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Journal of Integrative Agriculture  2019, Vol. 18 Issue (10): 2302-2310    DOI: 10.1016/S2095-3119(18)62136-7
Special Issue: 植物病毒合辑Plant Virus
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
Quantitative analysis of the interaction of heterologous viruses with Plum pox virus in C5 HoneySweet transgenic plums
Khushwant Singh, Tereza Neubauerová, Jiban Kumar Kundu
Plant Virus and Vector Interactions Group, Division of Crop Protection and Plant Health, Crop Research Institute, Prague 16106, Czech Republic
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Stone fruits are an important crop in most parts of the world and are heavily challenged by several viruses including Plum pox virus (PPV), Prune dwarf virus (PDV), Prunus necrotic ringspot virus (PNRSV), and Apple chlorotic leaf spot virus (ACLSV).  We validated the PPV resistance in C5 plum plants (commercially known as HoneySweet) grown in the Czech Republic for more than 16 years in a field trial experiment under natural environmental conditions.  We quantified single (PPV-Rec) and mixed viruses (PPV-Rec+ACLSV, PPV-Rec+PDV and PPV-Rec+ACLSV+PDV) in C5 transgenic plums inoculated for the period 2016 to 2018.  The accumulation of PPV-Rec was high (~5.43E+05 copies) compared with that of ACLSV (~8.70E+04 copies) in the inoculated graft of C5 transgenic plants.  Leaves close to the inoculum sources showed a differential level of virus titre in single and mixed infections (~10 to ~5×102 copies).  C5 plants with permanent virus pressure showed 103- to 105-fold fewer copies of viruses than those of the inoculated graft.  We observed high accumulation of conserved miRNAs such as miR167, miR69 and miR396 in C5 plants co-infected with PPV, ACLSV and PDV that are associated with its resistance against viruses.  Overall, i) C5 transgenic plums showed high resistance to PPV infection, and a low level (~32 copies) of PPV only accumulated in some grafted plants, ii) high accumulation of PPV was found in inoculated grafts in single PPV infection and mixed infections, iii) heterologous virus infection sustained by ACLSV or PDV did not suppress PPV resistance, and iv) high and low conserved microRNAs accumulated in C5 plants.
Keywords:  PPV        PDV        ACLSV        C5        HoneySweet        resistance  
Received: 19 October 2018   Accepted: 29 September 2019
Fund: Projects from the Ministry of Agriculture of the Czech Republic (NAZV QJ1610186 and MZE-RO0418) supported this work.
Corresponding Authors:  Correspondence Jiban Kumar Kundu, Tel: +420-233022410, Fax: +420-233310636, E-mail:   
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Khushwant Singh, Tereza Neubauerová, Jiban Kumar Kundu. 2019. Quantitative analysis of the interaction of heterologous viruses with Plum pox virus in C5 HoneySweet transgenic plums. Journal of Integrative Agriculture, 18(10): 2302-2310.

Ai T, Zhang L, Gao Z, Zhu C X, Guo X. 2011. Highly efficient virus resistance mediated by artificial microRNAs that target the suppressor of PVX and PVY in plants. Plant Biology, 13, 304–316.
Bouani A A, Rwahnih M, Ghanem-Sabanadzovic N A, Alami I, Zemzami M, Myrta A, Savino V. 2004. A preliminary account of the sanitary status of stone-fruit trees in Morocco. OEPP/EPPO Bulletin, 34, 399–402.
Chalupniková J, Kundu J K, Singh K, Bartaková P, Beoni E. 2017. Wheat streak mosaic virus: Incidence in field crops, potential reservoir within grass species and uptake in winter wheat cultivars. Journal of Integrative Agriculture, 16, 523–531.
García J A, Glasa M, Cambra M, Candresse T. 2014. Plum pox virus and sharka: A model potyvirus and a major disease. Molecular Plant Pathology, 15, 226–241.
Gümüs M, Paylan I C, Matic S, Myrta A, Sipahioglu H M, Erkan S. 2007. Occurrence and distribution of stone fruit viruses and viroids in commercial plantings of Prunus species in western Anatolia, Turkey. Journal of Plant Pathology, 89, 265–268.
Hily J M, Scorza R, Malinowski T, Zawadzka B, Ravelonandro M. 2004. Stability of gene silencing-based resistance to Plum pox virus in transgenic plum (Prunus domestica L.) under field conditions. Transgenic Research, 13, 427–436.
Hily J M, Scorza R, Webb K, Ravelonandro M. 2005. Accumulation of the long class of siRNA is associated with resistance to Plum pox virus in a transgenic woody perennial plum tree. Molecular Plant Microbe Interaction, 18, 794–799.
