, J. O. Journal of General Virology, Vol. 88, Issue 10 https://doi.org/10.1099/vir.0.83138-0	journal	October 2007
Gene Silencing without DNA: RNA-Mediated Cross-Protection between Viruses Ratcliff, Frank G.; MacFarlane, Stuart A.; Baulcombe, David C. The Plant Cell, Vol. 11, Issue 7 https://doi.org/10.1105/tpc.11.7.1207	journal	July 1999
Host-dependent differences during synergistic infection by Potyviruses with potato virus X Gonzalez-Jara, P.; Tenllado, F.; Martinez-Garcia, B. Molecular Plant Pathology, Vol. 5, Issue 1 https://doi.org/10.1111/j.1364-3703.2004.00202.x	journal	January 2004
Transcomplementation and synergism in plants: implications for viral transgenes? Latham, Jonathan R.; Wilson, Allison K. Molecular Plant Pathology, Vol. 0, Issue 0 https://doi.org/10.1111/j.1364-3703.2007.00441.x	journal	November 2007
Facilitative and antagonistic interactions between plant viruses in mixed infections: Plant virus interactions in mixed infections Syller, Jerzy Molecular Plant Pathology, Vol. 13, Issue 2 https://doi.org/10.1111/j.1364-3703.2011.00734.x	journal	July 2011
C2 from Beet curly top virus promotes a cell environment suitable for efficient replication of geminiviruses, providing a novel mechanism of viral synergism Caracuel, Zaira; Lozano-Durán, Rosa; Huguet, Stéphanie New Phytologist, Vol. 194, Issue 3 https://doi.org/10.1111/j.1469-8137.2012.04080.x	journal	March 2012
Antagonistic within-host interactions between plant viruses: molecular basis and impact on viral and host fitness: Antagonistic interactions between plant viruses Syller, Jerzy; Grupa, Anna Molecular Plant Pathology, Vol. 17, Issue 5 https://doi.org/10.1111/mpp.12322	journal	December 2015
Jasmonic acid-mediated defense suppresses brassinosteroid-mediated susceptibility to Rice black streaked dwarf virus infection in rice He, Yuqing; Zhang, Hehong; Sun, Zongtao New Phytologist, Vol. 214, Issue 1 https://doi.org/10.1111/nph.14376	journal	December 2016
Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene Abel, P.; Nelson, R.; De, B. Science, Vol. 232, Issue 4751 https://doi.org/10.1126/science.3457472	journal	May 1986
Crystallographic Analysis Reveals Octamerization of Viroplasm Matrix Protein P9-1 of Rice Black Streaked Dwarf Virus Akita, F.; Higashiura, A.; Shimizu, T. Journal of Virology, Vol. 86, Issue 2 https://doi.org/10.1128/JVI.00826-11	journal	November 2011
The Coat Protein and NIa Protease of Two Potyviridae Family Members Independently Confer Superinfection Exclusion Tatineni, Satyanarayana; French, Roy Journal of Virology, Vol. 90, Issue 23 https://doi.org/10.1128/JVI.01697-16	journal	September 2016
Infection with Strains of Citrus Tristeza Virus Does Not Exclude Superinfection by Other Strains of the Virus Folimonova, S. Y.; Robertson, C. J.; Shilts, T. Journal of Virology, Vol. 84, Issue 3 https://doi.org/10.1128/JVI.02075-09	journal	November 2009
Rice Reoviruses in Insect Vectors Wei, Taiyun; Li, Yi Annual Review of Phytopathology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev-phyto-080615-095900	journal	August 2016
CONTROL OF PAPAYA RINGSPOT VIRUS IN PAPAYA: A Case Study Gonsalves, Dennis Annual Review of Phytopathology, Vol. 36, Issue 1 https://doi.org/10.1146/annurev.phyto.36.1.415	journal	September 1998
Coat Protein-Mediated Resistance Against Virus Infection Beachy, R. N.; Loesch-Fries, S.; Tumer, N. E. Annual Review of Phytopathology, Vol. 28, Issue 1 https://doi.org/10.1146/annurev.py.28.090190.002315	journal	September 1990
Enhanced transgene expression in rice following selection controlled by weak promoters Zhou, Jie; Yang, Yong; Wang, Xuming BMC Biotechnology, Vol. 13, Issue 1 https://doi.org/10.1186/1472-6750-13-29	journal	January 2013
Development and use of three monoclonal antibodies for the detection of rice black-streaked dwarf virus in field plants and planthopper vectors Wu, Jianxiang; Ni, Yuequn; Liu, Huan Virology Journal, Vol. 10, Issue 1 https://doi.org/10.1186/1743-422X-10-114	journal	January 2013
Distribution and genetic diversity of Southern rice black-streaked dwarf virus in China Cheng, Zhaobang; Li, Shuo; Gao, Ruizhen Virology Journal, Vol. 10, Issue 1 https://doi.org/10.1186/1743-422X-10-307	journal	January 2013
Rice black-streaked dwarf virus P6 self-interacts to form punctate, viroplasm-like structures in the cytoplasm and recruits viroplasm-associated protein P9-1 Wang, Qian; Tao, Tao; Zhang, Yanjing Virology Journal, Vol. 8, Issue 1 https://doi.org/10.1186/1743-422X-8-24	journal	January 2011
Characterization of Rice Black-Streaked Dwarf Virus- and Rice Stripe Virus-Derived siRNAs in Singly and Doubly Infected Insect Vector Laodelphax striatellus Li, Junmin; Andika, Ida Bagus; Shen, Jiangfeng PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0066007	journal	June 2013
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 Tao, Tao; Zhou, Cui-Ji; Wang, Qian PLOS ONE, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pone.0177518	journal	May 2017
A self-perpetuating repressive state of a viral replication protein blocks superinfection by the same virus Zhang, Xiao-Feng; Sun, Rong; Guo, Qin PLOS Pathogens, Vol. 13, Issue 3 https://doi.org/10.1371/journal.ppat.1006253	journal	March 2017
Developing an understanding of cross-protection by Citrus tristeza virus Folimonova, Svetlana Y. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00076	journal	January 2013
Southern rice black-streaked dwarf virus: a white-backed planthopper-transmitted fijivirus threatening rice production in Asia Zhou, Guohui; Xu, Donglin; Xu, Dagao Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00270	journal	January 2013

Similar Records

Respiratory syncytial virus M2-1 protein induces the activation of nuclear factor kappa B

Journal Article · Wed Jan 19 23:00:00 EST 2005 · Virology · OSTI ID:20637195

Rice black‐streaked dwarf virus P10 acts as either a synergistic or antagonistic determinant during superinfection with related or unrelated virus

Citation Formats

References (55)

Similar Records

Related Subjects