Virus-viroid interactions: Citrus tristeza virus enhances the accumulation of citrus dwarfing viroid in mexican lime via virus-encoded silencing suppressors

Journal of Virology

Volumn 88, Issue 2, 2014, Pages 1394-1397

  Serra, Pedro ^a,b   Bani Hashemian, Seyed M ^a,c   Fagoaga, Carmen ^a   Romero, Juan ^a   Ruiz Ruiz, Susana ^b   Gorris, Maria T ^a   Bertolini, Edson ^a   Duran Vila, Núria ^a  

^a INSTITUTO VALENCIANO DE INVESTIGACIONES AGRARIAS IVIA   (Spain)

^b Universitat Politècnica de València   (Spain)

^c Iran Citrus Research Institute   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P20; PROTEIN P23; PROTEIN P25; RNA;

ARTICLE; CITRON; CITRUS DWARFING VIROID; CITRUS TRISTEZAVIRUS; LIME (FRUIT); MIXED INFECTION; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUPPRESSOR CELL; VIROIDAL PLANT DISEASE;

CAPSID PROTEINS; CITRUS; CLOSTEROVIRUS; COINFECTION; PLANT DISEASES; RNA INTERFERENCE; RNA-BINDING PROTEINS; VIRAL PROTEINS; VIROIDS;

EID: 84891718193     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02619-13     Document Type: Article

References (35)