Jarošová J, Gadiou S, Polak J, Ravelonandro M, Scorza R, Kundu J K. 2010. Evaluation of transgenic Prunus domestica L., clone C5 resistance to Plum pox virus. Julius-Kühn-Archiv, 427, 330–333.
Jarošová J, Kundu J K. 2010. Simultaneous detection of stone fruit tree viruses by one-step multiplex RT-PCR. Scientia Horticulturae, 125, 68–72.
Kundu J K, Briard P, Michel J, Michel H, Ravelonandro M, Scorza R. 2008. Role of the 25–26 nt siRNA in the resistance of transgenic Prunus domestica graft inoculated with Plum pox virus. Virus Genes, 36, 215–220.
Larkin M A, Blackshields G, Brown N P, Chenna R, McGettigan P A, McWilliam H, Valentin F, Wallace I M, Wilm A, Lopez R, Thompson J D, Gibson T J, Higgins D G. 2007. Clustal wand clustal X version 2.0. Bioinformatics, 23, 2947–2948.
Ma X, Tang Z, Qin J, Meng Y. 2015. The use of high-throughput sequencing methods for plant microRNA research. RNA Biology, 12, 709–719.
Malinowski T, Cambra M, Capote N, Zawadska B, Gorris M T, Scorza R, Ravelonadro M. 2006. Field trials of plum clones transformed with the Plum pox virus coat protein (PPV-CP) gene. Plant Disease, 90, 1012–1018.
Maliogka V I, Minafra A, Saldarelli P, Ruiz-García A B, Glasa M, Katis N, Olmos A. 2018. Recent advances on detection and characterization of fruit tree viruses using high-throughput sequencing technologies. Viruses, 10, 436–456.
Marandel G, Salava J, Abbott A, Candresse T, Decroocq V. 2009. Quantitative trait loci meta-analysis of Plum pox virus resistance in apricot (Prunus armeniaca L.): New insights on the organization and the identification of genomic resistance factors. Molecular Plant Pathology, 10, 347–360.
Massart S, Brostaux Y, Barbarossa L, Batlle A, Cesar V, Dutrecq O, Fonseca F, Guillem R, Komorowska B, Olmos A, Steyer S, Wetzel T, Kummert J, Jijakli M H. 2009. Interlaboratory evaluation of two reverse-transcriptase polymeric chain reaction-based methods for detection of four fruit tree viruses. Annals of Applied Biology, 154, 133–141.
Naqvi A R, Haq Q M R, Mukherjee S K. 2010. MicroRNA profiling of Tomato leaf curl New Delhi virus (ToLCNDV) infected tomato leaves indicates that deregulation of mir159/319 and mir172 might be linked with leaf curl disease. Virology Journal, 7, 281.
Pacheco R, García-Marcos A, Barajas D, Martiáñez J, Tenllado F. 2012. PVX-potyvirus synergistic infections differentially alter microRNA accumulation in Nicotiana benthamiana. Virus Research, 165, 231–235.
Peng C, Chen X, Wang X, Xu X, Wei W, Wang C, Xu J. 2018. Comparative analysis of miRNA expression profiles in transgenic and non-transgenic rice using miRNA-Seq. Scientific Reports, 8, 338.
Pérez-Quintero A L, Neme R, Zapata A, Lózez C. 2010. Plant microRNAs and their role in efence aginst viruses: A bioinformatices approach. BMC Plant Biology, 10, 138.
Polák J, Kundu J, Krška B, Beoni E, Komínek P, Pívalova J, Jarošová J. 2017. Transgenic plum Prunus domestica L, clone C5 (cv. HoneySweet) for protection against sharka disease. Journal of Integrative Agriculture, 16, 516–522.
Polák J, Pívalová J, Jokeš M, Svoboda J, Scorza R, Ravelonandro M. 2005. Preliminary results of interactions of Plum pox virus (PPV), Prune dwarf virus (PDV), and Apple chlorotic leafspot virus (ACLSV) with transgenic plants of plum Prunus domestica, clone C-5 grown in an open field. Phytopathology Polnica, 36, 115–122.
Polák J, Pivalová J, Kundu J K, Jokeš M, Scorza R, Ravelonandro M. 2008. Behaviour of transgenic Plum pox virus resistant Prunus domestica L. clone C5 grown in the open field under a high and permanent infection pressure of the PPV-Rec strain. Journal of Plant Pathology, 90, 33–36.
Pruss G, Ge X, Shi X M, Carrington J C, Vance V B. 1997. Plant viral synergism: The potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. The Plant Cell, 9, 859–868.
R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. [2018-09-20].
Ramesh S V, Ratnaparkhe M B, Kumawat G, Gupta G K, Husain S M. 2014. Plant miRNAome and antiviral resistance: A retrospective view and prospective challenges. Virus Genes, 48, 1–14.
Ravelonandro M, Scorza R, Bachelier J C, Labonne G, Levy L, Damsteegt V, Callahan A M, Dunez J. 1998. Resistance of transgenic Prunus domestica to Plum pox virus infection. Plant Disease, 81, 1231–1235.
Ravelonandro M, Scorza R, Kundu J, Briard P, Monsion M. 2007. The effect of co-infecting viruses on transgenic Plum pox virus resistant plums (Prunus domestica). Acta Horticulturae, 738, 653–656.
Rubio M, Pascal T, Bachellez A, Lambert P. 2010. Quantitative trait loci analysis of Plum pox virus resistance in Prunus davidiana P1908: New insights on the organization of genomic resistance regions. Tree Genetics and Genomes, 6, 291–304.
Schmittgen T D, Livak K J. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nature Protocol, 3, 1101–1108.
Scorza R, Callahan A, Dardick C, Ravelonandro M, Polák J, Malinowski T, Zagrai I, Cambra M, Kamenova I. 2013. Genetic engineering of Plum pox virus resistance: HoneySweet plum from concept to product. The Plant Cell, Tissue and Organ Culture, 115, 1–12.
Scorza R, Callahan A, Levy L, Damsteegt V, Webb K, Ravelonandro M. 2001. Post-transcriptional gene silencing in Plum pox virus resistant transgenic European plum containing the Plum pox potyvirus coat protein gene. Transgenic Research, 10, 201–209.
Scorza R, Callahan A M, Levy L, Damsteegt V, Ravelonandro M. 1998. Transferring potyvirus coat protein gene through hybridization of transgenic plants to produce Plum pox virus resistant plums (Prunus domestica). Acta Horticulturae, 472, 421–427.
Scorza R, Ravelonandro M, Callahan A M, Cordts J M, Fuchs M, Dunez J, Gonsalves D. 1994. Transgenic plum (Prunus domestica L.) express the Plum pox virus coat protein gene. Plant Cell Reports, 14, 18–22.
Simon-Mateo C, Garcia J A. 2006. MicroRNA-guided processing impairs Plum pox virus replication, but the virus readily evolves to escape this silencing mechanism. Journal of Virology, 80, 2429–2436.
Singh K, Kundu J K. 2017. Variation in coat protein sequence of Wheat streak mosaic virus among crop and no crop hosts. Crop and Pasture Science, 68, 328–336.
Singh K, Mazáková J, Zouhar M, Ryšánek P. 2014. Genome wide identification of the immunophilin gene family in Leptosphaeria maculans: A causal agent of Blackleg disease in oilseed rape (Brassica napus). OMICS: A Journal of Integrative Biology, 18, 645–657.
Sihelská N, Glasa M, Šubr Z W. 2017. Host preference of the major strains of Plum pox virus-opinions based on regional and world-wide sequence data. Journal of Integrative Agriculture, 16, 510–515.
Šubr Z, Glasa M. 2013. Unfolding the secrets of Plum pox virus: From epidemiology to genomics. Acta Virologica, 57, 217–228.
Šubr Z, Pittnerová S, Glasa M. 2004. A simplified RT-PCR-based detection of recombinant Plum pox virus isolates. Acta Virologica, 48, 173–176.
Sun G. 2012. MicroRNAs and their diverse functions in plants. Plant Molecular Biology, 80, 17–36.
Sunkar R, Chinnusamy V, Zhu J, Zhu J K. 2007. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Science, 12, 301–309.
Syller J. 2012. Facilitative and antagonistic interactions between plant viruses in mixed infections. Molecular Plant Pathology, 13, 204–216.
Tripathi A K, Singh K, Pareek A, Singla-Pareek S L. 2015. Histone chaperones in Arabidopsis and rice: Genome-wide identification, phylogeny, architecture and transcriptional regulation. BMC Plant Biology, 15, 42.
Tukey J. 1949. Comparing individual means in the analysis of variances. Biometrics, 5, 99–114.
Varga A, James D. 2005. Detection and differentiation of Plum pox virus using real-time multiplex PCR with SYBR Green and melting curve analysis: A rapid method for strain typing. Journal of Virological Methods, 123, 213–220.
Varga A, James D. 2006. Use of reverse transcription loop-mediated isothermal amplification for the detection of Plum pox virus. Journal of Virological Methods, 138, 184–190.
Zagrai I, Capote N, Ravelonandro M, Cambra M, Zagrai L, Scorza R. 2008. Plum pox virus silencing of C5 transgenic plums is stable under challenge inoculation with heterologous viruses. Journal of Plant Pathology, 90, 63–71.
Zhu H, Xia R, Zhao B, An Y Q, Dardick C D, Callahan A M, Liu Z. 2012. Unique expression, processing regulation, and regulatory network of peach (Prunus persica) miRNAs. BMC Plant Biology, 21, 149.
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