1. Flores R, Hernández C, Martínez de Alba AE, Darós JA, Di Serio F. 2005. Viroids and viroid-host interactions. Annu. Rev. Phytopathol. 43:117-139. http://dx.doi.org/10.1146/annurev.phyto.43.040204.140243.
2. Szychowski JA, McKenry MV, Walker A, Wolpert JA, Credi R, Semancik JS. 1995. The vein-banding disease syndrome: a synergistic reaction between grapevine viroids and fanleaf virus. Vitis 34:229-232.
3. Vidalakis G, Garnsey SM, Bash JA, Greer GD, Gumpf DJ. 2004. Efficacy of bioindexing for graft-transmissible citrus pathogens in mixed infections. Plant Dis. 88:1328-1334. http://dx.doi.org/10.1094/PDIS.2004.88.12.1328.
4. Murcia N, Bernad L, Serra P, Bani Hashemian SM, Duran-Vila N. 2009. Molecular and biological characterization of natural variants of citrus dwarfing viroid. Arch. Virol. 154:1329-1334. http://dx.doi.org/10.1007/s00705-009-0430-9.
5. Moreno P, Guerri J, Ballester-Olmos JF, Albiach R, Martínez ME. 1993. Separation and interference of strains from a citrus tristeza virus isolate evidenced by biological activity and double-stranded RNA (dsRNA) analysis. Plant Pathol. 42:35-41. http://dx.doi.org/10.1111/j.1365-3059.1993.tb01469.x.
6. Cambra M, Gorris MT, Román MP, Terrada E, Garnsey SM, Camarasa E. 2000. Routine detection of citrus tristeza virus by direct immunoprinting-ELISA method using specific monoclonal and recombinant antibodies, p 34-41. In da Graça JV, Lee RF, Yokomi RK (ed), Proc. 14th Conf. Intl. Org. Citrus Virologists. International Organization of Citrus Virologists, Riverside, CA.
7. Romero-Durbán J, Cambra M, Duran-Vila N. 1995. A simple imprint hybridization method for detection of viroids. J. Virol. Methods 55:37-47. http://dx.doi.org/10.1016/0166-0934(95)00043-T.
8. Bernad L, Duran-Vila N. 2006. A novel RT-PCR approach for detection and characterization of citrus viroids. Mol. Cell. Probes 20:105-113. http://dx.doi.org/10.1016/j.mcp.2005.11.001.
9. Garnsey SM, Cambra M. 1991. Enzyme-linked immunosorbent assay (ELISA) for citrus pathogens. In Graft-transmissible diseases of citrus: handbook for detection and diagnosis, p 193-216. Food and Agriculture Organization of the United Nations, Rome, Italy.
10. Bertolini E, Moreno A, Capote N, Olmos A, de Luis A, Vidal E, Pérez-Panadés J, Cambra M. 2008. Quantitative detection of citrus tristeza virus in plant tissues and single aphids by real-time RT-PCR. Eur. J. Plant Pathol. 120:177-188. http://dx.doi.org/10.1007/s10658-007-9206-9.
11. Vidal E, Yokomi RK, Moreno A, Bertolini E, Cambra M. 2012. Calculation of diagnostic parameters of advanced serological and molecular tissue-print methods for detection of citrus tristeza virus: a model for other plant pathogens. Phytopathology 102:114-121. http://dx.doi.org/10.1094/PHYTO-05-11-0139.
12. Baulcombe D. 2004. RNA silencing in plants. Nature 431:356-363. http://dx.doi.org/10.1038/nature02874.
13. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363-366. http://dx.doi.org/10.1038/35053110.
14. Lecellier CH, Voinnet O. 2004. RNA silencing: no mercy for viruses? Immunol. Rev. 198:285-303. http://dx.doi.org/10.1111/j.0105-2896.2004.00128.x.
15. Ruiz-Ferrer V, Voinnet O. 2009. Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60:485-510. http://dx.doi.org/10.1146/annurev.arplant.043008.092111.
16. Itaya A, Folimonov A, Matsuda Y, Nelson RS, Ding B. 2001. Potato spindle tuber viroid as inducer of RNA silencing in infected tomato. Mol. Plant Microbe Interact. 14:1332-1334. http://dx.doi.org/10.1094/MPMI.2001.14.11.1332.
17. Itaya A, Zhong X, Bundschuh R, Qi Y, Wang Y, Takeda R, Harris AR, Molina C, Nelson RS, Ding B. 2007. A structured viroid RNA is substrate for dicer-like cleavage to produce biologically active small RNAs but is resistant to RISC-mediated degradation. J. Virol. 81:2980-2994. http://dx.doi.org/10.1128/JVI.02339-06.
18. Papaefthimiou I, Hamilton AJ, Denti MA, Baulcombe DC, Tsagris M, Tabler M. 2001. Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post-transcriptional gene silencing. Nucleic Acids Res. 29:2395-2400. http://dx.doi.org/10.1093/nar/29.11.2395.
19. Martínez de Alba AE, Flores R, Hernández C. 2002. Two chloroplastic viroids induce the accumulation of small RNAs associated with posttranscriptional gene silencing. J. Virol. 76:13094-13096. http://dx.doi.org/10.1128/JVI.76.24.13094-13096.2002.
20. Carbonell A, Martínez de Alba AE, Flores R, Gago S. 2008. Double-stranded RNA interferes in a sequence-specific manner with infection of representative members of the two viroid families. Virology 371:44-53. http://dx.doi.org/10.1016/j.virol.2007.09.031.
21. Schwind N, Zwiebel M, Itaya A, Ding B, Wang MB, Krczal G, Wassenegger M. 2009. RNAi-mediated resistance to Potato spindle tuber viroid in transgenic tomato expressing a viroid hairpin RNA construct. Mol. Plant Pathol. 10:459-469. http://dx.doi.org/10.1111/j.1364-3703.2009.00546.x.
22. Moissiard G, Voinnet O. 2004. Viral suppression of RNA silencing in plants. Mol. Plant Pathol. 5:71-82. http://dx.doi.org/10.1111/j.1364-3703.2004.00207.x.
23. Lu R, Folimonov A, Shintaku M, Li WX, Falk BW, Dawson WO, Ding SW. 2004. Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc. Natl. Acad. Sci. U. S. A. 101:15742-15747. http://dx.doi.org/10.1073/pnas.0404940101.
24. Di Serio F, Martínez de Alba AE, Navarro B, Gisel A, Flores R. 2010. RNA-dependent RNA polymerase 6 delays accumulation and precludes meristem invasion of a viroid that replicates in the nucleus. J. Virol. 84:2477-2489. http://dx.doi.org/10.1128/JVI.02336-09.
25. Fagoaga C, López C, Moreno P, Navarro L, Flores R, Peña L. 2005. Viral-like symptoms induced by the ectopic expression of the p23 gene of Citrus tristeza virus are citrus specific and do not correlate with the pathogenicity of the virus strain. Mol. Plant Microbe Interact. 18:435-445. http://dx.doi.org/10.1094/MPMI-18-0435.
26. Domínguez A, Fagoaga C, Navarro L, Moreno P, Peña L. 2002. Regeneration of transgenic citrus plants under non selective conditions results in high-frequency recovery of plants with silenced transgenes. Mol. Genet. Genomics 267:544-556. http://dx.doi.org/10.1007/s00438-002-0688-z.
27. Fagoaga C, Pensabene-Bellavia G, Moreno P, Navarro L, Flores R, Peña L. 2011. Ectopic expression of the p23 silencing suppressor of Citrus tristeza virus differentially modifies viral accumulation and tropism in two transgenic woody hosts. Mol. Plant Pathol. 12:898-910. http://dx.doi.org/10.1111/j.1364-3703.2011.00722.x.
28. Siddiqui SA, Sarmiento C, Truve E, Lehto H, Lehto K. 2008. Phenotypes and functional effects caused by various viral RNA silencing suppressors in transgenic Nicotiana benthamiana and N. tabacum. Mol. Plant Microbe Interact. 21:178-187. http://dx.doi.org/10.1094/MPMI-21-2-0178.
29. Wang J, Turina M, Medina V, Falk BW. 2009. Synergistic interaction between the potyvirus, Turnip mosaic virus and the crinivirus, Lettuce infectious yellows virus in plants and protoplasts. Virus Res. 144:163-170. http://dx.doi.org/10.1016/j.virusres.2009.04.017.
30. Siddiqui SA, Sarmiento C, Kiisma M, Koivumaki S, Lemmetty A, Truve E, Lehto K. 2008. Effects of viral silencing suppressors on tobacco ringspot virus infection in two Nicotiana species. J. Gen. Virol. 89:1502-1508. http://dx.doi.org/10.1099/vir.0.83621-0.
31. Ruiz-Ruiz S, Navarro B, Gisel A, Peña L, Navarro L, Moreno P, Di Serio F, Flores R. 2011. Citrus tristeza virus infection induces the accumulation of viral small RNAs (21-24-nt) mapping preferentially at the 3'-terminal region of the genomic RNA and affects the host small RNA profile. Plant Mol. Biol. 75:607-619. http://dx.doi.org/10.1007/s11103-011-9754-4.
32. López C, Navas-Castillo J, Gowda S, Moreno P, Flores R. 2000. The 23-kDa protein coded by the 3'-terminal gene of citrus tristeza virus is an RNA-binding protein. Virology 269:462-470. http://dx.doi.org/10.1006/viro.2000.0235.
33. Ruiz-Ruiz S, Soler N, Sánchez-Navarro J, Fagoaga C, López C, Navarro L, Moreno P, Peña L, Flores R. 2013. Citrus tristeza virus p23: determinants for nucleolar localization and their influence on suppression ofRNA silencing and pathogenesis. Mol. Plant Microbe Interact. 26:306-318. http://dx.doi.org/10.1094/MPMI-08-12-0201-R.
34. Satyanarayana T, Gowda S, Ayllón MA, Albiach-Martí MR, Rabindram R, Dawson WO. 2002. The p23 protein of citrus tristeza virus controls asymmetrical RNA accumulation. J. Virol. 76:473-483. http://dx.doi.org/10.1128/JVI.76.2.473-483.2002.
35. Gambino G, Navarro B, Vallania R, Gribaudo I, Di Serio F. 2011. Somatic embryogenesis efficiently eliminates viroid infections from grapevines. Eur. J. Plant Pathol. 130:511-519. http://dx.doi.org/10.1007/s10658-011-9770-x.